Fungal disease incidence along tree diversity gradients depends on latitude in European forests

Ecology and Evolution

Volumn 6, Issue 8, 2016, Pages 2426-2438

  Nguyen, Diem ^a   Castagneyrol, Bastien ^b,c   Bruelheide, Helge ^d,e   Bussotti, Filippo ^f   Guyot, Virginie ^c,g   Jactel, Hervé ^b,c   Jaroszewicz, Bogdan ^h   Valladares, Fernando ⁱ   Stenlid, Jan ^a   Boberg, Johanna ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UMR 1202 BIOGECO   (France)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^e GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

^f UNIVERSITY OF FLORENCE   (Italy)

^g UMR 1201 Dynafor   (France)

^h UNIVERSITY OF WARSAW   (Poland)

ⁱ MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Diversity gradient; Europe; Foliar fungal pathogen; Forests; FunDivEUROPE; Latitudinal gradient; Tree species richness

Indexed keywords

EID: 84960533457     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.2056     Document Type: Article

References (76)

1. Baeten, L., K. Verheyen, C. Wirth, H. Bruelheide, F. Bussotti, L. Finér, et al. 2013. A novel comparative research platform designed to determine the functional significance of tree species diversity in European forests. Perspect. Plant Ecol. Evol. Syst. 15:281-291.
2. Barbosa, P., J. Hines, I. Kaplan, H. Martinson, A. Szczepaniec, and Z. Szendrei. 2009. Associational resistance and associational susceptibility: having right or wrong neighbors. Annu. Rev. Ecol. Evol. Syst. 40:1-20.
3. Bartoń, K. 2015. MuMIn: Multi-Model Inference. R package version 1.13.4.
4. Bates, D., M. Maechler, B. Bolker, and S. Walker. 2014. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Software 67:1-48.
5. Boyd, I. L., P. H. Freer-Smith, C. A. Gilligan, and H. C. J. Godfray. 2013. The consequence of tree pests and diseases for ecosystem services. Science 342:823-830.
6. Branco, M., E. G. Brockerhoff, B. Castagneyrol, C. Orazio, and H. Jactel. 2015. Host range expansion of native insects to exotic trees increases with area of introduction and the presence of congeneric native trees. J. Appl. Ecol. 52:69-77.
7. Bremer, B., K. Bremer, M. W. Chase, M. F. Fay, J. L. Reveal, D. Soltis, et al. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161:105-121.
8. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New York, NY, USA.
9. Camarero, J. J., A. Gazol, G. Sangüesa-Barreda, J. Oliva, and S. M. Vicente-Serrano. 2015. To die or not to die: early warnings of tree dieback in response to a severe drought. J. Ecol. 103:44-57.
10. Cardinale, B. J., K. L. Matulich, D. U. Hooper, J. E. Byrnes, E. Duffy, L. Gamfeldt, et al. 2011. The functional role of producer diversity in ecosystems. Am. J. Bot. 98:572-592.
11. Cardinale, B. J., J. E. Duffy, A. Gonzalez, D. U. Hooper, C. Perrings, P. Venail, et al. 2012. Biodiversity loss and its impact on humanity. Nature 486:59-67.
12. Carnol, M., L. Baeten, E. Branquart, J.-C. Grégoire, A. Heughebaert, B. Muys, et al. 2014. Ecosystem services of mixed species forest stands and monocultures: comparing practitioners' and scientists' perceptions with formal scientific knowledge. Forestry 87:639-653.
13. Castagneyrol, B., H. Jactel, C. Vacher, E. G. Brockerhoff, and J. Koricheva. 2014. Effects of plant phylogenetic diversity on herbivory depend on herbivore specialization. J. Appl. Ecol. 51:134-141.
14. Civitello, D. J., J. Cohen, H. Fatima, N. T. Halstead, J. Liriano, T. A. McMahon, et al. 2015. Biodiversity inhibits parasites: broad evidence for the dilution effect. Proc. Natl Acad. Sci. 112:8667-8671.
15. Crisp, M. D., and L. G. Cook. 2011. Cenozoic extinctions account for the low diversity of extant gymnosperms compared with angiosperms. New Phytol. 192:997-1009.
16. Crooks, J. A. 2002. Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153-166.
17. Fedorov, N., and J. Poleschuk. 1981. Conifer root rot studies in the USSR for the years 1976-1978. Eur. J. For. Pathol. 11:44-50.
18. Fisher, M. C., D. A. Henk, C. J. Briggs, J. S. Brownstein, L. C. Madoff, S. L. McCraw, et al. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186-194.
19. Gamfeldt, L., T. Snall, R. Bagchi, M. Jonsson, L. Gustafsson, P. Kjellander, et al. 2013. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun. 4:1340.
20. Gamfeldt, L., J. S. Lefcheck, J. E. K. Byrnes, B. J. Cardinale, J. E. Duffy, and J. N. Griffin. 2015. Marine biodiversity and ecosystem functioning: what's known and what's next? Oikos 124:252-265.
21. Gerlach, J. P., P. B. Reich, K. Puettmann, and T. Baker. 1997. Species, diversity, and density affect tree seedling mortality from Armillaria root rot. Can. J. For. Res. 27:1509-1512.
22. Gilbert, G. S., and C. O. Webb. 2007. Phylogenetic signal in plant pathogen-host range. Proc. Natl Acad. Sci. 104:4979-4983.
23. Giraudoux, P. 2012. pgirmess: Data analysis in ecology. R package version 1.5.9.
24. Haas, S. E., M. B. Hooten, D. M. Rizzo, and R. K. Meentemeyer. 2011. Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecol. Lett. 14:1108-1116.
25. Haase, J., B. Castagneyrol, J. H. C. Cornelissen, J. Ghazoul, J. Kattge, J. Koricheva, et al. 2015. Contrasting effects of tree diversity on young tree growth and resistance to insect herbivores across three biodiversity experiments. Oikos. 124:1674-1685.
26. Hantsch, L., U. Braun, M. Scherer-Lorenzen, and H. Bruelheide. 2013. Species richness and species identity effects on occurrence of foliar fungal pathogens in a tree diversity experiment. Ecosphere 4:art81.
27. Hantsch, L., S. Bien, S. Radatz, U. Braun, H. Auge, and H. Bruelheide. 2014a. Tree diversity and the role of non-host neighbour tree species in reducing fungal pathogen infestation. J. Ecol. 102:1673-1687.
28. Hantsch, L., U. Braun, J. Haase, O. Purschke, M. Scherer-Lorenzen, and H. Bruelheide. 2014b. No plant functional diversity effects on foliar fungal pathogens in experimental tree communities. Fungal Divers. 66:139-151.
29. Heybroek, H. M. 1982. Monoculture versus mixture: interactions between susceptible and resistant trees in a mixed stand. Pp. 326-341 in H.M. Heybroek B.R. Stephan and K. Von Weissenberg, eds. Resistance to diseases and pests in forest trees. De Dorschkamp, Wageningen, Netherlands.
30. Holdenrieder, O., M. Pautasso, P. J. Weisberg, and D. Lonsdale. 2004. Tree diseases and landscape processes: the challenge of landscape pathology. Trends Ecol. Evol. 19:446-452.
31. Jactel, H., and E. G. Brockerhoff. 2007. Tree diversity reduces herbivory by forest insects. Ecol. Lett. 10:835-848.
32. Jactel, H., B. C. Nicoll, M. Branco, J. R. Gonzalez-Olabarria, W. Grodzki, B. Långström, et al. 2009. The influences of forest stand management on biotic and abiotic risks of damage. Ann. For. Sci. 66:701.
33. Jactel, H., J. Petit, M.-L. Desprez-Loustau, S. Delzon, D. Piou, A. Battisti, et al. 2012. Drought effects on damage by forest insects and pathogens: a meta-analysis. Glob. Change Biol. 18:267-276.
34. Johansson, M., and E. Marklund. 1980. Antagonists of Fomes annosus in the rhizosphere of grey alder (Alnus incana) and Norway spruce (Picea abies). Eur. J. For. Pathol. 10:385-395.
35. Jucker, T., O. Bouriaud, D. Avacaritei, and D. A. Coomes. 2014. Stabilizing effects of diversity on aboveground wood production in forest ecosystems: linking patterns and processes. Ecol. Lett. 17:1560-1569.
36. Jules, E. S., A. L. Carroll, A. M. Garcia, C. M. Steenbock, and M. J. Kauffman. 2014. Host heterogeneity influences the impact of a non-native disease invasion on populations of a foundation tree species. Ecosphere 5:art105.
37. Keesing, F., R. D. Holt, and R. S. Ostfeld. 2006. Effects of species diversity on disease risk. Ecol. Lett. 9:485-498.
38. Kembel, S. W., P. D. Cowan, M. R. Helmus, W. K. Cornwell, H. Morlon, D. D. Ackerly, et al. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463-1464.
39. Kim, T. N., and N. Underwood. 2015. Plant neighborhood effects on herbivory: damage is both density and frequency dependent. Ecology 96:1431-1437.
40. Koricheva, J., H. Vehvilainen, J. Riihimaki, K. Ruohomaki, P. Kaitaniemi, and H. Ranta. 2006. Diversification of tree stands as a means to manage pests and diseases in boreal forests: myth or reality? Can. J. For. Res. 36:324-336.
41. Kozlov, M. V., V. Lanta, V. Zverev, and E. L. Zvereva. 2015. Global patterns in background losses of woody plant foliage to insects. Glob. Ecol. Biogeogr. 24:1466-8238.
42. Lamit, L. J., P. E. Busby, M. K. Lau, Z. G. Compson, T. Wojtowicz, A. R. Keith, et al. 2015. Tree genotype mediates covariance among communities from microbes to lichens and arthropods. J. Ecol. 103:840-850.
43. Letten, A. D., and W. K. Cornwell. 2015. Trees, branches and (square) roots: why evolutionary relatedness is not linearly related to functional distance. Methods Ecol. Evol. 6:439-444.
44. Lindén, M., and G. Vollbrecht. 2002. Sensitivity of Picea abies to butt rot in pure stands and in mixed stands with Pinus sylvestris in southern Sweden. Silva Fenn. 36:767-778.
45. Lodge, D. J., and S. Cantrell. 1995. Fungal communities in wet tropical forests: variation in time and space. Can. J. Bot. 73:1391-1398.
46. Maloney, P. E., S. C. Lynch, S. Kane, C. E. Jensen, and D. M. Rizzo. 2005. Establishment of an emerging generalist pathogen in redwood forest communities. J. Ecol. 93:899-905.
47. Mattila, U. 2005. Probability models for pine twisting rust (Melampsora pinitorqua) damage in Scots pine (Pinus sylvestris) stands in Finland. Forest Pathol. 35:9-21.
48. McCracken, A. R., and W. M. Dawson. 2003. Rust disease (Melampsora epitea) of willow (Salix spp.) grown as short rotation coppice (SRC) in inter- and intra-species mixtures. Ann. Appl. Bio. 143:381-393.
49. Menges, E. S., and O. L. Loucks. 1984. Modeling a disease-caused patch disturbance: Oak wilt in the midwestern United States. Ecology 65:487-498.
50. Morin, X., L. Fahse, C. de Mazancourt, M. Scherer-Lorenzen, and H. Bugmann. 2014. Temporal stability in forest productivity increases with tree diversity due to asynchrony in species dynamics. Ecol. Lett. 17:1526-1535.
51. Morrison, D., M. Cruickshank, and A. Lalumière. 2014. Control of laminated and Armillaria root diseases by stump removal and tree species mixtures: amount and cause of mortality and impact on yield after 40 years. For. Ecol. Manage. 319:75-98.
52. Murray, D. 1987. Rhizosphere microorganisms from the jarrah forest of western Australia and their effects on vegetative growth and sporulation in Phytophthora cinnamomi Rands. Aust. J. Bot. 35:567-580.
53. Nakagawa, S., and H. Schielzeth. 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4:133-142.
54. Oliva, J., J. B. Boberg, A. J. Hopkins, J. Stenlid, P. Gonthier, and G. Nicolotti. 2013. Concepts of epidemiology of forest diseases. Pp. 1-28 in P. Gonthier and G. Nicolotti, eds. Infectious forest diseases. CABI, Oxfordshire, UK.
55. Parker, I. M., M. Saunders, M. Bontrager, A. P. Weitz, R. Hendricks, R. Magarey, et al. 2015. Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520:542-544.
56. Pautasso, M., O. Holdenrieder, and J. Stenlid. 2005. Susceptibility to fungal pathogens of forests differing in tree diversity. Pp. 263-289 in M. Scherer-Lorenzen, C. Körner and E.-D. Schulze, eds. Forest diversity and function: temperate and boreal systems. Springer-Verlag, Berlin Heidelberg, Germany.
57. Piri, T., K. Korhonen, and A. Sairanen. 1990. Occurrence of Heterobasidion annosum in pure and mixed spruce stands in southern Finland. Scand. J. For. Res. 5:113-125.
58. Pollastrini, M., V. Holland, W. Brüggemann, J. Koricheva, I. Jussila, M. Scherer-Lorenzen, et al. 2013. Interactions and competition processes among tree species in young experimental mixed forests, assessed with chlorophyll fluorescence and leaf morphology. Plant Biol. 16:323-331.
59. Qian, H., and R. E. Ricklefs. 2007. A latitudinal gradient in large-scale beta diversity for vascular plants in North America. Ecol. Lett. 10:737-744.
60. R Core Team 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
61. Root, R. B. 1973. Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol. Monogr. 43:95-124.
62. Santini, A., L. Ghelardini, C. De Pace, M. L. Desprez-Loustau, P. Capretti, A. Chandelier, et al. 2013. Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol. 197:238-250.
63. Schielzeth, H. 2010. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1:103-113.
64. Schielzeth, H., and S. Nakagawa. 2013. Nested by design: model fitting and interpretation in a mixed model era. Methods Ecol. Evol. 4:14-24.
65. Setiawan, N. N., M. Vanhellemont, L. Baeten, M. Dillen, and K. Verheyen. 2014. The effects of local neighbourhood diversity on pest and disease damage of trees in a young experimental forest. For. Ecol. Manage. 334:1-9.
66. Sobek, S., C. Scherber, I. Steffan-Dewenter, and T. Tscharntke. 2009. Sapling herbivory, invertebrate herbivores and predators across a natural tree diversity gradient in Germany's largest connected deciduous forest. Oecologia 160:279-288.
67. Stenlid, J., J. Oliva, J. B. Boberg, and A. J. M. Hopkins. 2011. Emerging Diseases in European Forest Ecosystems and Responses in Society. Forests 2:486-504.
68. Thor, M., G. Ståhl, and J. Stenlid. 2005. Modelling root rot incidence in Sweden using tree, site and stand variables. Scand. J. For. Res. 20:165-176.
69. Tilman, D. 1999. The ecological consequences of changes in biodiversity: a search for general principles 101. Ecology 80:1455-1474.
70. Vacher, C., D. Vile, E. Helion, D. Piou, and M.-L. Desprez-Loustau. 2008. Distribution of parasitic fungal species richness: influence of climate versus host species diversity. Divers. Distrib. 14:786-798.
71. Valkama, E., J. Koricheva, J.-P. Salminen, M. Helander, I. Saloniemi, K. Saikkonen, et al. 2005. Leaf surface traits: overlooked determinants of birch resistance to herbivores and foliar micro-fungi? Trees 19:191-197.
72. Webb, C. O., D. D. Ackerly, and S. W. Kembel. 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098-2100.
73. Wikstrom, N., V. Savolainen, and M. W. Chase. 2001. Evolution of the angiosperms: calibrating the family tree. Proc. R. Soc. B Biol. Sci. 268:2211-2220.
74. Yachi, S., and M. Loreau. 1999. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl Acad. Sci. 96:1463-1468.
75. Zeglen, S. 2002. Whitebark pine and white pine blister rust in British Columbia, Canada. Can. J. For. Res. 32:1265-1274.
76. Zuur, A., E. N. Ieno, N. Walker, A. A. Saveliev, and G. M. Smith. 2009. Mixed effects models and extensions in ecology with R. Springer, New York, NY, USA.