Skip to main content Accessibility help
×
Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-22T20:56:23.607Z Has data issue: false hasContentIssue false

Chapter Fifteen - The ecological and evolutionary trajectory of oak powdery mildew in Europe

from Part III - Understanding wildlife disease ecology at the community and landscape level

Published online by Cambridge University Press:  28 October 2019

Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
Get access

Summary

Erysiphe alphitoides causes oak powdery mildew, an example of disease in a wild perennial plant that has shown dramatic changes over a century in Europe. There are several hypotheses for this: pathogen evolution towards lower virulence, a reciprocal increase in oak population resistance, and environmental factors. We show that understanding the pathosystem requires accounting of both seasonality and the occurrence of a pathogen complex, with several cryptic fungal species differing in their life-history traits. Observational data suggest that severity of annual epidemics is linked to interannual pathogen transmission, including winter survival and the infection success of the primary inoculum in spring. Climate-driven phenological synchrony between host and pathogen in spring appears to be critical. Several cryptic Erysiphe species are associated with the disease and co-occur at multiple spatial scales. A semi-discrete model combining a SIR model in the epidemic phase and a discrete-time model between years, based on a within–between season transmission trade-off, describes seasonality and the coexistence of pathogen species. We discuss model refinement by the introduction of host population age classes and other modelling approaches for the evolution of pathogen virulence and host resistance in a changing environment.

Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
, pp. 429 - 457
Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aguayo, J., Elegbede, F., Husson, C., Saintonge, F.X. & Marçais, B. (2014) Modeling climate impact on an emerging disease, the Phytophthora alni induced alder decline. Global Change Biology, 20, 32093221.CrossRefGoogle Scholar
Alizon, S., de Roode, J. C. & Michalakis, Y. (2013) Multiple infections and the evolution of virulence. Ecology Letters, 16, 556567.Google Scholar
Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. (2009) Virulence evolution and the trade‐off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology, 22, 245259.Google Scholar
Alizon, S. & Michalakis, Y. (2015) Adaptive virulence evolution: the good old fitness-based approach. Trends in Ecology & Evolution, 30, 248254.Google Scholar
Altizer, S., Ostfeld, R.S., Johnson, P.T., Kutz, S. & Harvell, C.D. (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science, 341(6145), 514519.Google Scholar
Amarasekare, P. (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecology Letters, 6, 11091122.Google Scholar
Anderson, R.M. & May, R.M. (1982) Coevolution of hosts and parasites. Parasitology, 85, 411426.CrossRefGoogle ScholarPubMed
Armstrong, R.A. & McGhee, R. (1980) Competitive exclusion. The American Naturalist, 115, 151170.CrossRefGoogle Scholar
Baucom, R.S. & de Roode, J.C. (2011) Ecological immunology and tolerance in plants and animals. Functional Ecology, 25, 1828.CrossRefGoogle Scholar
Bearchell, S.J., Fraaije, B.A., Shaw, M.W. & Fitt, B.D. (2005) Wheat archive links long-term fungal pathogen population dynamics to air pollution. Proceedings of the National Academy of Sciences of the United States of America, 102, 54385442.Google Scholar
Berendsen, R.L., Pieterse, C.M. & Bakker, P.A. (2012) The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478486.Google Scholar
Berngruber, T.W., Froissart, R., Choisy, M. & Gandon, S. (2013) Evolution of virulence in emerging epidemics. PLoS Pathogens, 9(3), e1003209.Google Scholar
Bert, D., Lasnier, J.-B., Capdevielle, X., Dugravot, A. & Desprez-Loustau, M.L. (2016) Powdery mildew decreases the radial growth of oak trees with cumulative and delayed effects over years. PLoS ONE, 11(5), e0155344.Google Scholar
Best, A., White, A. & Boots, M. (2014) The coevolutionary implications of host tolerance. Evolution, 68, 14261435.CrossRefGoogle ScholarPubMed
Bever, J.D., Mangan, S.A. & Alexander, H.M. (2015) Maintenance of plant species diversity by pathogens. Annual Review of Ecology, Evolution, and Systematics, 46, 305325.CrossRefGoogle Scholar
Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M. & West, G.B. (2004) Toward a metabolic theory of ecology. Ecology, 85, 17711789.Google Scholar
Brown, J.K. (2003) A cost of disease resistance: paradigm or peculiarity? Trends in Genetics, 19, 667671.Google Scholar
Budde, K.B., Nielsen, L.R., Ravn, H.P. & Kjær, E.D. (2016) The natural evolutionary potential of tree populations to cope with newly introduced pests and pathogens – lessons learned from forest health catastrophes in recent decades. Current Forestry Reports, 2, 1829.Google Scholar
Bull, J.J. (1994) Perspective: virulence. Evolution, 48, 14231437.Google ScholarPubMed
Bull, J.J. & Ebert, D. (2008) Invasion thresholds and the evolution of nonequilibrium virulence. Evolutionary Applications, 1, 172182.CrossRefGoogle ScholarPubMed
Burdon, J.J., Thrall, P.H. & Ericson, L. (2013) Genes, communities & invasive species: understanding the ecological and evolutionary dynamics of host–pathogen interactions. Current Opinion in Plant Biology, 16(4), 400405.Google Scholar
Busby, P.E., Ridout, M. & Newcombe, G. (2016) Fungal endophytes: modifiers of plant disease. Plant Molecular Biology, 90, 645655.Google Scholar
Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics, 31, 343366.CrossRefGoogle Scholar
Chuine, I., de Cortazar-Atauri, I.G., Kramer, K. & Hänninen, H. (2013) Plant development models. In: Schwarz, M.D. (ed.), Phenology: An Integrative Environmental Science (pp. 275293). Dordrecht: Springer.Google Scholar
Combes, C. (2001) Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago, IL: University of Chicago Press.Google Scholar
Cronin, J.P., Rúa, M.A. & Mitchell, C.E. (2014) Why is living fast dangerous? Disentangling the roles of resistance and tolerance of disease. The American Naturalist, 184, 172187.Google Scholar
Crous, P.W. & Groenewald, J.Z. (2005) Hosts, species and genotypes: opinions versus data. Australasian Plant Pathology, 34, 463470.CrossRefGoogle Scholar
Cunniffe, N.J., Koskella, B., Metcalf, C.J.E., et al. (2015) Thirteen challenges in modelling plant diseases. Epidemics, 10, 610.CrossRefGoogle ScholarPubMed
Dantec, C.F., Ducasse, H., Capdevielle, X., et al. (2015) Escape of spring frost and disease through phenological variations in oak populations along elevation gradients. Journal of Ecology, 103, 10441056.Google Scholar
Desprez-Loustau, M.L., Feau, N., Mougou-Hamdane, A. & Dutech, C.C. (2011) Interspecific and intraspecific diversity in oak powdery mildews in Europe: coevolution history and adaptation to their hosts. Mycoscience, 52, 165173.Google Scholar
Desprez-Loustau, M.L., Robin, C., Buee, M., et al. (2007) The fungal dimension of biological invasions. Trends in Ecology & Evolution, 22, 472480.CrossRefGoogle ScholarPubMed
Desprez-Loustau, M.L., Saint-Jean, G., Barres, B., Dantec, C. & Dutech, C.C. (2014) Oak powdery mildew changes growth patterns in its host tree: host tolerance response and potential manipulation of host physiology by the parasite. Annals of Forest Science, 71, 563573.CrossRefGoogle Scholar
Desprez-Loustau, M.L., Vitasse, Y., Delzon, S., et al. (2010) Are plant pathogen populations adapted for encounter with their host? A case study of phenological synchrony between oak and an obligate fungal parasite along an altitudinal gradient. Journal of Evolutionary Biology, 23, 8797.CrossRefGoogle Scholar
Doumayrou, J., Avellan, A., Froissart, R. & Michalakis, Y. (2013) An experimental test of the transmission–virulence trade-off hypothesis in a plant virus. Evolution, 67, 477486.CrossRefGoogle Scholar
Ducousso, A., Guyon, J.P. & Kremer, A. (1996) Latitudinal and altitudinal variation of bud burst in western populations of sessile oak (Quercus petraea (Matt) Liebl). Annals of Forest Science, 53, 775782.Google Scholar
Edwards, M.C. & Ayres, P.G. (1982) Seasonal changes in resistance of Quercus petraea (sessile oak) leaves to Microsphaera alphitoides. Transactions of the British Mycological Society, 78, 569571.Google Scholar
Emmons, C.W. (1930) Cicinnobolus cesatii, a study in host–parasite relationships. Bulletin of the Torrey Botanical Club, 57, 421441.Google Scholar
Ennos, R.A. (2015) Resilience of forests to pathogens: an evolutionary ecology perspective. Forestry, 88, 4152.CrossRefGoogle Scholar
Escriu, F., Fraile, A. & García-Arenal, F. (2003) The evolution of virulence in a plant virus. Evolution, 57, 755765.Google Scholar
Feau, N., Decourcelle, T., Husson, C., Desprez Loustau, M.L. & Dutech, C.C. (2011) Finding single copy genes out of sequenced genomes for multilocus phylogenetics in non-model fungi. PLoS ONE, 6(4), e18803.Google Scholar
Feau, N., Lauron-Moreau, A., Piou, D., et al. (2012) Niche partitioning of the genetic lineages of the oak powdery mildew complex. Fungal Ecology, 5, 154162.Google Scholar
Fisher, M.C., Henk, D.A., Briggs, C.J., et al. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature, 484(7393), 186194.Google Scholar
Fitt, B.D., Huang, Y., van den Bosch, F. & West, J.S. (2006) Coexistence of related pathogen species on arable crops in space and time. Annual Review of Phytopathology, 44, 163–82.Google Scholar
Flory, S.L. & Clay, K. (2013) Pathogen accumulation and long‐term dynamics of plant invasions. Journal of Ecology, 101, 607613.CrossRefGoogle Scholar
Francl, L.J. (2001) The disease triangle: a plant pathological paradigm revisited. Plant Health Instructor, DOI:10.1094/PHI-T-2001-0517-01Google Scholar
Gilchrist, M.A., Sulsky, D.L. & Pringle, A. (2006). Identifying fitness and optimal life-history strategies for an asexual filamentous fungus. Evolution, 60, 970979.Google Scholar
Glawe, D.A. (2008) The powdery mildews: a review of the world’s most familiar (yet poorly known) plant pathogens. Annual Review of Phytopathology, 46, 2751.Google Scholar
Guillaume, F. & Rougemont, J. (2006) Nemo: an evolutionary and population genetics programming framework. Bioinformatics, 22, 25562557.CrossRefGoogle ScholarPubMed
Hajji, M., Dreyer, E. & Marçais, B. (2009) Impact of Erysiphe alphitoides on transpiration and photosynthesis in Quercus robur leaves. European Journal of Plant Pathology, 125, 6372.Google Scholar
Halkett, F., Harrington, R., Hullé, M., et al. (2004) Dynamics of production of sexual forms in aphids: theoretical and experimental evidence for adaptive ‘coin-flipping’ plasticity. The American Naturalist, 163, E112E125.CrossRefGoogle ScholarPubMed
Hamelin, F.M., Bisson, A., Desprez-Loustau, M.L., Fabre, F. & Mailleret, L. (2016) Temporal niche differentiation of parasites sharing the same plant host: oak powdery mildew as a case study. Ecosphere, 7, e01517.CrossRefGoogle Scholar
Hamelin, F.M., Castel, M., Poggi, S., Andrivon, D. & Mailleret, L. (2011) Seasonality and the evolutionary divergence of plant parasites. Ecology, 92, 21592166.Google Scholar
Huot, B., Yao, J., Montgomery, B.L. & He, S.Y. (2014) Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Molecular Plant, 7, 12671287.Google Scholar
Jakuschkin, B., Fievet, V., Schwaller, L., et al. (2016) Deciphering the pathobiome: intra- and interkingdom interactions involving the pathogen Erysiphe alphitoides. Microbial Ecology, 72, 870880.Google Scholar
Jarosz, A.M. & Davelos, A.L. (1995) Effects of disease in wild plant populations and the evolution of pathogen aggressiveness. New Phytologist, 129, 371387.Google Scholar
Jeger, M.J. (2000) Theory and plant epidemiology. Plant Pathology, 49, 651658.CrossRefGoogle Scholar
Jousimo, J., Tack, A.J., Ovaskainen, O., et al. (2014) Ecological and evolutionary effects of fragmentation on infectious disease dynamics. Science, 344(6189), 12891293.Google Scholar
Keeling, M.J. & Rohani, P. (2008) Modeling Infectious Diseases in Humans and Animals. Princeton, NJ: Princeton University Press.Google Scholar
Kerling, L.C.P. (1966) The hibernation of the oak mildew. Plant Biology, 15, 7683.Google Scholar
Kermack, W.O. & McKendrick, A.G. (1927) A contribution to the mathematical theory of epidemics. Proceedings of the Royal Society of London A, 115, 700721.Google Scholar
Kisdi, E. (2012) F1000 Prime Recommendation of Hamelin FM et al., Ecology 2011, 92(12),2159–66. F1000 Prime.Google Scholar
Kiss, L., Russell, J.C., Szentiványi, O., Xu, X. & Jeffries, P. (2004) Biology and biocontrol potential of Ampelomyces mycoparasites, natural antagonists of powdery mildew fungi. Biocontrol Science and Technology, 14, 635651.Google Scholar
Lenski, R.E. & May, R.M. (1994) The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. Journal of Theoretical Biology, 169, 253265.Google Scholar
Limkaisang, S., Cunnington, J.H, Wui, L.K., et al. (2006) Molecular phylogenetic analyses reveal a close relationship between powdery mildew fungi on some tropical trees and Erysiphe alphitoides, an oak powdery mildew. Mycoscience, 47, 327335.CrossRefGoogle Scholar
Lively, C.M., de Roode, J.C., Duffy, M.A., Graham, A.L. & Koskella, B. (2014) Interesting open questions in disease ecology and evolution. The American Naturalist, 184(S1), S1S8.CrossRefGoogle ScholarPubMed
Liyanage, A.D.S. & Royle, D.J. (1976) Overwintering of Sphaerotheca humuli, the cause of hop powdery mildew. Annals of Applied Biology, 83, 381394.CrossRefGoogle Scholar
Loreau, M. (1992) Time scale of resource dynamics and coexistence through time partitioning. Theoretical Population Biology, 41, 401412.Google Scholar
Loreau, M. & Hector, A. (2001) Partitioning selection and complementarity in biodiversity experiments. Nature, 412(6842), 7276.CrossRefGoogle ScholarPubMed
Madden, L.V., Hughes, G. & Bosch, F. (2007) The Study of Plant Disease Epidemics. St Paul, MN: American Phytopathological Society (APS Press).Google Scholar
Mailleret, L., Castel, M., Montarry, J. & Hamelin, F.M. (2012) From elaborate to compact seasonal plant epidemic models and back: is competitive exclusion in the details? Theoretical Ecology, 5, 311324.Google Scholar
Mailleret, L. & Lemesle, V. (2009) A note on semi-discrete modelling in the life sciences. Philosophical Transactions of the Royal Society of London A, 367, 47794799.Google Scholar
Marcais, B. & Desprez-Loustau, M.L. (2014) European oak powdery mildew: impact on trees, effects of environmental factors, and potential effects of climate change. Annals of Forest Science, 71, 633642.Google Scholar
Marcais, B., Kavkova, M. & Desprez-Loustau, M.L. (2009) Phenotypic variation in the phenology of ascospore production between European populations of oak powdery mildew. Annals of Forest Science, 66, 814.Google Scholar
Marçais, B., Piou, D., Dezette, D. & Desprez-Loustau, M.L. (2017) Can oak powdery mildew severity be explained by indirect effects of climate on the composition of the Erysiphe pathogenic complex? Phytopathology, 107, 570579.Google Scholar
Menzel, A. (2000). Trends in phenological phases in Europe between 1951 and 1996. International Journal of Biometeorology, 44(2), 7681.Google Scholar
Montarry, J., Cartolaro, P., Delmotte, F., Jolivet, J. & Willocquet, L. (2008) Genetic structure and aggressiveness of Erysiphe necator populations during grapevine powdery mildew epidemics. Applied and Environmental Microbiology, 74, 63276332.Google Scholar
Mordecai, E.A. (2011) Pathogen impacts on plant communities: unifying theory, concepts, and empirical work. Ecological Monographs, 81, 429441.CrossRefGoogle Scholar
Mougou, A., Dutech, C.C. & Desprez-Loustau, M.L. (2008) New insights into the identity and origin of the causal agent of oak powdery mildew in Europe. Forest Pathology, 38, 275287.CrossRefGoogle Scholar
Mougou-Hamdane, A., Giresse, X., Dutech, C.C. & Desprez Loustau, M.L. (2010) Spatial distribution of lineages of oak powdery mildew fungi in France, using quick molecular detection methods. Annals of Forest Science, 67, 212.Google Scholar
Newcombe, G. (1998) A review of exapted resistance to diseases of Populus. European Journal of Forest Pathology, 28, 209216.Google Scholar
Pasco, C., Montarry, J., Marquer, B. & Andrivon, D. (2016) And the nasty ones lose in the end: foliar pathogenicity trades off with asexual transmission in the Irish famine pathogen Phytophthora infestans. New Phytologist, 209, 334342.Google Scholar
Pautasso, M., Aas, G., Queloz, V. & Holdenrieder, O. (2013) European ash (Fraxinus excelsior) dieback – a conservation biology challenge. Biological Conservation, 158, 3749.Google Scholar
Pautasso, M., Holdenrieder, O. & Stenlid, J. (2005) Susceptibility to fungal pathogens of forests differing in tree diversity. In: Scherer-Lorenzen, M., Körner, C. & Schulze, E.-D. (eds.), Forest Diversity and Function (pp. 263289). Berlin: Springer.Google Scholar
Pearson, R.C. & Gadoury, D.M. (1987) Cleistothecia, the source of primary inoculum for grape powdery mildew in New York. Phytopathology, 77, 15091514.CrossRefGoogle Scholar
Penczykowski, R.M., Walker, E., Soubeyrand, S. & Laine, A.L. (2015) Linking winter conditions to regional disease dynamics in a wild plant–pathogen metapopulation. New Phytologist, 205, 11421152.Google Scholar
Piepenbring, M., Hofmann, T.A., Kirschner, R., et al. (2011) Diversity patterns of Neotropical plant parasitic microfungi. Ecotropica, 17, 2740.Google Scholar
Plomion, C., Aury, J.M., Amselem, J., et al. (2018) Oak genome reveals facets of long lifespan. Nature Plants, 4, 440.CrossRefGoogle ScholarPubMed
Robinson, R.A. (1976) Plant Pathosystems. Berlin: Springer.Google Scholar
Roslin, T., Laine, A.-L. & Gripenberg, S. (2007) Spatial population structure in an obligate plant pathogen colonizing oak Quercus robur. Functional Ecology, 21, 11681177.Google Scholar
Roy, B.A. & Kirchner, J.W. (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution, 54, 5163.Google ScholarPubMed
Sacristan, S. & Garcia-Arenal, F. (2008) The evolution of virulence and pathogenicity in plant pathogen populations. Molecular Plant Pathology, 9, 369384.Google Scholar
Schoch, C.L., Seifert, K.A., Huhndorf, S., et al. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America, 109, 62416246.Google Scholar
Segarra, J., Jeger, M.J. & Van den Bosch, F. (2001) Epidemic dynamics and patterns of plant diseases. Phytopathology, 91, 10011010.Google Scholar
Soularue, J.P. & Kremer, A. (2012) Assortative mating and gene flow generate clinal phenological variation in trees. BMC Evolutionary Biology, 12, 79.CrossRefGoogle ScholarPubMed
Sparks, T.H. & Carey, P.D. (1995) The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736–1947. Journal of Ecology, 83, 321.Google Scholar
Sparks, T.H., Carey, P.D. & Combes, J. (1997) First leafing dates of trees in Surrey between 1947 and 1996. The London Naturalist, 76, 1520.Google Scholar
Spotts, R.A. & Chen, P.M. (1984) Cold hardiness and temperature responses of healthy and mildew-infected terminal buds of apple during dormancy. Phytopathology, 74, 542544.Google Scholar
Stukenbrock, E.H. & McDonald, B.A. (2008) The origins of plant pathogens in agro-ecosystems. Annual Review of Phytopathology, 46, 75100.Google Scholar
Susi, H., Barrès, B., Vale, P.F. & Laine, A.L. (2015) Co-infection alters population dynamics of infectious disease. Nature Communications, 6, 5975.Google Scholar
Tack, A.J. & Laine, A.L. (2014) Ecological and evolutionary implications of spatial heterogeneity during the off‐season for a wild plant pathogen. New Phytologist, 202, 297308.CrossRefGoogle ScholarPubMed
Takamatsu, S. (2013) Origin and evolution of the powdery mildews (Ascomycota, Erysiphales). Mycoscience, 54, 7586.Google Scholar
Takamatsu, S., Braun, U., Limkaisang, S., et al. (2007) Phylogeny and taxonomy of the oak powdery mildew Erysiphe alphitoides sensu lato. Mycological Research, 111, 809826.Google Scholar
Takamatsu, S., Ito, H., Shiroya, Y., Kiss, L. & Heluta, V. (2015) First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) I. The Microsphaera lineage. Mycologia, 107, 475489.Google Scholar
Tedersoo, L., Bahram, M., Põlme, S., et al. (2014) Global diversity and geography of soil fungi. Science, 346(6213), 1256688.CrossRefGoogle ScholarPubMed
Tian, D., Traw, M.B., Chen, J. Q., Kreitman, M. & Bergelson, J. (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature, 423(6935), 7477.Google Scholar
Tollenaere, C., Susi, H. & Laine, A.-L. (2016) Evolutionary and epidemiological implications of multiple infection in plants. Trends in Plant Science, 21, 8090.Google Scholar
van den Berg, F., Bacaer, N., Metz, J.A.J., Lannou, C. & van den Bosch, F. (2011) Periodic host absence can select for both higher or lower parasite transmission rates. Evolutionary Ecology, 25, 121137.CrossRefGoogle Scholar
Verdú, M. & Climent, J. (2007) Evolutionary correlations of polycyclic shoot growth in Acer (Sapindaceae). American Journal of Botany, 94, 13161320.Google Scholar
Viennot-Bourgin, G. (1968) Note sur des Erysiphacees. Bulletin Trimestriel de la Societe Mycologique de France, 84, 117118.Google Scholar
Viney, R. (1970) L’oïdium du Chêne: incident léger ou désastre. Revue Forestière Française, 22, 365369.Google Scholar
Vitasse, Y. (2013) Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytologist, 198, 149155.Google Scholar
Vitasse, Y., François, C., Delpierre, N., et al. (2011) Assessing the effects of climate change on the phenology of European temperate trees. Agricultural and Forest Meteorology, 151, 969980.Google Scholar
Vuillemin, P. (1910a) Le déclin de la maladie du blanc du chêne. Bulletin de l’Office forestier du Centre et de l’Ouest, 347350.Google Scholar
Vuillemin, P. (1910b) Un ennemi naturel de l’Oïdium du Chêne. Bulletin de la Société Mycologique de France, 26.Google Scholar
Weis, A.E., Simms, E.L. & Hochberg, M.E. (2000) Will plant vigor and tolerance be genetically correlated? Effects of intrinsic growth rate and self-limitation on regrowth. Evolutionary Ecology, 14, 331352.CrossRefGoogle Scholar
Woodward, R.C., Waldie, J.S.L. & Steven, H.M. (1929) Oak mildew and its control in forest nurseries. Forestry, 3, 3856.Google Scholar
Zandt, P.A.V. & Mopper, S. (1998) A meta-analysis of adaptive deme formation in phytophagous insect populations. The American Naturalist, 152, 595604.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×