Abstract
The success of invasive species largely depends on the resistance offered by the native communities. Dryocosmus kuriphilus is a cynipid native from China that is a serious pest of chestnuts worldwide. This species recruits natural enemies in the areas of introduction; nevertheless, their role in regulating pest population is frequently questioned, although the causes are not clear. We sampled parasitoids from 12,525 galls collected in 192 sites in four geographic areas differing in climate and residence time of the wasp of Galicia (NW Iberian Peninsula). We also dissected 2994 galls to assess the effects of gall characteristics on parasitism level. We found a rich community of native enemies that contributed to biotic resistance against the invasive: 19 species of native parasitoids were feeding on the wasp, with mortalities ranging from 14 to 37%. Rarefaction analyses indicated that this species list accounts for most of the native enemies that attack D. kuriphilus in inland Galicia. However, percent parasitism of D. kuriphilus by native parasitoids decreased greatly with time since introduction. This was because galls became larger, more thickly walled, and with more D. kuriphilus per gall as the abundance of D. kuriphilus increased. As the galls became larger and more populated, a declining fraction of the D. kuriphilus within were parasitized by native enemies (decrease from > 25% parasitism to < 2% as gall size increased from 0.2 to 3 cm3). Consequently, native parasitoids may play a role in slowing the invasive at low densities, but this effect becomes increasing inconsequential in highly invaded areas.
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References
Abrahamson WG, Weis AE (1997) Evolutionary ecology across three trophic levels: goldenrods, gallmakers and natural enemies. Princeton Monographs in Population Biology No. 29. Princeton Univ. Press, Princeton
Askew RR (1975) The organisation of chalcid-dominated parasitoid communities centred upon endophytic hosts. In: Price P (ed) Evolutionary strategies of parasitic insects and mites. Springer, Boston, pp 130–153
Askew RR, Shaw MR (1986) Parasitoid communities: their size, structure and development, In: Waage J, Greathead D (eds) Insect parasitoids, 13th symposium of royal entomological society of London. Academic Press, London, Elsevier, pp 225–264
Avtzis DN, Matošević D (2013) Taking Europe by storm: a first insight in the introduction and expansion of Dryocosmus kuriphilus in central Europe by mtDNA. J For Soc Croatia 137:387–394
Avtzis DN, Melika G, Matošević D, Coyle DR (2019) The Asian chestnut gall wasp Dryocosmus kuriphilus: a global invader and a successful case of classical biological control. J Pest Sci 92:107–115. https://doi.org/10.1007/s10340-018-1046-1
Bailey R, Schonrogge K, Cook JM, Melika G, Csoka G, Thuroczy C, Stone GN (2009) Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biol 7:e1000179. https://doi.org/10.1371/journal.pbio.1000179
Barbosa P (1988) Natural enemies and herbivore–plant interactions: influence of plant allelochemicals and host specificity. In: Barbosa P, Letourneau DK (eds) Novel aspects of plant interactions. Wiley Interscience Publication, New York, pp 201–229
Battisti A, Benvegnu I, Colombari F, Haack RA (2014) Invasion by the chestnut gall wasp in Italy causes significant yield loss in Castanea sativa nut production. Agric For Entomol 16:75–79. https://doi.org/10.1111/afe.12036
Berryman AA (1999) The theoretical foundations of biological control. In: Hawkins BA, Cornell HV (eds) Theoretical approaches to biological control. Cambridge University Press, Cambridge, pp 3–21
Bonal R, Vargas-Osuna E, Mena JD, Aparicio JM, Santoro M, Martín A (2018) Looking for variable molecular markers in the chestnut gall wasp Dryocosmus kuriphilus: first comparison across genes. Sci Rep 8:5631. https://doi.org/10.1038/s41598-018-23754-z
Bonello P, Campbell FT, Cipollini D, Conrad AO, Farinas C, Gandhi KJK, Hain FP, Parry D, Showalter DN, Villari C, Wallin KF (2020) Invasive tree pests devastate ecosystems—a proposed new response framework. Front For Glob Change 3:2. https://doi.org/10.3389/ffgc.2020.00002
Bonsignore CP, Bernardo U (2018) Effects of environmental parameters on the chestnut gall wasp and its complex of indigenous parasitoids. Sci Nat 105:20. https://doi.org/10.1007/s00114-018-1545-1
Borges RM (2018) The galling truth: limited knowledge of gall-associated volatiles in multitrophic interactions. Front Plant Sci 9:1139. https://doi.org/10.3389/fpls.2018.01139
Briggs CJ, Latto J (1996) The window of vulnerability and its effect on relative parasitoid abundance. Ecol Entomol 21:128–140. https://doi.org/10.1111/j.1365-2311.1996.tb01179.x
Brockerhoff EG, Liebhold AM, Richardson B, Suckling DM (2010) Eradication of invasive forest insects: concepts, methods, costs and benefits. New Zeal J For Sci 40(suppl):S117–S135
Carlsson NOL, Bustamante H, Strayer DL, Pace ML (2011) Biotic resistance on the increase: native predators structure invasive zebra mussel populations. Freshw Biol 56:1630–1637. https://doi.org/10.1111/j.1365-2427.2011.02602.x
Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733. https://doi.org/10.1111/j.1461-0248.2004.00616.x
Colwell RK (2013) EstimateS, version 9.1: statistical estimation of species richness and shared species from samples. http://viceroy.eeb.uconn.edu/estimates. Accessed 20 Feb 2020
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. https://doi.org/10.1603/0013-8746(2007)100%5b236:CAOAEG%5d2.0.CO;2
Cooper WR, Rieske LK (2010) Gall structure affects ecological associations of Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Environ Entomol 39:787–797. https://doi.org/10.1603/EN09382
Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera)—why and how. Am Midl Nat 110:225–234. https://doi.org/10.2307/2425263
Cornell HV, Hawkins BA (1993) Accumulation of native parasitoid species on introduced herbivores—a comparison of hosts as natives and hosts as invaders. Am Nat 141:847–865. https://doi.org/10.1086/285512
Craig TP, Itami JK, Price PW (1990) The window of vulnerability of a shoot-galling sawfly to attack by a parasitoid. Ecology 71:1471–1482. https://doi.org/10.2307/1938284
Dearborn KW, Heard SB, Sweeney J, Pureswaran DS (2016) Displacement of Tetropium cinnamopterum (Coleoptera: Cerambycidae) by its invasive congener Tetropium fuscum. Environ Entomol 45:848–854. https://doi.org/10.1093/ee/nvw045
Dlugosch KM, Cang FA, Barker BS, Andonian K, Swope SM, Rieseberg LH (2015) Evolution of invasiveness through increased resource use in a vacant niche. Nat Plants 1:15066. https://doi.org/10.1038/nplants.2015.66
EFSA Panel on Plant Health (2010) Risk assessment of the oriental chestnut gall wasp, Dryocosmus kuriphilus for the EU territory and identification and evaluation of risk management options. EFSA J 8(6):1619
Elton CS (1958) The ecology of invasions by animals and plants. Kluwer Academic Publishers, Chicago
EPPO (2005) Data sheets on quarantine pests. Dryocosmus kuriphilus. EPPO Bull 35:422–424
Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135. https://doi.org/10.1016/j.tree.2005.10.012
Fernandez-Conradi P, Borowiec N, Capdevielle X, Castagneyrol B, Maltoni A, Robin C, Selvi F, Van Halder I, Vetillard F, Jactel H (2018) Plant neighbour identity and invasive pathogen infection affect associational resistance to an invasive gall wasp. Biol Invasions 20:1459–1473. https://doi.org/10.1007/s10530-017-1637-4
Ferracini Ch, Ferrari E, Pontini M, Hernández Nova LK, Saladini MA, Alma A (2017) Post-release evaluation of non-target effects of Torymus sinensis, the biological control agent of Dryocosmus kuriphilus in Italy. Biocontrol 62:445–456. https://doi.org/10.1007/s10526-017-9803-2
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315. https://doi.org/10.1002/joc.5086
Francati S, Alma A, Ferracini Ch, Pollini A, Dindo ML (2015) Indigenous parasitoids associated with Dryocosmus kuriphilus in a chestnut production area of Emilia Romagna (Italy). Bull Insectol 68(1):127–134
Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, Von Holle B (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17. https://doi.org/10.1890/0012-9658(2007)88%5b3:TIPRPA%5d2.0.CO;2
Garnas JR, Auger-Rozenberg M, Roques A, Bertelsmeier C, Wingfield MJ, Saccaggi DL, Roy HE, Slippers B (2016) Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences. Biol Invasions 18:935–952. https://doi.org/10.1007/s10530-016-1082-9
Gehring E, Bellosi B, Quacchia A, Conedera M (2018) Assessing the impact of Dryocosmus kuriphilus on the chestnut tree: branch architecture matters. J Pest Sci 91:189–202. https://doi.org/10.1007/s10340-017-0857-9
Gibbs M, Schonrogge K, Alma A, Melika G, Quacchia A, Stone GN, Aebi A (2011) Torymus sinensis: a viable management option for the biological control of Dryocosmus kuriphilus in Europe? Biocontrol 56(4):527–538
Grabenweger G, Kehrli P, Zweimueller I, Augustin S, Avtzis N, Bacher S, Freise J, Girardoz S, Guichard S, Heitland W, Lethmayer C, Stolz M, Tomov R, Volter L, Kenis M (2010) Temporal and spatial variations in the parasitoid complex of the horse chestnut leafminer during its invasion of Europe. Biol Invasions 12:2797–2813. https://doi.org/10.1007/s10530-009-9685-z
Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273. https://doi.org/10.1146/annurev.en.38.010193.001343
Guyot V, Castagneyrol B, Vialatte A, Deconchat M, Selvi F, Bussotti F et al (2015) Tree diversity limits the impact of an invasive forest pest. PLoS ONE 10:e0136469. https://doi.org/10.1371/journal.pone.0136469
Hance T, van Baaren J, Vernon P, Boivin G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126. https://doi.org/10.1146/annurev.ento.52.110405.091333
Herbold B, Moyle PB (1986) Introduced species and vacant niches. Am Nat 128:751–760. https://doi.org/10.1086/284600
Herms DA, McCullough DG (2014) Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annu Rev Entomol 59:13–30. https://doi.org/10.1146/annurev-ento-011613-162051
Horrocks KJ, Ward D, Suckling DM (2020) Can natural enemies of current insect pests provide biotic resistance to future pests? Agric For Entomol 22:20–29. https://doi.org/10.1111/afe.12353
Hosmer DW, Lemeshow S (2000) Applied logistic regression, 2nd edn. Wiley, New York
Hufbauer RA (2004) Observations of sagebrush gall morphology and emergence of Rhopalomyiapomum (Diptera: Cecidomyiidae) and its parasitoids. Western N Am Nat 64(3):324–330
Jara-Chiquito JL, Askew RR, Pujade-Villar J (2020) The invasive ACGW Dryocosmus kuriphilus (Hymenoptera: Cynipidae) in Spain: native parasitoid recruitment and association with oak gall inducers in Catalonia. Forestry 93(1):178–186. https://doi.org/10.1093/forestry/cpz061
Jeffs CT, Lewis OT (2013) Effects of climate warming on host parasitoid interactions. Ecol Entomol 38:209–218. https://doi.org/10.1111/een.12026
Jonsson M, Wratten SD, Landis DA, Gurr GM (2008) Recent advances in conservation biological control of arthropods by arthropods. Biol Control 45:172–175. https://doi.org/10.1016/j.biocontrol.2008.01.006
Kato K, Hijii N (1997) Effects of gall formation by Dryocosmus kuriphilus Yasumatsu (Hym, Cynipidae) on the growth of chestnut trees. J Appl Entomol 121:9–15. https://doi.org/10.1111/j.1439-0418.1997.tb01363.x
Kato K, Hijii N (2001) Ovipositional traits of the chestnut gall wasp, Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Entomol Sci 4:295–299
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. https://doi.org/10.1016/S0169-5347(02)02499-0
Kenis M, Auger-Rozenberg M, Roques A, Timms L, Pere C, Cock MJW et al (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45. https://doi.org/10.1007/978-1-4020-9680-8_3
Kos K, Kriston E, Melika G (2015) Invasive chestnut gall wasp Dryocosmus kuriphilus Hymenoptera: Cynipidae), its native parasitoid community and association with oak gall wasps in Slovenia. Eur J Entomol 112(4):698–704. https://doi.org/10.14411/eje.2015.091
Liebhold AM, Berec L, Brockerhoff EG, Epanchin-Niell RS, Hastings A, Herms DA et al (2016) Eradication of invading insect populations: from concepts to applications. Annu Rev Entomol 61:335–352. https://doi.org/10.1146/annurev-ento-010715-023809
Lombardero MJ, Cabaleiro C (2015) Primeros resultados del seguimiento de Dryocosmus kuriphilus en castaños en Lugo. In: IX Spanish national congress of applied entomology. Valencia, Spain, October 2015
Lombardero MJ, Alonso-Rodriguez M, Roca-Posada EP (2012) Tree insects and pathogens display opposite tendencies to attack native vs. non-native pines. For Ecol Manag 281:121–129. https://doi.org/10.1016/j.foreco.2012.06.036
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. iForest 5:50–59. https://doi.org/10.3832/ifor0598-008
MARM (2011) Cuarto Inventario Forestal Nacional. Comunidad Autónoma de Galicia. Ed. Dirección General del Medio Natural y Política Forestal
Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373. https://doi.org/10.1034/j.1600-0706.2001.950301.x
Matošević D, Melika G (2013) Recruitment of native parasitoids to a new invasive host: first results of Dryocosmus kuriphilus parasitoid assemblage in Croatia. Bull Insectol 66(2):231–238
Matošević D, Lackovic N, Kos K, Kriston E, Melika G, Rot M, Pernek M (2017) Success of classical biocontrol agent Torymus sinensis within its expanding range in Europe. J Appl Entomol 141(9):758–767. https://doi.org/10.1111/jen.12388
MeteoGalicia (2019) Weather reports from Galicia. Xunta de Galicia. https://www.meteogalicia.gal/web/inicio.action?request_locale=es/. Accessed 20 Feb 2020
Metz CE (1978) Basic principles of ROC analysis. Semin Nucl Med 8:283–298
Moriya S, Shiga M, Adachi I (2003) Classical biological control of the chestnut gall wasp in Japan. In: Van Driesche RG (ed) Proceedings, symposium: biological control of arthropods, 14–18 January 2002, Honolulu, HI. USDA Forest Service, Morgantown, USA, pp 407–415
Murakami Y, Hiramatsu T, Maeda M (1994) Parasitoid complexes of the chestnut gall wasp (Hymenoptera, Cynipidae) in two localities before introduction of Torymus (Syntomaspis) sinensis (Hymenoptera, Torymidae), with special reference to prediction of results after release of the parasitoid. Jpn J Appl Entomol Zool 38:29–41. https://doi.org/10.1303/jjaez.38.29
Nieves-Aldrey JL (1983a) Contribución al conocimiento de los eulófidos (Hym., Chalcidoidea, Eulophidae) parásitos en las agallas de cinípidos producidas sobre especies de Quercus. Bol Asoc Esp Entom 7:43–54
Nieves-Aldrey JL (1983b) Sobre las especies de Sycophila Walker, asociadas con agallas de cinípidos en la Península Ibérica, con descripción de una nueva especie. Eos 59:179–191
Nieves-Aldrey JL (1984) Observaciones sobre los torímidos (Hym., Chalcidoidea, Torymidae) asociados con agallas de cinípidos (Hym., Cynipidae) sobre Quercus spp. en la zona centro-occidental de España. Bol Soc Esp Ent 8:121–134
Nieves-Aldrey JL, Gil-Tapetado D, Gavira ON, Boyero JR, Polidori C, Lombardero MJ, Blanco D, Rey del Castillo C, Rodríguez-Rojo MP, Vela JM, Wong ME (2019) Torymus sinensis Kamijo, a biocontrol agent against the invasive chestnut gall wasp Dryocosmus kuriphilus Yasumatsu in Spain: its natural dispersal from France and the first data on establishment after experimental releases. For Syst. https://doi.org/10.5424/fs/2019281-14361
Noyes JS (2020) Universal Chalcidoidea Database. World Wide Web electronic publication. http://www.nhm.ac.uk/chalcidoids/. Accessed 20 Feb 2020
Palmeri V, Cascone P, Campolo O, Grande SB, Laudani F, Malacrinò A, Guerrieri E (2014) Hymenoptera wasps associated with the Asian gall wasp of chestnut (Dryocosmus kuriphilus) in Calabria, Italy. Phytoparasitica 42:699–702. https://doi.org/10.1007/s12600-014-0411-8
Panzavolta T, Bernardo U, Bracalini M, Cascone P, Croci F, Gebiola M et al (2013) Native parasitoids associated with Dryocosmus kuriphilus in Tuscany, Italy. Bull Insectol 66:195–201
Panzavolta T, Croci F, Bracalini M, Melika G, Benedettelli S, Tellini Florenzano G, Tiberi R (2018) Population dynamics of native parasitoids associated with the Asian chestnut gall wasp (Dryocosmus kuriphilus) in Italy. Psyche, 2018, ID 8078049. https://doi.org/10.1155/2018/8078049
Patrício, Nunes L (2017) Density management diagrams for sweet chestnut high-forest stands in Portugal. iForest 10(6):865
Payne JA, Menke AS, Schroeder PM (1975) Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), an oriental chestnut gall wasp in North America. Coop Econ Insect Rep 25:903–905
Pérez-Otero R, Mansilla JP (2014) El cinípido del castaño Dryocosmus kuriphilus Yasumatsu, 1951 llega a Galicia (NO de la Península Ibérica). Arquivos Entomol 12:33–36
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288. https://doi.org/10.1016/j.ecolecon.2004.10.002
Price PW, Bouton CE, Gross P, Mcpheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65. https://doi.org/10.1146/annurev.es.11.110180.000353
Quacchia A, Moriya S, Bosio G, Scapin I, Alma A (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. https://doi.org/10.1007/s10526-007-9139-4
Quacchia A, Ferracini C, Nicholls JA, Piazza E, Saladini MA, Tota F et al (2013) Chalcid parasitoid community associated with the invading pest Dryocosmus kuriphilus in north-western Italy. Insect Conserv Diver 6:114–123. https://doi.org/10.1111/j.1752-4598.2012.00192.x
Quacchia A, Moriya S, Askew R, Schönrogge K (2014) Torymus sinensis: biology, host range and hybridization. Acta Hortic 1043:105–111. https://doi.org/10.17660/ActaHortic.2014.1043.13
Rivas-Martínez S (2004) Global bioclimatics. http://www.globalbioclimatics.org/book/bioc/global_bioclimatics_0.htm. Accessed 20 Feb 2020
Roques A, Rabitsch W, Rasplus JY, Lopez-Vaamonde C, Nentwig W, Kenis M (2009) Alien terrestrial invertebrates of Europe. In: Hulme PE (ed) Handbook of alien species in Europe. Springer, Dordrecht, pp 63–79. https://doi.org/10.1007/978-1-4020-8280-1
Rosenblatt AE, Schmitz OJ (2016) Climate change, nutrition, and bottom-up and top-down food web processes. Trends Ecol Evol 31:965–975. https://doi.org/10.1016/j.tree.2016.09.009
Schulz AN, Lucard RD, Marsico TD (2019) Successful invasions and failed biocontrol: the role of antagonistic species interactions. Bioscience 69:711–724. https://doi.org/10.1093/biosci/biz075
Simberloff D, Martin J, Genovesi P, Maris V, Wardle DA, Aronson J et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013
Stone GN, Schonrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668. https://doi.org/10.1146/annurev.ento.47.091201.145247
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 20 Feb 2020
Turlings T, Mccall PJ, Alborn HT, Tumlinson JH (1993) An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps. J Chem Ecol 19:411–425. https://doi.org/10.1007/BF00994314
Vercher R, Costa-Comelles J, Marzal C, Garcia-Mari F (2005) Recruitment of native parasitoid species by the invading leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) on citrus in Spain. Environ Entomol 34:1129–1138. https://doi.org/10.1093/ee/34.5.1129
Vet L, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172. https://doi.org/10.1146/annurev.en.37.010192.001041
Virtanen T, Neuvonen S (1999) Performance of moth larvae on birch in relation to altitude, climate, host quality and parasitoids. Oecologia 120:92–101. https://doi.org/10.1007/s004420050837
Viviani A, Bernardi R, Cavallini A, Rossi E (2019) Genotypic characterization of Torymus sinensis (Hymenoptera: Torymidae) after its introduction in Tuscany (Italy) for the biological control of Dryocosmus kuriphilus (Hymenoptera: Cynipidae). J Insect Sci 19(4):1–8. https://doi.org/10.1093/jisesa/iez080
Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bahrmann R et al (2003) Trophic levels are differentially sensitive to climate. Ecology 84:2444–2453. https://doi.org/10.1890/02-0266
Waage JK (1979) Foraging for patchily-distributed hosts by the parasitoid, nemeritis-canescens. J Anim Ecol 48:353–371. https://doi.org/10.2307/4166
Zhang ZY, Tarcali G, Radócz L, Feng YQ, Shen YY (2009) Chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu in China and in Hungary. J Agric Sci 38(Supplement):123–128
Acknowledgements
This work was supported by FEDER/Spanish Ministry of Economy and Competitiveness Research (Grant AGL2016-76262-R). The manuscript was improved by comments from Matt Ayres. Diana Blanco and Elva Rico provided assistance in the field and in the lab. We are grateful to Dr. R. R. Askew for let us the use of his unpublished key to chalcidoid parasitoids in oak cynipid galls.
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DG-T, FC-D, JLN-A and MJL contributed to study conception and design. Preparation of the first draft was completed by DG-T. All authors contributed to analysis, writing, review, editing and read and approved the final manuscript.
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Gil-Tapetado, D., Castedo-Dorado, F., Nieves-Aldrey, J.L. et al. Gall size of Dryocosmus kuriphilus limits down-regulation by native parasitoids. Biol Invasions 23, 1157–1174 (2021). https://doi.org/10.1007/s10530-020-02427-x
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DOI: https://doi.org/10.1007/s10530-020-02427-x