A Larval Parasitoid of the Alfalfa Weevil, Hypera Postica (Coleoptera: Curculionidae) in Japan
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Biological Control 34 (2005) 144–151 www.elsevier.com/locate/ybcon Establishment of Bathyplectes anurus (Hymenoptera: Ichneumonidae), a larval parasitoid of the alfalfa weevil, Hypera postica (Coleoptera: Curculionidae) in Japan Megumi Shoubu a,¤, Masami Okumura a, Akinori Shiraishi a, Hidenori Kimura a, Masami Takagi b, Takatoshi Ueno b a Moji Plant Protection Station, Ministry of Agriculture and Fisheries, Moji Ward, Kitakyushu City, Fukuoka 801-0841, Japan b Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan Received 15 November 2004; accepted 21 April 2005 Available online 1 June 2005 Abstract The alfalfa weevil invaded Japan in the early 1980s. In Southwestern Japan, the weevil infests Chinese milk vetch, which is a main source of honey products. Since apiarists avoid application of insecticides, four species of parasitoid wasps were introduced from the US into Japan for biological control of the weevil in 1988 and 1989. In 1996, one of the parasitoids, Bathyplectes anurus (Thomson) was recovered. Accordingly, we started the survey to assess the incidence and eVectiveness of this parasitoid in suppressing the alfalfa weevil. B. anurus expanded its distribution during 1998–2003. In 1998 and 1999, the percentages of parasitism were mostly less than 5% but quickly increased to about 40% in 2003. The survey also showed that the extent of damage of the weevil on Chinese milk vetch decreased from 2001 to 2004; there was a negative correlation between the extent of weevil damage and the percentage parasit- ism one year previously. These results suggest that the parasitoid reduced damage by the alfalfa weevil. 2005 Elsevier Inc. All rignts reserved. Keywords: Bathyplectes anurus; Astragalus sinicus; Chinese milk vetch; Classical biological control; Parasitism; Introduction 1. Introduction zona in 1939 (Wehrle, 1940) and Maryland in 1951 (Poos and Bissell, 1953) independently, and it subse- The alfalfa weevil Hypera postica (Gyllenhal) is native quently spread throughout the US. Like other pests that to the Old World and has a wide distribution there, invaded a new area without their natural enemies, the occurring throughout Europe and ranging to North alfalfa weevil became a destructive pest that damaged Africa, the Middle East, India, and Western Asia the production of alfalfa in North America; it was the (Clausen, 1977). The weevil mainly infests legumes (Essig most important pest of alfalfa in the US (USDA, 1968, and Michelbacher, 1933). It is rarely of economic impor- 1972). tance in its original range (Clausen, 1977; Essig and The alfalfa weevil was the target of biological control Michelbacher, 1933). after its introduction to the US; 12 parasitoids were In the US, the weevil was Wrst discovered in Utah in introduced as candidates for biological control in the 1904 (Titus, 1910). Then it was found to occur in Ari- states (Brunson and Coles, 1968; Bryan et al., 1993; Chamberlin, 1924a,, 1926). To date, biological control of alfalfa weevil has met great success in Northeastern and * Corresponding author. North Central States (Day, 1981; RadcliVe and Flan- E-mail address: [email protected] (M. Shoubu). ders, 1998). 1049-9644/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2005.04.009 M. Shoubu et al. / Biological Control 34 (2005) 144–151 145 In 1980s, the alfalfa weevil was accidentally intro- follow-up surveys had been held for 2 or 3 years after duced into Japan. Discovered in Okinawa Pref. and release except one location, Shiranoe, Moji Ward. How- Fukuoka Pref. in 1982, it infested leguminous forbs, ever, no parasitoid species were recovered for several including Vicia angustifolia L., Trifolium repens L., Medi- years after the release; the establishment appeared to cago polymorpha L., and Melilotus oYcinalis (L.) (Baba, have failed. 1983; Tao, 1984). In Japan, those legumes are “forbs”; In 1996, one cocoon of B. anurus was collected unex- they have no commercial value. The weevil was not pectedly in Shiranoe, Moji Ward, Kitakyushu City found to attack farm products in early 1980s. The most (33°56ЈN, 131°00ЈE), where the parasitoid had been lib- suitable host of the weevil, alfalfa, is commercially erated in 1991 and 1992 but no subsequent surveys had grown only in Hokkaido, a Northern Island where wee- unfortunately been done to conWrm establishment in vil damage has not been reported. Thus, there was no that place. A cocoon was discovered adjacent to the economic damage for some years after its invasion into release point, and there was no other release record of Japan (Baba, 1983; Tao, 1984). the species in Kitakyushu City or within 20 km around However, the weevil became a serious pest in Chinese Shiranoe. This suggested that one of introduced parasit- milk vetch, Astragalus sinicus L. after the late 1980s oid species became established in Moji Ward. (Morimoto, 1987). Chinese milk vetch had not recorded as Bathyplectes anurus is a solitary endoparasitoid of lar- a host plant of the weevil until then. It is originally from vae of the alfalfa weevil. It has one generation in each China (Yasue, 1987), where the alfalfa weevil does not year, and attacks the weevil larvae in spring (Bartell and present (Essig and Michelbacher, 1933). Hence, it is likely Pass, 1980; Brunson and Coles, 1968; Dowell and Horn, that Chinese milk vetch is a new host plant for the weevil. 1977). In the US, B. anurus is one of the key biological Chinese milk vetch is planted in fallow paddy Welds control agents of alfalfa weevil. This parasitoid was intro- from winter to spring as a green manure crop, and the duced from Europe and is well established (Berberet and Xowers are the main source of honey production in Bisges, 1998; Giles et al., 1994; Harcourt, 1990; Oloumi- Japan. Furthermore, honey collected from Chinese milk Sadeghi et al., 1993; Parr et al., 1993). France was the pri- vetch is thought to be of the best quality and the most mary source of the introduction (Dysart and Day, 1976). valuable among all kinds of honey (Yasue, 1987). There has been no study about the establishment, Chinese milk vetch Xowers during the period of incidence, and eVectiveness of this parasitoid since its weevil larval occurrence in Japan. The larvae of the introduction in Japan. In 1998, 2 years after the Wrst weevil feed on Xower buds and Xowers (Ono et al., 1987). recovery of B. anurus in Japan, we began a survey of When large numbers of weevil larvae are present, Xowers alfalfa weevil and the parasitoid in Kitakyushu City. Our of Chinese milk vetch are entirely devoured, and the pro- objectives were to conWrm the establishment of B. anu- duction of honey from Chinese milk vetch is greatly rus, and to assess its current eVectiveness in suppressing decreased. the alfalfa weevil. Abundance of weevil larvae, extent of Application of insecticides is avoided by apiarists damage of the weevil on Chinese milk vetch, and inci- because they may kill bees and possibly contaminate dence of the parasitoid were investigated in the Weld. The honey products. Accordingly, Moji Plant Protection Sta- relation between abundance of the weevil larvae in a tion initiated a project of biological control of the weevil. given year and percentage of parasitism in the previous Although there are several indigenous natural enemies in year was analyzed. Japan, they are ineVective in reducing populations of the alfalfa weevil (Okumura, 1991; Okumura et al., 1987; Yamaguchi et al., 1991). 2. Materials and methods Classical biological control of the weevil was planned accordingly. Through cooperation with USDA, APHIS- Surveys were conducted every spring from 1998 to 2004. PPQ (Bryan et al., 1993), four species of parasitoid Since preliminary observations had shown that emergence wasps, which had been collected in the US, were intro- of B. anurus adults reached the peak around early April in duced into Japan in 1988 and 1989; two parasitoids of Northern Kyushu, Weld surveys were conducted from late larvae, Bathyplectes anurus (Thomson) and B. curculio- April to early May. During this period, most of weevil lar- nis (Thomson) (Ichneumonidae) and two parasitoids of vae are in their fourth instars, i.e., the last larval instar, and adults, Microctonus aethiopoides Loan and Microctonus the oviposition period of B. anurus has been ended. Thus, colesi Drea (Braconidae). These parasitoids were cul- collecting weevil larvae in that period allows assessing the tured in the National Biological Control Laboratory, annual parasitism of the weevil. USDA. The three parasitoid species, except M. colesi, were released in various parts of Kyushu Island from 2.1. Establishment and disperse of the parasitoid 1989. Usually over 300 (at least 100) adults of one (rarely two or three) species were released per site, and then in Surveys were carried out to estimate the distribution the appropriate season for each parasitoid species, of the parasitoid in Kitakyushu City (Fig. 1) since 146 M. Shoubu et al. / Biological Control 34 (2005) 144–151 Fig. 1. The distribution and expansion of B. anurus in Kitakyushu City during the years of 2000–2003. Solid circle, locality where B. anurus detected; open circle, locality where B. anurus not detected. 1998–2003. Alfalfa weevil larvae were sampled from out, but was left in the paper bag to prevent loss of lar- legumes and Chinese milk vetch and were reared in the vae, and to provide a pupation site. Feeding was contin- laboratory to determine whether the parasitoid was dis- ued for about 2 weeks. Then paper bags were stored in tributed at each sampling location. Sampling locations the rearing room. One month later, cocoons of B. anurus were selected arbitrarily. Since many of sampling loca- were extracted from plant debris by rubbing dried mate- tions were in disturbed environments, like a levee, edge rials, to ascertain whether the parasitoid occurred at of a road or vacant land in residential areas, we could each sampling locations.