Phyllonorycter issikii
(lime leafminer)

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Identity

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Preferred Scientific Name

• Phyllonorycter issikii Kumata, 1963

Preferred Common Name

• lime leafminer

Other Scientific Names

• Lithocolletis issikii Kumata, 1963

International Common Names

• Russian: lipovaya mol-pestryanka

Local Common Names

• Czech Republic: klínenka lipová
• Finland: lehmusmiinajakoi
• Germany: Lindenminiermotte
• Hungary: hárslevél sátorosmoly
• Slovakia: ploskácik lipovy

EPPO code

• PRYCIS (Phyllonorycter issikii)

Summary of Invasiveness

Top of page The invasiveness of P. issikii is indicated by the manner and speed of its spread in Europe. See 'Distribution' for more details. Also Sefrová (2003) and Deschka (1995) indicated the possibility of its invasion to central Europe.

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Lepidoptera
•                         Family: Gracillariidae
•                             Genus: Phyllonorycter
•                                 Species: Phyllonorycter issikii

Notes on Taxonomy and Nomenclature

Top of page The species was described by Kumata in 1963 from the Japanese island of Hokkaido as Lithocolletis issikii. The genus name, Lithocolletis, was later considered to be synonymous with Phyllonorycter, now taken as the valid generic name.

Description

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The morphology of the adult was addressed by Kumata (1963) and Kumata et al. (1983). The caterpillar chaetotaxy was described by Kumata (1993) and the morphology of the pupa was described by Gregor and Patocka (2001). The morphology of all the stages, including the larval chaetotaxy was studied by Sefrová (2002).

Egg

The egg is slightly elongated, ellipsoidal, and has a delicate pitting on the chorion surface. It is 0.32-0.37 mm by 0.23-0.27 mm. It is greenish-ochreous, which corresponds to the undersides of the leaves on the host plant.

Larva

The larval morphology corresponds to the morphology of other Phyllonorycter larvae. The larva is whitish-ochreous and is 4.0-5.6 mm long in the final instar. There are five larval instars. The first three instars are flat with reduced mouthparts and legs (sometimes called sap-feeding instars e.g. Kumata, 1978). The triangulate head capsule shows prognathy without spinneret, labial and maxillary palpi. There is a close group of stemmata on the head near the antennal base of these instars. The triangular mandibles with three curved cusps are moved horizontally between the huge flat labrum and the labium. The thoracic segments are strikingly dilated (especially in the first instar) compared with the abdominal segments. This characteristic decreases with the next instars. The final two instars (tissue-feeding instars) show the morphology of exophagous caterpillars. Their heads are more globular, semiprognathous and have complete mouthparts. The mandibles are more or less rectangular with five cusps on the frontal edge and they move vertically. The stemmata form a quadrangle. The thoracic legs, abdominal prolegs (on the third to fifth segments) and anal prolegs are normally shaped. The 23-38 claws of each proleg are positioned in multiple, usually irregular circles. The individual instars can be primarily distinguished according to the width of the head capsule: I: 0.14-0.16 mm; II: 0.18-0.21 mm; III: 0.25-0.28 mm; IV: 0.25-0.30 mm; and V: 0.31-0.40 mm.

Pupa

The pupa is light brown to brownish-black and 3.2-4.0 mm long. Its frontal process is short and broad. It is in the shape of an equilateral triangle with distinct surface sculpture. Abdominal segments two to eight bear two pairs of rigid setae and their dorsal parts are covered with coarse thorns. The male genitalia only slightly protrude. The tenth abdominal segment is long, with a broad anal field. This has an elongate cremaster, which is round in ventral view, and elongate and strongly constricted in lateral view, with one pair of small hooked thorns at the end.

Adult

The wingspan is 6.3-8.3 mm. The adult exhibits distinct seasonal dimorphism. The aestival form has a whiteish-ochreous frons and labial palpus. The hair tuft on the head is ochreous with individual white scales. The antennae are greyish-white with black circles. The thorax is golden-ochreous, with three white lines. The forewing is golden-ochreous, with a long and narrow basal streak (occasionally indistinct), lacking a dark margin, or with individual dark scales only on its fore margin. The first (basal) transversal streaks are narrow and slope outwards. The dorsal streak is distinctly longer than the costal streak. The other three costal streaks are located close to each other before the apex. The second dorsal streak, which is before the tornus, occasionally fuses with a light tornal spot. The basal margins of all the streaks are more or less bordered with black scales. A distinct line of black scales divides the yellowish-white cilia. The hind wings and their cilia are pale grey.

The winter form (differences only) has a hair tuft on the head that is greyish-black or black with individual white scales, and is entirely white. The thorax is dark brown, and occasionally has white scales and white, indistinct lines. The forewing is grey, greyish-brown or greyish-black, mixed with white and brownish-black scales or spots. The ground colour of the winter form is very variable from pale grey to brownish-black. This striking habitual seasonal difference is possibly due to the fact that the hibernating individuals easily escape the attention of their predators in overwintering shelters. No sexual dimorphism has been observed.

Distribution

Top of page This species was described from the Japanese island of Hokkaido and it was also later discovered on other islands of Japan, in the adjacent part of the Primorsk Region (Primorsky Kray) and in Korea (Kumata, 1963; Ermolaev, 1978; Kumata et al., 1983).

During the 1980s, P. issikii was found in Moscow and later in several other towns of Russia and Ukraine (Osipova, 1990; Kozlov, 1991; Mey, 1991; Orlinskij et al., 1991; Sefrová, 2002). It seems that the species was introduced from eastern Asia to Moscow or to other towns of the European part of the USSR. Anemochoric (air current) transportation from eastern Asia to Russia or a stepwise spontaneous spread through Siberia are not possible because its food plant, Tilia spp., shows no continuous distribution between eastern and western parts of the Palaearctic region (e.g. Dubatolov and Kosterin, 2000).

During the 1980s, P. issikii was also recorded in Kiev, and since that time it has spread to the west, via the north. It was first found in southeastern Poland in 1996, in Lithuania in 1997 (Noreika, 1998) and in Belorussia and Latvia in 1998, when it occupied a third of eastern Poland (Buszko et al., 2000; Buszko and Nowacki, 2000). In 1999, it had reached the eastern half of Poland. In 2000, the first mines were observed in the Czech and Slovak Republics (Sefrová et al., 2000; Tokár 2002), southern Austria and northern Hungary (Sefrová, 2002; Szabóky and Csóka, 2003). In 2001, the mines were observed in eastern Germany and Estonia, and in 2002, in Finland (Leinonen and Kaitila, 2003). The spread of this species continues in a west and southwest direction.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Risk of Introduction

Top of page The species is not distributed with its host plant or with other plants. It is not a quarantine pest and any phytosanitary measures cannot stop or influence its spread.

Habitat

Top of page P. issikii prefers deciduous forest stands of lower and colline altitudes (up to 600 m in central Europe). It is a forest pest that spreads into man-made habitats and attacks trees in parks, alleys and cemetries, for example. Infestations of solitary urban trees follow an increase in the population density in preferred habitats. P. issikii prefers shady branches of trees and shrubs in thin forest stands. It avoids sunlit branches.

Habitat List

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Category	Sub-Category	Habitat	Presence	Status
Terrestrial

Hosts/Species Affected

Top of page P. issikii is an oligophagous miner of various Tilia species and cultivars, and shows no distinct preference for individual host taxa. In its native area, the food plants are Tilia amurensis, Tilia maximowicziana, Tilia japonica, Tilia kiusiana and Tilia mandshurica (Kumata, 1963; Kumata et al., 1983). In Europe, the mines have been found on Tilia cordata, Tilia platyphyllos, introduced ornamental species and their crosses, such as Tilia tomentosa and Tilia euchlora (Buszko et al., 2000; Sefrová, 2002). Kumata (1963) also names Betula platyphylla as a host plant, but this information requires confirmation.

Host Plants and Other Plants Affected

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Growth Stages

Top of page Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

Top of page The larvae mine the leaves of various Tilia species. The young larval mines are inconspicuous and whitish. They are gradually dilating, irregular, flat squares on the underside of the leaf. The mines of the fourth and fifth instars are easily visible as whitish areas of 1-1.5 cm² on the upper surface of the leaf. The leaf is more or less deformed at this stage. No differences between the symptoms in different host species have been observed.

List of Symptoms/Signs

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Biology and Ecology

Top of page P. issikii produces two or three generations annually and the last generation of adults hibernates. The eggs are oviposited on the lower surface of the leaf. The presence of mines and eggs on the upper surface is quite exceptional (only 0.5% of cases). The overwintering females begin oviposition at the beginning of May. The caterpillar hatches after 4-8 days. It has five instars, three of which are sap feeders and the last two are tissue feeders. The first- and second-instar mines are pale and gradually dilate in an irregular square. They may only be detected by careful observation of the lower surface of the leaf. The third-instar mine becomes more distinct and visible, and occupies 0.5-1.5 cm². The fourth-instar larva gradually constricts the leaf and it is also visible from the upper surface. The leaf starts to deform. From this point on, the larva only feeds on the surface of the spongy parenchyma. The fifth instar feeds in the palisade parenchyma and whitish dots are seen on the upper surface of the mine. The caterpillar pupates after 13-40 days in the mine. Pupation of the first generation is generally between the end of May and the middle of June, depending on the weather conditions. In general, the moths of the first summer generation emerge from the end of May up to the end of June after 10-15 days in natural conditions. The individual mines of this generation can be observed up to the end of July. The last mines of the first generation can be confused with the mines of the second generation, which are abundant in warmer territories and warmer years. The second generation develops from July to the middle of August.

Development of the summer generation is temperature-dependent and is usually completed in 4-7 weeks. In laboratory experiments at 25°C, the larvae develop in 13 days and the pupae develop in 6 days. At 20°C, the larva lasts 17 days and the pupa lasts 8 days. The development times of the individual larval instars are: I: 2-7 days; II: 2-8 days; III: 3-8 days; IV: 3-8 days; and V: 3-8 days.

The hibernating moths (dark winter forms) emerge after 10 August but generally only from the end of August and the beginning of September to 10 October. The pupae can also be recorded in the latter half of October. The complete development of this generation lasts 8-11 weeks. The leaf epidermis of Tilia spp. is very soft and thin so that it is easily disrupted and decays after the leaves drop. This is probably the main reason why the moths of this species hibernate after they emerge and before the leaves drop. The individuals of the summer and winter forms are dissimilar (cf. morphology).

Natural enemies

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Notes on Natural Enemies

Top of page Mey (1991), who recorded six eulophid species parasitizing P. issikii in Kiev, published the first information on parasitoids of P. issikii. Parasitism by Hymenoptera (Chalcidoidea, Braconidae) was 15-20% in various localities in the Czech and Slovak Republics during the first year of discovery (2000) of P. issikii. In the following years, up to 40% parasitism was recorded but the individual parasitoid taxa were not determined. Also several larvae died after infestation by fungal pathogens.

Means of Movement and Dispersal

Top of page Natural Dispersal (Non-Biotic)

P. issikii mostly shows a scattered distribution. There is no distinct boundary to its forward progression of dispersal. Long-distance dispersal appears to be on air currents. The adults are nocturnal and only move over short distances of upto 1000 m.

Movement in Trade

As with many other Phyllonorycter species, the dispersal of pupae in fallen leaves is impossible because the adults always emerge before the leaves drop. The transportation of eggs, larvae and pupae with the host plants is very improbable because lime plants (seedlings) are not evergreen and they are transported without leaves. The eggs and larvae can only survive in fresh living leaves. The adults hibernate in various crevices and other shelters and their passive transportation during hibernation in containers, boxes etc. is both possible and probable (Sefrová, 2002, 2003).

Plant Trade

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Plant parts not known to carry the pest in trade/transport
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Fruits (inc. pods)
Growing medium accompanying plants
Leaves
Roots
Seedlings/Micropropagated plants
Stems (above ground)/Shoots/Trunks/Branches
True seeds (inc. grain)
Wood

Wood Packaging

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Impact

Top of page The host trees, Tilia spp., are not endangered, and their growth and fitness are not affected by pest attack (e.g. Sefrová, 2002). Similarly no aesthetic harm is expected. This species prefers Tilia trees in shady forest stands and the mines are mostly found on the lower branches or on the undergrowth. The mines do not cause the leaves to dry out or change their colour and so the presence of the pest is not apparent.

Environmental Impact

Top of page P. issikii attacks the autochthonous Tilia. It has a preference for trees that grow in forest stands, for a host plant that is autochthonous and it has a scattered distribution. These facts indicate an ecological relation to the autochthonous species of the genus Phyllonorycter. This species will probably find a niche in the European forest communities. It will probably be controlled and limited by natural autochthonous enemies and non-biotic factors, respectively. Trophic competition with autochthonous species developing on Tilia spp. is very improbable. That is why there is no negative influence to endanger the autochthonous tree species and/or the related taxa of moths and other insects that show similar trophic demands in the corresponding communities. Nevertheless, monitoring of its spread, population density and ecological relations (parasitoid spectre, etc.), as a new member of the European insect fauna, appears to be important and useful.

Diagnosis

Top of page No laboratory or other special tests are required.

Detection and Inspection

Top of page The species can be easily detected by the whitish mines that are visible on the upperside of the leaf, partly by the deformed leaves or by the necrotic areas of old mines.

Similarities to Other Species/Conditions

Top of page The adults superficially resemble many other species of the genus Phyllonorycter, but only this species develops on Tilia spp. and the characteristic symptoms of larval damage cannot be confused.

Prevention and Control

Top of page It is possible that during the initial years of its spread, the population density of P. issikii may increase. However, the abiotic factors and the biotic antagonistic species, identical to those that regulate the densities of the related autochthonous taxa, may control this. This is demonstrated most efficiently by the fact that 10-20% parasitism of P. issikii, mostly by wasps of the superfamily Chalcidoidea, was observed during the first year of its discovery and up to 40% parasitism was observed in the following years. Chemical control or other control practices will probably be unnecessary.

References

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Buszko J; Nowacki J, 2000. The Lepidoptera of Poland. A distributional checklist. Polish Entomological Monographs, 1:1-178.

Buszko J; Sefrová H; Lastuvka Z, 2000. Invasive species of Lithocolletinae in Europe and their spreading (Gracillariidae). In: XII European Congress of Lepidopterology SEL, Programme and Abstracts. Bialowieza, Poland, 29 May-2 June 2000, 22-23.

CABI/EPPO, 2011. Phyllonorycter issikii. [Distribution map]. Distribution Maps of Plant Pests, No.June. Wallingford, UK: CABI, Map 751.

Deschka G, 1995. Schmetterlinge als Einwanderer. Stapfia 37, zugleich Kataloge des O+. Landesmuseum N. F., 84:77-128.

Dubatolov VV; Kosterin OE, 2000. Nemoral species of Lepidoptera (Insecta) in Siberia: a novel view on their history and the timing of their range disjunctions. Entomologica Fennica, 11:141-166.

EPPO, 2003. Phyllonorycter issikii. European and Mediterranean Plant Protection Organization, Paris, France. Retrieved September, 15, 2003 from http://www.eppo.org/QUARANTINE/Alert_List/Insects/phissikii.html.

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Ermolaev VP, 1978. [A review of the fauna and ecology of miner-moth (Lepidoptera, Gracillariidae) of the Primorye Territory]. Proceedings of the Zoological Institute. Academy of Sciences of the USSR, 70:98-116 (in Russian).

Graf F; Leutsch H; Nuss M; Stübner A; Wauer S, 2002. Aktuelle Daten zur Kleinschmetterlingsfauna von Sachsen mit Hinweisen zu anderen BundeslSndern (Lep.) III. Entomologische Nachrichten und Berichte, 46:99-104.

Gregor F; Patocka J, 2001. Die Puppen der mitteleuropischen Lithocolletinae (Insecta: Lepidoptera: Gracillariidae). Mitteilungen des Internationalen Entomologischen Vereins e. V. Frankfurt a. M., Suppl. 8:1-176.

Huisman KJ; Koster JC; Muus TST, 2013. Microlepidoptera in The Netherlands in 2007-2010. (Microlepidoptera in Nederland, vooral in 2007-2010: met een terugblik op 30 jaar faunistisch onderzoek.) Entomologische Berichten, 73(3):91-117. http://www.nev.nl

Kozlov MV, 1991. Lithocolletis issikii, a pest of lime. Zashchita Rastenii, No. 4:46

Kumata T, 1963. Taxonomic studies on the Lithocolletinae of Japan (Lepidoptera: Gracillariidae), I.-III. Insecta Matsumurana, 25:53-90, 26:1-48, 26:69-88.

Kumata T, 1978. A new stem-miner of alder in Japan, with a review of the larval transformation in the Gracillariidae (Lepidoptera). Insecta Matsumurana (NS), 13:1-27.

Kumata T, 1993. A contribution to the knowledge of the Malaysian Lithocolletinae (Gracillariidae, Lepidoptera), with a revision of Indian Cameraria associated with Leguminosae [Fabaceae]. Insecta Matsumurana, 48:85 pp.

Kumata T; Kuroko H; Park KT, 1983. Some Korean species of the subfamily Lithocolletin¦ (Gracillariidae, Lepidoptera). Korean Journal of Plant Protection, 22(3):213-227

Kuznetzov VI; Kozlov MV; Seksyaeva SV, 1988. To the systematics and phylogeny of mining moths Gracillariidae, Bucculatriciidae and Lyonetiidae (Lepidoptera) with consideration of functional and comparative morphology of male genitalia. Proceedings of the Zoological Institute. Academy of Sciences of the USSR, 176:52-71 (in Russian with English summary).

Leinonen R; Kaitila J, 2003. Keskilämpötilan nousu näkyy hyönteislajistossa - useiden lajien levinneisyysaule siirtynyt Suomessa satoja kilometrejlä pohjoisemmaksi. Retrieved September, 15, 2003 from http://www.vyh.fi/ajankoht/tiedote/kai/perhoset_03.htm.

Matosevic D, 2008. Newly discovered species of leaf miners of woody plants in Croatia and their danger. (Novounesene invazivne vrste lisnih minera drvenastog bilja u hrvatskoj i njihova stetnost.) Glasilo Biljne Zastite, 8(4):256-261.

Mey W, 1991. Über die Bedeutung autochthoner Parasitoidenkomplexe bei der rezenten Arealexpansion von vier Phyllonorycter-Arten in Europa (Insecta, Lepidoptera, Hymenoptera). Mitteilungen aus dem Zoologischen Museum in Berlin, 67:177-194.

Noreika R, 1998. Phyllonorycter issikii (Kumata) (Lepidoptera, Gracillariidae) in Lithuania. Acta Zoologica Lituanica, Entomologia, 8:34-37.

Orlinskii AD; Shakhramanov IK; Mukhanov SYu; Maslyakov VYu, 1991. Potential quarantine forest pests in the USSR. Zashchita Rastenii, No. 11:37-41

Osipova AS, 1990. Lepidoptera Gracillariidae and its role in the complex of phyllophages of lime trees in Prioksko-Terrasni biospheric reservation. In: Reservations in the USSR - their present and future. Novgorod, 107-109 (in Russian).

Peciulyte D; Kacergius A, 2012. Lecanicillium aphanocladii - a new species to the mycoflora of Lithuania and a new pathogen of tree leaves mining insects. Botanica Lithuanica, 18(2):133-146.

Sefrová H, 2002. Phyllonorycter issikii (Kumata, 1963) - bionomics, ecological impact and spread in Europe (Lepidoptera, Gracillariidae). Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 50(3):99-104.

Sefrová H, 2003. Invasions of Lithocolletinae species in Europe - causes, kinds, limits and ecological impact (Lepidoptera, Gracillariidae). Ekológia (Bratislava), 22:132-142.

Sefrová H; Lastuvka A; Petru M, 2000. Faunistic records from the Czech Republic - 122. Klapalekiana, 36:326.

Szabóky C; Csóka G, 2003. The occurrence of the leaf miner Phyllonorycter issikii Kumata, 1963 Lep. Gracillariidae in Hungary. Novenyvedelem, 39(1):23-24; 2 ref.

Tokár Z; Richter I; Pastorális G; Slamka F, 2002. New and interesting records of Lepidoptera of Slovakia from the years 1998-2001. Entomofauna Carpathica, 14:1-11.

Distribution Maps

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