Chalcid wasps (Hymenoptera: Chalcidoidea) are probably the most effective and abundant parasitoids of the horse chestnut leaf miner (Cameraria ohridella), an alien pest in Europe that lacks specialized enemies. We studied how the species richness and abundance of chalcids are influenced by altitude, direction of an alien spread and host abundance of C. ohridella. We quantified the numbers and species richness of chalcid wasps and the numbers of C. ohridella that emerged from horse chestnut (Aesculus hippocastanum) leaf litter samples collected from 35 sites in the Czech Republic. Species richness of chalcids, which was considered an indicator of the possible adaptation of parasitoids to this alien host, was unrelated to C. ohridella abundance, direction of spread, or altitude. Chalcid abundance, which was considered an indicator of parasitism of the alien host, was strongly and positively related to C. ohridella abundance. Chalcid abundance was negatively related to direction of spread and positively related, although in a non-linear manner, to altitude. The relationship of chalcid abundance with direction of spread and altitude was weaker than that with C. ohridella abundance. The results provide evidence that biological control of the alien pest C. ohridella by natural enemies might develop in the future.

Department of Forest Protection and Entomology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Prague Czech Republic

Department of Game Management and Wildlife Biology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Prague Czech Republic

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Arneberg P, Skorping A, Grenfell B, Read AF. Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London B: Biological Sciences. 1998;265:1283–1289. doi: 10.1098/rspb.1998.0431. DOI

Augustin S. Distribution of Cameraria ohridella. The Natural History Museum; 2013. Available at http://www.nhm.ac.uk/nature-online/species-of-the-day/biodiversity/alien-species/cameraria-ohridella/index.html .

Bivand R. The Spdep Package. Comprehensive R archive network. (Version 0.3-13) 2005 Available at http:// www.cran.r-project.org .

Blumel S, Hausdorf H. Versuche zur Kontrolle von Cameraria ohridella Deschka & Dimić mit insektiziden Wachstumsregulatoren. Forstschutz Aktuell. 1997;21:16–18.

Cornell HV, Hawkins BA. Accumulation of native parasitoid species on introduced herbivores: a comparison of hosts as natives and hosts as invaders. The American Naturalist. 1993;141:847–865. doi: 10.1086/285512. PubMed DOI

Freise JF, Heitland W, Sturm A. Host-plant range of the horse-chestnut leaf miner, Cameraria ohridella Deschka & Dimic (Lepidoptera, Gracillariidae), a pest of the white flowering horse-chestnut, Aesculus hippocastanum in Germany. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie. 2004;14:351–354.

Gilbert M, Svaton A, Lehmann M, Bacher S. Spatial patterns and infestation processes in the horse chestnut leafminer Cameraria ohridella: a tale of two cities. Entomologia Experimentalis et Applicata. 2003;107:25–37. doi: 10.1046/j.1570-7458.2003.00038.x. DOI

Girardoz S, Kenis M, Quicke D. Recruitment of native parasitoids by an exotic leafminer, Cameraria ohridella: host-parasitoid synchronization and influence of the environment. Agricultural and Forest Entomology. 2006;8:49–56. doi: 10.1111/j.1461-9555.2006.00281.x. DOI

Godfray HCJ. Parasitoids: behavioral and evolutionary ecology. Princeton: Princeton University Press; 1994.

Grabenweger G. Poor control of the horse chestnut leafminer, Cameraria ohridella (Lepidoptera: Gracillariidae), by native European parasitoids: a synchronisation problem. European Journal of Entomology. 2004;101:189–192. doi: 10.14411/eje.2004.023. DOI

Grabenweger G, Kehrli P, Zweimuller 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. Temporal and spatial variations in the parasitoid complex of the horse chestnut leafminer during its invasion of Europe. Biological Invasions. 2010;12:2797–2813. doi: 10.1007/s10530-009-9685-z. DOI

Grabenweger G, Lethmayer C. Occurrence and phenology of parasitic Chalcidoidea on the horse chestnut leafminer, Cameraria ohridella Deschka & Dimic (Lep., Gracillariidae) Journal of Applied Entomology. 1999;123:257–260. doi: 10.1046/j.1439-0418.1999.00347.x. DOI

Hawkins BA, Cornell HV, Hochberg ME. Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology. 1997;78:2145–2152. doi: 10.1890/0012-9658(1997)078[2145:PPAPAM]2.0.CO;2. DOI

Hastie T. GAM: generalized additive models. (R Package Version 1.04.1) 2011 Available at http://www.cran.r-project.org .

Heiberger RM. HH: statistical analysis and data display: Heiberger and Holland. (R package version 2.1-32) 2009 Available at http://www.cran.r-project.org .

Hogg BN, Wang XG, Levy K, Mills NJ, Daane KM. Complementary effects of resident natural enemies on the suppression of the introduced moth Epiphyas postvittana. Biological Control. 2013;64:125–131. doi: 10.1016/j.biocontrol.2012.10.008. DOI

Kehrli P, Bacher S. Date of leaf litter removal to prevent emergence of Cameraria ohridella in the following spring. Entomologia Experimentalis et Applicata. 2003;107:159–162. doi: 10.1046/j.1570-7458.2003.00043.x. DOI

Kehrli P, Bacher S. How to safely compost Cameraria ohridella-infested horse chestnut leaf litter on small compost heaps. Journal of Applied Entomology. 2004;128:707–709. doi: 10.1111/j.1439-0418.2004.00915.x. DOI

Lees DC, Lack HW, Rougerie R, Hernandez-Lopez A, Raus T, Avtzis N, Augustin S, Lopez-Vaamonde C. Tracking origins of invasive herbivores using herbaria and archival DNA: the case of the horse-chestnut leafminer. Frontiers in Ecology and the Environment. 2011;9:322–328. doi: 10.1890/100098. DOI

Lomolino MV, Riddle BR, Whittaker RJ, Brown JH. Biogeography. 4th edition. Sinauer; 2010.

Matosevic D, Melika G. Diversity of parasitoid assemblages of native and alien leaf miners in Croatia. Sumarski List. 2012;136:367–376.

Mertelik J, Kloudova K, Vanc P. Occurrence of Aesculus hippocastanum with high degree of resistance to Cameraria ohridella in the Czech Republic. Acta fytotechnica et zootechnica. 2004;7:204–205.

Nejmanova J, Cvacka J, Hrdy I, Kuldova J, Mertelik J, Muck A, Jr, Nesnerova P, Svatos A. Residues of diflubenzuron on horse chestnut (Aesculus hippocastanum) leaves and their efficacy against the horse chestnut leafminer, Cameraria ohridella. Pest Management Science. 2006;62:274–278. doi: 10.1002/ps.1165. PubMed DOI

Novakova P, Nakladal O. Pripadova studie parazitoidu klinenky jirovcove (Cameraria ohridella Deschka et Dimic, 1986) v Ceske republice v letech 2001–2005. Zprávy Lesnického Výzkumu. 2008;53:12–21.

Percival GC, Banks J, Keary I. Evaluation of organic, synthetic and physical insecticides for the control of horse chestnut leaf miner (Cameraria ohridella) Urban Forestry & Urban Greening. 2012;11:426–431. doi: 10.1016/j.ufug.2012.07.001. DOI

Percival GC, Barrow I, Noviss K, Keary I, Pennington P. The impact of horse chestnut leaf miner (Cameraria ohridella Deschka and Dimic; HCLM) on vitality, growth and reproduction of Aesculus hippocastanum L. Urban Forestry & Urban Greening. 2011;10:11–17. doi: 10.1016/j.ufug.2010.11.003. DOI

Pere C, Augustin S, Tomov R, Peng LH, Turlings TC, Kenis M. Species richness and abundance of native leaf miners are affected by the presence of the invasive horse-chestnut leaf miner. Biological Invasions. 2010;12:1011–1021. doi: 10.1007/s10530-009-9518-0. DOI

R Development Core Team . R: a language and environment for statistical computing. Version 3.0.2. Vienna: The R Foundation for Statistical Computing; 2013. Available at http://www.R-project.org/

Roy HE, Handley LJL, Schonrogge K, Poland RL, Purse BV. Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? BioControl. 2011;56:451–468. doi: 10.1007/s10526-011-9349-7. DOI

Schonrogge K, Crawley MJ. Quantitative webs as a means of assessing the impact of alien insects. Journal of Animal Ecology. 2000;69:841–868. doi: 10.1046/j.1365-2656.2000.00443.x. PubMed DOI

Sefrova H. Control possibility and additional information on the horse-chestnut leafminer Cameraria ohridella Deshka & Dimic (Lepidoptera, Gracillariidae) Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis. 2001;49:121–127.

Sefrova H. Invasions of Lithocolletinae species in Europe-causes, kinds, limits and ecological impact (Lepidoptera, Gracillariidae) Ekologia. 2003;22:132–142.

Sefrova H, Lastuvka Z. Dispersal of the horsechestnut leafminer, Cameraria ohridella Deschka & Dimic, 1986, in Europe: its course, ways and causes (Lepidoptera: Gracillariidae) Entomologische Zeitschrift. 2001;111:194–198.

Sivinski J, Pinero J, Aluja M. The distributions of parasitoids (Hymenoptera) of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biological Control. 2000;18:258–269.

Skillen EL, Pickering J, Sharkey MJ. Species richness of the Campopleginae and Ichneumoninae (Hymenoptera: Ichneumonidae) along a latitudinal gradient in eastern North American old-growth forests. Environmental Entomology. 2000;29:460–466. doi: 10.1603/0046-225X-29.3.460. DOI

Tognelli MF, Kelt DA. Analysis of determinants of mammalian species richness in South America using spatial autoregressive models. Ecography. 2004;27:427–436. doi: 10.1111/j.0906-7590.2004.03732.x. DOI

Toth P, Lukas J. Parasitic Ichneumonoidea on the horse chestnut leaf miner, Cameraria ohridella (Lepidoptera: Gracillariidae) in Slovakia. Journal of Pest Science. 2005;78:151–154. doi: 10.1007/s10340-005-0086-5. DOI

Valade R, Kenis M, Hernandez-Lopez A, Augustin S, Mari Mena N, Magnoux E, Rougerie R, Lakatos F, Roques A, Lopez-Vaamonde C. Mitochondrial and microsatellite DNA markers reveal a Balkanic origin for the highly invasive Horse-Chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae) Molecular Ecology. 2009;18:3458–3470. doi: 10.1111/j.1365-294X.2009.04290.x. PubMed DOI

Wagner DL, Peacock J, Carter JL, Talley SE. Field assessment of Bacillus thuringiensis on nontarget Lepidoptera. Environmental Entomology. 1996;25:1444–1454. doi: 10.1093/ee/25.6.1444. DOI

Walsh C, Mac Nally R. Package ‘hier.part’. 2011 Available at http:// www.cran.r-project.org .

Zappala L, Bernardo U, Biondi A, Cocco A, Deliperi S, Delrio G, Giorgini M, Pedata P, Rapisarda C, Garzia GT, Siscaro G. Recruitment of native parasitoids by the exotic pest Tuta absoluta in Southern Italy. Bulletin of Insectology. 2012;65:51–61.

Zwölfer H, Pschorn-Walcher H. Wie verhalten sich Insektenparasiten gegenüber eingeschleppten, faunenfremden Wirten? Anzeiger für Schädlingskunde. 1968;41:51–55. doi: 10.1007/BF02150940. DOI