Biological Invasions

, Volume 20, Issue 6, pp 1459–1473 | Cite as

Plant neighbour identity and invasive pathogen infection affect associational resistance to an invasive gall wasp

  • Pilar Fernandez-ConradiEmail author
  • Nicolas Borowiec
  • Xavier Capdevielle
  • Bastien Castagneyrol
  • Alberto Maltoni
  • Cécile Robin
  • Federico Selvi
  • Inge Van Halder
  • Fabrice Vétillard
  • Hervé Jactel
Original Paper


Theory predicts that mixed forests are more resistant to native pests than pure forests (i.e. associational resistance) because of reduced host accessibility and increased top-down control by natural enemies. Yet, whether the same mechanisms also apply to invasive pests remains to be verified. We tested the hypothesis of associational resistance against the invasive Asian chestnut gall wasp (ACGW, Dryocosmus kuriphilus) by comparing ACGW infestation rates on chestnuts (Castanea sativa) in stands varying in species composition (chestnut alone or associated with oaks, pines or ashes). We investigated the effects of reduced chestnut density and frequency in mixed stands, as well as the effect of biotic interactions between ACGW, its parasitoids and the chestnut blight disease (caused by Cryphonectria parasitica). ACGW infestation rates were significantly lower in chestnut–oak and chestnut–ash mixtures than in pure chestnut stands and chestnut–pine mixtures. Infestation rate decreased with decreasing chestnut relative proportion. The composition of native parasitoid communities emerged from galls significantly differed between pure and mixed chestnut stands, but not the species richness or abundance of parasitoids. The abundance of the introduced parasitoid Torymus sinensis was not correlated with ACGW infestation rates and was independent of stand composition. Blight symptoms modified ACGW infestation rates with taller trees being preferred when they were asymptomatic but avoided when they presented blight disease damage. Our results suggest that conservation biological control based on tree species mixtures could contribute to reducing the damage of invasive forest pests.


Biodiversity Associational resistance Invasive pest Dryocosmus kuriphilus Cryphonectria parasitica Natural enemies 



We thank Dr. John Parker and two anonymous reviewers for constructive comments on an earlier version of the manuscript. We thank Marcel Thaon and Benoit Cailleret (INRA, ISA) for assistance with parasitoid identification. Pilar Fernandez-Conradi was supported by a grant from INRA (Department of Forest, Grassland and Freshwater Ecology) and the French Ministry of Agriculture and Forestry.

Supplementary material

10530_2017_1637_MOESM1_ESM.docx (554 kb)
Supplementary material 1 (DOCX 554 kb)


  1. Aebi A, Schönrogge K, Melika G et al (2006) Parasitoid recruitment to the globally invasive chestnut gall wasp Dryocosmus kuriphilus. In: Ozaki K, Yukawa J, Ohgushi T, Price PW (eds) Galling arthropods and their associates. Springer, Berlin, pp 103–121CrossRefGoogle Scholar
  2. Aebi A, Schönrogge K, Melika G et al (2007) Native and introduced parasitoids attacking the invasive chestnut gall wasp Dryocosmus kuriphilus. EPPO Bull 37:166–171CrossRefGoogle Scholar
  3. Al Khatib F, Fusu L, Cruaud A et al (2014) An integrative approach to species discrimination in the Eupelmus urozonus complex (Hymenoptera, Eupelmidae), with the description of 11 new species from the Western Palaearctic. Syst Entomol 39:806–862CrossRefGoogle Scholar
  4. Al Khatib F, Fusu L, Cruaud A et al (2015) Availability of eleven species names of Eupelmus (Hymenoptera, Eupelmidae) proposed in Al khatib et al. (2014). ZooKeys 505:137–145. CrossRefGoogle Scholar
  5. Al Khatib F, Cruaud A, Fusu L et al (2016) Multilocus phylogeny and ecological differentiation of the “Eupelmus urozonus species group” (Hymenoptera, Eupelmidae) in the West-Palaearctic. BMC Evol Biol 16:13. PubMedPubMedCentralCrossRefGoogle Scholar
  6. Anderson MJ (2005) Permutational multivariate analysis of variance. Department of Statistics, University of Auckland, Auckland, vol 26, pp 32–46Google Scholar
  7. Askew RR, Melika G, Pujade-Villar J et al (2013) Catalogue of parasitoids and inquilines in cynipid oak galls in the West Palaearctic. Zootaxa 3643:1. PubMedCrossRefGoogle Scholar
  8. Baeten L, Verheyen K, Wirth C et al (2013) A novel comparative research platform designed to determine the functional significance of tree species diversity in European forests. Perspect Plant Ecol Evolut Syst 15:281–291. CrossRefGoogle Scholar
  9. Balvanera P, Pfisterer AB, Buchmann N et al (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156. PubMedCrossRefGoogle Scholar
  10. Barbosa P (1998) Conservation biological control. Academic AP Press, New YorkGoogle Scholar
  11. Barbosa P, Hines J, Kaplan I et al (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20. CrossRefGoogle Scholar
  12. Bates D, Martin M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 1:1–48Google Scholar
  13. Battisti A, Benvegnù I, Colombari F, Haack RA (2014) Invasion by the chestnut gall wasp in Italy causes significant yield loss in Castanea sativa nut production: chestnut gall wasp and impact on nut yield. Agric For Entomol 16:75–79. CrossRefGoogle Scholar
  14. Bernardo U, Iodice L, Sasso R et al (2013) Biology and monitoring of Dryocosmus kuriphilus on Castanea sativa in Southern Italy. Agric For Entomol 15:65–76. CrossRefGoogle Scholar
  15. Borowiec N, Thaon M, Brancaccio L et al (2014) Classical biological control against the chestnut gall wasp‘Dryocosmus kuriphilus’(Hymenoptera, Cynipidae) in France. Plant Prot Q 29:7Google Scholar
  16. Cabrera-Guzmán E, Crossland MR, Shine R (2012) Predation on the eggs and larvae of invasive cane toads (Rhinella marina) by native aquatic invertebrates in tropical Australia. Biol Conserv 153:1–9. CrossRefGoogle Scholar
  17. Cappuccino N, Lavertu D, Bergeron Y, Régnière J (1998) Spruce budworm impact, abundance and parasitism rate in a patchy landscape. Oecologia 114:236–242. PubMedCrossRefGoogle Scholar
  18. Cardoza YJ, Alborn HT, Tumlinson JH (2002) In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J Chem Ecol 28:161–174PubMedCrossRefGoogle Scholar
  19. Cardoza YJ, Lait CG, Schmelz EA et al (2003) Fungus-induced biochemical changes in peanut plants and their effect on development of beet armyworm, Spodoptera exigua Hübner (Lepidoptera: Noctuidae) larvae. Environ Entomol 32:220–228CrossRefGoogle Scholar
  20. Carmignani L, Lazzarotto A (2004). Geological map of Tuscany. Regione Toscana and University of SienaGoogle Scholar
  21. Case T (1990) Invasion resistance arises in strongly interacting species-rich model competition communities. Proc Natl Acad Sci U S A 87:9610–9614. PubMedPubMedCentralCrossRefGoogle Scholar
  22. Castagneyrol B, Jactel H (2012) Unraveling plant–animal diversity relationships: a meta-regression analysis. Ecology 93:2115–2124PubMedCrossRefGoogle Scholar
  23. Castagneyrol B, Giffard B, Péré C, Jactel H (2013) Plant apparency, an overlooked driver of associational resistance to insect herbivory. J Ecol 101:418–429. CrossRefGoogle Scholar
  24. Castagneyrol B, Jactel H, Vacher C et al (2014a) Effects of plant phylogenetic diversity on herbivory depend on herbivore specialization. J Appl Ecol 51:134–141. CrossRefGoogle Scholar
  25. Castagneyrol B, Regolini M, Jactel H (2014b) Tree species composition rather than diversity triggers associational resistance to the pine processionary moth. Basic Appl Ecol 15:516–523. CrossRefGoogle Scholar
  26. Clavero M, Garciaberthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110. PubMedCrossRefGoogle Scholar
  27. Conedera M, Tinner W, Krebs P, et al (2016) Castanea sativa in Europe: distribution, habitat, usage and threats. In: San-Miguel-Ayanz J, de Rigo D, Caudillo G, Houston Durrant T, Maurl A (eds) European atlas of forest tree speciesGoogle Scholar
  28. Cooper WR, Rieske LK (2007) Community associates of an exotic gallmaker, Dryocosmus kuriphilus (Hymenoptera: Cynipidae), in Eastern North America. Ann Entomol Soc Am 100:236–244.[236:CAOAEG]2.0.CO;2CrossRefGoogle Scholar
  29. Cooper WR, Rieske LK (2010) Gall structure affects ecological associations of Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Environ Entomol 39:787–797. PubMedCrossRefGoogle Scholar
  30. Cox JG, Lima SL (2006) Naiveté and an aquatic–terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680. PubMedCrossRefGoogle Scholar
  31. Csoka G, Stone GN, Melika G (2005) Biology, ecology and evolution of gall-inducing Cynipidae. In: Raman A, Schaefer CW, Withers T (eds) Biology, ecology, and evolution of gall-inducing arthropods. Science Publisher Inc, Enfield, pp 573–642Google Scholar
  32. Damien M, Jactel H, Meredieu C et al (2016) Pest damage in mixed forests: disentangling the effects of neighbor identity, host density and host apparency at different spatial scales. For Ecol Manag 378:103–110. CrossRefGoogle Scholar
  33. Dormann CF, Elith J, Bacher S et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46. CrossRefGoogle Scholar
  34. Dulaurent A-M, Porté AJ, van Halder I et al (2012) Hide and seek in forests: colonization by the pine processionary moth is impeded by the presence of nonhost trees. Agric For Entomol 14:19–27. CrossRefGoogle Scholar
  35. Eilenberg J, Hajek A, Lomer C (2001) Suggestions for unifying the terminology in biological control. Biocontrol 46:387–400. CrossRefGoogle Scholar
  36. Elton CS (1958) The ecology of invasions by animals and plants. Accessed 20 Mar 2017
  37. Erneberg M (1999) Effects of herbivory and competition on an introduced plant in decline. Oecologia 118:203–209. PubMedCrossRefGoogle Scholar
  38. Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia 90:14–20. PubMedCrossRefGoogle Scholar
  39. Ferracini C, Ferrari E, Saladini MA et al (2015) Non-target host risk assessment for the parasitoid Torymus sinensis. Biocontrol 60:583–594. CrossRefGoogle Scholar
  40. Francati S, Alma A, Ferracini C et al (2015) Indigenous parasitoids associated with Dryocosmus kuriphilus in a chestnut production area of Emilia Romagna (Italy). Bull Insectol 68:127–134Google Scholar
  41. Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar Pollut Bull 55:314–322. PubMedCrossRefGoogle Scholar
  42. Gamfeldt L, Snäll T, Bagchi R et al (2013) Higher levels of multiple ecosystem services are found in forests with more tree species. Nat Commun 4:1340. PubMedPubMedCentralCrossRefGoogle Scholar
  43. Germinara GS, De Cristofaro A, Rotundo G (2011) Chemical cues for host location by the chestnut gall wasp, Dryocosmus kuriphilus. J Chem Ecol 37:49–56. PubMedCrossRefGoogle Scholar
  44. Goméz JF, Nieves MH, Gayubo SF, Nieves-Aldrey JL (2017) Terminal-instar larval systematics and biology of west European species of Ormyridae associated with insect galls (Hymenoptera, Chalcidoidea). ZooKeys 644:51–88. CrossRefGoogle Scholar
  45. Guyot V, Castagneyrol B, Vialatte A et al (2015) Tree diversity limits the impact of an invasive forest pest. PLoS ONE 10:e0136469. PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hambäck PA, Beckerman AP (2003) Herbivory and plant resource competition: a review of two interacting interactions. Oikos 101:26–37. CrossRefGoogle Scholar
  47. Hambäck PA, Inouye BD, Andersson P, Underwood N (2014) Effects of plant neighborhoods on plant–herbivore interactions: resource dilution and associational effects. Ecology 95:1370–1383PubMedCrossRefGoogle Scholar
  48. Hatcher PE, Paul ND, Ayres PG, Whittaker JB (1994) The effect of a foliar disease (rust) on the development of Gastrophysa viridula (Coleoptera: Chrysomelidae). Ecol Entomol 19:349–360. CrossRefGoogle Scholar
  49. Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848. PubMedCrossRefGoogle Scholar
  50. Jactel H, Menassieu P, Vetillard F et al (2006) Tree species diversity reduces the invasibility of maritime pine stands by the bast scale, Matsucoccus feytaudi (Homoptera: Margarodidae). Can J For Res 36:314–323CrossRefGoogle Scholar
  51. Jactel H, Birgersson G, Andersson S, Schlyter F (2011) Non-host volatiles mediate associational resistance to the pine processionary moth. Oecologia 166:703–711. PubMedCrossRefGoogle Scholar
  52. Jactel H, Bauhus J, Boberg J et al (2017) Tree Diversity Drives Forest Stand Resistance to Natural Disturbances. Curr For Rep 3:223–243Google Scholar
  53. Jones TS, Bilton AR, Mak L et al (2015) Host switching in a generalist parasitoid: contrasting transient and transgenerational costs associated with novel and original host species. Ecol Evol 5(2):459–465PubMedPubMedCentralCrossRefGoogle Scholar
  54. Jost L (2006) Entropy and diversity. Oikos 113(2):363–375CrossRefGoogle Scholar
  55. Kaartinen R, Stone GN, Hearn J et al (2010) Revealing secret liaisons: DNA barcoding changes our understanding of food webs. Ecol Entomol 35:623–638. CrossRefGoogle Scholar
  56. Kambach S, Kühn I, Castagneyrol B, Bruelheide H (2016) The impact of tree diversity on different aspects of insect herbivory along a global temperature gradient-a meta-analysis. PLoS ONE 11:e0165815PubMedPubMedCentralCrossRefGoogle Scholar
  57. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. CrossRefGoogle Scholar
  58. Kennedy TA, Naeem S, Howe KM et al (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638. PubMedCrossRefGoogle Scholar
  59. Knoll V, Ellenbroek T, Romeis J et al (2017) Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland and their ability to parasitize the invasive Drosophila suzukii. Sci Rep 7:40697PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lazzarotto A (1993) Elementi di geologia e geomorfologia. In: Giusti F (ed) La storia naturale della Toscana meridionale. Silvana Editoriale, Siena, pp 19–87Google Scholar
  61. Leles B, Xiao X, Pasion BO et al (2017) Does plant diversity increase top-down control of herbivorous insects in tropical forest? Oikos 000:001–008. CrossRefGoogle Scholar
  62. Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40:573–592. CrossRefGoogle Scholar
  63. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. CrossRefGoogle Scholar
  64. Li Y, Ke Z, Wang S et al (2011) An exotic species is the favorite prey of a native enemy. PLoS ONE 6:e24299PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lotfalizadeh H, Askew RR, Fuentes-Utrilla P, Tavakoli M (2012) The species of Ormyrus Westwood (Hymenoptera: Ormyridae) in Iran with description of an unusual new species. Zootaxa 3300:34–44Google Scholar
  66. Maltoni A, Mariotti B, Tani A (2012) Case study of a new method for the classification and analysis of Dryocosmus kuriphilus Yasumatsu damage to young chestnut sprouts. IFor Biogeosci For 5:50–59. CrossRefGoogle Scholar
  67. Matošević D, Quacchia A, Kriston É, Melika G (2014) Biological control of the invasive Dryocosmus kuriphilus (Hymenoptera: Cynipidae)—an overview and the first trials in Croatia. South-East Eur For. CrossRefGoogle Scholar
  68. McManus PS, Ewers FW (1990) The effect of Cryphonectria parasitica on water relations of American chestnut. Physiol Mol Plant Pathol 36:461–470CrossRefGoogle Scholar
  69. Meijer K, Schilthuizen M, Beukeboom L, Smit C (2016) A review and meta-analysis of the enemy release hypothesis in plant–herbivorous insect systems. Peerj 4:e2778. PubMedPubMedCentralCrossRefGoogle Scholar
  70. Meyer JB, Gallien L, Prospero S (2015) Interaction between two invasive organisms on the European chestnut: does the chestnut blight fungus benefit from the presence of the gall wasp? FEMS Microbiol Ecol 91:fiv122. PubMedCrossRefGoogle Scholar
  71. Moriya S, Shiga M, Adachi I (2003) Classical biological control of the chestnut gall wasp in Japan. In: Proceedings of the 1st international symposium on biological control of arthropods. USDA Forest Service, Washington, pp 407–415Google Scholar
  72. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. CrossRefGoogle Scholar
  73. Nunez-Mir GC, Liebhold AM, Guo Q et al (2017) Biotic resistance to exotic invasions: its role in forest ecosystems, confounding artifacts, and future directions. Biol Invasions. CrossRefGoogle Scholar
  74. Oksanen J, Blanchet G, Friendly M, et al (2017) Vegan: community ecology package. R package version 2.4-2. Accessed 20 Mar 2017
  75. Palmeri V, Cascone P, Campolo O et al (2014) Hymenoptera wasps associated with the Asian gall wasp of chestnut (Dryocosmus kuriphilus) in Calabria, Italy. Phytoparasitica 42:699–702. CrossRefGoogle Scholar
  76. Panzavolta T, Bernardo U, Bracalini M et al (2013) Native parasitoids associated with Dryocosmus kuriphilus in Tuscany, Italy. Bull Insectol 66:195–201Google Scholar
  77. Quacchia A, Moriya S, Bosio G et al (2008) Rearing, release and settlement prospect in Italy of Torymus sinensis, the biological control agent of the chestnut gall wasp Dryocosmus kuriphilus. Biocontrol 53:829–839. CrossRefGoogle Scholar
  78. Quacchia A, Moriya S, Askew R, Schönrogge K (2014a) Torymus sinensis: biology, host range and Hybridization. Acta Hortic. CrossRefGoogle Scholar
  79. Quacchia A, Moriya S, Bosio G (2014b) Effectiveness of Torymus sinensis in the biological control of Dryocosmus kurophilus in Italy. Acta Hort 1043:199–204CrossRefGoogle Scholar
  80. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  81. Randlkofer B, Obermaier E, Hilker M, Meiners T (2010) Vegetation complexity—The influence of plant species diversity and plant structures on plant chemical complexity and arthropods. Basic Appl Ecol 11:383–395CrossRefGoogle Scholar
  82. Rigling D, Prospero S (2017) Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Mol Plant Pathol. PubMedCrossRefGoogle Scholar
  83. Rigot T, van Halder I, Jactel H (2014) Landscape diversity slows the spread of an invasive forest pest species. Ecography 37:648–658. CrossRefGoogle Scholar
  84. Riihimäki J, Kaitaniemi P, Koricheva J, Vehviläinen H (2005) Testing the enemies hypothesis in forest stands: the important role of tree species composition. Oecologia 142:90–97. PubMedCrossRefGoogle Scholar
  85. Rizvi SZM, Raman A, Wheatley W et al (2015) Influence of Botrytis cinerea (Helotiales: Sclerotiniaceae) infected leaves of Vitis vinifera (Vitales: Vitaceae) on the preference of Epiphyas postvittana (Lepidoptera: Tortricidae): Effect of B. cinerea infection on E. postvittana. Austral Entomol 54:60–70. CrossRefGoogle Scholar
  86. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124CrossRefGoogle Scholar
  87. Schielzeth H, Nakagawa S (2013) Nested by design: model fitting and interpretation in a mixed model era. Methods Ecol Evol 4:14–24. CrossRefGoogle Scholar
  88. Schuldt A, Both S, Bruelheide H et al (2011) Predator diversity and abundance provide little support for the enemies hypothesis in forests of high tree diversity. PLoS ONE 6:e22905. PubMedPubMedCentralCrossRefGoogle Scholar
  89. Schuldt A, Bruelheide H, Härdtle W et al (2015) Early positive effects of tree species richness on herbivory in a large-scale forest biodiversity experiment influence tree growth. J Ecol 103:563–571. PubMedPubMedCentralCrossRefGoogle Scholar
  90. Schuldt A, Hönig L, Li Y et al (2017) Herbivore and pathogen effects on tree growth are additive, but mediated by tree diversity and plant traits. Ecol Evol 7(18):7462–7474PubMedPubMedCentralCrossRefGoogle Scholar
  91. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176. CrossRefGoogle Scholar
  92. Sih A, Bolnick DI, Luttbeg B et al (2010) Predator-prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621. CrossRefGoogle Scholar
  93. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9(8):912–919PubMedCrossRefGoogle Scholar
  94. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1(1):21–32CrossRefGoogle Scholar
  95. Stone GN, Schönrogge K, Atkinson RJ et al (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668PubMedCrossRefGoogle Scholar
  96. Strauss SY, Cacho NI, Schwartz MW et al (2015) Apparency revisited. Entomol Exp Appl 157:74–85. CrossRefGoogle Scholar
  97. Tack AJM, Dicke M (2013) Plant pathogens structure arthropod communities across multiple spatial and temporal scales. Funct Ecol 27:633–645. CrossRefGoogle Scholar
  98. Tack AJM, Gripenberg S, Roslin T (2012) Cross-kingdom interactions matter: fungal-mediated interactions structure an insect community on oak: fungus–plant–insect interactions. Ecol Lett 15:177–185. PubMedCrossRefGoogle Scholar
  99. Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10:321–346. PubMedCrossRefGoogle Scholar
  100. Tosi L, Beccari G, Rondoni G et al (2015) Natural occurrence of Fusarium proliferatum on chestnut in Italy and its potential entomopathogenicity against the Asian chestnut gall wasp Dryocosmus kuriphilus. J Pest Sci 88:369–381. CrossRefGoogle Scholar
  101. Vannini A, Vettraino A, Martignoni D et al (2017) Does Gnomoniopsis castanea contribute to the natural biological control of chestnut gall wasp? Fungal Biol 121:44–52. PubMedCrossRefGoogle Scholar
  102. White JA, Whitham TG (2000) Associational susceptibility of cottonwood to a box elder herbivore. Ecology 81:1795–1803CrossRefGoogle Scholar
  103. Wilby A, Thomas MB (2002) Are the ecological concepts of assembly and function of biodiversity useful frameworks for understanding natural pest control? Agric For Entomol 4:237–243. CrossRefGoogle Scholar
  104. Wilcox RC, Fletcher RJ (2016) Experimental test of preferences for an invasive prey by an endangered predator: implications for conservation. PLoS ONE 11:e0165427. PubMedPubMedCentralCrossRefGoogle Scholar
  105. Wilsey BJ, Polley HW (2002) Reductions in grassland species evenness increase dicot seedling invasion and spittle bug infestation. Ecol Lett 5:676–684. CrossRefGoogle Scholar
  106. Zhang QH, Schlyter F (2004) Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer-inhabiting bark beetles. Agric For Entomol 6:1–19. CrossRefGoogle Scholar
  107. Zhang Z-Y, Tarcali G, Radocz L et al (2009) Chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu in China and in Hungary. J Agric Sci 38:123–128Google Scholar
  108. Zuur AF, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Pilar Fernandez-Conradi
    • 1
    Email author
  • Nicolas Borowiec
    • 2
  • Xavier Capdevielle
    • 1
  • Bastien Castagneyrol
    • 1
  • Alberto Maltoni
    • 3
  • Cécile Robin
    • 1
  • Federico Selvi
    • 4
  • Inge Van Halder
    • 1
  • Fabrice Vétillard
    • 1
  • Hervé Jactel
    • 1
  1. 1.Biogeco, INRAUniv. BordeauxCestasFrance
  2. 2.INRA, Equipe Recherche et Développement en Lutte Biologique, UMR 1355, INRA, CNRSUniversité Nice Côte d’Azur « Institut Sophia Agrobiotech »Sophia AntipolisFrance
  3. 3.GESAAF, Sez. Foresta Ambiente Legno PaesaggioUniversità di FirenzeFlorenceItaly
  4. 4.DISPAA, Laboratori di BotanicaUniversità di FirenzeFlorenceItaly

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