Abstract: The present study determined egg, larval and pupal parasitoids of the gypsy moth Lymantria dispar L. (Lepidoptera: Lymantriidae), which is an important forest pest in Turkey. High populations of the gypsy moth have been observed recently in oak forests and coniferous forests in the Lakes District of Turkey. Pinus brutia Ten and Cedrus libani A. Rich are reported for the 1st time in the world as host plants of L. dispar. Its parasitoid complex and impact were analyzed in a 2-years study. In larval and pupal stages of the pest, the tachinids Exorista segregata (Rond.), Compsilura concinnata Meigen, Drino inconspicua Meigen and Pales pavida Meigen, the chalcid Brachymeria intermedia (Nees), the torymid Monodontomerus aereus Walk. The braconid Apanteles xanthostigma (Haliday) and the egg parasitoids Ooencrytus kuvanae (Howard) (Hym. Encyrtidae), Anastatus disparis Rusch and Anastatus bifasciatus (Fonsc.) (Hym: Eupelmidae) were recorded. O. kuvanae had the greatest impact on L. dispar populations. A. xanthostigma is a new record for Turkey and also a new record for the world as a parasitoid of L. dispar.
INTRODUCTION
The gypsy moth, Lymantria dispar L. (Lep., Lymantriidae) is one of the most important defoliators of oak forest and is widely disturbed in Europe, Asia and America. Typically, outbreaks are in South and South west Europe and they can almost completely defoliate forests. It is known to be polyphagous on approximately 500 species in orchards and forest stands (Ozdemir, 1993). It feeds on 270 species in Romania, 300 species in Russia and 450 species in the USA. L. dispar is the main defoliator of Quercus, Carpinus, Fagus and Castanea trees in forests stands in Turkey (Oymen, 1982). It becomes a very important pest during outbreaks in the Lakes District Region of Turkey, especially on forest and fruit trees.
L. dispar is univoltine and overwinters in the egg stage. The female lays clusters of eggs in the lower parts of trees in July, they hatch at the end of April and larvae feed from that time to mid-June. Pupation takes place among leaves and the adults appear at the end of June in the Marmara region of Turkey (Oymen, 1982).
Predators and parasitoids are known to play an important role in reducing the population density of L. dispar. However, there is limited information about natural enemies of L. dispar in the forest ecosystem, especially for the Mediterranean region of Turkey.
Therefore, the objectives of the current study were to report on host plants and to determine parasitoids and quantify their impact on different stages of L. dispar in the Lakes District of Turkey.
MATERIALS AND METHODS
Host plants and parasitoids were determined in 2005 and 2006 at 9 forested localities in the Lakes District of south-west Turkey (Table 1).
The parasitoids were reared from L. dispar eggs, larvae and pupae. The eggs were collected from the stems and the larvae and pupae were taken from shoots and leaves of host plants. A total of 8,178 eggs from 144 egg clusters (mean 59.8) and 3,968 mature larvae and pupae were brought to the laboratory in 2005 and 2006. To explore parasitism qualitatively and quantitatively, L. dispar were collected in a stage-specific manner from the study plots. For evaluation of egg parasitism, L. dispar egg masses were collected several weeks before hatching and kept in glass petri dishes at room temperature (22-25°C) in the laboratory. They were checked daily; emerging gypsy moth neonates were removed and parasitoids were collected. Parasitoids were preserved in 80% alcohol prior to identification.
Specimens were also collected from each study plot during the mature larval and pupal stages. Field-collected larvae were reared in groups of 50 in containers (50x50x75 cm) on oak foliage.
| Table 1: | Study areas and their characteristics |
The larvae were checked daily and deceased larvae and larvae from which parasitoids had emerged were removed. Pupae were kept in containers and examined daily throughout the whole emergence period of parasitoids.
RESULTS AND DISCUSSION
New and preferred host plants of L. dispar: L. dispar was determined the most important pest of broad leaf forests in the Lakes District. In all stands, Quercus species were the main host. Pinus brutia Ten and Cedrus libani A. Rich were also host plants, especially in outbreak years and are reported as host plants of L. dispar for the 1st time.
All natural oak species of the region were hosts of the pest (Table 1). The greatest damage occurred in Q. coccifera stands. In these forests, outbreaks of L. dispar occur periodically. In addition to the experimental areas, larval damage was observed on Q. vulcanica in Kasnak Oak Nature Protected area in the Lakes District.
Larvae were observed feeding at high densities on P. brutia in Isparta-Gonen and on C. libani in Isparta Sav. Some trees had lost many of their needles. Eggs, larval and pupal samples were collected from those trees.
The parasitoid complex of L. dispar: Ten species were determined to be parasitoids of L. dispar. Ooencrytus kuvanae (Howard) (Hym.: Encyrtidae), Anastatus disparis Rusch and A. bifasciatus (Fonsc.) (Hym: Eupelmidae) were the egg parasitoids and the larval-pupal parasitoids were Compsilura concinnata Meigen, Exorista segregata (Rond.), Drino inconspicua Meigen, Pales pavida Meigen (Dip. Tachinidae); Brachymeria intermedia (Nees) (Hym.: Chalcididae); Monodontomerus aereus Walk. (Hym.: Torymidae) and Apanteles xanthostigma (Haliday) (Hym.: Braconidae).
| Table 2: | Egg parasitoids of Lymantria dispar in Lakes District |
| Table 3: | Larval and pupal parasitoids of Lymantria dispar in the Lakes District, Turkey |
Table 2 shows the egg parasitoids came from 2 hymenopteran families and Table 3 shows that larval-pupal parasitoids came from 4 dipteran and hymenopteran families.
In this study, 66.3% of the pest eggs were parasitized by 3 solitary parasitoid species. O. kuvanae was by far the most important egg parasitoid, reducing egg numbers by 64.6%. Its highest percentage emergence occurred in September. The other egg parasitoids were A. disparis which achieved parasitism of 0.9% and A. bifasciatus (8%) (Table 2). The strikingly high levels of parasitism by O. kuvanae indicate its singular importance in regulating larval numbers.
The mortality of L. dispar caused by larval and pupal parasitoids was 20.4%. The dipteran Tachinidae family had the largest representation of species (4) in larval and pupal parasitoids. The most important species was E. segregata, which reduced pest numbers by 9.0%, followed by M. aereus (5.8%), B. intermedia (4.5%), D. inconspicua (0.5%), C. concinnata (0.4%), P. pavida (0.1%) and A. xanthostigma (0.1%) (Table 3). A. xanthostigma is reported as a new parasitoid of L. dispar and also as a new record for the Turkish fauna.
In addition, Calosoma sp., particularly Calosoma sycophanta (L.) (Col.: Carabidae), destroyed many L. dispar larvae and pupae. C. sycophanta was abundant at both the larval and adult stages in the study plots.
During the current study at 9 localities in the Lakes District forests of South-West Turkey, 10 species were determined to be parasitoids of L. dispar. In an earlier study in Turkey, C. concinnata, P. pavida, E. segregata, D. inconspicua and B. intermedia were determined as parasitoids of L. dispar. In addition, C. sycophanta was mentioned as a predator. Parasitism rates of L. dispar larvae by C. concinnata were 5-14%, by P. pavida 2-3%, by E. segregate 2-7%, by D. inconspicua 1% and by B. intermedia 1-5% (Oymen, 1982).
Ozdemir (1993) reported O. kuvanae, A. disparis and A. bifasciatus as egg parasitoids. In that study, the hymenopterans Apanteles liparidis (Bouche), A. solitarius Ratz. (Braconidae), M. aereus Walk. (Torymidae) and B. intermedia (Nees) (Chalcididae) and the dipterans D. inconspicua, Zenillia libatrix (Panzer), C. concinnata, P. pavida, Exorista larvarum (L.) and Senometapia separata (Rondani) (Tachinidae), were determined as larval and pupal parasitoids. Also, C. sycophanta, Xylocoris flavipes Reuter, Cardiastethus nazarenus Reuter and Orius alpidipennis Reuter (Hem. Anthocoridae) were noted as predators of L. dispar.
The study of Ozkan (1988) recorded O. kuvanae for the 1st time in Turkey. Parasitism of L. dispar eggs by this species varied between 80 and 96%, compared to 64.6% in the current study. Kara and Tschorsnig (2003) reported C. concinnata, E. larvarum, E. segregata, D. inconspicua, S. separata, Z. libatrix, P. pavida and P. processioneae as tachinid parasitoids of L. dispar. Four of those species were recorded in the current study (Table 3).
The natural enemies of L. dispar have been studied throughout its known range. Among these studies, Hoch et al. (2006) recorded Glyptapanteles liparidis, G. porthetriae (Hym. Braconidae), B. intermedia (Hym. Chalcididae); Parasetigena silvestris, Z. libatrix, Blepharipa sp. (Dip. Tachinidae) and C. sycophanta as natural enemies of L. dispar in Austria. Zubrik and Novotny (1997) reported A. disparis and O. kuvanae as egg parasitoids of L. dispar in Slovakia. The total parasitization was 0.34% and A. disparis had 79.5% and O. kuvanae had 20.5% of that total. In contrast to Slovakia, the current study showed total parasitization by both species was much higher.
Among 28 species determined as egg, larval and pupal parasitoids by Hoch et al. (2001) in Austria, O. kuvanae, A. disparis, B. intermedia, D. inconspicua, C. concinnata and P. pavida were recorded in the current study. The much higher parasitoid diversity in the Austrian study may reflect more benign climatic conditions and greater ecological diversity generally in their study area. In a study conducted in the USA, Fuester et al. (2001) recorded Aphantorhaphopsis samarensis (Dip. Tachinidae) among the larval parasitoids. Brown and Cameron (1982) reported O. kuvanae, Dibrachys cavus (Walker) (Hym. Pteromalidae) and Pediobius sp. (Hym. Eulophidae) as egg parasitoids of L. dispar in Pennsylvania. In the same study, primarily ants (Hym. Formicidae); larvae of Cantharidae, Dermestidae and Trogositidae (Coleoptera), Chrysopidae (Neuroptera) species and Pentatomidae (Hemiptera) species, were reported as predators, with an average predation of 11%.
ACKNOWLEDGEMENTS
I would like to thank Prof. Dr. Ahmet Beyarslan (Trakya University), Prof. Dr. Miktat Doganlar (Mustafa Kemal University) and Assoc. Prof. Dr. Kenan Kara (Gaziosmanpaþa University) for identification of parasitoids and Gregory T. Sullivan of Ondokuz Mayis University in Samsun for English editing.