Biotechnology and the European corn borer: measuring historical farmer perceptions and adoption of transgenic Bt corn as a pest management strategy

A 3-yr, multi-state survey of farmers who had planted transgenic Bacillus thuringiensis (Bt) corn was conducted to evaluate perceptions of Bt corn performance and its utility as a management option for European corn borer, Ostrinia nubilalis (Hübner). A questionnaire was sent to farmers in Illinois, Iowa, Kansas, Minnesota, Nebraska, and Pennsylvania who had grown Bt corn during the growing seasons of 1996, 1997, or 1998. There were 7,427 usable questionnaires returned with the following response percentages: 1996 (42.1%), 1997 (35.0%), and 1998 (22.6%). Adoption rates, based on percentage of acreage planted to Bt corn, increased dramatically from 1996 (10.5%) to 1998 (40.7%). The states growing the highest percentage of Bt corn were Minnesota, Iowa, and then Nebraska However, Illinois, was adopting Bt corn at the fastest rate. Historical use of insecticides did not influence the adoption of Bt corn. In addition, of those farmers who used insecticides to control European corn borer, the percentage that decreased their use of insecticides nearly doubled from 13.2% (1996) to 26.0% (1998) over this 3-yr period. The primary reason farmers planted Bt corn was to eliminate the yield loss caused by European corn borer. Scouting for European corn borers decreased from 91% (scouting 2.2 times a year) in 1996 to 75% (scouting 1.8 times a year) in 1998. The percentage of farmers not scouting for European corn borers increased from 9.6% (1996) to 25% (1998). Most farmers believed yields of Bt hybrids were either similar to or greater than the yields of non-Bt hybrids. Minnesota farmers perceived the greatest yield advantages. Farmers are becoming more aware of insect resistance management guidelines; however, they also clearly show preferences for having the flexibility to use different spatial plantings of Bt and non-Bt corn. Finally, after having planted Bt corn and obtained excellent control of European corn borer, most farmers believed that this insect had been causing more yield loss than they previously had suspected in their non-Bt corn. The data represented here provide an historical foundation for how transgenic Bt corn was used by farmers during the first 3 yr of commercial availability, their initial perceptions on the performance of this technology, and their attitudes regarding management of the European corn borer.     

Release density,efficiency and disappearance ofTrichogramma nubilale for control of European corn borer

We evaluated how manyTrichogramma nubilale should be released at a single location to controlOstrinia nubilalis in sweet corn. Six 8.6×16 m plots received 18.4 to 2 090 ΦΦT. nubilale/SAI when plants were in the mid to late whorl stage, where SAI, surface area index, is the plant surface area/m². To evaluate the potential control by our releases, we exposed laboratory-rearedO. nubilalis egg masses to the released parasitoids at 4 times after the release. When an egg mass was parasitized byT. nubilale, 75.7% of the eggs in the egg mass were parasitized. We developed an equation to estimate the percent of egg masses that a single female was expected to parasitize in a day (efficiency of parasitism) and female disappearance (death and dispersal) rates, if both were constant during our experiment. The exponential disappearance rate was −0.52±0.03 day⁻¹, which implied that 40% of the remaining ΦΦ disappeared per day. The efficiency of parasitism was 0.050% parasitism/Φ/SAI/day, which implied that at least 351,000 ΦΦ/ha would be needed to achieve 90% parasitism. Clearly, forT. nubilale to be a successful biological control agent, efficiency of parasitism must be increased and disappearance rates must be reduced.      

Establishment of Cry9C susceptibility baselines for European corn borer and southwestern corn borer (Lepidoptera: Crambidae)

In 1997 and 1998, Cry9C susceptibility baselines were established for field-collected populations of European corn borer, Osrinia nubilalis (Hubner), and southwestern corn borer, Diatraea grandiosella Dyar. Bioassay of neonate European corn borer larvae of 16 colonies collected from the midwestern United States indicated LC50 values ranging from 13.2 to 65.1 ng of Cry9C protein per square centimeter. Neonate European corn borer LC50 values ranged from 46.5 to 214 ng/cm2. Neonate larvae of three colonies of southwestern corn borer collected from the southern and southwestern United States exhibited LC50 values from 16.9 to 39.9 ng of Cry9C protein per square centimeter. Southwestern corn borer neonate LC90 confidence limit values ranged from 40.3 to 157 ng of Cry9C protein per centimeter. The most sensitive southwestern corn borer colony was collected from the Mississippi delta exhibiting an LC50 value of 22.6 ng of Cry9C per cm2 and also displayed the widest LC0 confidence limits of 40.3-94.8 ng of Cry9C per cm2. Geographic baseline susceptibility data establishes the natural genetic variation and provides the foundation for future testing of insect populations exposed to increased use of Bacillus thuringiensis-based crops. Insect resistance management and stewardship of Cry9C will rely upon baseline data for the validation of discriminating dose assays for European corn borer and southwestern corn borer.     

Transgenic Bacillus thuringiensis corn hybrid performance against univoltine ecotype European corn borer (Lepidoptera: Crambidae) in South Dakota

The performances of Bt-corn hybrids against univoltine ecotype European corn borer larvae were evaluated in South Dakota from 1997 to 1999. The corn hybrids were exposed to natural seasonal fluctuations of a univoltine ecotype European corn borer population. Larval injury parameters, grain yields, and gross incomes were quantified during the 3-yr study. In general, the Bt-corn hybrids had significantly higher yields than the untreated non-Bt isolines in 1997 and 1998 when corn borer pressures were high. However, most of the Bt-corn hybrids did not produce significant yield advantages in 1999 when the European corn borer pressure was low. Some of the Bt-corn hybrids even produced significantly lower yields than their untreated non-Bt counterparts in 1999. The performances of non-Bt isolines that were treated with permethrin granules at whorl stage were similar to Bt-corn hybrids in 1998 when the corn borer pressure was high and similar to the untreated non-Bt isolines in 1999 when the corn borer pressure was low. Injury-free corn produced by Bt-corn hybrids did not necessarily translate into higher yields in some hybrid groups. Grain moisture at harvest, which can result in moisture penalty or dockage, was significantly higher in most Bt-corn hybrids. Gross incomes of the Bt-corn hybrids were generally higher than the untreated non-Bt isolines when the corn borer infestation was high, but were either similar to or lower than the untreated non-Bt isolines when the corn borer infestation was low.     

Population consequences of diapause in a model system: the European corn borer

The diapause biology of the European corn borer (ECB), Ostrinia nubilalis (Hübn.), is described based on natural and controlled environment studies of feral and lab-reared ECB's in North Carolina (NC). The diapause response is described as a function of photophase (h of light/day) as well as a function of larval age (instar) at onset of diapause-inducing conditions. A critical photophase of 14.4 h and a critical mean larval instar of 3.3 is found in the lab studies and supported by three years of insectary studies. Seven years of black light trapping of ECB moths in Goldsboro, NC, revealed the likelihood of up to four moth flights/year.Information about the diapause biology of this insect is used to explain both the number of flights and the relative magnitude of the final moth flights. On average, the majority of ECB lineages pass through three generations/year with early maturing ECB's producing a significant and predictable fourth generation. The timing and magnitude of the fourth flight can be partly explained on the basis of the critical photophase and the timing and age structure of previous ECB generations. In most years, the fourth flight is smaller than the third due to the majority of the fourth generation's predisposition towards diapause. However, in at least one case (1977), the fourth flight was unusually large and could be predicted by slight temporal shifts in the previous three flights resulting in the majority of the fourth generation larvae averting diapause. The value of the ECB-diapause interaction as a model system for the explanation and prediction of dynamic phenological events is discussed.

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Résumé La diapause d'O. nubilalis Hubn. est décrite d'après des études en conditions naturelles et programmées de souches sauvages ou élevées au laboratoire en Caroline du Nord. La diapause est décrite comme une fonction de la photophase (heures de jour/24 heures) et du stade larvaire au début des conditions inductrices de la diapause. Une photophase critique de 14,4 h et un stade critique larvaire de 3,3 ont été établis au laboratoire après 3 ans d'études en insectarium. 7 ans de piégeage à la lumière noire à Goldsboro, ont montré la vraisemblance de l'existence de 4 vols par an. Les données sur la diapause de cet insecte sont utilisées pour expliquer tant le nombre de vols que l'importance relative des derniers vols. En moyenne, la majorité des lignées ont 3 générations par an, O. nubilalis précoces produisant une quatrième génération conséquente et prédictible. La data et l'importance du 4ème vol peuvent être partiellement expliquées d'après la photophase critique, et la data et la structure en âge des générations précédentes. La plupart des années, le 4ème vol est moins important que le 3ème par suite de la prédisposition à la diapause de la majorité de la 4ème génération. Cependant, dans un cas au moins, en 1977, le 4ème était anormalement important et pouvait être prédit par de faibles changements temporels dans les 3 précédents vols, détournant de la diapause la majorité des chenilles de 4ème génération. La discussion porte sur la valeur du modèle fourni par la diapause de O. nubilalis pour expliquer et prédire la dynamique des évéments phénologiques.

     

Genetic control of voltinism characteristics in European corn borer races assessed with a marker gene

The post-diapause development (PDD) time for univoltine European corn borers (ECB) under diapause breaking conditions averages approximately 44 days, whereas the PDD time for bivoltine ECB under the same conditions is approximately 15 days. This difference is the principal component of the life cycle that determines the number of generations possible in a summer. Previous workers have demonstrated some genetic control of differences in voltinism among populations, including apparent control by sex-linked (Z-linked) genes. In the present study allozymes of the enzyme, triose phosphate isomerase (TPI), were used as markers of the Z chromosomes in crosses of a bivoltine colony (Tpi-1) and a univoltine colony (Tpi-2). The F₁ resulting from a cross of univoltine females (Z²W) and bivoltine males (Z¹Z¹) consisted of hemizygous Tpi-1 females (Z¹W) with a mean PDD time of 19 days and heterozygous Tpi-1/Tpi-2 males (Z¹Z²) with a mean PDD time of 34 days. The F₂ progeny consisted of Tpi-1 females (Z¹W) (mean PDD time = 15 days), Tpi-2 females (Z²W) (mean PDD time = 40 days), homozygous Tpi-1 males (Z¹Z¹) (mean PDD time = 16 days), and heterozygous Tpi-1/Tpi-2 males (Z¹Z²) (mean PDD time = 25 days). The close correlation of TPI phenotypes and PDD times in these crosses, along with similar results for the maternal and paternal backcrosses of the F₁ individuals, indicates that the PDD time is principally controlled by genes on the Z chromosome and that heterozygous males exhibit incomplete or partial dominance of these genes. © 1992 Wiley-Liss, Inc.     

Host plant constituents as oviposition stimulants for a generalist herbivore: European corn borer

Oviposition response of the polyphagous European corn borer,Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae), to chemical constituents in host plants was investigated in the laboratory using two-choice bioassays. Foliar extracts of corn (Zea mays L.), pepper (Capsicum annuum L.) and potato (Solanum tuberosum L.) were prepared using the solvents pentane, acetone and methanol. In all three host plants, chemicals soluble in pentane stimulated oviposition. In potato, chemicals extractable in acetone also elicited a positive oviposition response. When presented with a choice between pentane extracts of corn and pepper, females preferred corn. No preferences were exhibited between pentane extracts of corn and potato or pepper and potato. Pentane extracts of corn husks, tassels, silk, and corn leaves from plants at early whorl and tassel (pre-pollen shed) stages of development also stimulated oviposition. Similar extracts from plants at 2-leaf and blister (when kernels resemble blisters) stages were not stimulatory. This indicates that plant phenology affects chemically mediated oviposition response in European corn borer. The potential use of plant chemicals for management ofO. nubilalis in the field is suggested.     

Understanding successful resistance management: the European corn borer and Bt corn in the United States

The European corn borer, Ostrinia nubilalis Hübner (Lepidoptera: Crambidae) has been a major pest of corn and other crops in North America since its accidental introduction nearly a hundred years ago. Wide adoption of transgenic corn hybrids that express toxins from Bacillus thuringiensis, referred to as Bt corn, has suppressed corn borer populations and reduced the pest status of this insect in parts of the Corn Belt. Continued suppression of this pest, however, will depend on managing potential resistance to Bt corn, currently through the high-dose refuge (HDR) strategy. In this review, we describe what has been learned with regard to O. nubilalis resistance to Bt toxins either through laboratory selection experiments or isolation of resistance from field populations. We also describe the essential components of the HDR strategy as they relate to O. nubilalis biology and ecology. Additionally, recent developments in insect resistance management (IRM) specific to O. nubilalis that may affect the continued sustainability of this technology are considered.     

Comparative susceptibility of European corn borer, southwestern corn borer, and sugarcane borer (Lepidoptera: Crambidae) to Cry1Ab protein in a commercial Bacillus thuringiensis corn hybrid

One field strain each of the European corn borer, Ostrinia nubilalis (Hübner); southwestern corn borer, Diatraea grandiosella Dyar; and sugarcane borer, Diatraea saccharalis (F.); were collected from cornfields in northeastern Louisiana. Susceptibilities of the field strain and a corresponding laboratory strain of the three borer species to Cry1Ab protein in DK69-70 Bacillus thuringiensis (Bt) corn hybrid were determined by exposing neonates to intact leaf tissues from whorl stage plants or by feeding neonates or third instars on a meridic diet treated with different concentrations of Cry1lAb protein extracted from Bt corn leaves. Mortality and growth of larvae were evaluated after 2 and 4 d posttreatment in the bioassays by using intact leaf tissues or after 7 d in the bioassays by using diet incorporating Cry1Ab protein. D. saccharalis was the least susceptible species to Cry1Ab protein among the three species, followed by D. grandiosella, whereas O. nubilalis was most susceptible. The 2-d mortality of D. saccharalis neonates on intact Bt leaf tissues was lower than that of O. nubilalis and D. grandiosella. All neonates of O. nubilalis were killed on the diet treated with Cry1Ab protein at 0.5 and 1 mg/kg. The mortality of D. grandiosella was > 75% at 1 mg/kg, but it was < 6% for D. saccharalis at 1 mg/kg. The LC50 values of D. saccharalis were 3- and 11-fold higher than those of D. grandiosella and O. nubilalis, respectively. The LC90 values of D. saccharalis were 8- and 32-fold higher than those of D. grandiosella and O. nubilalis, respectively. Larval growth of the three species on Cry1Ab-treated diet was inhibited, but the inhibition was greater for O. nubilalis and D. grandiosella than for D. saccharalis. The lower susceptibility of D. saccharalis to Cry1Ab protein suggests that it is necessary to verify if a high-dose Bt corn for O. nubilalis and D. grandiosella is also a high dose for D. saccharalis.     

Use of solid state fermentation to produce Beauveria bassiana for the biological control of European corn borer

The production process of a new bioinsecticide against european corn borer is described. The entomopathogenic fungus, Beauveria bassiana, is cultivated by Solid State Fermentation (SSF). The culture support chosen, clay microgranules, humidified with optimal nutritive solution, is incubated in optimal conditions during 48 hours, then dried for 5 days. The bioinsecticide can be directly used after harvesting, without formulation.This process is original for several reasons : - The granulometry (500 microm) and the bulk density (0.6) of the microgranules are compatible with the mechanical standard application of pesticides on corn. - The bioinsecticide could be produced in a pilot reactor of 1600 1 capacity, on 0.5m-thick-layer.- The biomass bound to microgranules conserves its efficiency after storage for 12 months at 4 degrees C, unlike pure cells. - Like the chemical insecticides usually used, this bioproduct has a field efficiency of 80%. Moreover, the efficiency of the product persists during 3 weeks.     

Free amino acids of the haemolymph of the southwestern corn borer and the European corn borer in relation to their diapause

The titres of free amino acids present in the haemolymph of diapausing larvae of the southwestern corn borer, Diatraea grandiosella and the European corn borer, Ostrinia nubilalis, were examined. High titres of serine were found in the haemolymph of both species. Serine may serve as a storage form of compounds that are required for the synthesis of uric acid and other purines. The high titres of proline found in the haemolymph of O. nubilalis during the fall and winter may contribute to the freezing tolerance of this species. Alanine accumulated in the haemolymph of both species during the winter.     

Ancestral feeding and survival of offspring in European corn borer

Experiments were conducted to evaluate the influence of ancestral adult feeding by European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), on larval survival in the field and neonate movement behavior in laboratory. Larval survival was higher when either the grandparental or parental generation had fed, but the feeding sites of the surviving larvae were not affected by ancestral feeding condition. This is the first evidence that grandparental feeding could influence larval survival in the field. Larval movement was observed in the laboratory. Silking speed of neonates was faster when either grandparents or parents had fed, while walking speed was faster only when parents had fed. No broad-sense genetic correlation was found between silking speed and walking speed. Broad-sense heritability among feeding histories were not significant for silking speed, but was significantly greater than zero for walking speed when grandparents fed and parents did not. These intergenerational effects could induce complex population dynamics in this species.     

Dispersal behavior of neonate European corn borer (Lepidoptera: Crambidae) on Bt corn

European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), has historically been a significant economically important insect pest of corn (Zea mays L.) in the United States and Canada. The development in the 1990s of genetically modified corn expressing genes derived from Bacillus thuringiensis (Bt) that encodes insecticidal crystalline (Cry) proteins has proven to be effective in controlling this insect as well as other corn pests. The purpose of this study was to assess the movement and dispersal behavior of neonate European corn borer on Bt corn. We examined differences in neonate European corn borer dispersal behavior for the first 4 h after eclosion in the field among a stacked pyramid (Cry1F X Cry1Ab X Cry34/35Ab1) Bt corn, a Cry1F Bt corn, and a non-Bt sweet corn; and in the laboratory among a Bt corn hybrid containing Cry1F, a hybrid containing Cry1Ab, a pyramid combining these two hybrids (Cry1F X Cry1Ab), and a non-Bt near isoline corn. In field experiments, we found that dispersal was significantly higher on Bt corn compared with sweet corn. In laboratory experiments, dispersal was significantly higher on Cry1Ab Bt corn and Cry1F X Cry1Ab Bt corn than on non-Bt near isoline corn. Results indicated that neonate dispersal may be significantly greater in Bt cornfields compared with non-Bt cornfields. The findings on dispersal behavior in this study will be useful in evaluating the efficacy of a blended seed refuge system for managing European corn borer resistance in Bt corn.     

Late-instar European corn borer (Lepidoptera: Crambidae) tunneling and survival in transgenic corn hybrids

Field studies were conducted in 1996 and 1997 to determine injury by and survival of late-instar European corn borer, Ostrinia nubilalis (Hübner), on genetically altered Bacillus thuringiensis Berliner corn, Zea mays L. Cry1Ab events 176, Bt11, MON810, and MON802; Cry1Ac event DBT418; and Cry9C event CBH351 were evaluated. Plants of each corn hybrid were manually infested with two third-, fourth-, or fifth-instar O. nubilalis. Larvae were held in proximity to the internode of the plant above the ear with a mesh sleeve. Larvae were put on the plants during corn developmental stages V8, V16, R1, R3, R4, R5, and R6. This study shows that not all B. thuringiensis hybrids provide the same protection against O. nubilalis injury. Hybrids with B. thuringiensis events Bt11, MON810, MON802, and CHB351 effectively protected the corn against tunneling by late-instar O. nubilalis. Event 176 was effective in controlling late-instar O. nubilalis during V12 and V16 corn developmental stages; however, significant tunneling occurred by fourth instars during R3 and R5. Event DBT418 was not effective in controlling late-instar O. nubilalis during corn vegetative or reproductive stages of development. Whether the B. thuringiensis hybrids satisfied high- and ultra-high-dose requirements is discussed.     

Fungi associated with eggs and first-instar larvae of the European corn borer

Fungi isolated from field-collected egg masses of the European corn borer, Ostrinia nubilalis, were identified as Alternaria spp., A. porri, Fusarium spp., Fusarium oxysporum, Beauveria bassiana, Mucor spp., and an unidentified yeast. Most fungi were associated with predator injury to the egg mass. Bioassay of fungi on egg masses, however, showed that Alternaria spp. and A. porri reduced the hatch of both injured and uninjured egg masses, and Mucor sp. reduced the hatch only when the egg mass was injured.