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Macrocentrus cingulum (=grandii) Brischke
(Hymenoptera: Braconidae)

by William R. Morrison III, Department of Entomology, Michigan State University, 243 Natural Science, East Lansing, MI 48824

In 1926, Macrocentrus cingulum was introduced to the U.S. from France and Korea along with a range of other exotic natural enemies to control European corn borer (Ostrinia nubilalis; Parker, 1931; Baker et al., 1949; Watanabe, 1967), a moth whose caterpillars damage corn plants by boring into their stems. Macrocentrus cingulum attacks caterpillars of the European corn borer, exerting low to moderate levels of parasitism in the field (Winne and Chiang, 1982; Onstad et al., 1991). Macrocentrus cingulum may also be referred to by its synonymous (i.e. equivalent) names, M. grandii Goidanich, M. abdominalis Fab. or M. gifuensis Ashmead (Thompson and Parker, 1928; Parker, 1931; van Achterberg and Haeselbarth, 1983).

Appearance

Adults are usually 4 mm in length, and range in color from black to brick red (Fig. 1A). The head is usually dark brown to black (Watanabe, 1967). Adults have an elongated abdomen and a long egg-laying structure (ovipositor) protruding from the rear. The top of the abdomen usually has a pale colored band (Watanabe, 1967).

Habitat

Macrocentrus cingulum has been recorded from Europe, Japan, Korea and China (Watanabe, 1967), and was introduced to North America (Parker, 1931). It is the most abundant parasitoid of the European corn borer in the Midwestern and Northeastern U.S. (Peairs and Lilly, 1975; Andreadis, 1982; Romig et al., 1985; Cossentine and Lewis, 1987). In the lab, individuals of M. cingulum are attracted to odors released by corn, and to a lesser extent, potato and snap beans (Udayagiri, 1991; Udayagiri and Jones, 1992). This behavioral flexibility could allow it to locate its host, the generalist European corn borer, as it feeds on different plants (Jones, 1996). However, in nature M. cingulum has only been found attacking the European corn borer in cornfields (Losey et al., 2001).

Pests attacked

The main host for M. cingulum in North America is the European corn borer (Ostrinia nubilalis; Fig. 1B). However, it also parasitizes the Asian corn borer, Ostrinia furnacalis, in its native range in Eurasia (Nardo and Hopper, 2004).

European Corn Borer, main host of Macrocentrus cingulum

Photo by W.R.M. Source specimen material: Michigan State University's Albert J. Cook Research Collection

Life cycle

Females of M. cingulum lay eggs on 2nd to 4th instars (immature stages) of the European corn borer (Dittrick and Chiang, 1982). Opportunities to lay eggs are often scarce, because the corn borer uses the cavity it excavates in the corn stalk as a refuge (Edwards and Hopper, 1999). This species is polyembryonic, meaning that many individuals can develop from one egg and are all clones (genetically identical) to each other (Craig et al., 1997). On average, 25-26 wasps emerge from one corn borer host (Parker, 1931).

This species has a total of four larval stages. The first three of these feed on the European corn borer host from within. The fourth immature stage emerges from the host when the corn borer becomes a pupa (Fig. 2), and finishes feeding on the host from the outside. Each individual of M. cingulum spins its own cocoon near the body of the host; together these form a mass of spun cocoons (Parker, 1931). After remaining in the pupa for some period of days, the individuals all emerge around the same time. In the lab, adult females live around 21 days while males live 14 days (Fadamiro and Heimpel, 2001), but survival in the field is likely to be shorter. There are two generations of M. cingulum per year (Siegel et al., 1986).

Relative Effectiveness

The effectiveness of M. cingulum ranges from low to moderate, depending on location, infection by pathogens and other factors. In Pennsylvania, around 17% of corn borers were parasitized by this wasp (Losey et al., 1992), while in Illinois, the rate of parasitism ranged from 4%-23% (Siegel et al., 1986). Macrocentrus cingulum has been shown to transmit the protozoan Nosema pyrausta (York, 1961) between individuals of its host (Siegel et al., 1986). This protozoan causes disease in corn borer. Consequently, M. cingulum could provide a service by increasing the spread of this pathogen. From 17-75% of M. cingulum were infected with this protozoan, suggesting a high potential for M. cingulum to transmit this disease in corn borer populations (Siegel et al., 1986). However, this parasite can also decrease the lifespan of the adult wasp and depress reproduction (Andreadis, 1980; Siegel et al., 1986). Thus, infection by N. pyrausta may be one of the causes of low or decreasing effectiveness of M. cingulum in controlling European corn borer populations (Andreadis, 1982).

One of the attempts to increase the effectiveness of M. cingulum focused on managing the habitat surrounding fields. This wasp feeds primarily on nectar from native flowers, such as milkweed and ironweed (Orr and Pleasants, 1996). It is possible that planting these additional types of floral resources along field edges may increase the survival of M. cingulum and increase its control of European corn borer.

Pesticide Susceptibility

This parasitoid is susceptible to microbial infections, including N. pyrausta (Flexner et al., 1986), for reasons elaborated above. Transgenic Bt (insect resistant) corn and the insecticide permethrin were both shown to decrease the abundance of M. cingulum, likely as a result of decreased host availability (Bruck et al., 2006). Pesticide susceptibility has not been evaluated.

Commercial availability

Macrocentrus cingulum is not commercially available (Hunter, 1997).

Acknowledgements

W.R.M. is funded by a C.S. Mott Predoctoral Fellowship in Sustainable Agriculture and by a Michigan State University Extension Project GREEEN Grant (GR10-052). Thanks to the Gary Parsons at Michigan State University for providing specimens to photograph from the Albert J. Cook Arthropod Research Collection.

References

Andreadis, T.G. 1980. Nosema pyrausta infection in Macrocentrus grandii, a braconid parasite of the European corn borer, Ostrinia nubilalis. Journal of Invertebrate Pathology 35: 229-233.

Andreadis, T.G. 1982. Impact of Nosema pyrausta on field populations of Macrocentrus grandii, an introduced parasite of the European corn borer, Ostrinia nubilalis. Journal of Invertebrate Pathology 39: 298-302.

Baker, W.A., W.G. Bradley and C.A. Clark. 1949. Biological control of the European corn borer in the United States. USDA Technology Bulletin 983: 185.

Bruck, D.J., M.D. Lopez, L.C. Lewis, J.R. Prasifka and R.D. Gunnarson. 2006. Effects of transgenic Bacillus thuringiensis corn and permethrin on nontarget arthropods. Journal of Agriculture and Urban Entomology 23: 111-124.

Cossentine, J.E. and L.C. Lewis. 1987. Development of Macrocentrus grandii Goidanich within microsporidian-infected Ostrinia nubilalis (Hübner) host larvae. Canadian Journal of Zoology 65: 2532-2535.

Craig, S., L. Slobodkin, G. Wray and C. Biermann. 1997. The ‘paradox’of polyembryony: a review of the cases and a hypothesis for its evolution. Evolutionary Ecology 11: 127-143.

Ding, D., P.D. Swedenborg and R.L. Jones. 1989. Plant odor preferences and learning in Macrocentrus grandii (Hymenoptera: Braconidae), a larval parasitoid of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Journal of the Kansas Entomological Society 62: 164-176.

Dittrick, L.E. and H.C. Chiang. 1982. Developmental characteristics of Macrocentrus grandii as influenced by temperature and instar of its host, the European corn borer. Journal of Insect Physiology 28: 47-52.

Edwards, O.R. and K.R. Hopper. 1999. Using superparasitism by a stem borer parasitoid to infer a host refuge. Ecological Entomology 24: 7-12.

Fadamiro, H.Y. and G.E. Heimpel. 2001. Effects of partial sugar deprivation on lifespan and carbohydrate mobilization in the parasitoid Macrocentrus grandii (Hymenoptera: Braconidae). Annals of the Entomological Society of America 94: 909-916.

Flexner, J.L., B. Lighthart and B.A. Croft. 1986. The effects of microbial pesticides on non-target, beneficial arthropods. Agriculture, Ecosystems & Environment 16: 203-254.

Hunter, C.D. 1997. Suppliers of beneficial organisms in North America. Sacremento, CA.

Jones, R.L. 1996. Semiochemicals in host and mate finding behavior of Macrocentrus grandii Goidanich (Hymenoptera: Braconidae). Florida Entomologist 79: 104-108.

Losey, J.E., D.D. Calvin, M.E. Carter and C.E. Mason. 2001. Evaluation of noncorn host plants as a refuge in a resistance management program for European corn borer (Lepidoptera: Crambidae) on Bt-corn. Environ Entomol 30: 728-735.

Losey, J.E., P.Z. Song, D.M. Schmidt, D.D. Calvin and D.J. Liewehr. 1992. Larval parasitoids collected from overwintering European corn borer (Lepidoptera: Pyralidae) in Pennsylvania. Journal of the Kansas Entomological Society 65: 87-90.

Nardo, E.A.B. and K.R. Hopper. 2004. Using the literature to evaluate parasitoid host ranges: a case study of Macrocentrus grandii (Hymenoptera: Braconidae) introduced into North America to control Ostrinia nubilalis (Lepidoptera: Crambidae). Biological Control 31: 280-295.

Onstad, D.W., J.P. Siegel and J.V. Maddox. 1991. Distribution of parasitism by Macrocentrus grandii (Hymenoptera: Braconidae) in maize infested by Ostrinia nubilalis (Lepidoptera: Pyralidae). Environmental Entomology 20: 156-159.

Orr, D.B. and J.M. Pleasants. 1996. The potential of native prairie plant species to enhance the effectiveness of the Ostrinia nubilalis parasitoid Macrocentrus grandii. Journal of the Kansas Entomological Society 133-143.

Parker, H.L. 1931. Macrocentrus gifuensis Ashmead, a polyembryonic braconid parasite in the European corn borer.

Peairs, F.B. and J.H. Lilly. 1975. Parasites Reared from Larvae of the European corn borer, Ostrinia nubilalis (Hbn.), in Massachusetts, 1971-73 (Lepidoptera, Pyralidae). Journal of the New York Entomological Society 83: 36-37.

Romig, R.F., C.E. Mason and P.P. Burbutis. 1985. Parasitism of the European corn borer by Lydella thompsoni and Macrocentrus grandii in southeast Pennsylvania and Delaware. Entomological News 96: 121–128.

Siegel, J.P., J.V. Maddox and W.G. Ruesink. 1986. Impact of Nosema pyrausta on a braconid, Macrocentrus grandii, in central Illinois. Journal of Invertebrate Pathology 47: 271-276.

Thompson, W.R. and H.L. Parker. 1928. The European corn borer and its controlling factors in Europe. USDA Technology Bulletin 59: 1-62.

Udayagiri, S. 1991. A chemically mediated interaction between plants and Macrocentrus grandii Goidanich (Hymenoptera: Braconidae), a specialist parasitoid of European corn borer. University of Minnesota, Minneapolis, MN.

Udayagiri, S. and R.L. Jones. 1992. Role of plant odor in parasitism of European corn borer by braconid specialist parasitoid Macrocentrus grandii Goidanich: Isolation and characterization of plant synomones eliciting parasitoid flight response. Journal of Chemical Ecology 18: 1841-1855.

van Achterberg, C. and E. Haeselbarth. 1983. Revisionary notes on the European species of Macrocentrus Curtis sensu stricto (Hymenoptera: Braconidae). Entomofauna 4: 37-59.

Watanabe, C. 1967. Further revision of the genus Macrocentrus Curtis in Japan, with descriptions of two new species (Hymenoptera, Braconidae). Insecta Matsumurana 30: 1-16.

Winne, W.V. and H.C. Chiang. 1982. Seasonal history of Macrocentrus grandii [Hym.: Braconidae] and Eriborus terebrans [Hym.: Ichneumonidae], two parasitoids of the European corn borer, Ostrinia nubilalis [Lep.: Pyralidae]. BioControl 27: 183-188.

York, G.T. 1961. Microsporidia in parasites of the European corn borer. Journal of Insect Pathology 3: 101–102.

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