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Combined effects of soil properties and Phytophthora cinnamomi infections on Quercus ilex decline

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Abstract

Aims

The importance of soil properties as determinants of tree vitality and Phytophthora cinnamomi root infections was analysed.

Methods

The study comprised 96 declining stands in western Spain, where declining and non-declining holm oak (Quercus ilex L.) trees were sampled. Soil properties (soil depth, Ah horizon thickness, texture, pH, redox potential, soil bulk density and N-NH4 + and N-NO3 − concentrations) and P. cinnamomi infections were assessed.

Results

Tree mortality rates increased with low soil bulk densities, which were also associated with more P. cinnamomi-infected trees. Occurrence of infected trees was higher in fine textured soils and in thick Ah horizons. Fine textured soils favoured trees, but with the presence of P. cinnamomi their health status deteriorated. Soil under declining trees had higher N-NO3 −/N-NH4 + ratio values than under non-declining trees. Additional soil properties changes associated to grazing were not related to decline and P. cinnamomi infections.

Conclusions

The implications of P. cinnamomi in holm oak decline and the influence of soil properties as contributors to pathogen activity were demonstrated. Fine soil textures and thick Ah horizons, usually favourable for vigour and vitality of trees growing in the Mediterranean climate, were shown to be disadvantageous soil properties if P. cinnamomi was present. Fine soil textures and thick Ah horizons are frequently related with higher levels of soil moisture, which increase the inoculum of the pathogen and favours root infection. Grazing does not seem to be directly linked to Q. ilex health status or P. cinnamomi root rot.

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References

  • Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:419–449

    Article  Google Scholar 

  • Alameda D, Villar R (2009) Moderate soil compaction: implications on growth and architecture in seedlings of 17 woody plant species. Soil Tillage Res 103:325–331

    Article  Google Scholar 

  • Asner GP, Elmore AJ, Olander LP, Martin RE, Harris AT (2004) Grazing systems, ecosystem responses, and global change. Annu Rev Environ Resour 29:261–299

    Article  Google Scholar 

  • Balci Y, Balci S, Eggers J, MacDonald WL, Juzwik J, Long RP, Gottschalk KW (2007) Phytophthora spp. associated with forest soils in eastern and north-central U.S. oak ecosystems. Plant Dis 91:705–710

    Article  Google Scholar 

  • Bartlett RJ, James BR (1995) System for categorizing soil redox status by chemical field testing. Geoderma 68:211–218

    Article  CAS  Google Scholar 

  • Benson DM (1984) Influence of pine bark, matric potential, and pH on sporangium production by Phytophthora cinnamomi. Phytopathology 74:1359–1363

    Article  Google Scholar 

  • Berger TW, Glatzel G (2001) Response of Quercus petraea seedlings to nitrogen fertilization. For Ecol Manag 149:1–14

    Article  Google Scholar 

  • Brasier CM (1996) Evidence for Phytophthora cinnamomi involvement in Iberian oak decline. Environmental constraints including climate change. Ann For Sci 53:347–358

    Article  Google Scholar 

  • Camilo-Alves CSP, Clara MIE, Ribeiro NMCA (2013) Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review. Eur J Forest Res 132:411–432

    Google Scholar 

  • Corcobado T, Cubera E, Pérez-Sierra A, Jung T, Solla A (2010) First report of Phytophthora gonapodyides involved in the decline of Quercus ilex in xeric conditions in Spain. New Dis Reports 22:33–33

    Article  Google Scholar 

  • Corcobado T, Cubera E, Moreno G, Solla A (2013) Quercus ilex forests are influenced by annual variations in water table, soil water deficit and fine root loss caused by Phytophthora cinnamomi. Agric Forest Meteorol 169:92–99

    Article  Google Scholar 

  • Costa A, Pereira H, Madeira M (2010) Analysis of spatial patterns of oak decline in cork oak woodlands in Mediterranean conditions. Ann For Sci 67:204

    Article  Google Scholar 

  • Cubera E, Moreno G (2007) Effect of single Quercus ilex trees upon spatial and seasonal changes in soil water content in dehesas of central western Spain. Ann For Sci 64:355–364

    Article  Google Scholar 

  • Cubera E, Moreno G, Solla A (2009) Quercus ilex root growth in response to heterogeneous conditions of soil bulk density and soil NH4-N content. Soil Tillage Res 103:16–22

    Article  Google Scholar 

  • Dane JH, Topp GC (2002) Methods of soil analysis. Part 4: Physical methods. Soil Science Society of America Books Series: 5. Soil Science Society of America, Madison

    Google Scholar 

  • David TS, Ferreira MI, Cohen S, Pereira JS, David JS (2004) Constraints on transpiration from an evergreen oak tree in southern Portugal. Agr Forest Meteorol 122:193–205

    Article  Google Scholar 

  • Del Pozo JL (2006) Prospección de la seca en Extremadura. Análisis de los resultados. In: Espejo M, Martín M, Matos C, Mesías SJ (eds) Gestión ambiental y económica del ecosistema dehesa en la península ibérica. Junta de Extremadura, Mérida, pp 131–143

    Google Scholar 

  • Evans R (1998) The erosional impacts of grazing animals. Prog Phys Geogr 22:251–268

    Google Scholar 

  • Gallardo A (2003) Effect of tree canopy on the spatial distribution of soil nutrients in a Mediterranean dehesa. Pedobiologia 47:117–125

    Article  CAS  Google Scholar 

  • Gisi U (1983) Biophysical aspects of the development of Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora: Its biology, taxonomy, ecology, and pathology. The American Phytopathological Society, St Paul, pp 109–119

    Google Scholar 

  • Gómez-Aparicio L, Ibáñez B, Serrano MS, De Vita P, Ávila JM, Pérez-Ramos IM, García LV, Sánchez ME, Marañón T (2012) Spatial patterns of soil pathogens in declining Meditarranean forests: implications for tree species regeneration. New Phytol 194:1014–1024

    Article  PubMed  Google Scholar 

  • Hardham AR (1989) Lectin and antibody labelling of surface components of spores of Phytophthora cinnamomi. Aust J Plant Physiol 16:19–32

    Article  CAS  Google Scholar 

  • Heuscher SA, Brandt CC, Jardine PM (2005) Using soil physical and chemical properties to estimate bulk density. Soil Sci Soc Am J 69:51–56

    CAS  Google Scholar 

  • Jönsson U, Jung T, Sonesson K, Rosengren U (2005) Relationships between health of Quercus robur, occurrence of Phytophthora species and site conditions in southern Sweden. Plant Pathol 54:502–511

    Article  Google Scholar 

  • Jung T, Blaschke H, Neumann P (1996) Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. Eur J For Pathol 26:253–272

    Article  Google Scholar 

  • Jung T, Blaschke H, Oβwald W (2000) Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease. Plant Pathol 49:706–718

    Article  Google Scholar 

  • Khew KL, Zentmyer GA (1973) Chemotactic response of zoospores of five species of Phytophthora. Phytopathology 63:1511–1517

    Article  CAS  Google Scholar 

  • Kong P, Lea-Cox JD, Moorman GW, Hong C (2012) Survival of Phytophthora alni, P. kernoviae and P. ramorum in a simulated aquatic environment at different levels of pH. Microbiology 332:54–60

    CAS  Google Scholar 

  • Kozlowski TT (1999) Soil compaction and growth of woody plants. Scand J For Res 14:596–619

    Google Scholar 

  • Lloret F, Siscart D, Dalmases C (2004) Canopy recovery after drought dieback in holm-oak Mediterranean forests of Catalonia (NE Spain). Global Change Biol 10:2092–2099

    Article  Google Scholar 

  • Malajczuk N, Sanfelieu CL, Hossen S (1983) Production and survival of Phytophthora cinnamomi zoospores in suppressive and conducive soils. Trans Br Mycol Soc 80:305–312

    Article  Google Scholar 

  • Maurel M, Robin C, Capron G, Desprez-Loustau ML (2001) Effects of root damage associated with Phytophthora cinnamomi on water relations, biomass accumulation, mineral nutrition and vulnerability to water deficit of five oak and chestnut species. For Pathol 31:353–369

    Article  Google Scholar 

  • Moreno G, Obrador JJ, Cubera E, Dupraz C (2005) Fine root distribution in dehesas of central-western Spain. Plant Soil 277:153–162

    Article  CAS  Google Scholar 

  • Moreno G, Pulido FJ (2009) The functioning, management, and persistence of dehesas. In: Rigueiro-Rodríguez A, Mosquera-Losada MR, McAdam J (eds) Agroforestry systems in Europe. Springer, Amsterdam, pp 127–160

    Google Scholar 

  • Moreira AC, Martins JMS (2005) Influence of site factors on the impact of Phytophthora cinnamomi in cork oak stands in Portugal. For Pathol 35:145–162

    Article  Google Scholar 

  • Morillas L, Gallardo A, Portillo-Estrada M, Covelo F (2012) Nutritional status of Quercus suber populations under contrasting tree dieback. Forestry. doi:10.1093/forestry/cps035

    Google Scholar 

  • Oppermann R, Beaufoy G, Jones G (2012) High nature value farming in Europe. 35 European countries—experiences and perspectives. Verlag regionalkultur, Germany

    Google Scholar 

  • Oszako T, Delatour C (2000) Recent advances on oak health in Europe. Forest Research Institute, Warsaw

    Google Scholar 

  • Pegg KG (1977) Soil application of elemental sulphur as a control of Phytophthora cinnamomi root and heart rot of pineapple. Aust J Exp Agric Anim Husb 17:859–865

    Article  CAS  Google Scholar 

  • Pérez-Sierra A, López-García C, León M, García-Jiménez J, Abad-Campos P, Jung T (2013) Previously unrecorded low-temperature Phytophthora species associated with Quercus decline in a Mediterranean forest in eastern Spain. For Pathol. doi:10.1111/efp.12037

    Google Scholar 

  • Rozas V, García-González I (2012) Too wet for oaks? Inter-tree competition and recent persistent wetness predispose oaks to rainfall-induced dieback in Atlantic rainy forest. Global Planet Chang 94–95:62–71

    Article  Google Scholar 

  • Sánchez ME, Caetano P, Ferraz J, Trapero A (2000) El decaimiento y muerte de encinas en tres dehesas de la provincia de Huelva. Bol San Veg Plagas 26:447–464

    Google Scholar 

  • Sánchez ME, Caetano P, Ferraz J, Trapero A (2002) Phytophthora disease of Quercus ilex in south-western Spain. For Pathol 32:5–18

    Article  Google Scholar 

  • Sankaran MS, Augustine DJ (2004) Large herbivores suppress decomposer abundance in a semiarid grazing ecosystem. Ecology 41:45–58

    Google Scholar 

  • Santini A, Ghelardini L, De Pace C, Desprez-Loustau ML, Capretti P, Chandelier A, Cech T, Chira D, Diamandis S, Gaitniekis T, Hantula J, Holdenrieder O, Jankovsky L, Jung T, Jurc D, Kirisits T, Kunca A, Lygis V, Malecka M, Marcais B, Schmitz S, Schumacher J, Solheim H, Solla A, Szabò I, Tsopelas P, Vannini A, Vettraino AM, Webber J, Woodward S, Stenlid J (2013) Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol 197:238–250

    Article  PubMed  CAS  Google Scholar 

  • Schmitthenner AF, Canaday CH (1983) Role of chemical factors in development of Phytophthora diseases. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora: Its biology, taxonomy, ecology, and pathology. The American Phytopathological Society, St Paul, pp 189–196

    Google Scholar 

  • Schnabel S, Gómez Gutiérrez A, Lavado Contador JF (2009) Grazing and soil erosion in dehesas of SW Spain. In: Romero Díaz A, Belmonte Serrato F, Alonso Sarria F, Francisco López Bermúdez F (eds) Advances in studies on desertification. Editum, Murcia, pp 725–728

    Google Scholar 

  • Sempere A, Oliver J, Ramos C (1993) Simple determination of nitrate in soils by second-derivative spectroscopy. Eur J Soil Sci 44:633–639

    Article  CAS  Google Scholar 

  • Serrano MS, De Vita P, Carbonero MD, Fernández F, Fernández-Rebollo P, Sánchez ME (2012) Susceptibility to Phytophthora cinnamomi of the commonest morphotypes of holm oak in southern Spain. For Pathol 42:345–347

    Article  Google Scholar 

  • Shearer BL, Crane CE (2011) Habitat suitability of soils from a topographic gradient across the Fitzgerald River National Park for invasion by Phytophthora cinnamomi. Australas Plant Pathol 40:168–179

    Article  Google Scholar 

  • Singer FJ, Schoenecker KA (2003) Do ungulates accelerate or decelerate nitrogen cycling? For Ecol Manag 181:189–204

    Article  Google Scholar 

  • Solla A, García L, Pérez A, Cordero A, Cubera E, Moreno G (2009) Evaluating potassium phosphonate injections for the control of Quercus ilex decline in SW Spain: implications of low soil contamination by Phytophthora cinnamomi and low soil water content on the effectiveness of treatments. Phytoparasitica 37:303–316

    Article  CAS  Google Scholar 

  • Sparks DL (1996) Methods of soil analysis Part 3: Chemical methods. Soil Science Society of America and American Society of Agronomy, Madison

    Google Scholar 

  • Thomas FM, Büttner G (1998) Nutrient relations in healthy and damaged stands of mature oaks on clayey soils: two case studies in northwestern Germany. For Ecol Manag 108:301–319

    Article  Google Scholar 

  • Thomas FM, Hartmann G (1998) Tree rooting patterns and soil water relations of healthy and damaged stands of mature oaks (Quercus robur L. and Quercus petraea [Matt.] Liebl.). Plant Soil 203:145–158

    Article  CAS  Google Scholar 

  • Thomas FM, Blank R, Hartmann G (2002) Abiotic and biotic factors and their interactions as causes of oak decline in Central Europe. For Pathol 32:277–307

    Article  Google Scholar 

  • UNECE (2010) Manual on methods and criteria for harmonized sampling, assessment, monitoring and analysis of the effects of air pollution on forests. vTI Institute for World Forestry, Hamburg. http://www.icp-forests.org/pdf/FINAL_Crown.pdf

  • Watson GW, Kelsey P (2006) The impact of soil compaction on soil aeration and fine root density of Quercus palustris. Urban For Urban Green 4:69–74

    Article  Google Scholar 

  • Weste G, Marks GC (1987) The biology of Phytophthora cinnamomi in Australasian forests. Annu Rev Phytopathol 25:207–229

    Article  Google Scholar 

  • Wilson SD, Tilman D (1991) Interactive effects of fertilization and disturbance on community structure and resource availability in an old-field plant community. Oecologia 88:61–71

    Article  Google Scholar 

  • Zentmyer GA (1980) Phytophthora cinnamomi and the diseases it causes. Am Phytopathol Soc, St Paul, Monogr, 10

    Google Scholar 

  • Zhao Y, Peth S, Krümmelbein J, Horn R, Wang Z, Steffens M, Hoffmann C, Peng X (2007) Spatial variability of soil properties affected by grazing intensity in inner Mongolia grassland. Ecol Model 205:241–254

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to María Vivas, Andrea Pérez, Luis Miguel Rodríguez, Rubén Sepúlveda and Elisa Moreno for their valuable assistance with some of the field measurements, to Dr. Jorge Martín-García for his help with data analysis, to Dr. Thomas Jung for encouragement and technical assistance (Olores Locos team), to Dr. Luis Sampedro (CIF Lourizán, Pontevedra) for a critical review of the manuscript, and to Jane McGrath for correcting the manuscript. Useful technical advice provided by Prof. João Santos Pereira and Prof. Nuno Cortez (Instituto Superior de Agronomia, Lisboa) was made possible through Acción Integrada hispano-lusa (funded by MEC-UE). The study was funded by Junta de Extremadura (IV-PRI regional project), the European Union and Ministerio de Ciencia e Innovación (AGL2011-30438-C02-02) and was performed within the framework of COST Action “Established and Emerging Phytophthora: Increasing Threats to Woodland and Forest Ecosystems in Europe” (FP0801).

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Authors and Affiliations

  1. Grupo de Investigación Forestal, Ingeniería Forestal y del Medio Natural, Universidad de Extremadura, Avenida Virgen del Puerto 2, 10600, Plasencia, Spain

    Tamara Corcobado, Alejandro Solla & Gerardo Moreno

  2. Instituto Superior de Agronomia, Universidade Técnica de Lisboa, Tapada da Ajuda, 1349-017, Lisboa, Portugal

    Manuel A. Madeira

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  1. Tamara Corcobado
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  2. Alejandro Solla
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  3. Manuel A. Madeira
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Correspondence to Gerardo Moreno.

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Corcobado, T., Solla, A., Madeira, M.A. et al. Combined effects of soil properties and Phytophthora cinnamomi infections on Quercus ilex decline. Plant Soil 373, 403–413 (2013). https://doi.org/10.1007/s11104-013-1804-z

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  • DOI: https://doi.org/10.1007/s11104-013-1804-z

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