Fungal Diversity

, Volume 40, Issue 1, pp 1–11 | Cite as

Fungi associated with the decline of Pinus halepensis in Spain



Fungal species richness and composition within needles and twigs in 55 stands of Pinus halepensis, spread out over the whole Iberian Peninsula, were determined. The aim was to evaluate the relationships of fungal communities with local environmental variables, in order to analyze the potential causes of the current decline of this pine species in Spain. A total of 35 fungal taxa were isolated from 1980 moist chambers analysed (990 per vegetal tissue). A taxon within the Alternaria alternata complex was most frequent, followed by Leptostroma pinastri, Aspergillus niger, Diplodia pinea and Phomopsis sp. At the tree level, tissue was a significant response variable and a higher species richness was found in needles as compared to twigs. On the other hand, the multivariate analysis showed the environmental variables ‘age’, ‘shadow’, ‘elevation’, ‘mean temperature’, ‘illumination’ and ‘availability of water’ significantly influenced fungal species composition. In particular, ‘mean temperature’, was an important variable implicated in the general weakening of this thermophilic pine species, and appeared to be inversely correlated with the occurrence of several conifer pathogens such as Brunchorstia pinea, Cytospora sp., Diplodia pinea, Naemacyclus niveus, Pestalotiopsis stevensonii and Sclerophoma pythiophila. This study shows a possible combined effect of abiotic and biotic stresses in causing the general decline of Allepo pine in Spain.


Abiotic stress Allepo pine Forest pathogens Fungi Global warming Weakening 


  1. Abelló MA (1998) Historia y Evolución de las Repoblaciones Forestales en España. Universidad Complutense de Madrid, Madrid, p 749Google Scholar
  2. Anonymous (1989) SAS/STAT user´s guide, vol 1–2, 4th edn. SAS Institute, CaryGoogle Scholar
  3. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66CrossRefGoogle Scholar
  4. Arnold AE, Herre EA (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: ecological patterns and process in Theobroma cacao (Malvaceae). Mycologia 95:388–398CrossRefGoogle Scholar
  5. Bachi PR, Peterson JL (1985) Enhancement of Sphaeropsis sapinea stem invasion of pines by water deficits. Plant Dis 69:798–799Google Scholar
  6. Bahnweg G, Heller W, Stich S, Knappe C, Betz C, Heerdt C, Kehr RD, Ernst D, Langebartels C, Nunn AJ, Rothenburger J, Schubert R, Wallis P, Müller-Starck G, Werner H, Matyssek R, Sandermann H Jr (2005) Beech leaf colonization by the endophyte Apiognomia errabunda. Plant Biol 7:659–669CrossRefPubMedGoogle Scholar
  7. Brandt JP, Cerezke HF, Mallett KI, Volney WJA, Weber JD (2003) Factors affecting trembling aspen (Populus tremuloides Michx.) health in the boreal forest of Alberta, Saskatchewan, and Manitoba, Canada. For Ecol Manag 178:287–300Google Scholar
  8. Brener WD, Setliff EC, Norgren RL (1974) Sclerophoma pythiophila associated with a tip dieback of Juniper in Wisconsin. Plant Dis Rep 58:653–657Google Scholar
  9. Bussoti F, Ferreti M (1998) Air pollution, forest condition and forest decline in Southern Europe: an overview. Environ Pollut 101:49–65CrossRefGoogle Scholar
  10. Calamassi R, Paoletti E, Strati S (2001) Frost hardening and resistance in three Aleppo pine (Pinus halepensis Mill.) provenances. Isr J Plant Sci 49:179–186CrossRefGoogle Scholar
  11. Climent J, Costa e Silva F, Chambel MR, Pardos M, Almeida MH (2009) Freezing injury in primary and secondary needles of Mediterranean pine species of contrasting ecological niches. Ann For Sci 66:407CrossRefGoogle Scholar
  12. Collado J, Platas G, Peláez F (1996) Fungal endophytes in leaves, twigs and bark of Quercus ilex from central Spain. Nova Hedwigia 63:347–360Google Scholar
  13. Danti R, Sieber TN, Sanguineti G (2002) Endophytic mycobiota in bark of European beech (Fagus sylvatica) in the Apennines. Mycol Res 106:1343–1348CrossRefGoogle Scholar
  14. De Wet J, Burgess T, Slippers B, Preisig O, Wingfield BD, Winfield MJ (2003) Multiple gene genealogies and microsatellite markers reflect relationships between morphotypes of Sphaeropsis sapinea and distinguish a new species of Diplodia. Mycol Res 107:557–566CrossRefPubMedGoogle Scholar
  15. Desprez-Loustau ML, MarÇais B, Nageleisen LM, Piou D, Vannini A (2006) Interactive effects of drought and pathogens in forest trees. Ann For Sci 63:597–612CrossRefGoogle Scholar
  16. Farr D, Bills G, Chamuris G, Rossman A (1989) Fungi on Plants and plant products in the United States, St. Paul, MNGoogle Scholar
  17. Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327CrossRefPubMedGoogle Scholar
  18. Gil, L., Díaz-Fernández, P.M., Jiménez, M.P., Roldán, M., Alía, R., Agúndez, D., De Miguel, J., Martín, S. and De Tuerto, M. (1996). Las regiones de Procedencia del Pinus halepensis Mill., MadridGoogle Scholar
  19. Gimeno BS, Peñuelas L, Porcuna JL, Reinert RA (1995) Biomonitoring ozone phytotoxicity in eastern Spain. Water Air Soil Pollut 85:1521–1526CrossRefGoogle Scholar
  20. Giordano L, Gonthier P, Varese GC, Miserere L, Nicolotti G (2009) Mycobiota inhabiting sapwood of healthy and declining Scots pine (Pinus sylvestris L.) trees in the Alps. Fungal Divers 38:xx–xxGoogle Scholar
  21. Goidanich G (1990) Manuale di patologia vegetale. Edizioni Agricole della Calderini, Bologna, p 1283Google Scholar
  22. Gonthier P, Gennaro M, Nicolotti G (2006) Effects of water stress on endophytic mycota of Quercus robur. Fungal Divers 21:69–80Google Scholar
  23. Guo LD, Xu L, Zheng WH, Hyde KD (2004) Genetic variation of Alternaria alternata, an endophytic fungus isolated from Pinus tabulaeformis as determined by random amplified microsatellites (RAMS). Fungal Divers 16:53–65Google Scholar
  24. Hanlin RT (1998) Illustrated genera of ascomycetes, vol I and II. The American Phytopathology Society, St. PaulGoogle Scholar
  25. Hoff JA, Klopfenstein NB, McDonald GI, Tonn JR, Kim MS, Zambino PJ, Hessburg PF, Rogers JD, Peever TL, Carris LM (2004) Fungal endophytes in woody roots of Douglas-fir (Pseudotsuga menziesii) and ponderosa pine (Pinus ponderosa). Forest Pathol 34:255–271CrossRefGoogle Scholar
  26. Hu HL, Jeewon R, Zhou DQ, Zhou TX, Hyde HD (2007) Phylogenetic diversity of endophytic Pestalotiopsis species in Pinus armandii and Ribes spp.: evidence from rDNA and β-tubulin gene phylogenies. Fungal Divers 24:1–22Google Scholar
  27. Huang WY, Cai YZ, Hyde KD, Corke H, Sun M (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers 33:61–75Google Scholar
  28. Johnson JW, Gleason ML, Parker SK, Provin EB, Iles JK (1997) Duration of water stress affects development of Sphaeropsis canker on Scots pine. J Arboric 23:73–76Google Scholar
  29. Jurc M, Jurc D, Gogala N, Simoncic P (1996) Air pollution and fungal endophytes in needles of Austrian pine. Phyton-Annales Rei Botanicae 36:111–114Google Scholar
  30. Kiffer E, Morelet M (1999) The deuteromycetes. Mitosporic fungi. Classification and generic keys. Science Publishers Inc., EnfieldGoogle Scholar
  31. La Porta N, Capretti P, Thomsen IM, Kasanen R, Hietala AM, Von Weissenberg K (2008) Forest pathogens with higher damage potential due to climate change in Europe. Can J Plant Pathol 30:177–195Google Scholar
  32. Lanier L, Joly P, Bonodoux P, Bellemere A (1978) Mycologie et pathologie forestieres, vol 1. Masson, ParisGoogle Scholar
  33. Le Houerou HN (1992) Vegetation and land use in the Mediterranean basin by the year 2050: a prospective study. Edward Arnold, LondonGoogle Scholar
  34. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  35. Lehtijärvi A, Barklund P (2000) Seasonal patterns of colonization of Norway spruce needles by Lophodermium piceae. Forest Pathol 30:187–193CrossRefGoogle Scholar
  36. Magan N, Kirkwood IA, Mcleod AR, Smith MK (1995) Effect of open-air fumigation with sulfur-dioxide and ozone on Phyllosphere and endophytic fungi of conifer needles. Plant Cell Environ 18:291–302CrossRefGoogle Scholar
  37. Martín P, Pajares JA, Nanos N, Diez JJ (2004) Site and seasonal influences on the fungal community on leaves and stems of Pinus and Quercus seedlings in forest nurseries. Sydowia 56:23–47Google Scholar
  38. Müller MM, Hallaksela AM (1998) Diversity of Norway spruce needle endophytes in various mixed and pure Norway spruce stands. Mycol Res 102:1183–1189CrossRefGoogle Scholar
  39. Müller MM, Hallaksela AM (2000) Fungal diversity in Norway spruce: a case study. Mycol Res 104:1139–1145CrossRefGoogle Scholar
  40. Muñoz López C (1997) Presencia en España del hongo Sirococcus conigenus Cannon & Minter responsable de la muerte de brotes en Pinus halepensis Mill. XIV Reunión del Grupo de Trabajo Fitosanitario de Forestales, Parques y Jardines, pp 110–111Google Scholar
  41. Ninyerola M, Pons X, Roure JM (2005) Altas Climático Digital de la Península Ibérica. In: Metodología y aplicaciones en bioclimatología y geobotánica (ed) Bellaterra. Universidad Autónoma de BarcelonaGoogle Scholar
  42. Paoletti E, Danti R, Strati S (2001) Pre- and post- inoculation water stress affects Spaheropsis sapinea canker length in Pinus halepensis seedlings. Forest Pathol 31:209–218CrossRefGoogle Scholar
  43. Phillips DH, Burdekin DA (1992) Diseases of forest and ornamental trees. Macmillian, LondonGoogle Scholar
  44. Promputtha I, Lumyong S, Dhanasekaran V, McKenzie EHC, Hyde KD, Jeewon R (2007) A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb Ecol 53:579–590CrossRefPubMedGoogle Scholar
  45. Punithalingam E, Waterson J (eds) (1970) Diplodia pinea. Pathogenic fungi and bacterial, vol 2. Commonwealth Mycological Institute, KewGoogle Scholar
  46. Ranta H, Saloniemi I (2005) Distribution of fungal foliage and shoot pathogens in a natural Scots pine population in relation to environmental variables. Can J For Res-Revue Canadienne De Recherche Forestiere 35:503–510CrossRefGoogle Scholar
  47. Rishbeth J, Meredith DL (1957) Surface micoflora of pine needles. Nature 179:682–683CrossRefGoogle Scholar
  48. Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biol Rev 21:67–74CrossRefGoogle Scholar
  49. Santamaria O, Diez JJ (2005) Fungi in leaves, twigs and stem bark of Populus tremula from northern Spain. Forest Pathol 35:95–104CrossRefGoogle Scholar
  50. Santamaria O, Pajares JA, Diez JJ (2003) First report of Gremmeniella abietina on Pinus halepensis in Spain. Plant Pathol 52:425–425CrossRefGoogle Scholar
  51. Santamaria O, Tejerina L, Pajares JA, Diez JJ (2007) Effects of associated fungi Sclerophoma pythiophila and Cenangium ferruginosum on Gremmeniella abietina dieback in Spain. Forest Pathol 37:121–128CrossRefGoogle Scholar
  52. Santamaria, O., Botella, L. and Diez, J.J. (2008). Gremmeniella abietina in North-western Spain: Distribution and associated mycoflora. Acta Silvatica and Lignaria Hungarica, Spec. Edition: 137–145Google Scholar
  53. Sieber B (2007) Endophytic fungi of forest trees: are they mutualists? Fungal Biol Rev 21:75–89CrossRefGoogle Scholar
  54. Siebercanavesi F, Petrini O, Sieber TN (1991) Endophytic Leptostroma species on Picea abies, Abies alba, and Abies balsamea—a Cultural, Biochemical, and Numerical Study. Mycologia 83:89–96CrossRefGoogle Scholar
  55. SPCAN (1998) Distribución de Daños Soflamado Observados en Pinus halepensis Google Scholar
  56. Speer JH, Grissino-Mayer HD, Orvis KH, Greenberg CH (2009) Climate response of five oak species in the eastern deciduous forest of the southern Appalachian Mountains, USA. Can J Bot-Revue Canadienne De Botanique 39:507–518Google Scholar
  57. Stanosz GR, Blodgett JT, Smith DR, Kruger EL (2001) Water stress and Sphaeropsis sapinea as a latent pathogen of red pine seedlings. New Phytol 149:531–538CrossRefGoogle Scholar
  58. Stanosz GR, Smith DR, Leisso R (2007) Diplodia shoot blight and asymptomatic persistence of Diplodia pinea on or in stems of jack pine nursery seedlings. Forest Pathol 37:145–154CrossRefGoogle Scholar
  59. Stirling GR, Smith LJ, Licastro KA, Eden LM (1998) Control of root-knot nematode with formulations of the nematode-trapping fungus Arthrobotrys dactyloides. Biol Control 11:224–230CrossRefGoogle Scholar
  60. Sutton BC (1980) The coelomycetes. Fungi Imperfecti with Pycnidia Acervuli and Stromata. Commonwealth Mycological Institute, KewGoogle Scholar
  61. Sutton BC, Waterston JM (1970) Colletotrichum musae. CMI Description of pathogenic fungi and bacteria. CMI. No. 222Google Scholar
  62. Ter Braak CJF, Smilauer P (2002) CANOCO Reference Manual and CANODRAW for User´s Guide version 4.5., Ithaca, NYGoogle Scholar
  63. Thomas FM, Blank R, Hartmann G (2002) Abiotic and biotic factors and their interactions as causes of oak decline in Central Europe. Forest Pathol 32:277–307CrossRefGoogle Scholar
  64. Thomsen IM (2009) Precipitation and temperature as factors in Gremmeniella abietina epidemics. Forest Pathol 39:56–72CrossRefGoogle Scholar
  65. Wang Y, Guo LD, Hyde KD (2005) Taxonomic placement of sterile morphotypes of endophytic fungi from Pinus tabulaeformis (Pinaceae) in northeast China based on rDNA sequences. Fungal Divers 20:235–260Google Scholar
  66. Zamora P, Martinez-Ruiz C, Diez JJ (2008) Fungi in needles and twigs of pine plantations from Northern Spain. Fungal Divers 30:171–184Google Scholar

Copyright information

© Kevin D Hyde 2010

Authors and Affiliations

  1. 1.Departamento de Producción Vegetal y Recursos ForestalesUniversidad de ValladolidPalenciaSpain
  2. 2.Departamento de Ingeniería del Medio Agronómico y ForestalUniversidad de ExtremaduraBadajozSpain

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