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Possibilities for Biological Control of the Western Corn Rootworm, Diabrotica Virgifera Virgifera Leconte, in Central Europe

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Possibilities for Biological Control of the Western Corn Rootworm, Diabrotica Virgifera Virgifera Leconte, in Central Europe BiocontrolNews and Information 1998 Vol. 19 No. 2 59N–68N Review Article Possibilities for biological control of the western corn rootworm, Diabrotica virgifera virgifera LeConte, in Central Europe Ulrich Kuhlmann1 and Wiard A. C. M. van der Burgt2 1 CABI Bioscience Centre Switzerland, Delémont, Switzerland 2 Department of Entomology, University of Wageningen, The Netherlands Abstract The western corn rootworm, Diabrotica virgifera virgifera, was introduced to Europe from North America in the early 1990s. It spread rapidly from its site of introduction in Serbia and is now found over some 400,000 ha of southeastern Europe. The prospects for its classical biological control by introduction of natural enemies, including pathogens, nematodes and insects, from its area of origin are considered, based on a review of natural enemy–Diabrotica associations in the New World. The need for an integrated pest management (IPM) strategy is highlighted, and initial monitoring and management pro- grammes in central Europe are described. Research looking at the possibility of using augmentation and conservation biological control techniques, and behavioural control measures based on attractants and pheromones being conducted at various centres in Europe are also described. Introduction It is assumed that D. virgifera virgifera and maize evolved together in the tropics or subtropics of Mesoamerica The western corn rootworm, Diabrotica virgifera virgifera (Mexico/Central America) (Branson & Krysan, 1981). LeConte (Col., Chrysomelidae) is the most important Important natural enemies may occur locally in areas of pest of maize in the USA and Canada causing yield maize cultivation in southeastern Europe, particularly losses and chemical control costs of up to one billion US polyphagous predators, but specialized parasitoids, dollars annually (Krysan & Miller, 1986; Chandler et al., predators and pathogens may be lacking, because they 1995). In the early 1990s it was accidentally introduced have been left behind in the area of origin. In the from the USA to southeastern Europe. The beetle was absence of specialized natural enemies, Diabrotica popu- first observed in 1992 close to the Belgrade international lations in southeastern Europe are only limited by the airport, Serbia, occupying an area of only about 60 ha availability of suitable food, the influence of abiotic fac- (Baca, 1994). By 1997 the pest had spread widely tors, and the application of control treatments. Classical through Serbia, Bosnia-Herczegowina, Hungary, biological control has an important application in the Romania and Croatia (also probably Bulgaria but this management of invasive alien pest species in the agri- has not been confirmed), and occupies an area covering cultural crop environment, and allows the safe and approximately 400,000 ha (H. K. Berger pers. comm., selective control of pest species and thereby helps to 1997). It is expected that in the future, the pest will protect local biodiversity. Biological control has the potential to reduce local and regional populations of colonize Slovenia, Bulgaria, Austria, Italy, Moldova, western corn rootworm through the importation of spe- Ukraine and Slovakia, and eventually invade all maize cialized natural enemies from the region of origin of the producing countries in Eurasia. pest. About twenty thousand hectares of maize in Serbia were In South and North America, corn rootworms are heavily infested and showed economic damage in 1997 attacked by a range of pathogens, nematodes, predators (H. K. Berger pers. comm., 1997; W. A. C. M. van der and parasitoids, some of which appear to be rather spe- Burgt unpublished data, 1997). In countries which cialized natural enemies of D. virgifera virgifera and already have the western corn rootworm, about 6.5 mil- related species in the soil. Recent reviews on the man- lion hectares of maize are grown, while the total maize agement strategies of Diabrotica species deal only briefly growing area in Europe is about 14 million hectares. with natural control agents (Levine & Oloumi-Sadeghi, Therefore the problem is only just beginning to manifest 1991; Baca et al., 1995). This paper presents a detailed lit- itself and requires timely interventions to minimize the erature review on natural enemies–Diabrotica species impact of this invading pest. associations in South and North America. 59N 60N BiocontrolNews and Information 1998 Vol. 19 No. 2 Natural Enemies of Diabrotica Species undecimpunctata (von Tersch et al., 1994). Treatment of D. undecimpunctata howardi larvae and adults of D. virgifera Pathogens and Diabrotica longicornis (Say) with B. thuringiensis and Bacillus popilliae showed that application of spores to the Pathogens such as gregarine and microsporidian proto- food substrate did not increase mortality of corn root- zoa, fungi, bacteria and virus-like particles have been worms (Sutter, 1969). The bacterium Pseudomonas aerugi- found in corn rootworms; however the role these biolog- nosa, isolated from laboratory cultures of D. ical control agents play in the field is mostly unknown undecimpunctata in South Dakota, was tested and found (Levine & Oloumi-Sadeghi, 1991). Although the soil to have some value as a biological control agent against provides protection to biological control agents from D. undecimpunctata howardi and D. virgifera (Hamilton, desiccation and UV radiation, it also contains antagonistic 1968). The bacteria associated with the intestine of microorganisms that may limit the effectiveness of these Diabrotica balteata LeConte were surveyed in adults col- agents (Kinney et al., 1989). lected by Schalk et al. (1987); of the species identified Proteus mirabilis and Pseudomonas aeruginosa are insect Protozoa pathogens. Applications of the ice-nucleating-active bac- Brooks & Jackson (1990) reviewed studies on the eugre- terium Pseudomonas syringae to D. undecimpunctata garines of Diabrotica species. Occasional sampling indi- reduced its coldhardiness and Strong-Gunderson et al. cated that the incidence of gregarine infections in the (1992) proposed that ice-nucleating-active bacteria may field ranges from 5% to 100%. Gregarine infections have be used as a biological insecticide for the control of been shown to increase adult mortality and inhibit ovar- insect pests in winter. ian and fat body development in D. virgifera virgifera. It is concluded that eugregarines are debilitative and most Viruses virulent under suboptimal conditions or unnaturally Regarding viruses, in an ultrastructural study on the high intensity levels of infection, but only a few species testes and spermatheca of adults of D. virgifera virgifera, have potential as biological control agents (Brooks & large masses of 24- to 26-nm virus particles were found Jackson, 1990). in the cytoplasm of spermatocyst cells (Degrugillier et al., 1991). Degrugillier et al. (1991) showed that there was Fungi a high incidence of abnormal sperm but the virus did Corn rootworms probably acquire fungal infections in not appear to affect the chrysomelid adversely in terms the larval or pupal stage (Levine & Oloumi-Sadeghi, of life span, motility and mating behaviour. 1991). The fungus Beauveria bassiana (Bals.) Vuill. (Mitosporic fungi; formerly Deuteromycetes) can cause Nematodes natural epizootics in corn rootworm populations Tests to control Diabrotica spp. with nematodes have (Maddox & Kinney, 1989). Heineck-Leonel & Salles yielded diverging results. Laboratory tests have resulted (1997) carried out a survey of natural enemies of in high mortality, but the results of field tests depend Diabrotica speciosa (Germar) in southern Brazil and found very much on environmental conditions (i.e. insufficient B. bassiana and Metarhizium anisopliae (Metsch.) Sorok soil moisture is detrimental) and application techniques (Mitosporic fungi). Tonet & Reis (1979) demonstrated (Barbercheck, 1993; Jackson & Brooks, 1995). the pathogenicity of B. bassiana to D. speciosa in the laboratory and factors influencing sporulation were Among the entomopathogenic nematodes, the investigated with a view to its use in biological control Steinernematidae and Heterorhabditidae are the most as biopesticides. Branson et al. (1975) mentioned the studied species (Table 1). Steinernema carpocapsae occurrence of B. bassiana in laboratory rearings of D. vir- (Weisser, 1955) Wouts, Mracek, Gerdin & Bedding, 1982 gifera virgifera. This fungus occurs when the relative was most effective against the second and third corn humidity is higher than 75% to 80% and the temperature rootworm larval stages and in the pupal stage, where it varies between 24°C and 27°C. Soil moisture, soil type, was found to complete its life cycle (Jackson & Brooks, soil fertility, fungal strain and presence of other 1995). Larvae of D. virgifera virgifera were most suscepti- microbes have been identified as factors greatly affecting ble to a Mexican strain of S. carpocapsae (Jackson & the infectivity of B. bassiana in laboratory bioassays Brooks, 1989). In addition, D. virgifera virgifera was suc- (Tonet & Reis, 1979; Kinney et al., 1989). Kinney et al. cessfully parasitized by S. carpocapsae, showing a mortal- (1989) studied B. bassiana for many years in the field, but ity rate of more than 90% under controlled conditions its potential for reducing corn rootworm feeding dam- (Nickle et al., 1994). In field and laboratory experiments age has not been proven. Naranjo & Steinkraus (1988) S. carpocapsae caused 93.3% mortality of D. balteata and collected cadavers of Diabrotica barberi Smith
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