Poor Control of the Horse Chestnut Leafminer, Cameraria Ohridella (Lepidoptera: Gracillariidae), by Native European Parasitoids: a Synchronisation Problem

NOTE Eur. J. Entomol. 101: 189–192, 2004 ISSN 1210-5759

Poor control of the horse chestnut leafminer, Cameraria ohridella (Lepidoptera: Gracillariidae), by native European parasitoids: a synchronisation problem

GISELHER GRABENWEGER

Institute of Plant Protection, University of Natural Resources and Applied Life Sciences, Peter-Jordan-Straße 82, A-1190 Vienna, Austria; e-mail: [email protected]

Key words. Cameraria ohridella, Gracillariidae, introduced host, native parasitoids, Chalcidoidea, synchronisation

Abstract. Horse chestnut trees in many regions of Europe have suffered from epidemic infestations of C. ohridella for more than ten years. There has been no obvious decrease in the infestation level anywhere on the continent. One reason is, that the native natural enemies have not been able to control mass outbreaks of the leafminer. Parasitoid Hymenoptera have very little impact on the first generation of the moth in early summer, regardless of the number of parasitoids that overwintered in horse chestnut leaves. This study revealed that there is a considerable time lag between the emergence of the parasitoids from the leaflitter in spring and the appearance of suitable host instars in early summer. The poor control of C. ohridella by natural enemies may partly be due to the poor synchronisation between the life cycles of the introduced host and native parasitoid wasps.

INTRODUCTION since leafmining moths are quite common even in urban areas, e.g. Phyllonorycter platani and Phyllonorycter rob- Cameraria ohridella Deschka & Dimic 1986 is undoubtedly iniella in Southern and Central Europe. one of the best known insect pests in many European countries. 2. There are many examples of closely related parasitoid species This is mainly because the host plant of this leafminer, the attacking closely related host insects. Parasitoids from genera common horse chestnut Aesculus hippocastanum L., is a already involved in the parasitism of the host in its original popular ornamental tree and present in public parks, avenues area will more likely integrate the exotic species into their and private yards of almost every large city. For many years the spectrum. Of course this host shift may not necessarily result trees have been continuously heavily infested by the larvae of in effective pest control. Unfortunately, the origin and there- the horse chestnut leafminer, which cause severe damage. The fore the natural enemy complex of C. ohridella are unknown. symptoms are easily detectable even by non-scientists. In com- 3. The existence of polyphagous parasitoids with broad eco- parison with mass outbreaks of other leafmining moths, the logical amplitudes enhance the chances of effectively control- invasion of C. ohridella in Europe is remarkable for two ling a new pest. Investigations on the ecology of particular reasons. First, the abundance of the mining larvae in the leaves parasitoids are rare, nevertheless, some information may be exceeds by far that of other closely related species. Deschka extracted from the literature on various phytophagous host (1993) stated that during thirty years of practice he had never insects. Hellrigl (2001) has compiled important data on the previously observed such high numbers of miners per leaf. Sec- parasitoids of the horse chestnut leafminer. Some species ond, the infestation levels of the horse chestnut trees have not reared from C. ohridella parasitize nearly every leafmining declined anywhere in Europe due to natural control. At several insect in Europe, which indicates an ability to survive in a locations the horse chestnut leafminer has remained at epidemic great variety of environmental conditions. population densities for more than ten years, e.g. in Enns (Aus- 4. Rarely does an introduced pest insect encounter a highly tria) or Zagreb (Croatia), where the leafmines were first detected flexible native parasitoid species, which is able to adapt and in 1989 (Puchberger, 1995; Maceljski & Bertić, 1996). become an important natural enemy of the new host. So far It is not known whether the long term effect of continuous none of the horse chestnut leafminer´s parasitoid complex defoliation is fatal for horse chestnut trees. Nevertheless, this have become important antagonists. tree needs to be protected in some way because of its impor- 5. Specific physiological features or peculiarities in the pest’s tance in recreational areas in and around cities. Therefore, life cycle may prevent a high incidence of parasitism. The research has focused on the control of C. ohridella, e.g. Blümel latter may cause poor synchronisation of the life cycles of & Hausdorf (1996), Krehan (1997), Šefrová (2001). Aside from native antagonists with that of the introduced host. The con- the implementation of a plant protection scheme the investiga- trol of a new pest is only possible if the life cycles of the tions raised another scientifically interesting question. Why are parasitoids and the host are synchronised. Therefore, the lack the native European parasitoids unable to control the horse of suitable hosts when parasitoids are ovipositing will inhibit chestnut leafminer? the adaptation process. Zwölfer and Pschorn-Walcher (1968) studied the effect of native parasitoids on several pest insects introduced into North Results from previous studies on C. ohridella revealed evi- America. They listed some important factors influencing the dence for poor synchronisation especially in spring. The inci- probability that the native parasitoids will control the introduced dence of parasitism of the leafminer´s first generation in spring host species. is uniformly low, regardless of the incidence of parasitism of the preceding generation in autumn (Grabenweger, unpubl.). The 1. Adaptation to a foreign host insect is more likely if other parasitoid complex attacking C. ohridella in autumn is not close relatives of the pest species already exist in the environ- similar to that found in spring (Grabenweger, 1998). This sug- ment. This precondition is fulfilled in the case of C. ohridella, gests that the parasitoids that diapause in mines of C. ohridella

189 TABLE 1. Emergence of parasitoids (number of individuals) from horse chestnut leaflitter recorded at weekly intervals in spring 2001 (photoeclector data, N = 311). Collection date parasitoid total species (family) 7.3. 14.3. 21.3. 28.3. 4. 11.4. 18.4. 25.4. 2. 5. 9. 5. 16.5. 23.5. 30.5. 6. 13.6. 20.6. 27.6. Pnigalio agraules (Eulophidae) 5 17 19 7 10 3 1 62 Pnigalio pectinicornis 2 2 (Eulophidae) Minotetrastichus frontalis 26 41 64 61 9 3 3 207 (Eulophidae) Cirrospilus vittatus (Eulophidae) 1 4 5 Closterocerus trifasciatus 3 8 3 5 1 20 (Eulophidae) Chrysocharis nephereus 3 3 (Eulophidae) Eupelmus urozonus (Eupelmidae) 1 1 Pteromalus cf. semotus 1 3 4 1 9 (Pteromalidae) Colastes braconius (Braconidae) 1 1 Itoplectis alternans 1 1 (Ichneumonidae) in autumn are not the ones that attack the first leafminer genera- beginning of July, when the majority of the first leafminer gen- tion in spring. In this study the time of emergence of the parasi- eration had completed their development and the adults had toids after diapause and the phenology of the leafminer in spring emerged from the mines. are compared. The aim was to find out whether the low levels of Parasitism of the first generation parasitism of the horse chestnut leafminer by native European parasitoids are due to poor synchronisation. Preimaginal instars of parasitoids, which were detected during dissection of the mines were isolated and reared and the adults MATERIALS AND METHODS identified. The number of parasitoids was correlated with the sampling dates, the juvenile host stages and the developmental Data from three experiments are analysed in the present status of the leafminers in the leaves. For the latter the stages paper. were ranked (1st, 2nd, 3rd and 4th feeding instar (1– 4), 1st and 2nd Emergence of parasitoids after diapause spinning instar (5, 6) and pupa (7), emerged moths were not The appearance of the parasitoids in spring 2001 was included) and the ranks were multiplied by the abundances of recorded in four different public parks south of Vienna, Austria. the corresponding stages on each sampling date. The develop- Leaves are regularly removed in autumn, yet some leaflitter mental status allows the integration of the larval development remains beneath shrubs and bushes at these sites. Without into the time scale. exception, the parasitoids diapause in the mines of their hosts RESULTS and overwinter in the shed horse chestnut leaves. 20 litres of horse chestnut leaflitter, which has been heavily infested by the Emergence of parasitoids after diapause leafminer were put into a photoeclector in late autumn. The pho- The first parasitoid to emerge at the end of March was Ptero- toeclectors were set up in shady places at the sampling locations malus cf. semotus (Walker). The majority of the parasitoids and left there during the winter and following spring until sev- emerged three to five weeks later (Table 1). Three eulophid spe- eral weeks after the last parasitoids emerged from the leaves cies were particularly abundant. The most abundant, Minotet- (end of June). The photoeclectors were checked weekly and the rastichus frontalis (Nees), emerged between mid April and mid traps on top of the eclectors were replaced by new ones if they May. The peak emergence of Pnigalio agraules (Walker) was contained insects. about a week earlier than that of M. frontalis. Most of the Phenology of C. ohridella Closterocerus trifasciatus Westwood emerged a week later. By The second experiment dealt with the development of the the beginning of May, more than 90% of the parasitoids had host’s spring generation. As soon as the moths from the over- emerged from the leaflitter. At this time, the first C. ohridella wintering generation began to emerge from the leaflitter (the females started to lay their eggs on the young horse chestnut first moth was observed on 11th of April in 2001), the upper sur- leaves. faces of the new leaves on the surrounding horse chestnut trees Phenology of C. ohridella in spring were examined weekly for C. ohridella eggs and mines. After The first intensive survey of the horse chestnut leaves was the appearance of the first mines at the beginning of May, 10 carried out on May 6. At this time, only one first instar mine leaves were picked at random from the lower branches of the was found. One week later, there were more than five C. trees every week at one location. 10 mines per leaf were dis- ohridella larvae per leaflet and the dissection of mines was sected and the developmental stage of each leafminer instar was started. After the end of May, more than 50% of the preimaginal recorded. All dead, injured or parasitized stages were excluded stages in the leaves were late feeding larvae, spinning instars or from analysis because it was not possible to determine when pupae of the moth (Table 2). The sample taken on the 2nd June their development stopped. Dissections were continued until the was the first with all preimaginal leafminer stages present in the

190 TABLE 2. Phenology of the 1st generation (and part of the 2nd generation) of C. ohridella (number of alive stages and empty pupal exuviae found in horse chestnut leaves in the spring and early summer of 2001, N = 798) Developmental stage Dissection date of C. ohridella 12. 5. 20. 5. 27. 5. 2. 6. 10. 6. 16. 6. 25. 6. 1. 7. 8. 7. 1st larval instars 40 21 13 6 1 1 23 2nd larval instars 46 19 24 13 2 4 8 3rd larval instars 6 53 24 25 23 10 8 4th larval instars 22 20 31 40 11 2 1st spinning instars 7 11 9 4 1 2nd spinning instars 9 2 8 9 7 pupae 8 18 19 47 49 15 adult moths 13 27 39 leaves. In addition, the last adults of the overwintering genera- number of parasitoids and sampling date is significant (Spear- tion were still flying and laying eggs. At the end of June, empty mans ρ = 0.681; α = 0.044). If the developmental status of the pupal exuviae protruding from the leaf surface were detected, leafminer’s population is used instead of the dissection date, the which indicated that the first leafminers had completed their correlation is highly significant (Spearmans ρ = 0.874; α = development and emerged from the mines. Larvae of the second 0.002). generation were observed at the beginning of July. Nevertheless, the number of juvenile stages in the leaves decreased signifi- DISCUSSION cantly during this period due to adult emergence. It is clear from Table 3 and the highly significant correlation Parasitism of the first generation that parasitoids prefer late larval instars and pupae as hosts. Pre- Only 35 parasitized mines were recorded during dissections. vious investigations on the host stage preferences of chalcidoid Minotetrastichus frontalis was the most frequent parasitoid. species, including M. frontalis, gave similar results (Freise, Only a few individuals of Chrysocharis nephereus (Walker), 2001, Grabenweger, 2003). Sympiesis sericeicornis (Nees) and Pediobius saulius (Walker) Higher numbers of third instar larvae, which is the first host were found (Table 3). The latter two species did not occur in the stage suitable for parasitoid development, occur only after mid photoeclector samples. May. This finding was corroborated by the dissection results, None of the first instar larvae was parasitized and the two since the first parasitized mines were found at the end of May. parasitoids found in second instar larvae did not reach The samples with larger numbers of late instar larvae and pupae, adulthood. A few parasitoids occurred in the third larval instar the preferred host instars, were collected two or three weeks and several more in the fourth stage. In relation to their abun- later. dances in the leaves (cf. Table 2), the two spinning stages were Since the leafminer larvae grow older in the process of devel- the most frequently attacked and pupal parasitism was relatively opment, parasitism should increase in the course of the season. high. The correlation between the number of parasitoids and the This was born out by the significant correlation between para- age of the juvenile instars is highly significant (Spearmans ρ = sitism and sampling date. At first sight, the low level of para- 0.893; α = 0.007). sitism in the last sample (see Table 3) contravenes this result. The explanation is that most of the leafminers of the first gen- The first parasitized larvae were detected at the end of May, eration had completed their development at the end of June or the majority of the mines (more than 68% of all parasitized the beginning of July. They emerged from the mines and were ones), however, were attacked after mid June. The number of not present as hosts any more. At the same time, young second parasitoids reared increased steadily with sampling date except generation larvae were present in the leaves. In the last sample, for the last sample. Nevertheless, the correlation between the

TABLE 3. Parasitoids1 found in the mines of the 1st generation of C. ohridella (N = 35) Dissection date Developmental stage of host 12. 5. 20. 5. 27. 5. 2. 6. 10. 6. 16. 6. 25. 6. 1. 7. 8. 7. 1st larval instars 2nd larval instars 2 id 2 Mf 3rd larval instars 1 Mf 1 Mf 1 id 4th larval instars 2 id 1 Mf 3 Mf 1 Mf 1 Mf 1st spinning instars 1 Mf 1 Mf 1 Cn 1 Ss 1 Mf 2nd spinning instars 1 Mf 3 Mf 1 Mf 1 Ps 2 Ss pupae 3 Mf 1 Mf 2 Mf 1 Mf adult moths 1Mf = Minotetrastichus frontalis, Cn = Chrysocharis nephereus, Ss = Sympiesis sericeicornis, Ps = Pediobius saulius, id = parasitoid did not develop to adult stage, determination impossible.

191 they accounted for more than two thirds of the stages under con- Hymenoptera may overcome phenological incompatibilities and sideration (see Table 2). For this reason, the number of suitable switch to a new host. However, the time required for this will host stages present in the leaves decreased in the last sample, probably span evolutionary rather than ecological time scales. It although it was taken at the end of the moth´s first generation. is unlikely that the parasitoid species considered in this study In contrast to the sampling dates, the developmental status of will control C. ohridella in the near future. the leafminer’s population takes into account the overlap between the two leafminer generations. As with the analysis of ACKNOWLEDGEMENTS. Many thanks go to Christa the larval stages, the correlation between the developmental Lethmayer, Austrian Agency for Health and Food Safety, status of the host population and parasitism gave highly signifi- Vienna, for helpful comments on the manuscript. I am also cant results. Apparently, the parasitoids mainly attacked C. grateful to Peter Schausberger, University of Natural Resources ohridella in the final stages of development at the end of the and Applied Life Sciences, Vienna, for constructive criticism on investigation period. the manuscript and correction of English. The studies which A comparison of the photoeclector (Table 1) and the phe- contributed to this paper were financially supported by the Gov- nology data (Table 2) reveals a considerable time lag between ernment of Lower Austria by means of the “Landschaftsfonds” the emergence of the parasitoids from the horse chestnut leaf- and by the European Commission as part of the FP5 project litter and the appearance of suitable host stages. The end of the CONTROCAM, QLK5-CT-2000-01684. diapause of the parasitoids coincided with the emergence of the REFERENCES adult moths of the overwintering generation. Similar observa- tions were made in South Tyrol, Italy (Hellrigl, 2003). Between BENDEL-JANSSEN M. 1977: Zur Biologie, Ökologie und Ethologie mid April and beginning of May bud burst and growth of horse der Chalcidoidea (Hym.). Mitt. Biol. Bundesanst. Land- chestnut leaves occurred and C. ohridella adults swarmed. No Forstwirtsch. Berl.-Dahlem 176: 163. mines, not even eggs were found at that time. Nevertheless, BLÜMEL S. & HAUSDORF H. 1996: Versuche zur Bekämpfung der most of the parasitoids had emerged. Roßkastanienminiermotte. Gärtner & Florist 10: 4–6. S. sericeicornis and P. saulius were reared from the leaves CORNELL H.V. & HAWKINS B.A. 1993: Accumulation of native para- dissected in spring, although no adults emerged from the leaf- sitoid species on introduced herbivores: A comparison of hosts litter collected at the same sites. This indicates that the parasi- as natives and hosts as invaders. Am. Nat. 141: 847–865. toid complex associated with the leafminer´s first generation DESCHKA G. 1993: Die Miniermotte Cameraria ohridella Deschka & comes from sources other than horse chestnut leaflitter. On the Dimic, eine Gefahr für die Roßkastanie Aesculus hippocastanum other hand, M. frontalis dominated the parasitoid complex of L. (Insecta: Lepidoptera: Lithocolletidae). Linzer Biol. Beitr. 25: both, the first and previous diapausing generation of the leafmi- 141–148. FREISE J. 2001: Untersuchungen zur Biologie und Ökologie der ner. However, this does not prove that the M. frontalis larvae Roßkastanien-Miniermotte, Cameraria ohridella Desch. & Dim. found in the mines are the offspring of the individuals that (Lep., Gracillariidae). PhD Thesis, Dept. Appl. Zool., Technical hibernated in the horse chestnut leaflitter. M. frontalis is University of Munich, 216 pp. recorded from a large number of mostly leafmining hosts (more GRABENWEGER G. 1998: Die Parasitierung der Kastanienminier- than 60 different host records are available, see Noyes, 2002). motte (Cameraria ohridella Deschka & Dimic) in Wien und This species probably occurs in a wide range of habitats and is Niederösterreich. Master Thesis, Dept. Terr. Ecol., Inst. Ecol. able to switch to C. ohridella from another host species Conserv. Biol., University of Vienna, 79 pp. throughout the season. GRABENWEGER G. 2003: Parasitism of different larval stages of These results indicate that the majority of the parasitoids Cameraria ohridella. Biocontrol 48: 671–684. would have to survive at least a month in order to encounter HELLRIGL K. 2001: Neue Erkenntnisse und Untersuchungen über die leafminer instars suitable for parasitism. The lifespan of adult Roßkastanien-Miniermotte Cameraria ohridella Deschka & chalcidoids varies from a few days to several months (Bendel- Dimic, 1986 (Lepidoptera: Gracillariidae). Gredleriana 1: 9–81. Janssen, 1977). Therefore, it is theoretically possible for some HELLRIGL K. 2003: Cameraria ohridella: a che punto siamo arrivati? parasitoids to survive until the first suitable hosts develop in Relazioni della: Giornata di Studio Sulle Principali Avversità horse chestnut leaves. On the other hand, the parasitoid wasps dell’ Ippocastano: 14 Febraio 2003; Università di Bologna, pp. reared from the leaves are known to be polyphagous (Noyes, 63–68. 2002; Hellrigl, 2001). Therefore, in the weeks before they find KREHAN H. 1997: Roßkastanienminiermotte - Vergleich der the preferred C. ohridella instars, the parasitoids will probably Bekämpfungsverfahren. Forstschutz Aktuell 19/20: 2–7. encounter lots of other potential host species infesting other host MACELJSKI M. & BERTIÆ D. 1996: The horse chestnut leafminer - plants. Cameraria ohridella Deschka et Dimiæ (Lep.: Lithocolletidae) - a This implies that the parasitoids attacking the first generation new dangerous pest in Croatia (in Croatian, English abstr.) of C. ohridella in early summer are not those that emerged from Fragm. Phytomed. Herbol. 23: 9–18. the horse chestnut leaflitter in spring. Consequently, the parasi- NOYES J.S. 2002: Interactive Catalogue of World Chalcidoidea on tization of this leafminer´s first generation by native parasitoids CD-ROM (2001- second edition). Taxapad, Vancouver and The starts from the same low level each year. Natural History Museum, London. PUCHBERGER K.M. 1995: Zur Geschichte der ersten Ausbreitung von CONCLUSION Cameraria ohridella Deschka & Dimic 1986 in Österreich (Lepi- doptera: Gracillariidae). Entomol. Nachr. Bl. 1: 2–3. The annual break in the adaptation process of the native para- ŠEFROVÁ H. 2001: Control possibility and additional information on sitoids to the new host may account for the persistently low the horse-chestnut leafminer Cameraria ohridella Deschka & parasitism levels of C. ohridella, especially in the first genera- Dimiæ (Lepidoptera: Gracillariidae). Acta Univ. Agric. Silvic. tion. Therefore, the low incidence of parasitism of the horse Mendel. Brun. 49: 121–127. chestnut leafminer by European chalcidoids is at least in part a ZWÖLFER H. & PSCHORN-WALCHER H. 1968: Wie verhalten sich matter of poor synchronisation between the host insect and its Insektenparasiten gegenüber eingeschleppten, faunenfremden natural enemies. Cornell & Hawkins (1993) investigated the Wirten? Anz. Schädl-k. 4: 51–55. accumulation of native parasitoids on introduced herbivores. Some of their examples indicate that even specialist parasitoid Received May 14, 2003; revised September 5, 2003; accepted October 22, 2003

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