Gypsy moth (Lepidoptera: Lymantriidae) in ...

Gvpsvrnoth

(Lepidoptera: Lymantriidae)

in Cenal Asia Almazbek

A.Orozumbekov,

Andrew M. Liebhold, Vasily I.Ponomarev,

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Fig. 1. World distribution of the gypsy moth (shaded area) modified from Giese & Schneider (1979). Rectangle corresponds to Central Asia region shown in Fig. 2. 258

Asia appear to exhibit a broader range of host species. In addition to Quercus spp. (oak), which is the most common host in Europe and N. America, stands dominated by Larix (larch), Tilia (basswood), Diospyros (ebony), and Populus (aspen) spp. are capable of supporting massive outbreaks in Asia (Schaefer et al. 1984, 1988). Alhough some information about Asian gypsy moth populations in Japan, Siberia, and China is available in the western literature (e.g., Schaefer et al. 1988), relatively little information exists about populations in Central Asia (Fig. 2). We address this deficiency by providing an introductory description of the biology and ecology of the gypsy moth in Central Asia. We first describe the habitat in this region, which contains native walnut-fruit forests and thus is unique relative to other portions of the gypsy moth's range. Central Asia Geography In this article, we define Central Asia as the region covering Kyrgyzstan, Kazakhstan, Uzbekistan, Tajikistan, and Turkmenistan, extending from the Caspian Sea to the west, Mongolia and China to the east, south from the Ural Mountains and Siberia, and north from Iran and Afghanistan (Table 1, Fig. 2). This large region has varied geography, including high passes and mountains (Tien-Shan), vast deserts (Kara Kum, Kyzyl Kum, Taklamakan), and large and mostly treeless grassy steppes. The vast steppe areas of Central Asia are considered, together with the steppes of Eastern Europe, as a homogenous geographical zone known as the Euro-Asian steppe. Much of the area consists of steep mountain ranges reaching 7,495 m in elevation, largely covered by rock and devoid of extensive vegetation. Lowlands stretch from north to south for more than 3,000 km, and there is a gradient from a mixed zone to a zone of deciduous forests to forest steppe and steppe zones and finally to semiarid and arid zones. The climate is decidedly continental with a vast amplitude of summer and winter temperatures (Klein Tank et al. 2006). The region is rich in water resources that originate mostly from the winter snow pack in the mountains of Kyrgyzstan and Tajikistan that drains into the region's two main rivers, Syr Darya and Amu Darya. All of the region's rivers drain into the Aral Sea in Uzbekistan and Kazakhstan, which has no outlet and where all water eventually evaporates. During the Soviet era, large portions of these rivers were diverted for agriculture, causing a massive decline in the extent of the Aral Sea, which before 1960 was the forth largest lake in the world. In recent years, however, this trend has been partially reversed and the Aral's level has increased although it has not yet reached its previous size. American Entomologist.

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he gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae), is one of the most damaging pests of forests in its introduced range in North America and in its native distribution in temperate Europe, North Africa, and Asia (Fig. 1) (Giese and Schneider 1979, Montgomery and Wallner 1989). Over much of its range, gypsy moth populations periodically erupt to massive levels, causing extensive defoliation of broadleaf and coniferous forests. Many eruptions are spatially synchronized so that outbreaks occur concurrently over large geographic areas (Johnson et al. 2005, 2006), greatly exacerbating the economic and ecological costs associated with high-density populations. In North America, gypsy moth life stages were introduced outside of Boston in 1869, and it has since expanded its range (Fig. 1) (Liebhold et al. 1989). Females of North American populations cannot fly, which limits its rate of spread; however, increases in its range can still exceed 20 kmjyr (Liebhold et al. 1992, Tobin et al. 2007), mainly because of anthropogenic movement oflife stages. Outbreaks in North America have been observed to occur about every 8-12 yr (Johnson etal. 2006). In its native range in Europe, gypsy moth outbreaks are common, particularly in oak-dominated forests in the Mediterranean region. In the majority (but not all) of European gypsy moth populations, adult females are completely incapable of flight (Keena et al. 2008). The gypsy moth is also widely distributed through Asia, where there is tremendous variation in various biological traits among populations. Although most females are capable of flight in Asian populations, this is not the case in all areas (Keena et al. 2008). Also, populations across

and Patrick C. Tobin

Table 1. Characteristics

Country Kazakhstan Kyrgyzstan Tajikistan Turkmenistan Uzbekistan

of Central Asian countries (modified from FAO 2006)

Area (1,000 km')

Population (1,000)

Forested area (1,000 km')

Pistachio forest (1,000 km')

Walnut-fruit forest (1,000 km')

2,700 200 143 488 447

15,200 5,214 7,181 5,000 26,800

33.4 8.7 4.1 41.3 33.0

NA 0.4 1.2 0.8-1.0 0.2

NA 0.6 0.1 0.001 0.03

phy, Central Asian civilizations also remained highly isolated, and consequently societies in various regions have retained unique customs and traditions. The predominant religion in Central Asia today is Islam, which is thought to have arrived to the region in the 8th century.

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The Forests of Central Asia Despite the mountainous nature of Central Asia, forests cover a relatively small proportion of each country Following the Bolshevik Revolution in 1917 and up to 1991, (Table 1) and broad-leafed species dominate only a small fraction Central Asia was part of the Soviet Union, but it now consists of the of forests. Much of the forest area in Central Asia is dominated by independent republics of Kazakhstan, Uzbekistan, Turkmenistan, saxaul (Haloxylon spp.) and other shrubs found particularly in desert Kyrgyzstan and Tajikistan. Despite their unique histories, the Central and semi-desert areas of Kazakhstan, Turkmenistan, and UzbekiAsian countries have similarities in their historical development, stan. In the moist, mountainous areas of southeastern Kazakhstan which is apparent through the spiritual and cultural similarity of and northeastern Kyrgyzstan (the Tien Shan Mountains), there are Central Asian people. Central Asia contained much of the ancient Silk Route, which connected East Asia to southern Europe, and thus extensive thickets of Betula (birch), Abies (fir), Populus (aspen), and played an important role as a cultural and economic transcontinental Picea (spruce) spp. The spruce forests of Kyrgyzstan are composed link. In the 13th century, the Mongol empire of Genghis Khan extended of uneven-aged forest stands dominated by Picea schrenkiana Fisch (Musuraliev 1998), which grow in the mountain ranges surrounding over almost all of Central Asia. Various Mongolian leaders followed, Lake Issuk-Kul, the Naryn water basin of northern Kyrgyzstan, and but in later years the region was divided into smaller empires that in the Talas and Kyrgyz Mountain ranges in the south. were more regionally controlled. In the 18th century, much of Central Juniper-dominated forests are concentrated in the southern part Asia fell under the domain of the Chinese Qing dynasty. of the Turkestan-Alay forest vegetation area of Kyrgyzstan and these The Russians began their conquest of Central Asia under Peter forests are composed primarily of juniperus seravschfnica Kom., the Great in the 19th century, and Russian influence continued juniperus semiglobosa Rgl, and juniperus turkestanica Kom. Historiuntil the fall of the Soviet Union in 1991. For thousands of years before the formation of the Soviet Union, and even when under the cally, juniper was widespread throughout the valleys of Central Asia (Musuraliev 1998). Its current distribution, however, is sparse and domain of various empires and dynasties, the Central Asian people confined to a narrow, discontinuous belt over mountain slopes at were predominantly nomadic. Their livelihood and culture revolved elevation range from 1,800 to 3,500 m. Riparian forests are located around herding animals, predominantly horses that are native to in mountainous areas along the Naryn, Chy, Tup, Talas, Sysamur, Asia. With the advent of the Soviet Union, however, a large proporDjergalan, and Yassu rivers, as well as many smaller rivers where tion of the Central Asian population was settled on large collective they playa role in the regulation of water supply and protection farms. Following the collapse of the Soviet Union and consequent against soil erosion. These forests are composed of various species independence of the Central Asia states, most of these collective such as Populus nigra, P.diversifolia, Salix alba, S. cinerea, Eleagnus farms were dissolved, although most forest land has remained under government ownership. angustifolia, Tamarix laxa, Hippophae rhamnoides, and Ulmus spp. The walnut-fruit forest is unique to Central Asia and grows above As result of their history, Central Asian societies have been exthe steppe zone in warm, sheltered valleys in the western Pamir-Alai, posed to many cultural influences that have framed their customs Tien Shan, and Kopetdag mountains. The Tien Shan is the most and spiritual beliefs. However, because ofits mountainous topograrecent mountain range to emerge from the collision of the Indian subcontinent with Asia during the Cenozoic era. Currently rising about 1.5 cm/yr, the Tien Shan has N Russia never experienced glaciations, and its highest peak is Jengish Chokusu in Kyrgyzstan (7,439 m). Snow-covered peaks provide abundant moisture to fruit forests in valleys (Juniper 2007). The main walnut-fruit species that occur naturally in Central Asia are Persian walnut Uuglan regia), pistachio (Pistacia vera), apple (Malus sieversii, M. niedzwetzkyana), almond (Amygdalus communis L.), wild plum (Prunus sogdiana), wild cherry (Prunus ferganica), mountain ash (Sorb us persica), wild pear (Pyrus bucharica, Azerbaijan P. korchinsky), and other fruit-bearing trees and shrubs. The native range of Persian walnut extends from Nepal in the east, across Central Asia, to the Caucasus, and as far west as Turkey (Hemery 1998). The most extensive Iran a,DOD • 9.000 walnut forests are in Kyrgyzstan (Chatkal and Fergana -=-=:l__ ===>__ '~•••"" Mountains), Uzbekistan (Chatkal Mountains), Turk0'25'2$0 !SOO ~ 1,000 ~ ~ ~ - ~- ~ ~ - ~J'~ menistan (Kopetdag Mountains) and Kazakhstan (Ugam map). Citations for each location are provided in Supplemental Material, Table 1. available from authors in pdf. centre). In southern Kazakhstan the species is present, but

Forest Biodiversity and Sustainable Use There has been wide recognition of the tremendous importance of Central Asian walnut-fruit forests both as a genetic resource and as a source of biological diversity (Yazimirsky 1935, Shevchenko 1965, McGranahan and Leslie 1991, FAO1995, Hemery 1995, Kolov 1995, Musuraliev 1995). These forests represent a unique ecosystem not found elsewhere in the world and they contain several woody plant

Fig. 3. Gypsy moth and its defoliation in Kyrgyzstan. (a) Defoliated natural pistachio stand; (b) newly molted larva on walnut; (c) defoliated walnut stand; (d) defoliated apple stand.

260

species unique to the region. These forests also are dominated by nut- and fruit-producing tree species, many of which are relatives of species of eminent commercial importance worldwide (e.g., apple, pear, pistachio, and walnut). The preservation of genetic diversity from tree species that are unique to the Central Asian forests should thus be of global importance. Historically; the walnut-fruit forests have been important to the livelihoods of the rural people who live in and around them. Today, through the development of sustainable management practices for harvesting nuts and fruit, these forests have the potential to alleviate poverty. Productivity of walnut ranges from 40 to 350 kg of nuts per hectare of forest, depending upon growing conditions (Shevchenko 1965). Yields of pistachio nuts from natural stands are rather 10w,-1 kgper tree, although up to 15 kg per tree may sometimes be collected (Chernova 2004). The highest pistachio yields are typically obtained from 60-S0-yr old trees, although trees will continue to produce nuts for >300 yr. Pistachio trees in natural stands typically occur sparsely scattered over grassland with densities of only 30-70 trees per hectare. Since the early 19S0s, there have been efforts to identify highly productive pistachio strains and plant these in various portions of the foothill regions of the Central Asian steppe at elevations from SOOto 1,200 m to increase nut production. The walnut-fruit forests are of considerable importance for sustaining the livelihoods of more than 100,000 people living in the forest area (Favre 1997, Schmidt 2005). The human population in these regions containing walnut-fruit forests has increased considerably over the past 50 years and created intense pressure on the limited natural resources. Collecting nuts and fruit is of immense economic importance for households in the region. In many areas, almost all of the nuts are commercially harvested, which essentially eliminates natural regeneration. Historically, the mountain forests of Central Asia have been exploited for timber, fuel wood, and charcoal; however, recently, these activities have intensified because of increased human settlement and the accompanying demand for timber and fuel. These practices, coupled with hay-making and overgrazing of cattle, sheep, and goats, have caused extensive destruction of forested areas, including the fruit-nut forests of Central Asia. In addition to the human demands for Central Asian forest resources, the gypsy moth places an additional burden on the sustainability and productivity of the fruit-nut forests unique to the region. The Gypsy Moth in Central Asia The fruit-nut forests of Central Asia have been and continue to be threatened by a remarkably sustained outbreak of the gypsy moth over the past 30 years. The gypsy moth is apparently native to Central Asia, where it is widely distributed (Pogue and Schaefer 2007) (Fig 2). However, the Central Asian gypsy moth population is isolated from other Eurasian populations by deserts to the north, spruce forests in Tien-Shan to the northeast and east, and the Caspian Sea to the west. Little information is available about the distribution of the gypsy moth in southern portions of Central Asia, but it is likely that its patchy distribution continues from the high mountain valleys of Tajikistan into the Kashmir region of Pakistan and India. Central Asian gypsy moth populations could ultimately intergrade to the south with Lymantria obfuscata populations from India, Pakistan, and Afghanistan (Pogue et al. 2007). The gypsy moth is highly polyphagous, and in North America larvae feed on more than 300 host tree species (Liebhold et al. 1995) American Entomologist • Winter 2009


it does not form extensive forests; trees are scattered in small groves of 0.6 to O.Sha (Dzhangaliev et al. 2003). In Turkmenistan, walnut forests grow in Western Kopetdag in a 100-ha area (Allamuradov et al. 2005). In Uzbekistan, natural walnut forests cover 29S ha (Uzbek State Department of Forestry 2007). Pistachio, Pistacia vera, grows under dry conditions of the semidesert foothills of Central Asia (Fig. 3a, b). It is widely distributed throughout the Tien Shan foothills of the Kyrgyz Mountainous range (42° 5' latitude North). North Kyrgyzstan (on the foothills of the Kyrgyz Mountain chain), Uzbekistan (the Pskem and Chatkal Mountain chains), South Kazakhstan (the Talas, the Alatau, the Karatau), and North Tajikistan (the Kuramin Mountain chain) are sparsely populated, and there are a few isolated stands of pistachio. In the Central PamirAlay region, pistachio stands are widely distributed in the southern Tajikistan (along the Pandj, Karatau, Teriklitau, Arooktau, Sarsharak, and Chaltau mountain ranges), eastern Turkmenistan (Koogitau), and southern Uzbekistan (the Babatagmountains) regions at an altitude of 500-1,SOO ill. In this region, dense stands are found at SOO-1,200 ill. Isolated pistachio stands grow near Kososhka in the South Kopetdag region of southwest Turkmenistan at elevations ranging from 600 to 1,000 m (Kaimov et al. 1995, Chern ova 2004). Wild stands of apple in Central Asia have received global interest because they are a reservoir of genetic diversity from which domestic cultivars may be drawn (Miller 2006). The species Malus sieversii Lebed. is native to Central Asia and is recognized as a major progenitor of the domesticated apple, M.pumila Mill.In ancienttimes, apple seeds and trees were likely transported from Central Asia into China to the east and Europe to the west across the Silk Route (Forsline etal. 2003). Phylogenic studies show that wild apple (Malus sieversiI) from Central Asia is quite similar to domesticated apples, and that several other Malus species are almost indistinguishable (Juniper 2007). Another important Central Asian apple species is Malus niedzwetskayana, which is an endangered species. Because of the potential importance of M. niedzwetskyana as a genetic resource, it is paramount to preserve it and other wild apple species from Central Asia.

(Table 2). None of the genera most commonly defoliated elsewhere in the range of the gypsy moth (Le.,Quercus, Larix, and Populus) are native to Central Asia, nor are they commonly present in Central Asia today. Instead, most gypsy moth outbreaks in Central Asia occur in stands of Pistacia and Malus, although several other tree species are also known to be suitable hosts.' Reliable data on historical defoliation by the gypsy moth in the region are lacking but the first known record of an outbreak population in Central Asia dates back to 1938 in Kazakhstan (Gninenko 1986). Despite the lack of reliable data, our investigations indicate that gypsy moth outbreaks in Central Asia have become increasingly more extensive over the past two decades. In 2007 alone, several thousand hectares were defoliated, mostly in Kyrgyzstan and Kazakhstan.2

'Tables 1 and 2 in Supplementary POE 'Table 1 in Supplementary

Material, which is available from the author in

Material, which is available from the author in POE

Table 2. Principle gypsy moth host trees by Region Region

Genera

Reference( s)

Europe

Crataegus, Quercus, Salix

Grijpma 1989, Wulf 1993, Hoch et al. 2001

East Asia

Abies, Acer, Alnus, Betula, Carpinus, Castanea, Castanopsis, Celtis, Cerasus, Cydonia, Diospyros, Eriobotrya, Eurya, Fagus, Fraxinus, Hamamelis,juglans, Larix, Lespedeza, Liquidambar, Malus, Morus, Populus, Prunus, Quercus, Rosa, Robina, Rubus, Salix, TWa, Ulmus, Wisteria, Xylosma, Zelkova

Kim et al. 1982, Schaefer et a1.1984, * Schaefer et a1.1988, Lee et al. 2002, Schaefer et al. 2004

North America

Larix, Liquidambar, Lithocarpus, Ostrya, Populus, Quercus, Salix, TWa

Barbosa and Greenblatt etal. 1995*

East Siberia

Larix, Pinus

Kozhanchikov

East-West Siberia

Betula, Populus

Kozhanchikov1950,

Central Asia

Abies, Acer, Amygdalus, Apricot, Berberis, Betula, Crataegus,juglans, Larix, Malus, Pinus, Pistacia, Populus, Prunus, Quercus, Rosa, Rubus, Salix, Spirea, Ulmus

Gershun 1951, Semenov 1951, Tuzkov et al. 1950, Kostin 1958, Grechkin 1958, Kuznetsov 1960, Degtyareva 1964, Abdullaev 1966, Makhnovsky 1966, Khamdam-Zade 1972, Romanenko 1984, Gninenko 1986, Ashimov 1989, Toktoraliev 1993, Orozumbekov 2001, Ponomarev et al. 2002, Orozumbekov 2003, Sultanov et al. 2005

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1979, Lechowicz and Jobin 1983, Liebhold

1950, Gninenko and Orlinsky 2003 Gninenko and Orlinsky 2003

261


The Role of Natural Enemies of the Gypsy Moth in Central Asia A nucleopolyhedrosis virus (LdMNPV) occurs in almost every gypsy moth population worldwide, and it is considered to be a primary of source of mortality and consequent outbreak collapse in dense gypsy moth populations. Based on limited information, it appears that LdMNPV plays a similar role in Central Asian gypsy moth populations (Orlovskaya 1968, Il'inykh etal. 2005). In 1983, the All-Russian Scientific Research Institute of Forestry and Mechanization, Pushkino, Moscow, built a laboratory for the mass production of LdMNPVin Djalalabat city, Kyrgyzstan. This laboratory operates today, and viral preparations from the lab are directly "painted" on the surface of egg masses in the field for management purposes, although the efficacy of this method is not well documented. The fungus, Entomophaga maimaiga (Zycomycotina: Entomophthoraceae), is a common gypsy moth pathogen in Japan, where epizootics are frequent. This pathogen was discovered in North America in 1989 and subsequently caused extensive epizootics and gained much appreciation as an additional cause of gypsy moth mortality (Hajek 1999). However, this fungal pathogen does

not appear to be present in Central Asia, most likely because the dry climatic conditions are quite different from those in North America and Japan. Small mammals (particularly the deermouse, Peromyscus maniculatus, and white-footed mouse, Peromyscus leucopus) are important predators of the gypsy moth in North America (Bess et al. 1947, Campbell 1975). Predation by small mammals on gypsy moth pupae has been documented as the dominant source of mortality in low-density gypsy moth populations in North America and decreases in small mammal abundance are associated with increases of gypsy moth populations from low to outbreak levels (Bess 1961, Campbell 1975, Cook et al. 1995, Elkinton et al. 1996, Liebhold et al. 2000). Limited information suggests that small mammals in the genus Apodemus also playa similar role in the dynamics of gypsy moth populations in Europe and East Asia (Liebhold et al. 1998, Gschwantner et al. 2002). Based upon our very limited sampling of small mammal populations in the walnut-forests of south Kyrgyzstan, it appears that Apodemus spp. are present, but at very low densities. It is possible that small mammal populations in the region have been negatively affected by intense grazing and subsequent elimination of forest understory cover, as well as by the extensive harvesting of nuts on which small mammal populations depend for food, especially during winter. It remains to be determined whether small mammal predator populations have declined in Central Asia,and if so, if this has played a role in the apparent increase in gypsy moth outbreaks in the area. Many invertebrate predators are known to attack various gypsy moth life stages. For example, several species of ground beetles, Calosoma spp. (Coleoptera: Carabidae), were introduced from Europe to North America in the early 1900's as part of biological control efforts (Howard and Fisk 1911, Burgess and Crossman 1929). In Central Asia, two ground beetle species, C.sycophanta and C. auropunctatum, have been found preying on gypsy moth larvae in the walnut-fruit forests (Abullaev 1966, Romanenko 1984, Orozumbekov 2001), but little is known about their role in gypsy moth dynamics, and in particular, in their ability to regulate low-density gypsy moth populations. Gypsy moth populations in North America have been the target of extensive biological control programs since the early 1900s (Howard

Table 3. Primary gypsy moth parasitoids established in the United States, and Central Asia

Species

Established in the u.s.

Hymenoptera: Eupelmidae Hymenoptera: Encyrtidae Hymenoptera: Ichneumonidae Hymenoptera: Ichneumonidae Hymenoptera: Ichneumonidae Hymenoptera: Ichneumonidae Hymenoptera: Ichneumonidae Hymenoptera: Ichneumonidae Hymenoptera: Braconidae Hymenoptera: Braconidae Hymenoptera: Braconidae Hymenoptera: Chalcididae Hymenoptera: Diapriidae Diptera: Tachinidae Diptera: Tachinidae Diptera: Tachinidae

Anastatus japonicus Ashmead

Diptera: Tachinidae Diptera: Tachinidae Diptera: Tachinidae

Drino inconspicua (Meigen)

Ooencyrtus kuwanae (Howard) Phobocampe unicincta (Gravenhorst) Phobocampe lymantriae

Gupta

Pimpla instigator F. Pimpla turionellae (L.) Pimpla disparis (Vierick) Caenocryptus ruftventris (Gravenhorst) Cotesia melanoscelus

(Ratzeburg)

Glyptapanteles liparidis Bouche Dolichogenidea lacteicolor (Viereck) Brachymeria intermedia

(Nees)

Tetramopria aurocincta Wasmann Compsilura concinnata (Meigen) Blepharipa pratensis (Meigen) Parasitigena silvestris (Robineau-

Desvoidy) Exorista larvarum (L.) Exorista rossica Mesnil

and Fiske 1911, Burgess and Crossman 1929). Beginning in 1906, more than 60 species of egg, larval, and pupal parasitoids, predators, and pathogens were introduced, but most failed to establish (Hoy 1976). Only 11 parasitoids, two predators, and two pathogens became established, and among these several became major natural enemies of the gypsy moth in North America (Reardon 1981) (Table 3). The species composition of parasitoids of the gypsy moth varies throughout Eurasia (Howard and Fiske 1911), although because of taxonomic difficulties (misidentification and synonyms), the number, relative importance as mortality factors, and geographical distribution of the various species are difficult to evaluate (Reardon 1981). A list of gypsy moth parasitoids that have been recorded from Central Asian gypsy moth populations is provided in Table 3. Almost every known gypsy moth parasitoid present in North America is present in Central Asia, although the reverse is not true. The one exception is Glyptapanteles liparidis (Hymenoptera: Braconidae) which is present in worldwide gypsy moth populations including Central Asia. Although its introduction has been attempted in North America, it failed to establish due to a lack of alternative hosts of other reasons (Howard and Fiske 1911). Future Worldwide, gypsy moth outbreaks exhibit spatial synchrony and periodicity; outbreaks recur every 5-10 yr (Johnson et al. 2005, 2006). Outbreaking populations usually collapse following epizootics by one of two gypsy moth pathogens, the virus LdMNPV;which is omnipresent in worldwide gypsy moth populations, and the fungus E. maimaiga, whose abundance is influenced by climate and which is thus not usually present in xeric environments such as in Centra Asia. In Kazakhstan, gypsy moth outbreaks have been observed to recur every 8-10 yr in most forested areas; however, gypsy moth outbreaks in the walnut-fruit forests of Kyrgyzstan have occurred almost continuously for the past 30-35 yr (Gninenko 1986, Orozumbekov et al. 2003). Although one of the main regulators of high-density gypsy moth populations, E.maimaiga, is not found in the walnut-fruit forests, this does not seem to explain the lack of effective high-density gypsy 262

Established in Central Asia

Acknowledgments We sincerely thank B. A. Toktoraliev, Z.A. Teshebaeva, A. M. Mamytov, and S. H. Kojoev (Osh Technological University); A. O. Sagitov, J. D. Ismukhambetov, M. M. Isin, M.A. Kochorov, and B. Duisembekov (Kazakh Research Institute for Plant Protection); S. Kenjebaev and M. Nurmanbayev (Institute of Biosphere of National Academy of Science); O.S.Telegina (Kazakh Forest Research Institute), R.A. Sultanov and E. A. Butkov (Uzbek Republican Scientific Production Centre of Decorative Horticulture and Forestry); and E. M. Andreeva, V. N. Shatalin, O.V.Tolkach (Plant Protection Lab, Ural Division of Russian Academy of Science, Yekaterinburg). This project was supported by the Fulbright Program, Council for International Exchange of Scholars, U.S. Department of State. Additional logistic and technical support was provided by K. Gottschalk, G. Luzader, and L. Blackburn (USDA Forest Service, Northern Research Station, Morgantown, WV). We are also very grateful to R. Reardon ((USDAForest Service, Forest Health Technology Enterprise Team, Morgantown, WV) and Roger Fuester (USDA Agricultural Research Service, Newark, DE) who provided valuable taxonomic expertise. ••••• References Cited Abdullaev, E.N. 1966. Entomophages ofthe gypsy moth (Porthetria dispar L.)in Uzbekistan. Ph.D.thesis. Samarkand State University.Samarkand, USSR(in Russian). Allamuradov A., A.Abdurakhimov, andA. Kuliev.2005. Forest resources assessmentfor.sustainable forest management. Country statement. U.N. Economic Commission for Europe, Food and Agriculture Organization workshop, Prague. (in Russian). Ashimov, K. S. 1989. Biology,ecology and dynamics quantified of gypsy moth in the walnut-fruit forests of southern Kyrgyzstan. Ph.D.thesis. Voronezh State Agricultural University,Voronezh, USSR(in Russian). Barbosa, P., and J. Greenblatt. 1979. Suitability, digestibility and assimilation of various host plants ofthe gypsy moth, Lymantria dispar L.Oecologia43: 111-119. Bess, N.A. 1961. Population ecology of the gypsy moth Porthetria dispar L. (Lepidoptera: Lymantriidae). New Haven,Conn.Agric.Exp.Stn.Bull.43. Bess, N.A.,S.H. Spurr, and E.W.Littlefield. 1947. Forest site conditions and the gypsy moth. Harvard For.Bull.22. Burgess A.,F.,and S. S.Crossman. 1929. Imported insect enemies ofthe gypsy moth and the brown-tail moth. u.s. Dept. Agric.Tech. Bull.86. Campbell, R.W. 1975. The gypsy moth and its natural enemies. U.S.Dept. American Entomologist.

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Order: Family

moth population regulation. In North America, outbreaks have historically collapsed, even during the early period ofits invasion and even in the absence of E. maimaiga, which was not present in North America until at least 1989 (Hajek 1999). Indeed, we have observed many LdMNPVepizootics in Kyrgyzstan, but the cycling of populations does not appear to be geographically synchronized and consequently outbreak populations are present in the region virtually every year. Although the reasons for this lack of synchrony and consequent sustained gypsy moth outbreaks in walnut-fruit forests remains a mystery, it is clear that additional studies of the biology and ecology of gypsy moth in Central Asia are needed to sustain this valuable Central Asian resource.

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in periodicity and synchrony among gypsy moth populations. I. Anim. Ecol. 74: 882-892. Johnson, D. M.,A. M. Liebhold, and O.N. Bj0rnstad. 2006. Geographical variation in the periodicity of gypsy moth outbreaks. Ecography 29: 367-374 Juniper, B. E. 2007. The mysterious origin of the sweet apple. Am. Sci. 29: 44-51. and w: E. Wallner. 2008. World distribution of female flight and genetic variation in Lymantria dispar (Lepidoptera: Lymantriidae). Environ. Entomol. 37: 636-649. Kim, C.H., S.H. Nam, and S.M. Lee. 1982. Illustrated flora and fauna of Korea. Insecta 26(8): 588-615 (Samwha, Seoul). Klein, T.A.M.G., T. C. Peterson, D. A. Quadir, S. Dorji, X. Zou, H. Tang, K. Santhosh, U. R. Joshi, A. K. Jaswal, R. K. KoIIi, A. Sikder, N. R. Deshpande, J. V Revadekar, K. Yeleuova, S. Vandasheva, M. Faleyeva, P. Gomboluudev, K. P. Budhathoki, A. Hussain, M. Afzaal, L. Chandrapala, H. Anvar, D. Amanmurad, VS. Asanova, P.D. Jones, M. G. New, and T. Spektorman. 2006. Changes in daily temperature and precipitation extremes in central and south Asia. I. Geophys. Res. 111 (D16105), doi:10.1029 j20051D006316. Kolov, 0.V1998. Ecological characteristics of the walnut-fruit forests, pp. 5961. In I.B1aser,I.Carte,r and D.Gilmour [Eds.]. Biodiversity and sustainable use of Kyrgyzstan's walnut-fruit forests (English version). International Union for Conservation of Nature, Intercooperation, Cambridge, UK. Kostin, I. A. 1958. Gypsy moth outbreak in East Kazakhstan in 1953-1955. Institute of Zoology, Academy of Science of Kazakh, Alma-Ata, USSR (in Russian). Kozhanchikov, I. V 1950. Fauna of the USSR.Lepidopteran insects. Orgyidae. Academy of Science ofSSR. Moscow-Leningrad. 12: 582 (in Russian). Kuznetsov, VI. 1960. Manuscript of fauna and ecology of lepidopterans (Lepidoptera) of western Kopet-Dag. Zoological Institute, Turkmenistan Academy of Science, Leningrad. (in Russian). Lechowicz, M. J., and L. Jobin. 1983. Estimating the susceptibility of tree species to attack by the gypsy moth, Lymantria dispar. Ecol. Entomol. 8: 171-183. Lee, J. H., H.P. Lee, P. w: Schaefer, R. w: Fuester, J. D. Park, B. Y.Lee, and C. H. Shin. 2002. Gypsy moth parasite complex, Mt Halla National Park, Cheju Island, Korea .Entomol News 113: 103-112. Liebhold, A. M., V C. Mastro, and P. w: Schaefer. 1989. Learning from the legacy of Leopold Trouvelot. Bull. Entomol. Soc. Am. 35: 20-22. Liebhold, A. M., J. Halverson, and G. Elmes. 1992. Quantitative analysis of the invasion of gypsy moth in North America. I. Biogeog. 19: 513-520. Liebhold, A. M., K. w: Gotschalk, R. M. Muzika, M. E. Montgomery, R. Young, K. O'Day, and B. Kelley. 1995. Suitability of North American tree species to the gypsy moth: A summary offield and laboratory tests. u.s. Dept. Agric. For. Servo Gen. Tech. Rep.NE-211. Liebhold, A. M., Y. Higashiura, and A. Unno. 1998. Forest type affects predation on gypsy moth (Lepidoptera: Lymantriidae) pupae in lapan. Environ. Entomol. 27: 858-862. Liebhold, A. M., J. S. Elkinton, D. Williams, and R. M. Muzika. 2000. What causes outbreaks of the gypsy moth in North America? Popul. Ecol. 42: 257-266. Makhnovsky, I. K.1966. Pest of mountain forests and their control. Forest Product Press, Moscow (in Russian). McGranahan, G., and C. Leslie. 1991. Walnut Uuglans L.). pp. 907-951. In I. N. Moore and I. R. Ballington [Eds.]. Genetic resources of temperate fruit and nut crops. International Society for Horticulture Science, Wageningen, Netherlands. Miller, D. 2006. Wild and domesticated apples in the Kyrgyz Republic. Midwest Apple Improvement Assoc. Newsletter 8: 2-6. Montgomery, M. E., and Wallner W. E. 1989. The gypsy moth a westward migrant. pp. 353-373. In A.A. Berryman [Ed.] Dynamics offorestinsect populations, patterns, causes, implications. Plenum, New York. Musuraliev, T. S. 1998. Forest management and policy for the walnut-fruit forests ofthe Kyrgyz Republic, pp. 3-17. In I. Blaser, I. Carter, and D. Gilmour [Eds.], Biodiversity and sustainable use of Kyrgyzstan's walnut-fruit forests (English version). International Union for Conservation of Nature, Intercooperation, Cambridge, U.K. Orlovskaya, E. V 1968. Geographic distribution and manifestation ofviroses dendrophilous insect pests in Soviet Union. lournal of Entomological Obozrenie 4: 741-756 (in Russian). Orozumbekov, A. A. 2001. The Natural enemies and diseases of the Gypsy 263


Agric. Inf. Bull. 381. Chernova, G. M. 2004. Bioecological features of selection of Pistacia vera L. in Central Asia. In Publisher, Bishkek. (in Russian). Cook, S. P., H. R. Smith, F.P. Hain, and F.L. Hastings. 1995. Predation of gypsy moth (Lepidoptera: Lymantriidae) pupae by invertebrate at low small mammal populations densities. Environ. Entomol. 24: 1234-1238. Degtyareva, V I. 1964. The gypsy moth. (Lepidoptera). Tajikistan Academy of Science, Dushanbe, Tajik USS. (in Russian). Dzhangaliev, A. D, T. N. Salova, and P. M. Turekhanova. 2003. The wild fruit and nut plants of Kazakhstan. Hortic. Rev. 29: 305-371. Elkinton, J. S., w: M. Healy, J. P. Buonaccorsi, G. H. Boettner, A. M. Hazzard, H. R. Smith, and A. M. Liebhold. 1996. Interactions among of gypsy moth, white-footed mice and acorns. Ecology. 77: 2332-2342. FAO (Food and Agriculture Organization of the United Nations). 1995. Collecting woody perennials. pp. 485-510. In I. Guarino, I., v. R. Rao, and R. Reid [Eds.], Collecting plant genetic diversity: Technical guidelines. CAB International, Wallingford, UK. Favre, J. C. 1997. Importance et retombees socio-economiques de I'utilisation des forets de noyers du Sud Kirghizistan. Ecole Polytechnique Federale, Zurich. Forsline, P. L., H. S. Aldwinckle, E. E. Dickson, J. J. Luby, and S. Hokanson. 2003. Collection, Maintenance, Characterization and utilization of wild apples of Central Asia. Hortic. Rev. 29: 1-61. Gershun, M. S. 1951. Forest pests in Uzbekistan. Uzbek Forest Research Institute, Moscow, USSR (in Russian). Giese, R. L., and M. I. Schneider. 1979. Cartographic comparisons of Eurasian gypsy moth distribution (Lyman tria dispar L.; Lepidoptera: Lymantriidae). Entomol. News 90: 1-16. Gninenko, Y. 1.1986. Elements of monitoring of the gypsy moth populations in Kazakhstan. I. For. 4: 45-49 (in Russian). Gninenko, Y.I., and A. D. Orlinskii. 2003. Outbreaks of Lymantria dispar. Russian forests during the 1990s. OEPP JEPPO (Organisation Europeenne et Mediterraneenne pour la Protection des PlantesjEuropean and Mediterranean Plant Protection Organization) Bull. 33: 325-329 Grechkin, V P. 1958. Some of main representatives of insect pests in the mountain forests of Tajikistan. I. Zool. 35: 37-40 (in Russian). Grijpma, P. 1989. Overview of research of Lymantriids in eastern and western Europe. In Proceedings, Lymantriidae: a comparison offeatures of New and Old World tussock moths. U.S. Dept. Agric. For. Servo NE For. Exp. Stn. Genrl. Tech. Rep. NE-123: 21-49. Gschwantner, T., G. Hoch, and A. Schopf. 2002. Impact of predators on artificially augmented populations of Lyman tria dispar L. pupae (Lep., Lymantriidae). I. Appl. Entomol. 126: 66-73. Hajek, A. E. 1999. Pathology and epizootiology of Entomophaga maimaiga infections in forest Lepidoptera. Microbiol. Mol. BioI. Rev. 63: 814-835. Hamdam-Zade, T. K. 1972. Gypsy moth and its control in peach gardens in northeast of Central Asia. Ph.D. thesis. Tashkent State University; UzbekUSSR (in Russian). Hemery, G. E. 1998. Walnut Uuglans) seed-collecting expedition to Kyrgyzstan and Central Asia. Quart. I. For. 92: 153-157. Hoch, G., M. Zubrik, J. Novotny, and A. Schopf. 2001. The natural enemy complex ofthe gypsy moth, Lymantria dispar (Lep.: Lymantriidae) in different phases of its population dynamics in eastern Austria and Slovakia: a comparative study. I. Appl. EntomoI.125: 217-227. Howard, L. 0., and w: F. Fiske. 1911. The importation into the United States of the parasites of the gypsy moth and brown-tail moth. U.S. Dept. Agric. Bur. Entomol. Bull. 91. Hoy, M. A. 1976. Establishment of gypsy moth parasitoids in North America: An evaluation of possible reasons for establishment or non -establishment. pp. 215-232. In I. F.Andreson and N. K. Kaya [Eds.), Perspectives in forest entomology. Academic Press, New York. I1'inykh, A. V, S. V Kuz'minov, E. G. U1'yanova, S. H. Kojoev, and P. A. I1'inykh. 2005. Effect of polyhedrosis on populations of gypsy moth and nun moth. I. Plant Prot. Q. 3: 53-54 (in Russian). Kaimov, A. K., R. A. Sultanov, and G. M. Chernova. 1998. Pistacia in Central Asia. pp. 49-55. In Proceedings, Toward a comprehensive documentation and use of Pistacia genetic diversity in Central and West Asia, North Africa and Europe. International Plant Genetic Research Institute, Irbid, lordan. Keena, M. A., M.-J. Cote, P. S. Grinberg, a Johnson, D. M., A. M. Liebhold, O. N. Bj0rnstad, and M. L. McManus. 2005. Circumpolar variation

Shevchenko, V S. 1968. Fast-growing of walnut forms.llim, Frunse, USSR (in Russian). Sultanov, R. A. 2005. Gypsy moth monitoring by pheromone traps in the walnut-fruit forests in Uzbekistan. Ministry of Water and Agriculture. Production Centre of Decorative Horticulture and Forestry. Technical Report P 12-5 (Tashkent, Uzbek., in Russian). Tobin, P. c., A. M. Liebhold, and E. A. Roberts. 2007. Comparison of methods for estimating the spread of a nonindigenous species. J. Biogeogr. 34: 305-312. Toktoraliev, B.A. (1993). Insects - Xylophagous of the forests of Kyrgyzstan. Ph.D. thesis. Moscow State University of Forest, USSR (in Russian). Tuzkov, LV, Kharitonova, VI. 1964. Natural enemies of gypsy moth. J. Plant Protection of Pests and Diseases 11: 37. (in Russian). Uzbek State Department of Forestry. 2007. Uzbek Forest inventory report. Tashkent, Uzbek. (in Russian). Wulf, A. 1993. Schwammspinner-Massenvermehrung 1993. Resiimee und Ausblick. In A. Wulf and K.-H. Berendes [Eds.]. SchwammspinnerKalamitat im Forst. Mitt. BioI. Bundesanst. Land-Forstwirtsch. BerlinDahlem, Heft 293. Yazimirsky, K. V 1938. The walnut Forests in Aman- Kutan, pp. 9-17 In Proceedings of the Forestry Field Station. Tashkent, USSR (in Russian). Almazbek Orozumbekov is a member of the Department of Biology at the Kyrgyz National Agrarian University in Bishkek. His research focuses on the population ecology of the gypsy moth and its control in Central Asia. Andrew Liebhold is a Research Entomologistwith the USDAForest Service, Northern Research Station, in Morgantown, wv. The principal topics of his research are forest insect outbreak spatial dynamics and invasion biology. Vasily Ponomarev is a Senior Research Scientist, Head of Plant Protection Lab atthe Ural Division of the Russian Academy of Sciences. Dr. Ponomarev's research focuses on the role of population quality in the population dynamics of the gypsy moth. Patrick Tobin is a Research Ecologist with the USDAforest Service, Northern Research Station, in Morgantown, wv. He studies the popu1ation ecology and biology of biological invasions in forest ecosystems.

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American Entomologist.

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moth in the habitat of the walnut-Fruit Forests of southern Kyrgyzstan. Ph.D. Thesis. Institute of Biology and Pedology of National Academy of Science of Kyrgyz Republic. Bishkek, Kyrgyz Republic. (in Russian). Orozumbekov, A. A., V I. Ponomarev, A. Mamytov, E. M. Andreeva, and A. M. Liebhold. 2003. Population ecology of gypsy moth in Kyrgyzstan. pp. 49-50. In Gottschalk, K.w. (ed). Proceedings, U.S. Department of Agriculture interagency research forum on gypsy moth and other invasive species 2003, U.s. Dept. Agric. For. Servo Gen. Tech. Rep. NE-315. Pogue, M. G., and P. w: Schaefer. 2007. A review of selected species of Lymantria Hiibner [1819] including three new species (Lepidoptera: Noctuidae: Lymantriinae). U.s. Department of Agriculture, Forest Health Technology Enterprise Team, FHTET-2006-07, Morgantown, Wv. Ponomarev VI., Orozumbekov A.A., Toktoraliev B.A. (2002). Ecology of the gypsy moth in the southern Kyrgyzstan. Moscow State University of Forest, Vestnik MGUL 318: 138-145 (in Russian). Reardon, R. 1981. Parasites. U.S. Dept. Agric. For. Servo Tech. Bull. 1584: 299-421. Romanenko, K. Y. 1984. Pistachio pests in Kyrgyzstan and their control. llim, Frunse, USSR. (in Russian). Schaefer, P. W:, R. M. Weseloh, X. L. Sun, w: E. Wainer, and J. J. Van. 1984. Gypsy moth, Lymantria (=Ocneria)dispar (1..)(Lepidoptera: Lymantriidae) in the People's Republic of China. Environ. Entomol. 13: 1535-1539. Schaefer, P. W., K. Ikebe, and Y.Higashuira. 1988. Gypsy moth, Lymantria dispar (1..) and its natural enemies in the Far East (especially Japan). Annotated bibliography and guide to the literature through 1986 and host plants list for Japan. U. Del. Agric. Environ. Stn. Bull. 176. Schaefer, P. W:, B. A. Tuulaikhuu, C. E. Goulden, and T. Kira. 2004. The Asian gypsy moth situation in Mongolia. Proceedings, U.S.Department of Agriculture interagency research forum on gypsy moth and other invasive species 2003, U.S. Dept. Agric. For. ServoGen. Tech. Rep. NE-332: 72. Schmidt, M. 2005. Utilisation and management changes in South Kyrgyzstan's mountain forests. J. Mtn. Sci. 2: 91-104. Semenov, A.Y.1951. Destructive entomofauna of un irrigated orchards in Kondar. Academy of Science, USSR. Leningrad (in Russian).


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