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1 August 2012 Parasitoids of the Sawfly, Arge pullata, in the Shennongjia National Nature Reserve
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Larvae of the argid sawfly, Arge pullata (Zaddach) (Hymenoptera: Argidae), feeds on leaves of birch (Betula spp.) in China, Europe, Siberia, and Japan. Parasitoids of A. pullata were studied in Shennongjia National Nature Reserve, Hubei Province, China, in 2009 and 2010. Five parasitoid species were found: Pleolophus suigensis (Uchida), Mastrus nigrus Sheng, Endasys parviventris nipponicus (Uchida) (Hymenoptera: Ichneumonidae), Vibrissina turrita (Meigen) (Diptera: Tachinidae) and Conura xanthostigma (Dalman) (Hymenoptera: Chalcididae). The average parasitism rate of A. pullata by parasitoids was as high as 11.0%. V. turrita was the dominant species, attacking 10.0% of the A. pullata cocoons. The emergence peak of V. turrita was from late May to early June. Three hyperparasitoids of V. turrita emerged from cocoons of A. pullata: Mesochorus ichneutese Uchida (Hymenoptera: Ichneumonidae), Pediobius sp. (Hymenoptera: Eulophidae), and Taeniogonalos maga (Teranishi) (Hymenoptera: Trigonalidae). Hyperparasitism rates were about 1.0% to 3.0%, with an average rate of 1.7%.


The argid sawfly, Arge pullata (Zaddach) (Hymenoptera: Argidae), is an injurious leaf feeder of birch, Betula spp., in China, Europe, Siberia, and Japan (Escherich 1942; Takizawa 1962; Austara et al. 1984; Li and Yuan 1993; Zhelochovtsev and Zinovjev 1995; Nuorteva and Nuorteva 2007; Hara and Shinohara 2008; Min et al. 2010). In China, this sawfly was first recorded in Tianzhu and Yongdeng, Gansu Province, and Huzhu, Qinghai Province. Heavy infestations in birch forests were caused by the larvae in Qilian Mountains in 1991, in Huzhu County, Qinghai, in 1996 and 1997, and in Shennongjia Forest, Hubei, in 2008 and 2009 (Li and Yuan 1993; Qi 2000; Min et al. 2010). In addition to the damage to birch, the larvae of A. pullata have a toxin that, if ingested, causes poisoning of sheep, cattle, and goats in Denmark (Brummerstedt et al. 1987; Thamsborg et al. 1987).

The biology, occurrence, and integrated management of A. pullata have been studied less in China (Li and Yuan 1993; Qi 2000) than elsewhere. In Japan, this sawfly was first recorded in Sugadaira, Nagano Prefecture, central Honshu, where it had a univoltine life cycle (Takizawa 1962). Hara and Shinohara (2008) reviewed the taxonomy, distribution, life history, and economic importance of A. pullata in Sapporo, Hokkaido, where A. pullata probably had two generations a year. In China, A. pullata had a univoltine life cycle (Li and Yuan 1993; Qi 2000).

High population levels of sawflies are not only affected by natural collapse, but are regulated by natural enemies (Luo et al. 2005). In China, most studies on parasitoids of sawflies have involved Diprionidae, Pamphiliidae, and some Tenthredinidae that damage forest trees (Wang et al. 1996; Zhang and Zhou 1996; Wang et al. 2000; Sheng and Chen 2001; Sheng et al. 2002; Chen and Sheng 2007). Worldwide, little is known about parasitism of Argidae, although they support a parasitoid complex that is highly distinctive (Pschorn-Walcher and Kriegl 1965).

Parasitoids play an important role in biological control of agriculture and forest pests. Up until now, only two parasitoids, Endasys parviventiris nipponicus (Uchida) and Mastrus nigrus Sheng (Hymenoptera: Ichneumonidae), have been reported on A. pullata (Min et al. 2010; Sheng and Zeng 2010). The data on additional parasitoids presented here are important for understanding the natural control of A. pullata, and future biological control effect against this economically important sawfly.

Materials and Methods

Overwintering cocoons of A. pullata under the bark of Betula spp. were collected on four occasions at the same site in Shennongjia National Nature Reserve, Hubei Province, in October 2009 and April 2010. The first sample (N = 2971) was collected on 8 October 2009, whereas the additional three samples (N = 4497, 12082 and 7075) were taken on 26 April 2010. The cocoons were reared in the laboratory at room temperature, and misted with distilled water one to two times per week in order to prevent desiccation. After one week, cocoons were stored individually in glass tubes (100 mm long and 15 mm in diameter) with a piece of filter paper dipped in distilled water (to prevent desiccation), and plugged with absorbent cotton.

All cocoons were checked daily for sawfly and parasitoid emergence until late autumn. Emerged parasitoid larvae and pupae were kept in glass tubes at room temperature until adult emergence. After emergence of sawflies and parasitoids was complete, all remaining cocoons were dissected, and their condition (i.e., status of argid sawfly, and parasitism) was recorded.

Tachinid parasitoids were identified by Dr. Chun-Tian Zhang (Shenyang Normal University), chalcid parasitoids were identified by Dr. Yan-Zhou Zhang (Institute of Zoology, Chinese Academy of Sciences), trigonalid wasps were identified by Dr. David R. Smith (Department of Entomology, National Museum of Natural History, Smithsonian Institution, United States of America). All specimens were deposited in the Insect Museum, General Station of Forest Pest Management, State Forestry Administration, P. R. China.

Parasitism rates data (p) were transformed by arcsin(p)½ in order to better fit the assumptions of normality and homogeneity of variances for ANOVA. The means were analyzed by one-way ANOVA, followed by the Ryan-Einot-Gabriel-Welsh (REGW) multiple Q test (SPSS 13.0 for Windows) at α = 0.05.



Five parasitoid species were reared from A. pullata: Pleolophus suigensis (Uchida), Mastrus nigrus Sheng, Endasys parviventris nipponicus (Uchida) (Hymenoptera: Ichneumonidae), Vibrissina turrita (Meigen) (Diptera: Tachinidae), and Conura xanthostigma (Dalman) (Hymenoptera: Chalcididae). The overall parasitism rates of A. pullata larvae by these parasitoids ranged from 8.1% to 13.8%, with an average rate of 11.0% (Table 1).

Only seven adults of the three parasitic ichneumonids, P. suigensis, M. nigrus, and E. parviventris nipponicus (Hymenoptera: Ichneumonidae), emerged from the cocoons of A. pullata, and 0, 28, 26 and 25 larvae were discovered from dissecting host larvae of the samples 1–4, respectively. The larval ichneumonids were indistinguishable from each other, so their parasitism rates were pooled and discussed as a group. Parasitism rates of A. pullata cocoons by ichneumonids were from 0.1% to 0.6%, with an average rate of 0.3%. Ichneumonids pupated inside the sawfly cocoons after feeding on the sawfly larva. Adults made an irregular emergence hole in the sawfly cocoons when emerging.

V. turrita larvae developed in the body of final instar A. pullata larvae, and killed them after they emerged from hosts. The tachinid final instar larvae pupated inside or outside the sawfly cocoon until adult emergence. Emergence holes were observed on the sawfly cocoons. One dead tachinid pupa was found inside the final instar larva of A. pullata when dissected. There were 401, 245, 694, and 535 adults tachinids that emerged from the cocoons of A. pullata in each sample, respectively. Parasitism rates of A. pullata larvae by V. turrita were from 7.0% to 13.5%, with an average rate of 10.0%.

C. xanthostigma larvae developed in the body of final instar A. pullata larvae, killed them after they emerged from hosts, and pupated inside the sawfly cocoon until adult emergence, leaving their puparium in the sawfly cocoon. Parasitism rates of A. pullata larvae by C. xanthostigma were from 0.1% to 1.6%, with an average rate of 0.6%.

There were significant differences in the parasitism rates among the three groups of parasitoids (F = 54.97; df = 2, 9; p < 0.001). V. turrita was the dominant parasitoid, with its parasitism rates being significantly higher than those of both ichneumonids and C. xanthostigma (p < 0.001). There were no significant differences in the parasitism rates between the latter two parasitoid groups (p > 0.05) (Figure 1).

The seasonal occurrence of V. turrita adults emerging from final instar larvae of A. pullata was recorded in 2010 (Figure 2). The emergence of V. turrita had two peaks. The first peak occurred from 22–28 May 2010, with 114 flies emerging on 28 May, 2010. The second peak was on 1 June 2010, with 111 flies emerging. The number of V. turrita emerging dropped gradually from 3 June 2010, and ended on 15 June 2010. Overall, the emergence peaks of V. turrita were from late May to early June.


Three species of hyperparasitoids, Mesochorus ichneutese Uchida (Hymenoptera: Ichneumonidae), a species of Pediobius sp. (Hymenoptera: Eulophidae), and Taeniogonalos maga (Hymenoptera: Trigonalidae), were reared from V. turrita. Hyperparasitism rates were from 1.0% to 2.8%, with the average of 1.7%. M. ichneutese was only found in the 4th sample of A. pullata cocoons, with a hyperparasitism rate of 1.1%. One to two Pediobius sp. emergence holes were found on the puparium of V. turrita, and its hyperparasitism rates ranged from 0.2% to 0.7%, with an average rate of 0.5%. An irregular emergence hole on the pupae of V. turrita was characteristic of T. maga. Its hyperparasitism rates were from 0.2% to 1.6%, with an average rate of 1.0% (Table 2).

Table 1.

Parasitism rates (%) of Arge pullata cocoons by parasitoids in Shennongjia, Hubei Province.


Table 2.

Hyperparasitoids and their hyperparasitism rates (%) of Vibrissina turrita puparia reared from Arge pullata cocoons.


Figure 1.

Mean parasitism rates (+ SE, n = 4) of Arge pullata by parasitoids in Shengnongjia. Bars with the same letter are not significantly different (ANOVA on arcsin (p)½, followed by the Ryan-Einot-Gabriel-Welsh (REGW) multiple Q test, at : α = 0.05). High quality figures are available online.


Figure 2.

Seasonal occurrence of Vibrissina turrita adults emerging from final instar larvae of Arge pullata in 2010. High quality figures are available online.



Under the experimental conditions, the average parasitism rate of A. pullata by parasitoids was as high as 11.0%. There may be a difference in parasitism rate between our experiment and field conditions. Natural enemies can continuously parasitize sawflies, so the parasitism rate for A. pullata sawflies in nature may be higher than it was in experimental conditions. Parasitoids play an important control effect on A. pullata populations in nature.

V. turrita was the dominant parasitoid, attacking 10.0% of A. pullata larvae, and it plays an important role in controlling these pests. V. turrita has also been recorded as a parasite on other sawflies, such as Allantus luctifer (Smith), Craesus varus (Villaret), Eriocampa ovata (L.), Empria abdominalis (Fabricius), Athalia rosae ruflcornis Jakovlev, Macrophya albicincta (Schrank), Pristiphora erichsonii (Hartig), Arge ustulata (L.), A. enodis (L.), A. pagana (Panzer), and A. ochropus (Gmelin) (Herting 1960; Shima 1983; Nagasaka 1988; Campadelli 1997). Most of V. turrita adults emerged from late May to early June, so timing was an important factor when using this parasitoid to control A. pullata.

Most Trigonalidae are recorded as hyperparasitoids of endoparasitic ichneumonids and tachinids, or parasitoids of vespids (Yamane and Yamane 1975; Gelhaus 1987; Smith 1996; Smith and Stocks 2005). Some trigonalids are parasitoids of sawflies, such as Taeniogonalos venatoria Riek on Perga affinis affinis Kirby (Raff 1934; Carne 1969). The biology and host relationships of trigonalid wasps were studied by Clausen (1931), Carmean (1991), Weinstein and Austin (1991), and Smith (1996).

Hyperparasitism rates of Compsilura concinnata (Meigen) by trigonalid wasps were from 16.0% to 47.0% (Kellogg et al. 2003). Hyperparasitism rates of V. turrita by T. maga were from 0.2% to 1.6%. The biology and host relationships of T. maga need more investigation.

The populations and effectiveness in biological control of parasitoids are sometimes restrained by hyperparasitoids. Marietta carnest (Howard) and Ablerus perspeciosus Girault are hyperparasitoids of Coccobius azumai Tachikawa, which was introduced from Japan to China (Huang 1994). Hyperparasitism can be as high as 16.0% in nature (Huang et al. 2005). The parasitoid Aphidius gifuensis Ashmead is a very important agent in biological control efforts against of Myzus persicae (Sulzer). However, hyperparasitoids have one of the main restriction factors in M. persicae control (Ren et al. 2000).

In biological control, introduced natural enemies may sometimes compete with native natural enemies, and weaken their overall control effect on target pests. Thus, future studies on host-parasite-hyperparasite interactions, and relations between foreign and native natural enemies, would provide valuable information needed for a successful biological control program against target pest insects, including the argid sawfly, A. pullata.


We are extremely grateful to Dr. David R. Smith (Department of Entomology, National Museum of Natural History, Smithsonian Institution, United States of America), and two anonymous reviewers for reviewing the manuscript and providing helpful comments. We would also like to thank Dr. David R. Smith, Dr. Chun-Tian Zhang (Shenyang Normal University), and Dr. Yan-Zhou Zhang (Institute of Zoology, Chinese Academy of Sciences) for identifying the parasitoids of Trigonalidae, Tachinidae, and Chalcidoidea. We also thank Xiao-Guang Chen for his help during field collections. This research was supported by the National Natural Science Foundation of China (NSFC, No. 30872035, No. 31010103057).



Q Austara , E Annila , B Bejer , B Ehnstrom . 1984. Insect pests in forests of the Nordic countries 1977–1981. Fauna Norvegica, Series B: Norwegian Journal of Entomology 31: 8–15. Google Scholar


E Brummerstedt , A Kristensen , R Nielsen , V Bille-Hansen . 1987. Death of a puppy after eating sawfly larvae. Case report. Dansk Veterinaertidsskr 70: 758–760. Google Scholar


G Campadelli . 1997. Notes on the biology of Vibrissina turrita (Meigen) (Dipt. : Tachinidae) on the Arge ochropus Gmel. (Hym.: Argidae) host. Bollettino dell'Istituto di Entomologia “Guido Grandi” della Università degli Studi di Bologna 51(1): 161– 170. Google Scholar


D Carmean . 1991. Biology of the Trigonalyidae (Hymenoptera), with notes on the vespine parasitoid Bareogonalos canadensis. New Zealand Journal of Zoology 18: 209–214. Google Scholar


PB Carne . 1969. On the population dynamics of the Eucalypt-defoliating sawfly Perga affinis affinis Kirby (Hymenoptera). Australian Journal of Zoology 17: 113–141. Google Scholar


TL Chen , ML Sheng . 2007. An important parasitoid of Acantholyda erythrocephala, Xenoschesis crassicornis Uchida (Hymenoptera: Ichneumonidae). Entomotaxonomia 29(1): 79–80. Google Scholar


CP Clausen . 1931. Biological notes on the Trigonalidae (Hymenoptera). Proceedings of the Entomological Society of Washington 33: 72–81. Google Scholar


K Escherich . 1942. Die Forstinsekten Mitteleuropas, fünfter band. Paul Parey-Verlag. Google Scholar


JK Gelhaus . 1987. A detritivore Tipula (Diptera: Tipulidae) as a secondary host of Poecilogonalos costalis (Hymenoptera: Trigonalidae). Entomological News 98(4): 161–162. Google Scholar


H Hara , A Shinohara . 2008. Taxonomy, distribution and life history of Betula-feeding sawfly, Arge pullata (Insecta, Hymenoptera, Argidae). Bulletin of the National Museum of Nature and Science, Series A, Zoology 34(3): 141–155. Google Scholar


B Herting . 1960. Biologie der westpalaarktischen Raupenfliegen (Diptera: Tachinidae). Monographien zur Angewandten Entomologie 16: 1–188. Google Scholar


J Huang . 1994. Systematic studies on Aphelinidae of China (Hymenoptera: Chalcidoidea). Chongqing Publishing House. Google Scholar


J Huang , ZH Wang , QY Lin . 2005. Notes on the two species of hyperparasitoids (Hymenoptera: Aphelinidae) of Hemiberlesia pitysophila (Homoptera: Diaspididae). Journal of Fujian Agriculture and Forestry University (Natural Science Edition) 34(2): 148–152. Google Scholar


SK Kellogg , LS Fink , LP Brower . 2003. Parasitism of native luna moths, Actias luna (L.) (Lepidoptera: Saturniidae) by the introduced Compsilura concinnata (Meigen) (Diptera: Tachinidae) in central Virginia, and their hyperparasitism by trigonalid wasps (Hymenoptera: Trigonalidae). Environmental Entomology 32(5): 1019–1027. Google Scholar


PR Li , ZX Yuan . 1993. The biological characteristics and controlling techniques of Arge pullata Zaddach. Forest Pest and Disease 2: 18–19. Google Scholar


JG Luo , YC Li , GF Chen . 2005. Review of research on insect parasite-Ichneumon wasps. Jiangxi Forestry Science and Technology 4: 34–37. Google Scholar


SF Min , MQ Wang , ML Sheng . 2010. A new Chinese record species of Ichneumonidae parasitizing Arge sp. (Hymenoptera). Acta Zootaxonomica Sinica 35(1): 251–253. Google Scholar


K Nagasaka . 1988. A new host of Vibrissina turrita (Diptera, Tachinidae) in Kyoto, Japan. Kontyû, Tokyo 56(3): 522. Google Scholar


M Nuorteva , H Nuorteva . 2007. Hävinneeksi luokitellun koivutuholaisen, pulskamailapistiäisen massaesiintymä Ylämaalla. Metsätieteen aikakauskirja 3: 313– 316. Google Scholar


H Pschorn-Walcher , M Kriegel . 1965. Zur Kenntnis der Parasiten der Bürstenhorn-Blattwespen der Gattung Arge Schrank (Hymenoptera: Argidae). Zeitschrift für angewandte Entomologie 56(3): 263–275. Google Scholar


SS Qi . 2000. Occurrence regularity and integrated control of Arge similes Vollenhoven. Forest Pest and Disease 6: 24–25. Google Scholar


JW Raff . 1934. Observations on saw-flies of the genus Perga, with notes on some reared primary parasites of the families Trigonalidae, Ichneumonidae, and Tachinidae. Proceedings of the Royal Society of Victoria 47: 54–77. Google Scholar


GW Ren , HJ Qin , WH Shi , GF Wang . 2000. Review on research of Aphidius gifuensis in China. Chinese Tobacco Science 1: 27–30. Google Scholar


ML Sheng , GF Chen . 2001. Ichneumonidae parasitizing sawflies from China (Hymenoptera). Entomofauna 22(21): 413– 420. Google Scholar


ML Sheng , LX Gao , SP Sun , Y Zhang , HT Zhang , JS Huang , HB Zhang . 2002. Studies on the parasitoids of Pachynematus itoi and their control abilities. Journal of Liaoning Forestry Science and Technology 2: 1–3. Google Scholar


ML Sheng , XF Zeng . 2010. Species of the genus Mastrus Förster (Hymenoptera, Ichneumonidae) of China with descriptions of two new species parasitizing sawflies (Hymenoptera). Zookeys 57: 63–73. Google Scholar


H Shima . 1983. Study on the tribe Blondeliini from Japan (Diptera, Tachinidae) IV. A revision of the genus Vibrissina Rondani. Kontyû, Tokyo 51(4): 635–646. Google Scholar


DR Smith . 1996. Trigonalyidae (Hymenoptera) in the eastern United States: seasonal flight activity, distributions, hosts. Proceedings of the Entomological Society of Washington 98(1): 109–118. Google Scholar


DR Smith , IC Stocks . 2005. A new trigonalid wasp (Hymenoptera: Trigonalidae) from eastern North America. Proceedings of Entomological Society of Washington 107(3): 530–535. Google Scholar


Y Takizawa . 1962. Notes on a Betula-feeding sawfly, Kanba-ruri-churenji (new Japanese name) (Interim report). Transactions of the Japanese Forestry Society 72: 340–342. Google Scholar


SM Thamsborg , RJ Jorgensen , E Brummerstedt . 1987. Sawfly poisoning in sheep and goats. Veterinary Record 121(11): 253–255. Google Scholar


G Wang , JW Sun , SC Ma , ML Sheng . 1996. A new species of Endasys Foerster (Hymenoptera: Ichneumonidae) parasitizing Pachynematus itoi Okutani (Hymenoptera: Tenthredinidae). Entomotaxonomia 18(3): 230–232. Google Scholar


HZ Wang , XG Li , JX Tong . 2000. The parasite and predator enemy of European pine sawfly Neodiprion sertifer (Geoffroy). Shaanxi Forest Science and Technology 3:30– 34. Google Scholar


P Weinstein , AD Austin . 1991. The host relationships of trigonalyid wasps (Hymenoptera: Trigonalyidae), with a review of their biology and catalogue to world species. Journal of Natural History 25(2): 399–433. Google Scholar


S Yamane , S Yamane . 1975. A new trigonalid parasite (Hymenoptera, Trigonalide) obtained from Vespula nests in Taiwan. Kontyû, Tokyo 43(4): 456–462. Google Scholar


Z Zhang , SZ Zhou . 1996. Study on the natural enemies of Chinese diprionid sawflies. Natural Enemies of Insects 18(4): 182–186. Google Scholar


AN Zhelochovtsev , AG Zinovjev . 1995. A list of the sawflies and horntails (Hymenoptera, Symphyta) of the fauna of Russia and adjacent territories. I. Entomologicheskoe Obozrenie 74(2): 395–415. Google Scholar
This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed.
Tao Li, Mao-Ling Sheng, Shu-Ping Sun, and You-Qing Luo "Parasitoids of the Sawfly, Arge pullata, in the Shennongjia National Nature Reserve," Journal of Insect Science 12(97), 1-8, (1 August 2012).
Received: 9 August 2011; Accepted: 1 February 2012; Published: 1 August 2012

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