Parasitoid complexes (Hymenoptera, Eulophidae) of leafminers of the genus Phyllonorycter (Lepidoptera, Gracillariidae) in the Middle Volga Basin

ISSN 0013-8738, Entomological Review, 2009, Vol. 89, No. 8, pp. 903–911. © Pleiades Publishing, Inc., 2009. Original Russian Text © Z.A. Yefremova, A.V. Krayushkina, A.V. Mishchenko, 2009, published in Zoologicheskii Zhurnal, 2009, Vol. 88, No. 10, pp. 1213–1221.

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Parasitoid Complexes (Hymenoptera, Eulophidae) of Leafminers of the Genus Phyllonorycter (Lepidoptera, Gracillariidae)

in the Middle Volga Basin Z. A. Yefremova, A. V. Krayushkina, and A. V. Mishchenko

Ul’yanovsk State Pedagogical University, Ul’yanovsk, 432700 Russia e-mail: [email protected]

Received June 10, 2008

Abstract—The parasitoid complexes of 22 species of the genus Phyllonorycter reared from 20 host plants were studied in the Middle Volga Basin. From a total of 124 host-parasitoid associations analyzed, 88 had been previ-ously unknown. Minotetrastichus frontalis, Sympiesis sericeicornis, Pnigalio soemius, Closterocerus formosus, and S. gordius were the most frequent species. The highest percentage of parasitoids reared was observed in Ph. ulmifo-liella (58.6%) and Ph. sylvella (54%), and the lowest one, in Ph. salictella (15%). Ph. corylifoliella (95.7%), Ph. populifoiella (95.5%) and Ph. insignitella (95.5%) had the highest mortality due to parasitoids. The number of endoparasitoid species prevailed over that of ectoparasitoids in the parasitoid complexes of the genus Phyl-lonorycter, but the number of individuals reared was 4 times greater for ectoparasitoids. The parasitoid complexes were the most similar in Ph. harrisella and Ph. quercifoliella on Quercus robur. The gregarious ectoparasitoid M. frontalis predominated over parasitoids of Phyllonorycter. DOI: 10.1134/S0013873809080041

The parasitoid associations of leafminers of the ge-nus Phyllonorycter were studied in detail by British entomologists in the 1970s. In Great Britain, the asso-ciations of 23 leafminer species and their parasitoids were examined (Askew and Shaw, 1974, 1979a, 1979b). The first generation of Phyllonorycter was shown to have high mortality rates due to ectoparasi-toids, while endoparasitoids prevailed in the second generation. Later, it was demonstrated that the rate of eulophid infestation of invasive Phyllonorycter spe-cies was not higher than that of local leafminers of this genus (Godfray et al., 1995). A.S. Rott and H.C.J. Godfray (2000) analyzed the structure of para-sitoid complexes of 12 Phyllonorycter species and characterized the effect of the number of emerging females on the abundance of the subsequent moth generation. There were publications devoted to parasi-toid complexes of some species of Phyllonorycter: Ph. corylifoliella Hw. (Fry, 1989; Vidal, 1993; Bel-lostas et al., 1998; Balazs and Thuroczy, 2000; To-mov, 2001, 2002; Rizzo and Massa, 2002; Mineo et al., 2003; Amiri et al., 2008), Ph. cerasicolella H.-Sch. (Hansson, 1985; Vidal, 1993), Ph. emberizaepen-nella Bouche (Askew and Shaw, 1974; Hansson, 1985, 1987; Yefremova and Erlebach, 2001), Ph. populifo-liella Tr. (Sulkhanov, 1990), and Ph. issikii Kumata

(Mey, 1991; Ikeda, 1996; Kamijo and Ikeda, 1997; Yefremova and Mishchenko, 2008). Some data were obtained on parasitoids of Ph. medicaginella Grsm. (Mey, 1991; Vidal, 1993), Ph. pomonella Z. (Askew and Coshan, 1973; Vidal, 1993), Ph. pyrifoliella Grsm. (Tomov, 2001, 2002), Ph. salictella Z. (Haesel-barth, 1985), Ph. sorbi Frey (Hansson, 1985, 1987), and Ph. ulmifoliella Hbn. (Askew and Shaw, 1979) in Europe. There are interesting data on parasitoids of 11 Phyllonorycter species distributed in the US (Davis and Deshka, 2001), of which only one species, Ph. ap-parella H.-Sch., occurs in the Middle Volga Basin. In Russia, the species composition of the parasitoid com-plex was studied only for the poplar leaf miner Phyl-lonorycter populifoliella (Sulkhanov, 1990). The eulo-phid assemblage comprised both ecto- and endoparasi-toid forms. The dominant species, not identified to species, belonged to the genus Chrysocharis. The sec-ond dominant species, Sympiesis gordius (Walker), is included in the parasitoid complex of the poplar moth in the Middle Volga Basin as well.

The genus Phyllonorycter has a ubiquitous distribu-tion, comprising 244 species in the Palaearctic Region (De Prins and De Prins, 2005). A considerably smaller number, about 150 species, occur in European Russia (Kuznetsov, 1981; Kuznetsov and Baryshnikova,

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1998); of these, 28 have been found in Ul’yanovsk Province (Mishchenko and Zolotukhin, 2003).

The aim of our work was to characterize the species composition of leafminer parasitoids in the Middle Volga Basin, to study all the possible host-parasitoid associations, and to estimate the mortality rates of different Phyllonorycter species due to ecto- and endoparasitoids.

MATERIALS AND METHODS

The field and laboratory studies were carried out in 24 localities within the forest-steppe zone of Ul’yanovsk Province (52–54° N, 46–49° E). The taxo-nomic composition of leafminer moths and their para-sitoids was studied by rearing them from leaf mines in 2004–2007. The leaves with mines were collected from the lower crown level (0.5–2.5 m above the ground) in June–September. The mines were cut from the laminae and kept in 0.5 l plastic bags at 23 ± 5°C until the moths and their parasitoids emerged. If the mines at the moment of sampling were smaller than 0.1 cm2, whole branches with leaves were kept in the water until the mines grew to 1–2 cm2. The moths emerged 7–10 days, and the parasitoids, 10–14 days after pupation. The parasitoids were reared separately from each host. The species of Phyllonorycter were identified by A.V. Mishchenko using the key compiled by V.I. Kuznetsov (1981). The frequency of occur-rence of each parasitoid species, the total abundance of parasitoids, and partial rates of infestation by ecto- and endoparasitoids were determined. The results were processed using the following formulae:

22

11

%100

i i

iba

kP , where P1 is the frequency of oc-

currence of each parasitoid species, k is the number of parasitic complexes, ai is the number of parasitoids of a particular species reared in the given complex, and bi is the total number of parasitoids reared in this com-plex;

10012

Nn

P , where P2 is the emergence rate of

parasitoids (%), n1 is the number of parasitoids reared, and N is the number of mines collected;

10021

33

nnn

P , where P3 is the partial rate of in-

festation by ectoparasitoids (%) for each Phyl-lonorycter species, n1 is the number of parasitoids

reared, n2 is the number of moths reared, and n3 is the number of ectoparasitoids reared;

10021

44

nnnP , where P4 is the partial rate of in-

festation by ectoparasitoids (%) for each Phyl-lonorycter species, n1 is the number of parasitoids reared, n2 is the number of moths reared, and n4 is the number of endoparasitoids reared.

RESULTS AND DISCUSSION In all, 278 individuals of leafminer moths, belong-

ing to 22 species of the genus Phyllonorycter, were reared from mines collected on 20 species of host plants, belonging to 14 genera from 9 families (Table 1). It is interesting that Ph. schreberella was for the first time reared from mines collected from the smoothleaf elm Ulmus caprinifolia, previously re-corded only in Astrakhan Province (Puplesis et al., 1991). This species was previously found only on U. scabra and U. foliacea (Kuznetsov and Baryshnik-ova, 1998). The best studied species were Ph. compar-ella on Populus alba, Ph. issikii on Tilia cordata, and T. platyphyllos and Ph. ulmifoliella on Cerasus fruti-cosa. The greatest number of mines was observed on T. cordata. In 2007, the moth Ph. comparella was observed to form mines on the poplar Populus alba more actively than in the preceding seasons. Most species of the genus Phyllonorycter form 1–2 mines per leaf. Their larvae make peculiar blotchy, folded, or vesicular mines on the upper or the lower part of the leaf lamina. The Phyllonorycter leafminers in Ul’yanovsk Province develop in 2 generations, less frequently in 3 generations (Ph. issikii; see Yefremova and Mishchenko, 2008). The flight starts when the mean daily temperature rises above 10°C, which in the Middle Volga Basin takes place in mid-May–early June. Mining usually starts in early June and lasts until the end of September. Most leafminer species develop on deciduous trees, and only Ph. insignitella and Ph. medicaginella, on herbaceous plants. The first mines to appear are those of Ph. issikii, Ph. apparella, Ph. sylvella, and Ph. comparella. The larvae develop with 5 instars, ranging in size from 1 mm (I instar) to 5 mm (V instar). The larvae pupate inside the mines 7–10 days after hatching. The rates of larval mortality caused by weather conditions, fungal infections, and predation by birds are much lower than mortality due to ectoparasitic eulophids infesting III–V instar larvae (Askew and Shaw, 1979). Some endoparasitoids may already infest I instar larvae (Bryan, 1980, 1983).

PARASITOID COMPLEXES (HYMENOPTERA, EULOPHIDAE)


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The leafminer moths have specific parasitoid com-plexes. Mischotetrastichus petiolatus (Erdos) was found on Ph. issikii in the Middle Volga Basin. This species was previously recorded in the parasitoid complex of the same host in Japan (Kamijo and Ikeda, 1997).

In all, 907 individuals of parasitoids were reared, belonging to 36 eulophid species (Table 2) from three subfamilies: Eulophinae (15 species, 368 ind.), Ente-doninae (17 species, 286 ind.), and Tetrastichinae (4 species, 253 ind.). The subfamily Entedoninae had the greatest species diversity, and Eulophinae pre-

Fig. 1. Occurrence of eulophid parasitoids in the parasite complexes examined. Ordinate: ratio of occurrence of each parasitoid species (P1, %) to the number of complexes in which it was found (K). The parasitoid species: Minotetrastichus frontalis (1), Sympiesis gordius(2), S. sericeicornis (3), Closterocerus formosa (4), Pnigalio soemius (5), Chrysocharis phryne (6), Ch. laomedon (7), Ch. alpinus (8), Ch. pubicornis (9), Cirrospilus elegantissimus (10), S. gregori (11), Hemiptarsenus ornatus (12), Pediobius cassidae (13), Cirrospilus viticola (14), Achrysocharoides butus (15), Neochrysocharis aratus (16), P. routensis (17), Diaulinopsis arenaria (18), Hyssopus geni-culatus (19), Pnigalio nemati (20), Chrysocharis sp. (21), Ch. nephereus (22), Omphale rubigus (23), P. metallicus (24), C. lyncus (25), Aprostocetus sp. n. (26), C. pictus (27), Pnigalio pectinicornis (28), Elachertus pulcher (29), Ch. amyite (30), P. crassicornis (31), Neochrysoharis sp. (32), P. acanthi (33), C. diallus (34), M. petiolatus (35), and Oomyzus incertus (36).

Table 3. Degree of knowledge of host-parasitoid associations of the genus Phyllonorycter in the Middle Volga Basin Families

of host plants Number of Phyl-

lonorycter species Number of parasi-

toid species Number of possi-ble associations

Number of stud-ied associations

Fraction of studied asso-ciations, %

Aceraceae 1 2 2 2 100 Betulaceae 2 10 20 11 55.00 Caprifoliaceae 1 13 13 13 100 Fabaceae 2 7 14 8 57.14 Fagaceae 2 4 8 5 62.50 Rosaceae 5 17 85 32 37.65 Salicaceae 6 16 96 30 31.25 Tiliaceae 1 16 16 16 100 Ulmaceae 2 6 12 7 58.33 Total 22 36 266 124 46.27

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vailed with respect to the number of individuals reared. Although most eulophid species have already been found in the Middle Volga fauna (Yefremova et al., 2000; Yefremova, 2002; Yefremova and Mishchenko, 2008), such species as Achrysocharis butus (Walker 1839), Chrysocharis amyite (Walker 1839), C. nephrereus (Walker 1839), C. pubicornis (Zetterstedt 1838), Neochrysocharis aratus (Walker 1838), Pediobius crassicornis (Thomson 1878), and M. petiolatus are reported here for the first time from the region under investigation.

We have studied 124 host-parasitoid associations, or 46.3% of the theoretically possible number (266; see Table 3). Data on 88 associations are reported here for the first time (Table 2). The prevalent species with respect to the number of individuals were Sympiesis gordius (Walker 1839), M. frontalis (Nees 1834), and C. laomedon (Walker 1839). More adequate parame-ters are the number and frequency of occurrence of parasitoid complexes of different Phyllonorycter spe-cies (Fig. 1). The first place in term of occurrence was shared by M. frontalis and S. sericeicornis (Nees

1834), the second place was occupied by Pnigalio soemius (Walker 1839), and the third, by Closteroce-rus formosus Westwood 1833. Although the occur-rence of S. gordius (Walker 1839), C. laomedon, and Hyssopus geniculatus (Hartig 1838) was generally lower, these species prevailed on some hosts, in par-ticular, on Phyllonorycter issiki.

The number of species reared and their relative abundance was compared to those of the moth larvae and pupae (Fig. 2). The greatest percentage of parasi-toid emergence was observed in Ph. ulmifoliella (59%), Ph. sylvella (54%), and Ph. insignitella (53%), and the smallest, in Ph. populifoliella, Ph. sagitella, and Ph. salictella. The populations of Ph. ulmifoliella and Ph. sylvella appear to be most significantly con-trolled by parasitoids.

The effect of parasitoids on survival of leafminer moths was estimated by determining the rates of infes-tation of each Phyllonorycter species (Table 4). The highest infestation by ecto- and endoparasitoids was observed in Ph. corylifoliella, Ph. populifoliella,

Fig. 2. Parasitoid emergence rate and the number of parasitoid species infesting different species of Phyllonorycter. Ordinate: ratio of emergence rate (P2, %) to the number of parasitoid species controlling the particular most species (L). Species of Phyllonorycter: Ph. ulmifoliella (1), Ph. sylvella (2), Ph. insignitella (3), Ph. harrisella (4), Ph. emberizaepennella (5), Ph. cerasicolella (6), Ph. coryli(7), Ph. comparella (8), Ph. apparella (9), Ph. corylifoliella (10), Ph. pomonella (11), Ph. medicaginella (12), Ph. agilella (13), Ph. schreberella (14), Ph. pastorella (15), Ph. pyrifoliella (16), Ph. sorbi (17), Ph. issikii (18), Ph. quercifoliella (19), Ph. populifoliella(20), Ph. sagitella (21), and Ph. salictella (22).



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Ph. insignitella, and Ph. pastorella, indicating the highest mortality of these species due to parasitoids. The lowest mortality was recorded in Ph. coryli and Ph. pomonella. The introduced species Ph. issikii re-vealed a comparatively high mortality rate: 74.2%.

The group of 36 eulophid species included 20 endo-parasitoid’s and 16 ectoparasitoid’s species. The ratio of the number of ectoparasitoids (723 ind.) and endoparasitoids (184 ind.) was about 4 : 1. The parasi-toid complexes of Ph. populifoliella, Ph. schrebella, Ph. sagitella, and Ph. sylvella included only ectopara-sitoids, and in 9 more leafminer species this group prevailed. Such species as Ph. corylifoliella and Ph. pyrifoliella showed the same mortality rate due to ecto- and endoparasitoids. Endoparasitoids prevailed in the complexes of Ph. cerasicolella, Ph. emberiza-epennella, Ph. insignitella, Ph. pomonella, Ph. salic-tella, and Ph. sorbi, whereas the complex of Ph. coryli comprised only endoparasitoids. Mortality due to ec-toparasitoids was about 60%, and due to endoparasi-toids, 16%.

All reared eulophids are parasites of larvae and pu-pae, most of them are solitary. The hosts of gregarious parasitoids should have larger larvae than those of solitary parasitoids. Such species are, for example, Ph. salictella and Ph. sorbi, from which the parasitoid M. frontalis was reared in 2006 (Yefremova and Mishchenko, 2008). M. frontalis develops as a gre-garious parasitoid on the larvae of Ph. issikii, Ph. comparella, Ph. sylvella, and Ph. ulmifoliella, and as a solitary parasitoid on Ph. agilella, Ph. sagitella, Ph. emberizaepennella, Ph. harrisella, Ph. quercifo-liella, Ph. salictella, and Ph. sorbi. The parasitoid P. soemius may become gregarious on Ph. issikii while being solitary on the rest of the hosts. The ectoparasi-toid larvae are more than 3 times smaller than the larva of Phyllonorycter issikii (on average 6 to 8 mm).

The greatest similarity (25%) of the species compo-sition of parasitoid complexes was observed in Ph. harrisella and Ph. quercifoliella on Quercus ro-bur. The species composition of parasitoids changes when the leafminer changes one feeding plant for an-other one, for example, Ph. issikii spreading from T. cordata onto T. platyphyllos.

In conclusion, it should be noted that the biological resources of parasitoids of Phyllonorycter leafminers facilitates the ecosystem stability: defoliation of the host plants was never observed in the Middle Volga Basin.

ACKNOWLEDGMENTS

The authors are grateful to S.V. Baryshnikova (the Zoological Institute, RAS) for help with identification of some species of the genus Phyllonorycter.

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Table 4. Ecto- (P3) and endoparasitism (P4) on Phyl-lonorycter species, %

Species of Phyllonorycter P3 P4

Ph. agilella 77.78 11.11 Ph. apparella 42.86 14.29 Ph. cerasicolella 11.11 77.78 Ph. comparella 54.35 17.39 Ph. coryli 0 33.33 Ph. corylifoliella 47.83 47.83 Ph. emberizaepennella 22.86 68.57 Ph. harrisella 42.86 14.29 Ph. insignitella 40.91 54.55 Ph. issikii 66.11 8.09 Ph. medicaginella 50.00 12.50 Ph. pastorella 36.11 27.78 Ph. pomonella 45.45 50.00 Ph. populifoliella 33.33 0 Ph. pyrifoliella 45.45 45.45 Ph. quercifoliella 50.00 25.00 Ph. sagitella 40.00 0 Ph. salictella 18.75 75.00 Ph. schreberella 60.00 0 Ph. sorbi 37.50 43.75 Ph. sylvella 95.24 0 Ph. ulmifoliella 50.00 16.67

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Parasitoid complexes (Hymenoptera, Eulophidae) of leafminers of the genus Phyllonorycter (Lepidoptera, Gracillariidae) in the Middle Volga Basin