## Parasitoids of Phyllonorycter populifoliella (Treitschke, 1833) on Populus balsamifera L. (Salicaceae) in western European Russia (Lepidoptera: Gracillariidae)

### Parasitoides de Phyllonorycter populifoliella (Treitschke, 1833) sobre Populus balsamífera L. (Salicaceae) en el oeste europeo de Rusia (Lepidoptera: Gracillariidae)

I. V. Ermolaev ermolaev-i@udm.net
Nechkinskii National Park, Rusia
Z. A. Yefremova * eulophids@mail.ru
Ulyanovsk State Pedagogical University, Rusia The George S. Wise Faculty of Life Sciences Tel-Aviv University, Israel
A. V. Trubitsyn izhevskman@mail.ru
Nechkinskii National Park, Rusia

Abstract: The assemblage of hymenopteran parasitoids associated with the poplar leaf blotch miner moth Phyllonorycter populifoliella (Treitschke, 1833) (Lepidoptera: Gracillariidae) developing on the Balsam Poplar (Populus balsamifera L., 1753) was studied in Izhevsk. The assemblage included 35 species of parasitoids belonging to the Eulophidae (Eulophinae, Entedoninae, and Tetrastichinae), Pteromalidae, Encyrtidae, Ichneumonidae, and Braconidae, with 18 species being reported as Ph. populifoliella parasitoids for the first time. Sympiesis sericeicornis, Chrysocharis laomedon and Sympiesis gordius were major elements of the assemblage. While S. gordius showed a confident negative correlation with the population density of the miner, none of the other two species had confident relationships with the population density of the host. Possible causes of the low efficacy of the parasitoid assemblage on Ph. populifoliella population are briefly outlined.

Keywords: Lepidoptera, Gracillariidae, Hymenoptera, Eulophidae, parasitoids, Phyllonorycter populifoliella , Balsam Poplar, population dynamics, Russia.

Resumen: Fue estudiado en Izhevsk la asociación de himenópteros parasitoides asociados al minador de hojas Phyllonorycter populifoliella (Treitschke, 1833) desarrollándose sobre el álamo balsemífero (Populus balsamifera L., 1753). La asociación de parasitoides incluyen 35 especies perteneciendo a los Eulophidae (Eulophinae, Entedoninae y Tetrastichinae), Pteromalidae, Encyrtidae, Ichneumonidae y Braconidae, con 18 especies que se citan por primera vez sobre Ph. populifoliella. Sympiesis sericeicornis, Chrysocharis laomedon . Sympiesis gordius fueron los más abundantes. Mientras que S. gordius mostraba una correlación negativa con la densidad de población del minador, ninguna de las otras dos especies estaban relacionadas con la densidad de la planta del minador. Se da una idea general de las posibles causas de la baja eficacia de las reunión de parasitoides sobre la población de Ph. populifoliella.

Palabras clave: Lepidoptera, Gracillariidae, Hymenoptera, Eulophidae, parasitoides, Phyllonorycter populifoliella , álamo balsamífero, dinámica de poblaciones, Rusia.

### Introduction

The poplar leaf blotch miner moth Phyllonorycter populifoliella (Treitschke, 1833) (Lepidoptera: Gracillariidae) is a typical Palaearctic species (DAVIS & DESCHKA, 2001) and a common element in the fauna of populated areas in the European Russia (POLEZHAEV, 1934; RUMYANTSEV, 1934; STROKOV, 1956; BELOVA, 1981, 1985; BELOVA & VORONTSOV, 1987; SULKHANOV, 1990, 1992; BONDARENKO, 2008; YEFREMOVA et al., 2009, 2011; SELIKHOVKIN, 2010), Western Siberia (BARANNIK, 1979; GRODNITSKIY, 1997; KOLOMIETS & BOGDANOVA, 1992; BAKULIN, 2005; EREMEEVA, 2008; SELIKHOVKIN, 2010), Eastern Siberia (FROLOV, 1948; TOMILOVA, 1973; SELIKHOVKIN, 2010), and Far East (YURCHENKO, 2006).

Occasional outbreaks of the moth may last considerable length of time. Thus, the eruptive (>1 mine per leaf) density of the moth population was observed in 1969-1980 in some parks of Yekaterinburg (DANILOVA et al., 1984). An outbreak of the miner in Moscow lasted from 1974-1989 (BELOVA, 1994).

Analysis of the taxonomic composition of parasitoids of Ph. populifoliella is fragmentary and represented in only few publications. Studied are some areas in Europe (FULMEK, 1962; BOUÈEK & ASKEW, 1968), the Caucasus (MIRZOYAN, 1977), Iran (ZARGARAN et al., 2010; SADEGHI & LOTFALIZADEH, 2013), and Kyrgyzstan (ROMANENKO, 1959). In Russia, Moscow received the best coverage (POLEZHAEV, 1934; RUMYANTSEV, 1934; STROKOV, 1956; BELOVA, 1981, 1985; BELOVA & VORONTSOV, 1987; SULKHANOV, 1990, 1992). Some information exists for St. Petersburg (STROKOV, 1956), Ulyanovsk Region (YEFREMOVA et al., 2009, 2011) and Maritime Territory (ALEEKSEEV et al., 2012).

According to published data, the assemblage of Ph. populifoliella parasitoids includes 48 species (Table 1). Representatives of Eulophidae constitute 82.6%, Ichneumonidae and Braconidae make up 6.5%, while Pteromalidae and Encyrtidae amount to 2.2%. The assemblage also includes unidentified species in the following genera: Pteromalus and Eulophus (RUMYANTSEV, 1934; FULMEK, 1962; ZARGARAN et al., 2010), Pnigalio (MIRZOYAN, 1977; BELOVA, 1985; BELOVA & VORONTSOV, 1987; SULKHANOV, 1990, 1992), Sympiesis (MIRZOYAN, 1977; SULKHANOV, 1990, 1992), Cirrospilus (POLEZHAEV, 1934; RUMYANTSEV, 1934; FULMEK, 1962), Derostenus (ROMANENKO, 1959; FULMEK, 1962), Chrysocharis (BELOVA, 1981; SULKHANOV, 1990, 1992; FULMEK, 1962), Tetrastichus (POLEZHAEV, 1934; ROMANENKO, 1959), and Mesochorus (SULKHANOV, 1990, 1992).

All previous studies dealt with parasitoids of the poplar leaf blotch miner moth developing on the Black Poplar (Populus nigra L., 1753). Our research targeted the species composition of parasitoid assemblage of the poplar leaf blotch miner moth Ph. populifoliella developing on the Balsam Poplar (Populus balsamifera L., 1753) in Izhevsk and its role in the miner outbreak control. The natural distribution of the Balsam Poplar covers northern regions of the USA and almost entire Canada. In Russia, it naturally occurs only in the eastern Chukotka where it forms low shrubs (KATENIN, 1993). The Balsam Poplar is commonly used for planting green belts in European Russia (e.g., URAZGILDIN et al., 1997; IGNATJEVA & KONECHNAYA, 2004; BUKHARINA et al., 2012; MINGALEVA, 2012), the Urals, Western and Eastern Siberia (DANILOVA, 1970; BAKULIN, 1990; SELENINA et al., 2011; SOKOLOVA et al., 2011; VOITYUK, 2011; RUNOVA & GNATOVICH, 2013).

##### Table 1
Parasitoids of Ph. populifoliella based on published data.

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### Material and methods

The study was conducted in Izhevsk, the capital of the Udmurt Republic that occupies 42,100 km2 in the Vyatka-Kama interfluve. Izhevsk (56º 51’ 00” N, 53º 13’ 59” E) is a large (333.2 km2) city with population over 610,000.

The assessment of survival and parasitoid infestation rate of larvae and pupae of the first generation of the miner was done in the field in 2010. In various parts of the city (including both the centre and suburbs), forty-one Balsam Poplar trees (P. balsamifera) (Fig. 1) were selected with the infestation density of 0.4-20 mines per leaf. We divided the sample into two groups. Group I included leaves with miner density of 0-10 mines per leaf (22 trees); group II included leaves with miner density of 10-20 mines per leaf (19 trees).

During moth pupation, the average of 60 mined leaves was collected from first-order branches in the lower crown of the northern exposition of each tree. In total, 4338 mines were cut out with scissors and placed in labelled Petri dishes. Emerging moths and parasitoids were recorded daily. Over 2978 Ph. populifoliella and 345 parasitoid specimens were reared during the course of the study.

The following indicators were calculated: the density of the first-generation moths on each tree = (total number of mines on three branches in the lower crown) × (total number of leaves on these branches)-1, as number of mines per 100 leaves; survival rate of pupae = (number of moths emerged from mines) × (total number of collected mines)-1 × 100%; moth mortality rate caused by parasitoids = (total number of parasitoids) × (total number of collected mines)-1 × 100% (ERMOLAEV et al., 2011).

The arithmetic mean and error were calculated in each case. The linear correlation (IVANTER & KOROSOV, 2011) was used for the statistical treatment of the material. The significance of differences between samples was estimated by Student’s .-test. Percentages were normalized by j=2arcsin Öc — transformation.

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Figure 1
Schematic distribution of 41 sampled balsam poplar trees (Populus balsamifera L.) in Izhevsk.

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### Results and discussion

The poplar leaf blotch miner moth gives periodical outbreaks in Izhevsk. The last one started in 2002 and ended by the autumn 2010 due to unusually hot weather.

The miner can produce two generations a year under the environmental conditions of Izhevsk (Table 2). Overwintering moths appear on poplar tree trunks by the time when leaves start unfolding (beginning of May), and copulate soon afterwards. Gravid females lay eggs between leaf veins, mainly on the lower surface. Caterpillars finish feeding by the end of June. The pupal stage lasts for about ten days. The mass eclosion of adults happens before or around mid-July. The second generation of the moth develops during August-September, and often does not complete its cycle die due to low temperatures. Adults overwinter in bark crevices, as well as in cracks and on uneven surfaces of nearby buildings.

##### Table 2
Phenology of the poplar leaf blotch miner moth Ph. populifoliella in Izhevsk in 2010.

#####

In the field lab, Ph. populifoliella moth eclosion was observed from 5-21 July, i.e. over 17 days (Fig. 2). The majority of adults emerged on 10 July. The survival rate of the first generation pupae was positively and confidently linked to the average density of the moth population (.=0.29, .=41, .<0.05) and constituted 63.7±2.7%.

The mortality rate of pupae was 36.3±2.7% and was in inverse relationship with the population density (.=-0.29, .=41, .<0.05). Mortality due to unknown causes constituted 29.0±2.6%, mortality caused by parasitoids was 7.3±0.7%.

In group I the total mortality is 38.5±2.9 % (7.7±1.0% due to parasitoid effect and 30.8±3.1% due to an unknown factor), and in group II the total mortality is 33.7±4.7% (6.8±0.9.0% due to parasitoids and 33.7±4.71% due to an unknown factor). Our results have demonstrated the absence of significant differences (P<0.05) between these parameters at variable miner density.

In the former case, the confident relationship with the population density of the miner was not established (.=-0.22, .=41, .>0.05); in the latter, the correlation was significantly positive (.=0.45, .=41, .<0.05). Coefficient of correlation between mortality and miner density per leaf in group I due to parasitoids is .=0.22 and due to an unknown factor is -0.10, and in group II due to parasitoids is -0.48 (. < 0.05) and due to an unknown factor is -0.37.

The emergence of parasitoids was observed from 5-23 July, with maximum numbers on 11 July (Fig. 2).

#####
Figure 2
Dynamics of Ph. populifoliella and its parasitoids eclosion in the field lab 2010.

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Our study resulted in the discovery of 35 species of parasitoids belonging to three subfamilies of the Eulophidae (Eulophinae, Entedoninae, and Tetrastichinae), as well as to the families Pteromalidae, Encyrtidae, Ichneumonidae, and Braconidae (Table 3). Eighteen species have been reported as the miner parasitoids for the first time, viz Pnigalio mediterraneus, Elachertus fenestratus, Elachertus gallicus, Elachertus sp., Pediobius metallicus, Chrysocharis amanus, Chrysocharis crassiscapus, Chrysocharis gemma, Chrysocharis laomedon, Chrysocharis pentheus, Chrysocharis phryne, Chrysocharis pubicornis, Chrysocharis prodice, Chrysocharis viridis, Chrysocharis sp., Neochrysocharis aratus, Neochrysocharis cuprifrons, and Neochrysocharis formosa.

##### Table 3
The share of Ph. populifoliella parasitoids. The asterisk denotes an ectoparasitoid. In all cases, n = 41.

#####

The assemblage of Ph. populifoliella parasitoids was apparently formed by polyphages that actively attack various members of Gracillariidae, Nepticulidae, Tischeriidae, Tortricidae and some families of Coleoptera. Thus, fifteen species of parasitoids in Izhevsk are common for both the poplar leaf blotch miner moth and the lime leaf miner Ph. issikii Kumata, 1963 (ERMOLAEV et al., 2011): Pnigalio soemius, Sympiesis dolichogaster, S. gordius, S. sericeicornis, Cirrospilus diallus, C. lyncus, C. pictus, Elachertus fenestratus, Chrysocharis laomedon, Ch. nephereus, Ch. phryne, Ch. pubicornis, Neochrysocharis cuprifrons, N. formosa, and Minotetrastichus frontalis. The ratio of ecto- and endoparasitoids in the parasitoid assemblage of Ph. populifoliella is 16:19 (Table 2).

The core of the parasitoid assemblage of the poplar leaf blotch miner moth in Izhevsk consists of Sympiesis sericeicornis (22.6%), Chrysocharis laomedon (17.2%) and Sympiesis gordius (14.2%). The species S. sericeicornis is a predominantly solitary primary or secondary ectoparasitoid of caterpillars and pupae of mining moths, including representatives of Phyllonorycter (BOUÈEK & ASKEW, 1968). Chrysocharis laomedon is a primary (sometimes secondary) solitary endoparasitoid, also favouring caterpillars and pupae of Gracillariidae moths (BOUÈEK & ASKEW, 1968). Sympiesis gordius is a solitary ectoparasitoid, which acts mostly as a primary parasite and infest caterpillars and pupae of a number of hymenopteran and lepidopteran families, favouring caterpillars of the genus Phyllonorycter (Gracillariidae) (BOUÈEK & ASKEW, 1968).

Neither S. sericeicornis nor C. laomedon had significant relationships with the population density of the host (.=-0.02, .=41, .>0.05 and .=0.13, .=41, .>0.05, correspondingly). Of the three species, only S. gordius showed a significant negative correlation of it’s parasitism. Coefficient of correlation between mortality and the density of the miner in group I is -0.45 (.<0.05) and in group II is 0.20.

The absence of the effect of parasitoids on the population density of the miner is apparently a usual phenomenon in a large city. The negative correlation of the level of Ph. populifoliella parasitism and the average population density of the moth on unspecified species and hybrids of Populus had been shown for Moscow (SULKHANOV, 1995a). Inefficacy of parasitoids in centres of cities is complex and defined by at least three factors. First, this is destruction of natural overwintering sites by man. It is widely known that most parasitoids overwinter in leaf litter. Continuous collection, removal and destruction of fallen leaves results in decreasing number of entomophages. Second, this is an exceptionally low number of flowering plants that may provide additional food to parasitoids during the maturation of eggs. Third, a high level of the air pollution inevitably leads to shrinking of the parasitoid species diversity from the periphery to the city centre (SULKHANOV, 1995b).

### Acknowledgments

Dr Sergey Sinev (Zoological Institution, Russian Academy of Sciences, St. Petersburg, Russia) is thanked for encouraging the study of hymenopteran parasitoids associated with the poplar leaf blotch miner moth in Udmurtia.

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### Author notes

* Autor para la correspondencia / Corresponding author