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Parasitoid complex of the Asian gypsy moth (Lymantria dispar) (Lepidoptera: Lymantriidae) in Primorye Territory, Russian Far East Jang-Hoon Lee a;Robert W. Pemberton b a Research Institute for Natural Science, Dongguk University-Seoul, Seoul, Korea b Invasive Plant Research Laboratory, USDA-ARS, FL, USA
Online publication date: 14 December 2009
To cite this Article Lee, Jang-Hoon andPemberton, Robert W.(2010) 'Parasitoid complex of the Asian gypsy moth (Lymantria dispar) (Lepidoptera: Lymantriidae) in Primorye Territory, Russian Far East', Biocontrol Science and Technology, 20: 2, 197 — 211 To link to this Article: DOI: 10.1080/09583150903447802 URL: http://dx.doi.org/10.1080/09583150903447802
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RESEARCH ARTICLE Parasitoid complex of the Asian gypsy moth (Lymantria dispar) (Lepidoptera: Lymantriidae) in Primorye Territory, Russian Far East Jang-Hoon Leea* and Robert W. Pembertonb
aResearch Institute for Natural Science, Dongguk University-Seoul, 100-715, Seoul, Korea; bInvasive Plant Research Laboratory, USDA-ARS, 3225 College Ave. Ft. Lauderdale, FL 33314, USA (Received 18 August 2009; returned 28 September 2009; accepted 27 October 2009)
A study of the moth parasitoid complex attacking gypsy moth, Lymantria dispar (L.) was carried out in Primorye territory, Russia Far East. Season-long collections at three sites in the Vladivostok area and collections at seven sites of central region of Primorye revealed the 18 primary parasites: one egg parasitoid, 11 larval parasitoids, one larval-pupal parasitoid, one parasitic nematode, one ectoparasitoid, and three diseases including NPV (nuclear polyhedrosis virus) and Entomophaga maimaiga. Phobocampe species (Ichneu- monidae) dominated the parasitoid complex, parasitizing 5.5% of the larvae in the Vladivostok area and 9.3% in central Primorye, rates which are much higher than those detected from other Asiatic regions of Russia and Northeastern Asia. The insect parasitoid complex was found to be somewhat depauperate. The 11.8% average total parasitism in eastern Russian is similar to the 12% recorded in the US. Both regions have large gypsy moth outbreaks, but other factors including diseases have compensated for the rather low mortality exerted by the parasitoid complex in the Russian Far East. Keywords: Lymantria dispar; Russia Far East; parasitoids
Introduction The gypsy moth Lymantria dispar (L.), has been a serious pest of forests in the northeastern part of the United States since its accidental introduction from Europe into North America in 1868 (Drea and Fuester 1979). In 1991, the Asian form of the
Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 gypsy moth was accidentally introduced into North America from Russia (USSR) (Bogdanowicz, Wallner, Bell, Odell, and Harrison 1993). During the summer and fall of 1991, adults of the Asian form of the gypsy moth were found in Portland, Oregon, and Tacoma, Washington in the United States, and in Vancouver, British Columbia in Canada. They were believed to be introduced on ships carrying logs from the Russian Far East (USDA-Forest Service 1991). This introduction of the Asian form of the gypsy moth was alarming because the female moths can fly, unlike the European form, greatly increasing the risk of spread from the areas of colonization to much of the continent (Wallner, Humble, Levin, Baranchikov, and Carde´ 1995). The Asian Parasite Laboratory of the US Department of Agriculture was based in Seoul, South Korea had been doing research on Korean and Japanese enemies of the
*Corresponding author. Email: [email protected]
ISSN 0958-3157 print/ISSN 1360-0478 online This work was authored as part of Contributor’s official duties as an employee of the United States Government and is therefore a work of the United States Government. In accordance with 17 U.S.C. 105 no copyright protection is available for such works under U.S. law. DOI: 10.1080/09583150903447802 http://www.informaworld.com 198 J.-H. Lee and R.W. Pemberton
Asian gypsy moth for many years in hopes of finding natural enemies that could contribute to the control of the European form of the moth. In 1992, the laboratory was instructed to expand its gypsy moth research to try to locate new natural enemies of L. dispar in Asia that could be useful to control the Russian moth that had invaded the west coast of North America. The goals were to find and introduce new and known parasitoids not established in North America, and to augment the existing gene pool of species established during the earlier introduction programs (Drea and Fuester 1979). The most obvious and desirable area to explore was the Russian Far East but this region was closed to foreigners. Early in 1992, because of the political changes in Russia, the Russian Far East was opened for the first time in almost a century. The co-author visited the Russian Academy of Sciences Entomology Laboratory in Vladivostok in April 1992 and obtained permission and assistance to enable the Asian Parasite Laboratory to conduct gypsy moth research during the field season during the summer of 1992. The objectives of this study were to determine the species composition of the parasitoid complex, the relative importance of each species, and to compare the results obtained in Primorye Territory with those obtained in Asiatic region including mainland Korea, China, and Japan. The Asian gypsy moth has been successfully eradicated from the United States (Espinosa and Hodges 2009). Nevertheless, newly discovered parasitoids of the moth would be of interest for evaluation for potential introduction against the Asian forms of the gypsy moth in North America if the gypsy moths were to become established again and eradication efforts were to fail.
Materials and methods Through the courtesy of the Russian Academy of Sciences, Vladivostok, a laboratory room in the Department of Entomology was modified into a rearing facility for field- collected gypsy moth larvae. In addition, a technician was obtained, and military trucks with drivers were made available for the field collections. The research was led and largely carried out by the senior author.
Study region The natural enemies of the Asian gypsy moth in Primorye Territory, Far East Russia Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 were studied through sets of season-long collections at three sites near Vladivostok. In addition, survey collections to identify and to evaluate gypsy moth parasitoids were made in central Primorye territory.
Season long collections at three sites in the Vladivostok area The Vladivostok area containing the study sites is bounded by 131857?25ƒ and 132826?10ƒE longitude and by 43815?53ƒ’ and 43847?28ƒN latitude. Gypsy moth larvae were collected at ca. weekly intervals at three sites from May 15 through July 6, 1992, and season long collections were made at each of the following sites: (1) Zhavodskoe 1.5 km (The site names denote the nearest named place and distance from the collection sites) (elevation 55 m) was 48 km NW of Vladivostok, where eight collections (May 21 to July 6) were made primarily from Quercus mongolica Biocontrol Science and Technology 199
Fisch., Lespedeza bicolor Turcz., Maackia amurensis Rurp. et Maxim. Corylus heterophylla Fish., Betula dahurica Pall. (2) Banevirovo 3 km (elevation 155 160 m) was 66 km N of Vladivostok, where seven collections (May 26 to July 6) were made from Q. mongolica, Salix sp, L. bicolor, C. heterophylla, M. amurensis, Populus sp. Pyrus ussuriensis Maxim., B. dahurica; and (3) Shtikovo 2 km E (elevation 65 m), artificial population site, on 40 km NE of Vladivostok, where seven collections (May 15 to June 29) were made mainly from Q. mongolica Fisch., and L. bicolor. We created an artificial population at Shtikovo through the release of egg masses since gypsy moth population was very low. A total of 1050 egg masses were collected in Mnogoudobnoe Village (700 egg mass) (55.8 km NE of Vladivostok) and Nikolayevka (350 egg masses) (94 km N of Vladivostok) and released at the sites by stapling plastic cups (160 mL), containing an average of 10 egg masses each, to tree trunks at chest height (35 trees 30 egg masses). The cups had screened bottoms to drain rain water.
Survey collections in central Primorye The central Primorye collection area is circumscribed by 13385?55ƒ and 134857?40ƒ E longitude and by 44808?09ƒ and 45806?19ƒN latitude. Survey collections were made during early June and July within the region. Collections were made on mainly Quercus spp. in the quantities, dates, and locations as follows: 128 third to fifth instar larvae on June 8 at Arseneve (157 km NE of Vladivostok); 184 second to fourth instar larvae on June 8 at Tshugevka (158 km NE of Vladivostok); 395 second to fifth instar larvae on June 9 at Samarka 20 km (elevation 260 m, 257 km NE of Vladivostok) and Samarka 5 km (elevation 140 m, 242 km NE of Vladivostok); 348 second to fifth instar larvae on June 10 and July 2th in Rudniy (278 km NW of Vladivostok); and 539 first to fourth larvae on 10 June and 2 July at Shumniy (elevation 180 m, 252 km NE of Vladivostok).
Hand collection and rearing Most collections were made along access roads in forests and forest margins extending up to 100 meters into the forests from roads. Smaller or less dense gypsy moth populations required collections from larger areas of forests. The areas of
Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 collection were usually 20,000 30,000 m2. The larvae were collected by hand to 2.5 m up a tree trunk, and then taken to the laboratory where they were reared in screen- topped plastic boxes (20.5 28 16.5 cm) in groups of up to 50 and fed Quercus dentata leaves. The containers were checked every other day for parasitoid emergence. The pupae that were reared were held in small lots in Petri dishes (1.5 9 cm) or in clear plastic containers (19.5 4.5 cm) until parasitoids or adult moth emerged. Egg masses of the gypsy moth were collected from several different infestation sites in the Vladivostok area and stored in a refrigerator at 58C and used for the gypsy moth population supplementation efforts at the Shtikovo site. A small portion (four to five egg masses) was also set aside from each collection site and placed in a 9-cm diameter Petri dish. Egg masses were held in the laboratory at ambient temperature and observed for evidence of parasitization or assessments of development. 200 J.-H. Lee and R.W. Pemberton
Parasitoid identifications were made by the authors and by comparison with authoritatively determined voucher material from the former USDA-ARS Asian Parasite Laboratory collection of natural enemies of gypsy moth from eastern Asia.
Gypsy moth population estimation Gypsy moth population estimates were made for each site by calculating the number of larvae and pupae collected per person per hour. Parasitism was also analyzed in terms of host population phase affinities. In order to determine the population phase, egg mass density, the ratio of new to old egg masses, the ratio of adult female to males emerged during rearing, and hourly density of immature stages were determined. The number of new to old egg masses were counted during 5-min walks (n 12) (Schneeberger 1987). Although 5-min walks are very practical and convenient for judging relative abundance of egg mass density, they are not recommended for estimation of absolute density (Liebhold, Twardus, and Buonac- corsi 1991). Egg masses were uncommon in our collection sites.
Analysis Different indices of parasitism, previously described by Pemberton, Lee, Reed, Carlson, and Han (1993), were used in this study to evaluate the relative importance of each parasitoid: (1) the percentages of parasitism by each species were calculated by dividing the number of larvae producing each parasitoid species by the number of larvae collected. These parasitism percentages for individual parasitoid species were added to yield combined parasitism rates for collection dates, sites, and ultimately, the entire study. (2) Maximum or peak parasitism was the highest rate observed for a given species at any site and sampling date. (3) Season-long parasitism was calculated by dividing the numbers of parasitized hosts by the number of gypsy moth immature individuals obtained in a season-long collection at a particular site. (4) Host-stage parasitism was calculated by dividing the number of individuals of each stage killed by the parasitoid by the numbers collected in each stage. Gregarious parasitoids emerging from a single larva were counted as one parasitoid. Parasitoid- host associations were generally determined by the cocoon aggregations on or near the host cadavers, e.g., Glyptapanteles liparidis (Bouche´). The method used to calculate percentage parasitism underestimates parasitism Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 because all larval stages were included rather than only those stages that were susceptible to the particular parasitoids (Van Driesche 1983). Despite its bias, this method does allow the Russian fauna of the gypsy moth to be easily compared with published accounts of fauna attacking gypsy moth in other countries.
Results A list of the parasitoids we recovered from the larvae of L. dispar in Primorye territory is presented in Table 1. In the Vladivostok area, a total of 1424 larvae were collected from May 15 to July 6. In central Primorye territory, 1594 larvae were collected from June 9 to July 3. The collection numbers in the Vladivostok area were: Zhavodskoe, eight samples averaging 93 larvae each from May 21 to July 6; Banebirovo, seven samples averaging 61 larvae from May 28 to July 6; Shtikovo, Table 1. Percentage parasitism by natural enemies reared from the Asian gypsy moth in Primorye Territory, Russia Far East, 1992.
Vladivostok area Central Primorye
Localitiesa Zhavo. Bane. Shti.b Sama. Rud. Tshu. Shum. Arce.
Collection date 21 May 06 July 28 May 06 July 15 May 29 July 09 June 10 June, 02 July 08 June 10 June, 02 July 08 June Host stagec L1 L5 L1 L6 L1 L4 L2 L5 L2 L5 L2 L4 L1 L4 L3 L5 No. host collected 757 424 243 395 348 184 539 128
Parasitoids Technology and Science Biocontrol Braconidae Aleiodes lymantriae 0.1 0 0 3.8 0 0 0 0 Cotesia melanoscelus 0.1 0 0 0 0 0 0 0 Cotesia sp. 0.4 0 0 0 0 0 0 0 Glyptapanteles liparidis 1.5 0 0 0 0 0 0 0 Meteorus pulchricornis 0.1 0.2 0 0 0 0 0 0 Meteorus sp. 0.1 0 0 0 0.3 0 0 0 Eulophidae
Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 May 10 19:26 At: Library] Agricultural National [USDA By: Downloaded Elachertus sp. 0.3 0 0.4 0 0 0 0 0 Ichneumonidae Casinaria arjuna 0.5 1.6 0 0 0 0.5 0.2 0 Phobocampe spp.d 5.7 7.1 3.7 12.2 7.2 10.3 16.7 0 Tachinidae Blepharipa schineri 0.4 0.2 0.4 0 0 0 0 0 Parasetigena silvestris 4.0 5.4 2.5 2.8 2.3 1.6 0.7 0.8 Sarcophagidae 0 0 0 0 0 0 0.4 0 Mermithidae Unidentified sp. 0 0 0 0.5 0 0 0 0 Baculoviridae NPV 15.5 21.5 7.4 22.8 23.6 40.2 34.0 59.4 201 202
Table 1. (Continued). Vladivostok area Central Primorye .H e n ..Pemberton R.W. and Lee J.-H. Localitiesa Zhavo. Bane. Shti.b Sama. Rud. Tshu. Shum. Arce.
Entomophthoraceae Entomophthora maimaiga 11.1 4.2 1.2 3.8 4.0 0 3.5 0.8 Beauveria sp. 3.3 1.9 0.4 2.0 3.2 1.6 3.9 0 Unknown dead larvae 41.7 42.7 64.7 41.3 55.5 34.2 38.2 32.8 Unknown dead pupae 3.8 11.6 6.2 5.3 1.1 6.0 1.1 2.3 Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 May 10 19:26 At: Library] Agricultural National [USDA By: Downloaded Host emergence ( , ) 5.7/6.2 1.9/1.7 8.2/4.9 3.3/2.3 1.7/1.1 1.1/4.3 0/0.9 0.8/3.1 Total parasitism 12.7 14.5 7.0 19.2 9.8 12.5 18.0 0.8
aZhavo. Zhavodskoe; Bane. Banevjrovo ; Shti. Shtikovo; Sama. Samarka; Rud. Rudniy; Tshu. Tshuguevka; Shum. Shumniy; Arce. Arcennev. bGypsy moths at this site were established through the release of eggs. cL1 6 first to sixth instar larvae. dIncludes Phobocampe lymantriae and P. unicinta. Biocontrol Science and Technology 203
seven samples averaging 35 larvae each from May 15 to June 29. In central Primorye territory: Rudniy 348 larvae on June 10 and July 3; Tshuguevka 184 larvae on June 8; Shumniy 539 larvae on June 10 and July 2; and Arceneve 128 larvae on June 8. The hourly collections of larvae per person averaged 68.8, 44.6, and 24.3 for Zhavodskoe, Banebirovo, and Shtikovo, respectively. The gypsy moth populations at all sites in the Vladivostok area were designated as being in decline or an innocuous phase as indicated by rare egg mass presented in study sites and male biased emergence rate recorded from all of natural populations (Table 1). This result agrees well with that of Gnimenko and Orlinskii (2003), who reported survey data on gypsy moth populations in Primorye territory. However, gypsy moth egg masses were usually observed around residential areas with the degree of infestation varying with sites. The gypsy moth population at central Primorye territory was relatively higher than in the Vladivostok area. Total parasitism was 13.4%, because parasitoids killed 404 of the 3018 larvae reared (Table 1).
Season long collections in the Vladivostok area The season-long parasitism in these collections ranged from 7.0 to 14.4% in the Vladivostok area, depending upon the site (Table 1). Sixteen species of natural enemies of the gypsy moth were found: one egg parasitoid, 11 larval parasitoids, one larval-pupal parasitoid, and three diseases. Egg parasitoids (Anastatus disparis) were obtained from eggs collected at different infestation sites from April to May 1992, but data were not quantified and only presence of the parasitoid was confirmed. Weekly data on numbers of hosts collected and percentage parasitism for the dominant larval parasitoids appear in Figure 1.
Hymenoptera Braconidae Six species of braconids were recovered from the larvae of L. dispar collected at Zhavodskoe but they were barely recovered from other sites. Glyptapanteles liparidis (Bouche´) is a gregarious, oligophagous, bivoltine parasitoid. The highest parasitism it induced (8.1%) was recorded from 136 host larvae collected on 16 June at Zhavodskoe with the season long rate of 1.5%. No larvae from the other two Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 collection sites were parasitized by this wasp (Table 1). The remaining braconids, Aleiodes lymantriae (Watanabe), Cotesia melanoscelus (Ratzeburg), Cotesia sp., Meteorus pulchricornis (Wesmael), and Meteorus sp. accounted for less than 0.4%, respectively, for season-long parasitism and appeared to be insignificant.
Ichneumonidae Phobocampe spp. (Phobocampe lymantriae (Gupta) and Phobocampe unicincta (Gravenhorst)), solitary and univoltine parasitoids were recovered from samples collected from 21 May to 30 June at the Vladivostok area. They were the dominant parasitoids of early and middle instar larvae (Figure 1 and Table 2). They caused the highest season-long parasitism, making them the most important parasitoids in this study. This parasitoid was found in all three season-long collections, where 3.7 7.1% 204 J.-H. Lee and R.W. Pemberton
30 150 No. larvae collected larvae No. Zhavodskoe 120 20 90
60 10 % Parasitization % Parasitization 30
0 0 V-15 V-21 V-27 VI-02 VI-09 VI-16 VI-22 VI-29 VII-06
30 150 Gypsy moth collected larvae No. Banevirovo P. silvestris 120 20 Phobocampe spp.* 90
60 10
% Parasitization % Parasitization 30
0 0 V-15 V-21 V-28 VI-05 VI-10 VI-16 VI-23 VI-30 VII-06
30 150 No. larvae collected larvae No. Shtikovo 120 20 90
60 10 % Parasitization % Parasitization 30
0 0 V-15 V-20 V-29 VI-04 VI-09 VI-16 VI-24 VI-29 VII-06 Date
Figure 1. Phenology of Asian gypsy moth larval parasitism and number of larvae collected in the Vladivostok area of Primorye Territory, Far East Russia, in the post outbreak population cycle. *Includes Phobocampe lymantriae and P. unicinta.
parasitism was obtained (Table 1). They caused 7.1% parasitism in first and second instar larvae, 8.8% in third instar larvae, 1.6% in fourth instar larvae, and 2.1% in
Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 fifth to sixth instar larvae (Table 2). Casineria arjuna (Maheshwary & Gupta) emerged from samples collected at Zhavodskoe and Banevjrovo from May 21 to June 10 and it accounted for 0.3 and 1.6% of the mortality, respectively (Table 1). The parasitoid emerged from second and third instar larvae (Table 2). The ectoparasitoid, Elachertus sp. (Eulophidae), was found on one second instar larva collected on June 2 at Zhavodskoe and two larvae collected June 4 at Shitikovo.
Diptera Tachinidae Parasetigena silvestris (Robineau-Desvoidy), an oligophagous, univoltine species that lays macrotype eggs on the integument of large larvae, was recovered at all three Biocontrol Science and Technology 205
Table 2. Stage specific parasitism of immature stages of the gypsy moth in Primorye Territory, Russian Far East in 1992.
Parasitisma
Instars Parasitoids Vladivostok area Central Primorye
First to second instar Cotesia sp. 0.4 0 Meteorus sp. 0 0.5 Elachertus sp. 0.5 0 Casinaria arjuna 0.7 0 Phobocampe sppb 7.1 10.4 Parasetigena silvestris 0.7 0 Blepharipa schineri 0.2 0 Sarcophgidae 0 0.5 Subtotal 9.5 10.9 NPV 9.7 21.3 Entomophaga maimaiga 0 0.9 Bauveria sp. 0 4.3 Unknown 61.5 62.1
Third instar Aleiodes lymantriae 0.3 0 Cotesia sp. 0.3 0 Casinaria arjuna 1.3 0.1 Phobocampe spp.b 8.8 16.0 Parasetigena silvestris 8.0 0.7 Blepharipa schineri 0.3 0 Sarcophgidae 0 0.1 Subtotal 18.9 17.2 Nematode 0 0.2 NPV 14.5 28.2 E. maimaiga 5.4 3.0 Bauveria sp. 1.3 1.5 Unknown 52.9 47
Fourth instar Aleiodes lymantriae 0 3.8 Cotesia melanoscelus 0.3 0 Phobocampe spp.b 1.6 2.8 Meteorus pulchricornis 0.3 0
Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 Meteorus sp. 0.3 0.3 Parasetigena silvestris 5.4 3.0 Blepharipa schineri 0.3 0 Subtotal 11.0 9.9 NPV 23.1 43.5 E. maimaiga 18.0 5.0 Bauveria sp. 7.0 2.0 Unknown 40.2 37.0
Fifth to sixth instar Phobocampe spp.b 2.1 0 Parasetigena silvestris 4.2 8.2 Blepharipa schineri 2.1 0 Subtotal 8.3 8.2 NPV 30.2 26.0 206 J.-H. Lee and R.W. Pemberton
Table 2. (Continued). Parasitisma
Instars Parasitoids Vladivostok area Central Primorye
E. maimaiga 17.7 2.7 Bauveria sp. 3.1 13.7 Unknown 36.5 38.3
aThe total numbers of hosts examined in each host group from Vladivostok were: 566 first to second instar larvae; 386 third instar larvae; 373 fourth instar larvae; 96 fifth to sixth instar larvae (mostly fifth instar), from Central Primorye; 211 first to second instar larvae (mostly second instar); 847 third instar larvae; 398 fourth instar larvae; 73 fifth instar larvae. bIncludes Phobocampe lymantriae and P. unicinta.
sites, where its season-long parasitism rate ranged from 2.5 to 5.4% and averaged 4.0% (Table 1). It was the second most dominant parasitoid in Vladivostok with peak parasitism of 8.6% on 9 June at Zhavodskoe and 8.5% on 5 June at the Banevjrovo site (Figure 1). It caused the highest parasitism 8.0% in third instar larvae (Table 2). Blepharipa schineri Mesnil is an oligophagous, univoltine larval-pupal parasitoid which lays microtype eggs on foliage. Larvae of all ages can ingest these eggs as they feed, and subsequently become parasitized. B. schineri occurred in all three season- long collections (Table 1), but was generally scarce. This fly parasitized only one larva of 42 second to third instar larvae collected at Shtikovo on June 4 and 46 fourth to fifth instar larvae collected at Banevjrovo on June 30.
Diseases A nuclear polyhedrosis virus (NPV) was present in all collections. The larval mortality in the laboratory averaged 14.8%. The highest season-long infection rate 21.5% was recorded at Banevjrovo, with lower rates 15.5 and 7.4% at the other sites (Table 1). Entomophthora maimaiga (Humber, Shimazu, Soper and Hajek) [Zygomycotina: Zygomycetes Entomophthoracea] a fungal pathogen that attacks the larvae, was also detected in all collections. This specialist fungus of the gypsy moth produced the Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 second highest mortality with the mean infection rate of 5.5%. Beauveria sp. [Deuteromycotina: Zygomycetes] is a fungus that attacks gypsy moth larvae and many other insects (Tanada and Kaya 1993). The fungus caused relatively little mortality, with the mean infection rate of 1.9%.
Survey collections in central Primorye Territory The parasitism in these collections ranged from 0.8 to 19.2%, depending upon the site (Table 1). Nine natural enemies of the gypsy moth were found: five larval parasitoids, three diseases, and one sarcophgid fly. Data on the number of hosts collected and percentage parasitism for the dominant larval parasitoids appears in Table 1. Biocontrol Science and Technology 207
Hymentopera Braconidae The larval parasitoid, Aleiodes lymantriae (Watanabe) (Rogas lymantriae Watanabe) was the only important braconid parasitoid, with season long parasitism of 3.8%. It emerged from 15 out of 395 second to fifth larvae collected in Samarka on June 9. It caused the highest parasitism rate of 3.8% in the fourth instar larval grouping in central Primorye. Meteorus sp. parasitized only one larva collected at Rudniy. No other braconid parasitoids were recovered in this area.
Ichneumonidae Phobocampe spp. (Pobocampe lymantriae and P. unicinta) attacked second to fourth instar larvae. These species caused the highest parasitism in this area, making them the most important parasitoids in this study. They were recovered from most collection sites except Arceneve, and the highest total parasitism rate of 16.7% which was found at Shumniy, and total parasitism rates ranging 0 12.2% at the remaining sites, and averaging 9.3% (Table 1). The highest parasitism rate of 19.5% was produced in 371 first to fourth instar larvae collected at Shumniy on 10 June. They caused 16% parasitism in third instar collected in this area (Table 2). Casinaria arjuna a parasitoid found in Tshuguevka and Shumniy where its parasitism rate appeared to be very low (50.5) (Table 1).
Diptera Tachinidae Parasetigena silvestris was recovered from all collection sites, where its parasitism rates (site related parasitism) ranged from 0.8 to 2.8% and averaged 1.6% across the sites, making it second in importance in this study (Table 1). It caused 3% parasitism in fourth instar larvae collected across this area, although the highest parasitism (7.0%) in third instar larvae was found in a Rudniy collection of 114 fourth and fifth instar larvae. It was the third most common parasitoid at Samarka (2.8% on 9 June, 11/395 second to fifth instar larvae) and the second most common at Rudniy (peak
Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 parasitism of 7.0% on 3 July, 8/114 fourth to fifth instar larvae).
Diseases In central Primorye Territory, NPV (nuclear polyhedrosis virus) was more abundant than in the Vladivostok area for early mid larvae (first to fourth instar), but in late larvae, it caused a similar degree of mortality in both regions. NPV was present in all collections. The larval mortality in the laboratory averaged 36%. The highest infection rate 59.4% was recorded at Arceneve, while the lowest rate 22.8% was seen at Samarka (Table 1). Entomophaga maimaiga produced the second highest mortality with a mean infection rate of 2.4%. Beauveria sp. caused relatively little mortality, with a mean infection rate of 2.1%. 208 J.-H. Lee and R.W. Pemberton
Nematode Nematode-induced mortality was rare in the study. A Hexamermis sp. was recovered from two out of 97 third instar larvae collected at Samarka on 9 June.
Discussion A total of 18 species of natural enemies including one species of egg parasitod was reared from L. dispar in Primorye territory in Russia. Twelve of these parasitoids were previously observed from Asiatic part of USSR (Amur region, Irkutsk region, Tyva Republic, Primorye Territory) (Kolomiets 1987; Belokobylskij 1996) and Khavarovsk region (Turova 1989). The five additional species of natural enemies not previously reported in this area are; Meteorus sp. Casinaria arjuna, Elachertus sp., Entomophaga maimaiga, and the mermithid nematode. No new gypsy moth natural enemies were discovered except possibly for the Cotesia sp. and the Meteorus sp. In general, the composition of the parasitoid complex found in the Russian Far East does not differ greatly from that associated with gypsy moth at the other localities in Northern Asia. However, the parasitoids causing the most mortality in the gypsy moth differs from other studied areas in Asia (Pemberton et al. 1993; Lee et al. 2002). Phobocampe spp. were the most important larval parasitoids in Primorye Territory, although they were only minor components of previous surveys in the Asiatic part in USSR (Amur region, Tyva Republic, Primorye territory) (Kolomiets 1987) and around Khabarovsk (Turova 1989). Phobocampe species are widespread in Europe (Drea 1978; Hoch, Zubrik, Novotny, and Schopf 2001; Zolubas, Gedminas, and Shields 2001) and in Northeast Asia (Schaefer, Yan, Sun, Wallner, and Weseloh 1984; Pemberton et al. 1993), where they are the most important ichneumonid larval parasitoids. But, in these regions, the tachinid Parasetigena silvestris is usually more important than the Pobocampe spp. Parasetigena silvestris was the second most important parasitoid in central Priymorye with mean parasitization of 2.2%. The average parasitism by this fly (4.0%) was higher in the Vladivostok area than in central Primorye (1.6%). It was a major parasitoid of L. dispar throughout much of Eurasia (Drea and Fuester 1979; Schaefer 1981; Fuester, Drea, Gruber, and Mercadier 1983; Schaefer et al. 1984; Kolomiets 1987; Fuester, Gruber, Drea, and Hoyer 1988; Hoch et al. 2001; Zolubas Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 et al. 2001). In mainland Korea, it was the dominant parasitoid of L. dispar, with season-long parasitism rates ranging from 0.11 to 30.01% (mean 9.88%) (Pember- ton et al. 1993). Blepharipa schineri, another tachinid was scarce in the Vladivostock area and it was not found in our central Primorye collections. This tachinid was recovered at only one site in the present study, but was a dominant parasitoid in the Khavarovsk area of the Russsian Far East (Turova 1989). This fly is common in Europe and in Northeastern Asia. In Europe, this species was assumed to be effective against late instar larvae and pupae, appearing at high rates in the first post-outbreak year (Fuester et al. 1988). Pemberton et al. (1993) reported that B. schineri was the control agent responsible for most pupal mortality of gypsy moth in mainland Korea, where it averaged 37.5%, with peak parasitism of 76.2%. This species was also found in Japan (Schaefer 1981) and the Far East of Russia (Amur region) (Kolomiets 1987). Biocontrol Science and Technology 209
The braconid wasp, Aleiodes lymantriae (Watanabe) (Rogas lymantriae Wata- nabe), was the most important species in Samarka inducing 3.8%, parasitism, although it was not recovered from any other collection sites except Zhavodskoe. Parasitism rate by this species was not previously reported in the Russian Far East (Kolomiets 1987; Turova 1989, 1992) although the presence of the parasitoid was recorded in this area (Belokobylskij 1996). This parasitoid is not important in gypsy moth populations in Europe. In Lithuania (Zolubas et al. 2001), a related Rogas sp. was reported to parasitize gypsy moth larvae. The range of parasitism rates in the Primorye area were mostly far below that reported from other countries (Drea 1978; Pemberton et al. 1993; Zhang, and Quarles 1995). Rather, the parasitism rates, ranging from 0.8 to 19.2 in this study, are similar to the US, where they ranged between 3 and 17% (Reardon 1981). It is interesting that some of the dominant larval parasitoids known to be important control agents of Lymantria dispar in Europe and Asia (the braconids Cotesia melanoscelus (Ratzeburg), Cotesia schaeferi (Marsh), and G. liparidis (Pemberton et al. 1993), were rare in Primorye. In contrast to low insect parasitism in our study, disease infection or unknown mortalities were very high at all collection sites. NPV- infected gypsy moth larvae were abundant in all of the field collections. Likewise, the fungus Entomophaga maimaiga caused a similarly high mortality. Notably, unknown mortality was responsible for a very high degree of mortality of collected gypsy moth larvae, with a mean mortality rate of 43.6%. Overall gypsy moth mortality between sites in this study ranged from 99.1 to 82.1%. The composition of the gypsy moth’s larval parasitoid complex changes over time and parasitism by many species is related to the phase of the host population cycle (Ticehurst, Fusco, Kling, and Unger 1978). In Europe, Phobocampe species caused high levels of parasitism during the post-outbreak years (Fuester et al. 1983; Hoch et al. 2001). Studies in Yugoslavia (Sisojevic´ 1975) and Austria (Fuester et al. 1983) indicated that B. pratensis was a major factor in reducing populations during the first post-outbreak years of the gypsy population gradation. However, the ecological homologue of B. pratensis, Blepharipa schineri attacking late instar larvae in Asiatic regions (Pemberton et al. 1993) appeared to be unimportant in this study. At most of our study sites, Phobocampe species attacked mainly middle larvae of gypsy moth and exhibited their highest rate of parasitism. There were no reports of serious gypsy moth infestations in Primorye until 1991, when outbreaks estimated at a 100-fold increase occurred (Gnimenko and Orlinskii 2003). In any case, the Downloaded By: [USDA National Agricultural Library] At: 19:26 10 May 2010 parasitoid complex in this area appears to be somewhat depauperate. High incidence of disease and other significant unknown mortality factors may negatively influence the degree of parasitism (Lee and Pemberton 2009), although these mortality factors probably have compensated for the rather low mortality exerted by parasitoids. Thus, limited level of parasitoid impact in this region probably contributes to outbreaks of gypsy moth and subsequent likelihood of transport of Asian gypsy moths to the US.
Acknowledgements We thank Drs Nikolai V. Kurzenko, Victor N. Kuznetsov, and Arkady S. Lelej, and all of the staff (Dr L. Esipenko, Mr Shasha, and Mrs Nina) in the Laboratory of Entomology, Institute of Biology and Soil Sciences, Russian Academy of Sciences, Vladivostok for assistance and friendship during this study. 210 J.-H. Lee and R.W. Pemberton
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