Ostrinia nubilalis (European maize borer)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Hosts/Species Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Natural enemies
- Notes on Natural Enemies
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Ostrinia nubilalis (Hübner)
Preferred Common Name
- European maize borer
Other Scientific Names
- Botys nubilalis Robin & Laboulbène, 1884
- Botys silacealis Hübner, 1796
- Micracris nubilalis
- Micractis nubilalis Hübner
- Pyralis nubilalis Hübner, 1796
- Pyrausta nubilalis Meyrick, 1890
- Pyrausta silacealis
International Common Names
- English: corn borer, European; corn moth; European corn borer; stalk borer
- Spanish: barrenador del maiz; gusano barrenador europeo; piral del maíz; taladro del maiz
- French: pyrale du maïs
Local Common Names
- Denmark: majsborer
- Finland: maissikoisa
- Germany: Maiszünslers; Zuensler, Hirse-; Zuensler, Hopfen-; Zuensler, Mais-
- Israel: norer hatirus haeropi
- Italy: Piralide del canapa; Piralide del granturco; Piralide del mais
- Japan: Awa-nomeiga
- Netherlands: Maisboorder; Maisboorder, wrattige
- Norway: maisborer
- Sweden: majsmott
- Turkey: misir kurdu
- PYRUNU (Ostrinia nubilalis)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Arthropoda
- Subphylum: Uniramia
- Class: Insecta
- Order: Lepidoptera
- Family: Crambidae
- Genus: Ostrinia
- Species: Ostrinia nubilalis
Notes on Taxonomy and NomenclatureTop of page The genus Ostrinia includes 20 species (Mutuura and Munroe, 1970). Only four of these are recognized as pests: O. nubilalis and O. furnacalis are pests primarily of maize; O. obumbratalis is a minor pest of maize; and O. zaguliaevi is a pest of legumes. O. nubilalis is the most important of these pests and attacks the greatest number of plant species. This species was first described by Hübner in 1796. Mutuura and Munroe (1970) report generic combinations and synonyms; only those most frequently used are listed. Three subspecies are recognized: Ostrinia nubilalis nubilalis (Hübner); Ostrinia nubilalis mauretanica (Mutuura and Munroe), which is similar to the nominate subspecies but smaller and paler; and Ostrinia nubilalis persica (Mutuura and Munroe), which differs slightly in its male genitalia and in male forewing and hindwing colour.
DescriptionTop of page Eggs
The egg is nearly flat and ca 1mm in diameter. It is white when first laid but later turns yellow, and the black head of the larva can be seen just before hatching. The eggs are laid in a mass and overlap like tiles on a roof. The average number of eggs per egg mass is 30, but it is possible to find egg masses with >50 eggs or some with only 4-5 eggs.
First-instar larvae are ca 1.5 mm long and mature larvae reach a length of 2-2.5 cm. Heinrich (1919) described the immature stages of the borer. The head and the prothoracic shield are black in the first instars and by the fourth instar they turn dark brown. The full-grown larva (fifth instar) is grey to light brown or pink. Dorsally in each segment there is a series of four anterior spots followed by two small posterior spots, and each spot has a seta. The ventral side of the body is cream-coloured and unmarked.
Female pupae are ca 2 cm; male pupae are generally smaller and thinner. Pupae are light to dark reddish-brown.
Mutuura and Munroe (1970) published an illustrated technical description of the adults of O. nubilalis nubilalis and noted distinguishing features of the other subspecies (O. nubilalis mauretanica and O. nubilalis persica).
The forewings of O. nubilalis are ca 30 mm long. The female is a moth with a robust body. The colour varies from a pale yellow to light brown. The male moth is slightly smaller, more slender bodied, and darker than the female and the male genitalia characteristics are described by Mutuura and Munroe (1970).
DistributionTop of page O. nubilalis attacks a variety of cereals and other crops in North America, Europe and North Africa. Brindley and Dicke (1963) and Brindley et al. (1975) reviewed the distribution of O. nubilalis and other studies on O. nubilalis in the USA and Canada.
It is likely that records of the pest in China (Hubei, Nei Menggu, Ningxia and Xinjiang (Anon., 1988)) and Taiwan (Horng et al., 1988) represent misidentifications of several species that have been isolated as separate species by Mutuura and Munroe (1970), and those in India (EPPO, 2003), Indonesia (EPPO, 2003; Waterhouse, 1993), Singapore (APPPC, 1987), Thailand and Vietnam (Waterhouse, 1993) represent misidentifications, possibly of O. furnacalis.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Present||Present based on regional distribution.|
|-Gansu||Present||Liu and Hou, 2004|
|-Hebei||Present||Li et al., 2003|
|-Jilin||Present||Schmutzenhofer et al., 1996|
|-Liaoning||Present||Schmutzenhofer et al., 1996|
|-Nei Menggu||Present||Schmutzenhofer et al., 1996|
|-Xinjiang||Present||Li et al., 2003|
|Georgia (Republic of)||Present||IIE, 1991; EPPO, 2014|
|India||Absent, unreliable record||EPPO, 2014|
|Indonesia||Absent, unreliable record||EPPO, 2014|
|Iran||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|Israel||Present||IIE, 1991; EPPO, 2014|
|Lebanon||Present||IIE, 1991; EPPO, 2014|
|Syria||Present||IIE, 1991; EPPO, 2014|
|Turkey||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|Algeria||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|Egypt||Present||IIE, 1991; EPPO, 2014|
|Libya||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|Morocco||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|Tunisia||Present||IIE, 1991; EPPO, 2014|
|-Alberta||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|-Manitoba||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|-New Brunswick||Present||IIE, 1991; EPPO, 2014|
|-Newfoundland and Labrador||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|-Nova Scotia||Present||IIE, 1991; EPPO, 2014|
|-Ontario||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|-Prince Edward Island||Present||IIE, 1991; EPPO, 2014|
|-Quebec||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|-Saskatchewan||Present||IIE, 1991; EPPO, 2014|
|-Alabama||Present||IIE, 1991; EPPO, 2014|
|-Arkansas||Present||McLeod et al., 2007|
|-Colorado||Present||IIE, 1991; EPPO, 2014|
|-Connecticut||Present||IIE, 1991; EPPO, 2014|
|-Delaware||Present||IIE, 1991; EPPO, 2014|
|-Florida||Present||United States Department of Agriculture, 1977|
|-Georgia||Present||IIE, 1991; EPPO, 2014|
|-Illinois||Present||IIE, 1991; EPPO, 2014|
|-Indiana||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|-Iowa||Present||IIE, 1991; EPPO, 2014|
|-Kansas||Present||Calvin et al., 1988; EPPO, 2014|
|-Kentucky||Present||IIE, 1991; EPPO, 2014|
|-Louisiana||Present||IIE, 1991; EPPO, 2014|
|-Maine||Present||Kuhar et al., 2004|
|-Maryland||Present||IIE, 1991; EPPO, 2014|
|-Massachusetts||Present||IIE, 1991; EPPO, 2014|
|-Michigan||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|-Minnesota||Present||IIE, 1991; EPPO, 2014|
|-Mississippi||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|-Missouri||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|-Nebraska||Present||IIE, 1991; EPPO, 2014|
|-New Hampshire||Present||IIE, 1991; EPPO, 2014|
|-New Jersey||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|-New York||Present||IIE, 1991; EPPO, 2014|
|-North Carolina||Present||IIE, 1991; EPPO, 2014|
|-North Dakota||Present||IIE, 1991; EPPO, 2014|
|-Ohio||Present||IIE, 1991; EPPO, 2014|
|-Oklahoma||Present||IIE, 1991; EPPO, 2014|
|-Pennsylvania||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|-Rhode Island||Present||IIE, 1991; EPPO, 2014|
|-South Carolina||Present||IIE, 1991; EPPO, 2014|
|-South Dakota||Present||IIE, 1991; EPPO, 2014|
|-Tennessee||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|-Texas||Present||Stodola et al., 2006|
|-Vermont||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|-Virginia||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|-West Virginia||Present||IIE, 1991; EPPO, 2014|
|-Wisconsin||Present||IIE, 1991; EPPO, 2014|
|Austria||Restricted distribution||193*||IIE, 1991; EPPO, 2014|
|Belarus||Present||Trepashko et al., 2013|
|Belgium||Present||IIE, 1991; EPPO, 2014|
|Bulgaria||Widespread||****||IIE, 1991; EPPO, 2014|
|Croatia||Present||Ivezic and Raspudic, 2001; Augustinovic et al., 2005|
|Cyprus||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|Czech Republic||Present||Cagan et al., 2006; EPPO, 2014|
|Czechoslovakia (former)||Restricted distribution||****||IIE, 1991; EPPO, 2014|
|Denmark||Present||IIE, 1991; EPPO, 2014|
|France||Widespread||IIE, 1991; EPPO, 2014|
|Germany||Present, few occurrences||****||IIE, 1991; EPPO, 2014|
|Greece||Present||IIE, 1991; EPPO, 2014|
|Hungary||Restricted distribution||****||IIE, 1991; EPPO, 2014|
|Ireland||Present||Haynes, 1989; EPPO, 2014|
|Italy||Present||IIE, 1991; EPPO, 2014|
|-Sardinia||Present||IIE, 1991; EPPO, 2014|
|-Sicily||Present||Mutuura and Munroe, 1970; EPPO, 2014|
|Montenegro||Present||Radonjic and Hrncic, 2011|
|Netherlands||Present||IIE, 1991; EPPO, 2014|
|Norway||Present||Aarvik, 1990; EPPO, 2014|
|Poland||Present||IIE, 1991; Cagan et al., 2006; EPPO, 2014|
|Portugal||Widespread||Mutuura and Munroe, 1970; EPPO, 2014|
|Romania||Present||IIE, 1991; EPPO, 2014|
|Russian Federation||Present||EPPO, 2014|
|-Russia (Europe)||Present||EPPO, 2014|
|Serbia||Present||Keresi et al., 2004; Kere?i and Alma?i, 2009; EPPO, 2014|
|Slovakia||Present||Cagan et al., 2006|
|Slovenia||Present||Carlevaris et al., 2003; Gomboc, 2003; EPPO, 2014|
|Spain||Present||IIE, 1991; Mutuura and Munroe, 1970; EPPO, 2014|
|Sweden||Present||IIE, 1991; EPPO, 2014|
|Switzerland||Widespread||IIE, 1991; EPPO, 2014|
|UK||Restricted distribution||EPPO, 2014|
|-England and Wales||Restricted distribution||EPPO, 2014|
|Ukraine||Present||IIE, 1991; EPPO, 2014|
|Yugoslavia (Serbia and Montenegro)||Present||IIE, 1991|
Hosts/Species AffectedTop of page O. nubilalis has a very wide host range. Although it can survive by feeding on many different species of cultivated plants and weeds, its favoured host is maize. However, host preference is influenced by plant size. In many areas, particularly in North American agroecosystems, the female moths may prefer to lay eggs on potato early in the season, when maize plants are small, or late in the season, after maize has matured (Anderson et al., 1984). However, this is not clear in Europe as damage on potato has not been reported. O. nubilalis can develop on Capsicum annuum and Phaseolus vulgaris, and attacks are common both in Nearctic and Palearctic zones. O. nubilalis larvae may also be found on fruit trees, for example boring apples or peaches. This damage is generally detected when the summer is hot and dry and other crops such as maize are ripe and ready for harvest. In this situation, the females lay eggs on well-irrigated plants and the host preference is strongly influenced to environmental conditions.
Growth StagesTop of page Flowering stage, Fruiting stage, Vegetative growing stage
SymptomsTop of page Horizontal rows of holes in the young leaves, caused by larval feeding, provide an early indication of O. nubilalis attack. The borer begins feeding in the whorl of maize. When the leaf expands, the holes made by the larvae appear in a typical transverse line. Larval feeding inside the maize stem destroys vascular tissue. As a result, heavily attacked plants are smaller and produce fewer kernels per ear.
First-generation larvae usually bore into the upper part of the maize plant so that the stem near the tassel can be easily broken by the wind. Later, tunnelling of stem internodes by second-generation larvae produces extensive galleries. Frass and holes are easily visible on stems, or on the apical part of maize ears. Larval tunnelling weakens the stalks and causes them to break during windy weather. Tunnelling in ear shanks causes the ears to drop and prevents them from being harvested mechanically. In maize, attacks are generally most severe in susceptible hybrids. High larval survival and heavy damage may occur in maize grown for seed, silage and grain, as well as in sweetcorn.
The presence of larvae in the fruit of Capsicum annuum is difficult to detect. Only after damage has already occurred does an inspection (cutting and splitting the fruit) reveal the presence of larvae or pupae inside the fruits. In C. annuum larvae move among fruits, spreading pathogens such as Erwinia carotovora. Rotten fruits are generally symptoms of borer attacks. In potato, the newly hatched larvae tunnel into leaf petioles or leaf axils. Large larvae tunnel in main stems of the potato vines. During the course of development, larvae move among potato stems, producing an average of five tunnels per larva (Nault and Kennedy, 1996). Soft rot lesions, caused by Erwinia spp., may develop in association larval tunnels (Anderson et al., 1981). In green beans (Phaseolus vulgaris), the larvae tunnel in to the pods.
List of Symptoms/SignsTop of page
|Fruit / external feeding|
|Leaves / external feeding|
|Seeds / external feeding|
|Stems / internal feeding|
|Whole plant / internal feeding|
Biology and EcologyTop of page O. nubilalis is one of the most widely studied agricultural pests in the world. More than 1000 papers were published on the pest between 1925 and 1973 (Brindley et al., 1975).
The adults are active at night, anchored to the plant and remaining still during the day, in areas of dense vegetation at the crop border in conditions of high humidity (dew). The average adult lifespan is 10-15 days and adults can mate more than once.
Females release a sex pheromone to attract males and mate on the night of emergence or on the 2-3 subsequent nights of adult life. The sex pheromone is a blend of components. The two main components are: Z-11-tetradecenyl acetate (Z11-14Ac) and E-11-tetradecenyl acetate (E11-14Ac). The ratio of these two isomers in the pheromone blend is critical to eliciting a male response. There are two distinct strains of European corn borer, which differ in ratio of Z to E isomers of 11-14Ac that constitute the primary components of their sex pheromone. Males of the Z strain respond optimally to an isomeric ratio of 2E:98Z, whereas males of the E strain respond optimally to an isomeric ratio of 99E:1Z. F1 hybrid males from crosses between the two strains produce a pheromone blend with an isomeric ratio of 65E:35Z but respond to a broad range of isomeric ratios ranging from 2 to 98% E (Glover et al., 1987; Linn et al., 1997).
This intraspecific pheromonal variation of O. nubilalis was first reported in North America and Europe by Klun et al. (1975) and later found to occur in Egypt and China by Anglade et al. (1984). The Z strain is most common. The E strain is mainly present in parts of Europe and in the eastern, USA (Showers 1993). However, sympatric populations of the E and Z strains as well as inter-strain hybrids exist at some locations (Roelofs et al., 1985).
Sex pheromone production and perception in the European corn borer is determined by autosomal and sex-linked genes (Roelofs et al., 1987). The blend produced by an individual corn borer is controlled by two alleles at a single locus inherited in a Mendelian fashion (Klun and Maini, 1979; Zhu et al., 1996) Pheromone biosynthesis and perception have been investigated (Zhu et al., 1996; Anton et al., 1997; Linn et al., 1999).
During mating a capsule of sperm (spermatophore) is deposited in the female bursa copulatrix (one or three, depending on number of matings). Mated and virgin females can be readily distinguished by squeezing the abdomen to extrude the sclerified spermatophore. The sprmatophore looks like a small black seed (Showers et al., 1974).
In addition to the two known pheromone strains, there are three known ecotypes of European corn borer, which differ in voltinism. These are the uni- bi- and multi-voltine ecotypes. In some areas, more than one ecotype and sex pheromone strain occur sympatrically (Showers, 1993). Fecundity is strongly related to strains and ecotypes, and the maximum number of eggs produced per female is 800-900 (average 500-600 eggs/female). Females that have mated multiple times are significantly more fecund than females that mate only once; similarly those that mate within less than 3 days after emergence are more fecund than those that experience a 3-day delay in mating (Fadamiro and Baker, 1999). Eggs are laid in egg masses of between 5 and 50 (30 on average). The eggs are usually laid on the lower leaf surfaces or directly on fruit (for example, on Capsicum annuum). In a healthy population, 95% of fertile eggs hatch. The sex ratio is 1:1 and a slight protandry has been detected by some authors (i.e. males emerge hours or days earlier than the females). Matteson and Decker (1964) reported the duration of development at two temperatures. At 21°C, development times were: egg - 6 days, L1 - 4.5 days, L2 - 4 days, L3 - 4 days, L4 - 4 days, L5 - 10 days and pupa - 12 days. At 26° C, they were: egg - 3.5 days, L1 - 3 days, L2 - 2 days, L3 - 2 days, L4 - 2.5 days, L5 - 6.5 days and pupa - 7 days.
The number of generations per year ranges from one to six and is related to strains and geographic area. In temperate areas such as the mid-western USA, south-western France and Italy there are usually two or three overlapping generations present. The diapause is influenced by many factors (Beck, 1989) and the fully-grown larva (L5) is the overwintering stage. Larvae may pass the winter inside their tunnels in stubble, stalks and maize ears, or in wild plants. Usually the endophytic larvae prepare a hole for emergence, drink water and then return to the tunnel to spin a flimsy cocoon before they pupate. Pupation and emergence of the moth take place when several conditions are present. Lower development thresholds are: 14°C (egg stage), 11°C (larval stage) and 12°C (pupal stage). The minimum threshold temperature for flight activity is 13-15°C. Eggs can be desiccated by warm and dry wind. The black head capsule of the larva is visible within the egg shortly before the eggs are ready to hatch. Depending on relative humidity, newly hatched larvae disperse to feed outside on leaves, but in dry and warm weather they prefer to bore into silks of maize cobs or directly into young stems. Many neonates drop from the plant on silk threads and disperse. Mortality factors include predators and parasitic diseases, as well as abiotic factors. Conditons that are too dry or too wet cause mortality to eggs, and first- and second-instar larvae.
Models of temperature-dependent development (Anderson et al., 1982a; Got et al., 1996), diapause induction (Ellsworth et al., 1989), post- diapause development (Anderson et al., 1982b; Magai et al., 1997), long-term population dynamics (Onstad, 1988; Labatte et al., 1997), host plant adaptation (Onstad and Gould, 1998a, b) and damage on maize (Labatte and Got, 1991) have been described in the literature.
Monitoring techniques include sampling adults with a sweep net, egg mass scouting, light traps and sex pheromone traps (Sappington and Showers, 1983; Legg and Chiang, 1984). For a variety of reasons, larval moth catches in pheromone and light traps are not reliable predictors of the size of the larval infestation that subsequently develops in a crop. However, monitoring of moth flights provides valuable information on the timing of oviposition.
Several meridic diets for rearing O. nubilalis larvae have been reported. Mass-rearing of O. nubilalis is described by Guthrie et al. (1965).
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Bacillus thuringiensis||Pathogen||Larvae||Europe; Illinois; Iowa|
|Bacillus thuringiensis aizawai||Pathogen||Larvae||Italy|
|Bacillus thuringiensis darmstadiensis||Pathogen||Larvae|
|Bacillus thuringiensis galleriae||Pathogen||Larvae|
|Bacillus thuringiensis kenyae||Pathogen||Larvae|
|Bacillus thuringiensis kurstaki||Pathogen||Larvae||Pennsylvania|
|Bacillus thuringiensis thuringiensis||Pathogen||Larvae|
|Bacillus thuringiensis tolworthi||Pathogen||Larvae|
|Bracon brevicornis||Parasite||Larvae||Canada; USA||maize; sorghum|
|Campoplex alkae||Parasite||Canada; USA||maize|
|Coleomegilla maculata||Predator||Eggs/Larvae||USA; New York||Phaseolus vulgaris; squashes|
|Diadegma terebrans||Parasite||Larvae||Connecticut; Minnesota; Nebraska; USA||vegetables; maize ì ì|
|Echthromorpha agrestoria fuscator||Parasite||Canada||maize|
|Exeristes roborator||Parasite||Canada; USA||maize|
|Glyptapanteles thompsoni||Parasite||Larvae||Canada; USA||maize|
|Hippodamia tredecimpunctata tibialis||Predator|
|Lydella thompsoni||Parasite||Larvae||Canada; Delaware; France; Minnesota; Nebraska; North America; USA||maize; sorghum; vegetables|
|Macrocentrus grandii||Parasite||Larvae||Canada; Connecticut; Delaware; Minnesota; USA; USA; Illinois||maize; vegetables|
|Phaeogenes nigridens||Predator/parasite||Larvae||Canada; USA||maize; vegetables|
|Platymya mitis||Parasite||Larvae||Canada; USA ì ì ì ì||maize|
|Pseudoperichaeta erecta||Parasite||Larvae||Canada; USA||maize|
|Pseudoperichaeta nigrolineata||Parasite||Larvae||Canada; USA||maize|
|Sympiesis viridula||Parasite||Larvae||Canada; Nebraska; North Dakota; USA||maize; vegetables|
|Trichogramma buesi||Parasite||Eggs||Europe; Italy|
|Trichogramma evanescens||Parasite||Eggs||Austria; Bulgaria; Czechoslovakia; France; Germany; Moldova; Romania; Switzerland; Ukraine|
|Trichogramma maidis||Parasite||Eggs||Bulgaria; France; Italy; Switzerland||maize|
|Trichogramma minutum||Parasite||Eggs||USA; New York||Phaseolus vulgaris; squashes|
|Trichogramma nubilale||Parasite||Eggs||Delaware; USA||maize|
|Trichogramma ostriniae||Parasite||Eggs||Shandong; USA; Massachusetts||maize|
Notes on Natural EnemiesTop of page Natural control is not sufficient to reduce the damage caused by O. nubilalis larvae below an economic threshold in some crops (for example seed maize, sweetcorn, potato, Capsicum, Phaseolus vulgaris). Many species of beneficial arthropods (predators and parasitoids) and diseases contribute to suppression of European maize borer populations in grain maize. In Nearctic areas biological control experiments began as soon as O. nubilalis was detected. The pest was introduced in the USA, near Boston, in 1917, and in 1919 entomologists began searching for its natural enemies in Europe and the Orient (Baker et al., 1949).
Much work was subsequently carried out in the USA and Canada to confirm the establishment of these exotic natural enemies. The only natural enemies that definitely established were Lydella thompsoni, Diadegma terebrans and Macrocentrus grandii. A new association was that of Trichogramma nubilale, a Nearctic egg parasitoid. Trichogramma brassicae (= maidis) is common in Europe and was first described as T. evanescens. The population of T. brassicae reaches a maximum at the end of the summer T. Brassicae overwinter as pupae inside the host egg.
Mass-rearing of Trichogramma on factitious eggs has been developed in commercial insectaries for biological control against O. nubilalis in maize, sweetcorn and Capsicum annuum (see Biological Control).
In China and other oriental countries, several species of Trichogramma are reared and augmentative releases are carried out against O. nubilalis and the related stalk borer O. furnacalis.
Parasitoids, predators and pathogens of O. nubilalis are listed in Baker et al. (1949) and in several later reviews. Pictures of the parasitoids can be seen in the following datasheets: Lydella thompsoni, Trichogramma brassicae and Sinophorus turionus.
ImpactTop of page Introduction
Most of the literature regarding the economic impact of O. nubilalis is centered on damage to maize (Zea mays), the primary host of O. nubilalis. There are reports of damage to other crops of economic value, but details of the total crop impact are lacking. The extent of damage caused by O. nubilalis varies from year to year and between geographic locations within years. Some of this variation is due to the number of generations possible in a geographic location, climatic conditions for a given year, physiological stage of the crop at infestation, and natural mortality.
Chiang and Holdaway (1959, 1965) assessed larval feeding and tunneling on maize in the USA. Many subsequent reports were published on O. nubilalis attacks and damage on maize in other countries and in North America (Stengel, 1969; Lynch, 1980; Lynch et al., 1980; Landi and Maini, 1982; Umeozor et al., 1985; Jarvis et al., 1986; Calvin et al., 1988). O. nubilalis larvae are reported to reduce maize yield by 1) tunneling into the ear shank causing ears to drop before harvest and 2) tunneling into stems reducing water and nutrient transfer (physiological damage). Lynch (1980) showed that yield losses in Iowa were primarily from physiological damage rather than from unharvestable ears.
Several studies have been conducted to measure the economic loss resulting from O. nubilalis infestations. Patch et al. (1951) reported a loss of 3% per borer per plant. Calvin et al. (1988) reported a loss of 5.56% per borer per plant. Jarvis et al. (1986) showed a 7 to 11% reduction in total yield, 9 to 18% reduction in harvestable yield, and a 2.5 to 7% reduction in kernel weight between natural infested plots and protected plots. Lynch (1980) conducted a 3-year study of yield loss by various densities of O. nubilalis egg masses. He reported a 1, 9, and approximately 12% reduction in yield for infestation levels of 1, 2 and 4 egg masses per plant during the first 2 years of the study. The last year of the study had larger yield reductions, which he attributed to drought conditions that magnified the physiological damage. Lynch (1980) reported a greater yield reduction in the kernel blister stage as compared with the whorl stage. Mason et al. (1996) estimated O. nubilalis cost US farmers more than 1 billion dollars per year when considering control costs and yield losses. The number of generations of O. nubilalis in the US range from 1 in the northern states to 4 in the southern states. Calvin et al. (1988) reported that O. nubilalis is bivoltine in Kansas, and that the first generation populations are generally low. They reported that the greater the proportion of growing degree days (GDD) remaining to physiological maturity when second generation larvae initiate tunneling, the greater the reduction in grain dry matter.
Data from central Europe report variation in geographical areas and between years (Bohn et al., 1999). However, some areas appear to have significant annual infestations historically even though only one generation occurs. Bohn et al. (1999) reported that long term monitoring showed in general that greater than 95% of the maize plants were damaged by O. nubilalis in the Trebur area. In their study to evaluate maize hybrids for resistance, they reported natural infestations ranged from 18 to 58% damaged plants and 0 to 0.4 larvae per plant except for the Trebur area. In the Trebur area, 100% of the plants were damaged by O. nubilalis and larvae per plant was greater than 3.6. They reported that across all locations larval damage reduced yield by 8% compared with insecticide treatment plots. Greater than 25% reduction in grain yield was observed in the Trebur area, Germany. They reported a reduction of 0.28% grain yield for each 1% of the plants damaged by O. nubilalis and 6.05% for each larva per plant.
Cabanettes (1984) reported moderate infestations of O. nubilalis in France resulting in yield losses of 300 kg/ha. Anglade (1985) reported that more severe infestations in France resulted in yield losses of 2 t/ha. Foott and Timmins (1981) reported infestations in Ontario, Canada during 1973 of 650 larvae per 100 plants in treated fields and 770 larvae per 100 plants in untreated fields for early-planted maize. However, maize planted later in the year had infestations of 1380 larvae per 100 plants, and 1160 larvae per 100 plants for treated and untreated fields, respectively.
Some studies have focused on economic impact of O. nubilalis on maize not grown specifically for grain production. Sayers et al. (1994) studied the economic threshold for O. nubilalis on maize grown for seed. They suggested that a threshold of 2 to 3% plants with larvae in the whorl stage and 10 to 17% plants with larvae in the flowering stage should warrant treatment. Thompson and White (1977) studied the yield reduction of maize grown for silage on Prince Edward Island where O. nubilalis has one generation per year. They reported a reduction in the grain component for 1974, but did not find a reduction in grain or whole plant during 1975 or 1976. They reported infestation levels of 37, 32, and 46% plants with borer for the respective years, and 80, 176 and 170 tunnels per 100 plants for the respective years. Myers and Wedberg (1999) reported that first generation O. nubilalis caused greater yield reduction than second generation in Wisconsin silage based on artificial infestation studies. Raemisch and Walgenbach (1984) reported similar findings for natural infestations in South Dakota.
O. nubilalis larvae in sorghum (Sorghum bicolor) were reported as early as 1928 in the USA according to Painter and Weibel (1951). Atkins et al. (1963) reported yield reductions ranging from 1 to 23% for various sorghum genotypes in Iowa. Ross et al. (1982) reported total grain yield reductions in sorghum following artificial infestations of O. nubilalis of 13%, and 18% reduction in combine grain yield (excluding lodged stalks and heads).
The occurrence of O. nubilalis in US cotton (Gossypium hirsutum) was first reported in 1955 (Anon., 1984) in Franklin County, Tennessee. Subsequent infestations were reported in several of the Southeastern cotton growing states (Alabama, Florida, Louisiana, Mississippi and South Carolina). O. nubilalis has only recently become a pest of economic importance, primarily in the Carolinas (Mason et al., 1996). Larvae damage plants by 1) boring into the main stem reducing water and nutrient uptake as well as often causing the stem to break, 2) boring into leaf petioles reducing photosynthesis, and 3) boring into boll (fruit) reducing yield. Luttrell et al. (1999) reported an infestation of O. nubilalis in large plot studies conducted in Leflore County, Mississippi. Data showed 25% damaged bolls in an untreated plot, 20% damaged bolls in a plot treated for Helicoverpa zea and Heliothis virescens, and 4% damaged bolls in a plot of transgenic cotton expressing the insecticidal protein of Bacillus thuringiensis.
Although peppers are not a preferred host of O. nubilalis, moths will utilize the crop if maize becomes unattractive and other suitable hosts are not present (Mason et al, 1996). Damage to peppers includes 1) boring into the stem or 2) boring into the fruit. Damaged fruit will often rot or be rejected upon processing. Burbutis and Lesiewicz (1974) reported studies in Delaware with 30% of the pepper fruit infested with O. nubilalis for the untreated plots. Elliott et al. (1978) reported 83% damaged pepper fruit in Ontario.
O. nubilalis larvae may damage potatoes by boring into plants causing plants to wilt, break and eventually die (Mason et al., 1996). Studies in North Carolina reported infestation level resulting in more than 30 tunnels per plant, but no yield reduction attributable to O. nubilalis was found (Kennedy, 1983). However, the borer damage to the plants increased the incidence of fruit disease and thereby reduced marketability.
In Clintondale, New York, O. nubilalis was identified infesting newly planted apple trees during 1980 (Weires and Straub, 1982). Damage levels ranged from 0.2 to 27.2% of the orchard trees examined in 8 orchards (total of 5500 trees examined). Snapbeans, soyabeans and wheat are additional crops that are possible hosts of O. nubilalis (Mason et al., 1996).
Detection and InspectionTop of page Field infestations of O. nubilalis in maize are surveyed by counting egg masses and observing signs of early damage by first-instar larvae. If there are more than a threshold number, a control method needs to be selected (Chiang, 1973). Adults can be detected by simple sweep-net operations around maize fields or positioning light traps, sex pheromone traps or sex pheromone plus food attractant multi-baited traps. (For further information, see Pheromonal Control.) In potato, scouting involves surveying for signs of early damage by first-instar larvae to the petioles and stems, and a sequential sampling system has been reported (Nault and Kennedy, 1996).
Similarities to Other Species/ConditionsTop of page O. nubilalis resembles other species of Ostrinia in external characteristics but is morphologically distinct. Mutuura and Munroe (1970) provide a full description and identification keys. In the past, many authors have confused O. nubilalis (European maize borer) with O. furnacalis (Asian maize borer): the adults are morphologically similar and both larvae bore maize in the same way.
In North America, O. nubilalis can be confused with O. obumbratalis, the smartweed borer (Heinrich, 1919; Mutuura and Munroe, 1970). The three recognized subspecies: Ostrinia nubilalis nubilalis (Hübner); Ostrinia nubilalis mauretanica (Mutuura and Munroe) and Ostrinia nubilalis persica (Mutuura and Munroe) are similar and may be confused. Ostrinia nubilalis mauretanica is similar to Ostrinia nubilalis nubilalis but is smaller and paler. The subspecies differ slightly in their male genitalia and in male forewing and hindwing colour.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.Cultural Control
Farmers can reduce the level of O. nubilalis larval injury by adjusting planting dates. In areas characterized by more than one generation of O. nubilalis, early planted sweetcorn usually escapes appreciable damage to the ears. In Capsicum annuum and green beans (Phaseolus vulgaris) heavy damage typically occurs late in the season and is caused by second- and third-generation larvae. Early planting can minimize the exposure of these crops to this damage. In agroecosystems characterized by high crop diversity, crops that are less attractive than other crops to ovipositing moths during a particular corn borer generation may gain a significant degree of protection by their proximity to more attractive crops (Kennedy and Storer, 2000). Overwintering survival of O. nubilalis is influenced by tillage practices (Umeozor et al., 1985; Schaafsma et al., 1996), although there is little relationship between overwinter survival and population size the following season (Chiang et al., 1961; Showers et al., 1978). Nonetheless, sanitation by ploughing at the end of the maize-growing season is compulsory in some countries.
Biological control was attempted as soon as O. nubilalis was introduced in North America. Some parasitoids imported from Europe became established and are still present. In Europe, indigenous parasitoids are not able to maintain O. nubilalis populations at tolerable densities. Some crops like sweetcorn, maize (grown for seeds), Capsicum annuum and Phaseolus vulgaris must be treated by another control method.
Biological control of O. nubilalis using augmentative and inundative releases of Trichogramma sp. is now used with some success in maize and C. annuum in Europe and North America (Voegelé et al., 1975; Hassan et al., 1978; Maini et al., 1983; Kanour and Burbutis, 1984; Bigler and Brunetti, 1986; Kabiri et al., 1991; Prokrym et al., 1992; Burgio and Maini, 1995). Several biofactories produce and sell these egg parasitoids by rearing them on factitious hosts. The effectiveness of Trichogramma releases in controlling O. nubilalis is influenced by a number of factors including the quality of the wasps released; weather conditions at the time of release, especially temperature; and plant architecture; as well as the frequency of releases and number of release sites per hectare (Andow et al., 1995; Dutton et al., 1996; Chihrane and Lauge, 1996; Gunie and Lauge, 1997; Wang et al., 1997).
Microbial control using formulations of Bacillus thuringiensis subsp. kurstaki (Bt) generally gives good results, particularly when the treatments are correctly applied and target first stage larvae. The larvae, which are endophagous and ectophagous, must ingest sufficient quantities of Bt toxins to be killed. Granular formulations applied to whorl stage maize so that the granules drop into the whorl are generally more effective than sprayable formulations. Because Bt is harmless to predators and parasitoids in maize agroecosystems, microbial treatments do not produce the negative side effects caused by some insecticide sprays, such as an increase in the number of aphid and spider mite infestations. Foliar applications of Bt kurstaki and Bt aizawai also have shown promise for control of European corn borer in Phaseolus vulgaris (Curto, 1996). The integration of microbial control and augmentative releases of egg parasitoids has been carried out successfully.
Other biological control methods such as the use of Beauveria bassiana or Perezia pyraustae preparations have been in research trials, but they are difficult to apply economically in the field.
Brindley and Dicke (1963) reviewed early studies on maize resistance to O. nubilalis. Several investigations demonstrated a difference in host-plant resistance related to strains of O. nubilalis and geographic area. To avoid such variations an International Working Group Ostrinia (IWGO) was constituted during the International Congress of Entomology, which was held in Moscow in 1968. The aim was to standardize genetic experiments and exchange maize lines. The IOBC publishes the IWGO Newsletter to update research on O. nubilalis and other maize pests.
Guthrie (1974) reported techniques, results and the potential of breeding for resistance to O. nubilalis. Klun et al. (1967) demonstrated that the resistance factor (antibiosis) to leaf feeding in whorl stage plants is correlated with the concentration of the aglucone DIMBOA in the maize plant. Gallun et al. (1975) reviewed the chemical basis of resistance in whorl stage maize (referred to as resistance to first-generation larvae).
More recent investigations on allelochemicals that influence the leaf feeding of O. nubilalis larvae on maize are reported by Houseman et al. (1992). Resistance in reproductive stage maize (referred to as resistance to second-generation larvae) was found after an exhaustive evaluation of maize lines (Jennings et al., 1974; Barry and Darrah, 1991). It is important to note that the resistance expressed in whorl stage plants and that expressed in reproductive stage plants are distinct and under separate genetic control. Consequently, plant material resistant to larval attacks during the vegetative stage of development may not be resistant during pollen shedding and later stages. Resistance to European corn borer, at some level, is now common in commercial maize hybrids. Of 400 maize hybrids, approximately 90% expressed some resistance to O. nubilalis during the whorl stage and 75% expressed some resistance during the reproductive stage (Barry et al., 1997). Molecular marker assisted selection is currently being used to facilitate the incorporation of maize genes conferring resistance to O. nubilalis into inbred lines used in the production of commercial hybrids (Benson and Mihm, 1997; Sagers et al., 1997).
In addition to antibiosis-based resistance, modern maize hybrids possess high levels of tolerance to European corn borer injury. The development of tolerant maize hybrids with strong, robust stalks that do not lodge when tunnelled by O. nubilalis larvae has contributed greatly to minimising harvest losses associated with corn borer damage.
Advances in recombinant DNA technology have led to the ability to genetically transform maize and other plants to express foreign genes coding for specific traits. In 1996, maize hybrids genetically transformed to express the Bacillus thuringiensis gene coding for the Cry1Ab or Cry1Ac toxin, which is highly toxic to O. nubilalis, became commercially available in the USA. This maize possesses high levels of resistance to leaf feeding, stalk tunnelling and yield loss by O. nubilalis (Koziel et al., 1993; Armstrong et al., 1995; Jansens et al., 1997; Rice and Pilcher, 1998; Graeber et al., 1999). In addition, Bt maize hybrids resistant to O. nubilalis experience reduced levels of Fusarium ear rot and symptomless infections in their kernels, as well as reduced mycotoxin concentrations because of the reduction in kernel damage by O. nubilalis larvae (Munkvold et al., 1997, 1999). By 1999, Bt maize hybrids resistant to O. nubilalis constituted 26% of the US maize crop and 4% of the US sweetcorn crop. Hyde et al. (1999) developed a dynamic programming model to analyse the economic value of Bt maize under a range of production conditions and O. nubilalis infestation levels.
Although there has been concern that the widespread planting of Bt maize hybrids may have an adverse effect on non-target organisms, and several laboratory studies have indicated the possibility of such effects (Hilbeck et al., 1998, 1999), field studies have failed to detect significant, adverse, non-target effects (Orr and Landis, 1997; Pilcher et al., 1997; Lozzia, 1999; Pimentel and Raven, 2000; Wraight et al., 2000). As is the case with other Bt crops and their targeted pests, there has also been concern that the widespread planting of Bt maize hybrids will result in the rapid selection for resistance in O. nubilalis to the Bt toxins expressed in maize. Laboratory selection experiments have demonstrated the ability of O. nubilalis populations to develop resistance to Bt toxins (Huang et al., 1997; Bolin et al., 1999). Although alleles for at least partial resistance to Bt toxins are uncommon in field populations <0.013 in Minnesota, USA) (Huang et al., 1997; Andow et al., 1998), they are sufficiently common that potential for resistance to develop is being taken seriously. The dynamics of adaptation by O. nubilalis to Bt maize under different resistance management scenarios have been investigated using population genetics models (Alstad and Andow, 1995; Onstad and Gould, 1998a, b; Hurley et al., 1999; Onstad and Guse, 1999). Efforts to mitigate the development of resistance in O. nubilalis to Bt maize involve use of the 'high dose/refuge' strategy for resistance management. Bt maize hybrids expressing a high dose of the toxin are planted in conjunction with plantings of refuge areas of maize that do not express Bt toxins and in which O. nubilalis is not controlled. The size and location of refuge plantings must be such that any homozygous resistant moths selected on the transgenic crop mate with homozygous susceptible moths produced in the refuge. The progeny of such matings would be heterozygous for the resistance allele and would be killed if they fed on the transgenic crop (Gould, 1998).
Difficulties in application, the use of tolerant maize hybrids, the concealed habitats in which borers feed, and the costs of pesticides generally preclude the use of chemical control against O. nubilalis. Chemical control may also interfere with natural control by parasitoids and predators and increase the risks of environmental pollution and other harmful side effects. Chemical control methods are therefore considered inadequate against this pest on maize grown for grain. Because O. nubilalis causes direct injury to fruits and pods of Capsicum and Phaseolus vulgaris, respectively, and the tolerance for injury is very low, chemical control is an important component of O. nubilalis management on those crops. Insecticides are commonly used in managing O. nubilalis on sweetcorn and potato as well, and thresholds and sampling schemes have been developed (Nault and Kennedy, 1996; Riggs et al., 1998).
The main chemical components of the female sex pheromone used to attract males are trans 11-tetradecenyl acetate (E11-14 Ac) and cis 11-tetradecenyl acetate (Z11-14 Ac) (Klun, 1968; Klun et al., 1973; Kochannsky et al., 1975). The use of sex pheromones to control European corn borer is complicated by the existence of distinct strains of European corn borer differing the precise isomeric blend of these components that is used as a sex pheromone and by the fact that mating typically occurs in 'aggregation sites' outside of crop fields. To date sex pheromones have not been used in mass trapping or mating disruption programmes to control the European corn borer. Although at least one study indicates that the frequency of matings by females can be suppressed using sex pheromones (Fadamiro et al., 1999), the levels of mating disruption were not sufficient to effect control.
Sex pheromones have been used primarily as a monitoring tool to detect the presence of moths and to identify periods of moth activity and oviposition. Both trap design and trap placement are important determinants of trap efficiency (Webster et al., 1986; Derrick et al., 1992; Burgio and Maini, 1994; Mason et al, 1997; Bartels and Hutchison, 1998) and the possibility of combining the sex pheromone with another lure to attract females has been demonstrated by Maini and Burgio (1993). When sex pheromone baited traps are used for monitoring moth flights, it is critical that the pheromone blend used to bait the traps is representative of the blend being used by the local population of European corn borers (Sorenson et al., 1992; Bourguet et al., 1999). Although moth catches in pheromone-baited traps frequently do not provide a quantitative indicator of the larval infestation that subsequently develops, monitoring of moth flights provides valuable information on the timing of oviposition. Maini and Burgio (1994, 1999) reported that the number of male and female moths caught in traps baited with a combination of sex pheromone and the maize kariomone phenylacetaldehyde was correlated with subsequent larval infestations in Capsicum annum and in maize.
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