Correspondence – Notes 201

Norberg, U, Fenton, M. (1988): Carnivorous bats? Biological Journal 3. Biological Dynamics of Forest Fragments Project, National of the Linnean Society 33: 383–394. Institute for Amazonian Research (INPA) and Smithsonian Tropical Nunes, V.D.S. (1988): Vocalizations of treefrogs (Smilisca sila) in Research Institute, C.P. 478, Manaus, AM 69011-970, Brazil. response to bat predation. Herpetologica 44: 8-10. 4. Departamento de Biologia, Instituto de Ciências Biológicas, Mesquita, R.C.G., Ickes, K., Ganade, G., Williamson, G.B. (2001): Universidade Federal do Amazonas, Av. General Rodrigo Octávio Alternative successional pathways in the Amazon Basin. Journal Jordão Ramos, 3000, Japiim, Manaus, AM. 69077-000. Brazil. of Ecology 89: 528-537. 5. Museu de Ciències Naturals de Granollers, Àrea Investigació en Oliveira, A.A., Mori, S.A. (1999): A Central Amazonian terra firme Quiròpters, Av. Francesc Macià 51, 08402 Granollers, Catalonia. forest. I. High tree species richness on poor soils. Biodiversity *Corresponding author, R. Rocha, Email: [email protected] and Conservation 8: 1219-1244. Perachhi, A.L., Albuquerque, S.T., Raimundo, S.D.L. (1982): Notas para o conhecimento dos hábitos alimentares de Trachops cirrhosus (Spix, 1983) (Mammalia, Chiroptera, Phyllostomidae). Arquivos da Universidade Federal Rural do Rio de Janeiro 5: 1- 3. Pine, R.H., Anderson, J.E. (1979): Notes on stomach contents in Asian sweet gallwasp, Trachops cirrhosus (Chiroptera: Phyllostomatidae). Mammalia 43: 568–570. kuriphilus (, Rodrigues, F.H.G., Reis, M.L., Braz, V.S. (2004): Food habits of the frog-eating bat, Trachops cirrhosus, in Atlantic Forest of Cynipidae): first record for Romania Northeastern Brazil. Chiroptera Neotropical 10: 180-182. Rocha, R., Silva, I., dos Reis, A.M., Rosa, G.M. (2012): Another frog on the menu: predation of Trachops cirrhosus (Chiroptera: The Asian chestnut gallwasp (ACGW) (Dryocos- Phyllostomidae) upon Osteocephalus oophagus (Anura: Hylidae). mus kuriphilus Yasumatsu), is a member of the so- Chiroptera Neotropical 18: 1136-1138. called “oak gall wasps” (Hymenoptera, Cynipi- Santana, S.E., Geipel, I., Dumont, E.R., Kalka, M.B., Kalko, E.K. (2011): All you can eat: high performance capacity and plasticity dae, Cynipini) (Fig. 1). This tribe comprises phy- in the common big-eared bat, Micronycteris microtis (Chiroptera: tophagous gall-inducing and gall-associated (in- Phyllostomidae). PLoS ONE 6: e28584. quiline) cynipoid wasps with about 1000 known Simmons, NB. (2005): Order Chiroptera. Pp. 312-529. In: Wilson DE, Reeder DM (eds.), Mammal species of the World: a taxonomic species worldwide which associate with Fagaceae, and geographic reference. Smithsonian Institution Press. mainly Quercus L. (Csóka et al. 2004). Hungary Surlykke, A., Jakobsen, L., Kalko, E.K., Page, R.A. (2013): and Romania are among the most oak gallwasp Echolocation intensity and directionality of perching and flying fringe-lipped bats, Trachops cirrhosus (Phyllostomidae). Frontiers species rich parts of Europe (Melika et al., 2000, in Physiology 4: 143. 2003). ACGW emerged as a in the mid- Toledo, L.F. (2005): Predation of juvenile and adult anurans by twentieth century and is now one of the most invertebrates: current knowledge and perspectives. Herpetological Review 36: 365-400. dangerous pests of chestnut globally (Casta- Toledo, L.F., Ribeiro, R.S., Haddad, C.F.B. (2007): Anurans as prey: nea spp.) (Aebi et al. 2006, Gibbs et al. 2011). This an exploratory analysis and the size relationships between pest species disrupts growth by inducing gall for- predators and their preys. Journal of Zoology 271: 170-177. Tuttle, M.D, Ryan, M.J. (1981): Bat predation and the evolution frog mation on new shoots and leaves, eliminating nut vocalizations in the Neotropics. Science 214: 677-678. production and causing a gradual decline in the Tuttle, M.D., Taft, L.K., Ryan, M.J. (1982): Evasive behaviour of a vigor of these long-lived and slow-growing trees frog in response to bat predation. Behaviour 30: 393-397. Whitaker, J.O., Findley, J.S. (1980): Foods eaten by some bats from (EFSA 2010). ACGW is the only species in Cynip- Costa Rica and Panama. Journal of Mammology 61: 540-544. ini tribe which induces galls on Castanea spp. Williams, S.L., Genoways, H.H. (2007): Subfamily Phyllostominae. While oak gallwasps rarely affect their host tree’s pp. 255-299. In: Gardner A.L. (ed.), Mammals of South America. The University of Chicago Press. fitness, attack by ACGW on chestnut commonly reduces wood production and fruit yield by 50– Key words: amphibians, bats, Brazil, Amazonia, diet, 80% (Melika et al. 2003, Quacchia et al. 2012). The trophic interaction. damage may continue for many years. Addition- ally, severe consecutive attacks may result in the Article No.: e157501 death of the tree, probably in combination with Received: 02. January 2014 / Accepted: 26. June 2015 Available online: 31. May 2016 / Printed: June 2016 other detrimental factors such as fungal infection, drought or severe attack by other herbivores (Dixon et al. 1986, Szabó et al. 2014). 1,2,3, 4 Ricardo ROCHA *, Marcelo GORDO Originating from , it was established as 1,2,5 and Adrià LÓPEZ-BAUCELLS a pest in Japan (1958), South Korea (1958), USA

1. Centre for Ecology, Evolution and Environmental Changes, (1974), and Nepal (1999) (Gibbs et al. 2011). In Faculdade de Ciências da Universidade de Lisboa, Bloco C2, Europe it was first recorded near Cuneo, Pied- Campo Grande, 1749-016 Lisboa, Portugal. mont region, in 2002 (Brussino et al. 2002). 2. Metapopulation Research Group, Faculty of Biosciences, University of Helsinki, PO Box 65 (Viikinkaari 1), FI-00014 Helsinki, Since 2002 the pest had spread and established all Finland. over Italy, and (2005), 202 North-Western Journal of Zoology 12(1) / 2016

Figure 1. The Asian chestnut gallwasp (ACGW), Dryocosmus kuriphilus (photo by Gy. Csóka)

(2009), Croatia (2010), Slovakia and the Czech Re- public (2011), Spain (2012), Hungary (2013) (Szabó et al. 2014), Turkey and Portugal (2014) (pers. comm.). Till the detection of ACGW in Romania, Hungary was the most eastern European bound- ary of ACGW distribution. It has spread naturally over the south and south-western part of Hungary in two years: it was first detected in the most southwestern Zala county in 2013 (penetrated from Slovenia), then spread into Vas and Somogy counties in 2014. It was found in large numbers in Figure 2. Typical ACGW galls on chestnut leaves Budapest, Pilis Mountains, Visegrad, Nagymaros in Sălard, Romania (photos by L. Radócz) in 2015 (pers. data, GyCs., GM) where it was probably introduced with infested trees carried from Northern Italy as plant for planting (Csóka et al. 2009). The human exchange of infected culti- vars and material for grafting among chestnut growers, and the natural range expansion within nearby natural and planted stands are the main factors facilitating the rapid spread of ACGW.

Fresh developing galls of ACGW were found by visual observations in a orchard (4.1 hectares) which is located near Sălard (Bihor County, Romania). The orchard was established in 2012 and the plant propa- gation material was imported directly from Italy. Typical ACGW leaf galls were detected on 3 chestnut trees (GPS coordinates: N 47º13’11”, E 22º06’38”, 125 m a.s.l.) (Fig. 2). According to the owner, infected leaves and galls on Figure 3. Withered ACGW galls on chestnut twigs twigs were removed last year. On those trees we found in Sălard, Romania (photo by L. Radócz) also withered galls from the previous year (Fig. 3).

Life Cycle of ACGW. ACGW has one generation tion of galls inside which the gallwasp larvae de- per year. Only the parthenogenetic females are velop. Each gall comprises 1 to 15 larval chambers, known which laying eggs in the buds of Castanea with an average of 3.5 larvae per gall. The fully spp. during summer, which then hatch in 30–40 developed adult females stay for about 10-15 days days. First-instar larvae overwinter and grow in the gall before starting to emerge. After the slowly until the following spring at which point emergence, females start to lay eggs (Gibbs et al. their growth rate increases leading to the forma- 2011). Correspondence – Notes 203

Options for ACGW control. Strict control of native community is short, however, the movement of infested plant material can re- the attack rates of indigenous parasitoid species duce long-distance dispersal of ACGW to new ar- are typically low (2-4.7%) (Aebi et al. 2006, Gibbs eas within Europe. However, there are limited op- et al. 2011, Szabó et al. 2014); only in some years tions available for managing existing ACGW the parasitization rate might increase up to 32% populations and reducing their impact and spread (Santi & Maini 2011). Thus, native on European chestnut plantations. Mechanical re- cannot effectively control the ACGW and keep moval of infested twigs (pruning) and the protec- their populations under economic threshold. tion of seedlings with nets, although effective, do The only solution seems to be the classical bio- not represent practical solutions because of their logical control, the introduction of a chalcid para- labour intensiveness and high expenses. Since the sitoid, Torymus sinensis Kamijo (TS) (Hymenop- larval and pupal stages are protected within the tera: ), native to China and known as a galls formed by this species, conventional chemi- highly specialized parasitoid of ACGW (Quacchia cal control is regarded as largely ineffective (EFSA et al. 2012). Classical biological control using TS 2010). Developing resistant varieties of Castanea has been proven to be the only effective method of spp., for example a japanese-european Bo- controlling the populations of ACGW and has che de Bètizac, could potentially be a viable man- been successfully applied in Japan, South Korea, agement option, but this will only be beneficial for USA (Moriya et al. 2002, Cooper & Rieske 2011). new planting and will not help existing chestnut The introduction of TS to Europe was initiated in plantations (EFSA 2010). Italy in 2005, in 2011 in France. In both cases the The most effective method for reducing introduction was very successful and the ACGW ACGW infestation to date is the use of hymenop- population densities were essentially reduced teran parasitoids as biological control agents in (Bosio et al. 2013, Borowiec et al. 2014, Matošević two possible ways: conservation and/or augmen- et al. 2014). The parasitoid was introduced to tation (using native parasitoids shifted onto the Hungary (Kriston et al. 2014) and Croatia (Ma- new host, ACGW) and the classical biological con- tošević et al. 2014) in 2014, and to Slovenia in 2015 trol with the introduction of a non-native parasi- (pers. comm., GM). TS must be introduced to Ro- toid species from the place of origination, China mania as soon as possible, which will definitely (Bosio et al. 2013). slow down the spreading of ACGW all over the Within their native range in China ACGW country. populations are kept at low densities by natural enemies (Aebi et al. 2006). Despite having arrived Acknowledgements. We are grateful for the valuable in Europe without any natural enemies, the chest- comments given by referees: Dr. Gy. Csóka, Dr. D. Matošević and one anonymous referee. nut gallwasp has quickly recruited native parasi- toids. These originate from oak and/or rose galls, References which the native parasitoids regularly attack Aebi, A., Schönrogge, K., Melika, G., Alma, A., Bosio, G., Quacchia, within their range. We are studying the native A., Picciau, L., Abe, Y., Moriya, S., Yara, K., Seljak, G., Stone, G.N. (2006): Parasitoid Recruitment to the globally invasive parasitoid complexes of ACGW across its expand- chestnut Dryocosmus kuriphilus. pp. 103–121. In: Ozaki, ing range in Italy (since 2002), Slovenia (since K., Yukawa, J., Ohgushi, T., Price, P.W. (eds.), Ecology and 2010), Croatia (since 2011) and Hungary (since evolution of galling and their associates. Springer- Verlag, Tokyo. 2013). Thirtynine native European parasitoid spe- Borowiec, N., Thaon, M., Brancaccio, L., Warot, S., Vercken, E., cies from 6 Chalcidoidea (Hymenoptera) families Fauvergue, X., Ris, N., Malausa, J.C. (2014): Classical biological have been recorded so far on ACGW from Italy till control against the chestnut gall wasp Dryocosmus kuriphilus Hymenoptera, Cynipidae) in France. Plant Protection Quarterly 2013 (Melika et al. 2014), 27 from Slovenia (Kos et 29(1): 7–10. al. 2015), 18 from Croatia, and 11 from Hungary Bosio, G., Armando, M., Moriya, S. (2013): Verso il controllo (Matošević & Melika 2013, Szabó et al. 2014). Re- biologico del cinipide del castagno. L'Informatore Agrario 14: 60–64. cruitment of parasitoids to ACGW depends on the Brussino, G., Bosio, G., Baudino, M., Giordani, R., Ramello, F., actual parasitoid species composition of oak gall- Melika, G. 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