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Genetically Engineered Bt Corn and Range Expansion of the Western Bean Cutworm (Lepidoptera: Noctuidae) in the United States: A Response to Greenpeace Germany

(CC)
William D. Hutchison , Thomas E. Hunt , Gary L. Hein , Kevin L. Steffey , Clinton D. Pilcher , Marlin E. Rice
DOI: http://dx.doi.org/10.1603/IPM11016 B1-B8 First published online: 1 December 2011

Abstract

The western bean cutworm, Striacosta albicosta (Smith), is a pest of corn and dry beans in North America. Before the late 1990s, economic infestations of the insect were restricted mostly to the western Great Plains and Idaho. During 1999–2009, it greatly expanded its range and moved across the central and eastern regions of the Corn Belt, eventually reaching northeastern Atlantic coast states. Greenpeace Germany issued a 2010 report claiming that the dramatic range expansion of the western bean cutworm was due entirely to “pest replacement” that resulted from the adoption of genetically engineered Bt corn, which suppressed one pest species and allowed another species—the western bean cutworm, in this case—to take its place. We maintain that the scientific literature does not provide empirical field-collected data to support the Greenpeace Germany claim that Bt corn is the sole factor that influenced the range expansion of the western bean cutworm. We propose broader ecological and agronomic factors to explain why the western bean cutworm has recently expanded its geographic range to include all of the major corn-growing areas in the central and eastern United States. These additional factors may include insect biology, insect and corn phenology synchrony, reduced insecticide use, conservation tillage, soil type, glyphosate-resistant crops, insect genetics, insect pathogens, preexisting insect population densities, and climate change.

  • Bt maize
  • transgenic crops
  • pest replacement theory
  • Striacosta albicosta

In March, 2010, Greenpeace Germany sponsored a technical report (Then 2010) that summarized their interpretation of the primary factor that has facilitated the eastward range expansion of the western bean cutworm, Striacosta albicosta (Smith) (Lepidoptera: Noctuidae), in the United States. Despite the cutworm's broad endemic range in western North America, extending from northern Mexico to southwestern Canada (Keaster 1999), its status as an agricultural pest historically has been limited primarily to Idaho, Colorado, and Nebraska (Seymour et al. 2004, Miller et al. 2009). In these states, western bean cutworm (Fig. 1) is well known as an economic pest of field corn (maize), sweet corn (both Zea mays L.), and dry beans (Phaseolus vulgaris L.) (Douglass et al. 1957, Blickenstaff 1979, Blickenstaff and Jolly 1982, Appel et al. 1993, Seymour et al. 2004). As noted by Then (2010), the cutworm expanded its range during 1999–2009 throughout much of the United States Corn Belt and as far east as New York and Quebec, Canada (O'Rourke and Hutchison 2000, Rice 2000, Dorhout and Rice 2004, DiFonzo and Hammond 2008, Michel et al. 2010).

Fig. 1

Western bean cutworm, S. albicosta, adult (A), larva (B), and larval damaged ears (C).

However, Then (2010) offered a surprisingly simplistic conclusion that the range expansion of the western bean cutworm is due solely to “pest replacement theory,” as influenced by the adoption of transgenic corn. Briefly, within the context of transgenic corn adoption in the United States. Rice and Dorhout (2006) first proposed the idea that the decline of historically important pests such as the European corn borer, Ostrinia nubilalis (Hübner), may be one of the factors that allowed the western bean cutworm to become a more consistent economic pest of corn in the central U.S. Corn Belt (see also Dorhout and Rice 2010). Since the first U.S. approvals for transgenic corn in 1996, seed companies have commercialized numerous corn hybrids that express insecticidal proteins produced by the bacterium, Bacillus thuringiensis (Bt), including the Cry1Ab toxin, which provides 100% control of European corn borer (Ostlie et al. 1997, Burkness et al. 2002, Hutchison et al. 2010). However, the same corn hybrids that express the Cry1Ab protein (genetic events MON810 or Bt11) provide only moderate control (70–85%) of corn earworm, Helicoverpa zea (Boddie) (Storer et al. 2001, Horner et al. 2003, Daly and Buntin 2005, Burkness et al. 2010). Although a recent study provided evidence for regional suppression of European corn borer in the central Corn Belt (Hutchison et al. 2010), similar studies for corn earworm have been limited to the Atlantic coast states (Storer et al. 2008) and the southeastern region (Adamczyk and Hubbard 2006) of the United States, where western bean cutworm is not known to occur or has not been detected as a pest of corn.

One field study revealed that genetically engineered corn that expressed the Cry1Ab protein, which is not toxic to western bean cutworm, had greater levels of infestation of western bean cutworm than European corn borer in corn ears (Catangui and Berg 2006). To date, however, a larval competition study has not been replicated in the central or eastern Corn Belt regions where the western bean cutworm expansion has occurred. In addition, results with greater survival of western bean cutworm than European corn borer in the field can be confounded with the timing and magnitude of oviposition by each species. More research is needed to isolate these factors under field conditions. A recently published laboratory study showed that because corn earworm larvae are stunted when feeding on corn silks that express the Cry1Ab protein, western bean cutworm of the same or larger size can compete well with corn earworm when the two species are placed in the same arena (Dorhout and Rice 2010). These results also occurred when western bean cutworm were placed on the same Cry1Ab-expressing silks with both corn earworm and European corn borer, resulting in higher survival of western bean cutworm. However, placing these results in proper context, Dorhout and Rice (2010) clearly cautioned, “... this artificial laboratory experiment does not answer the question of intraguild competition in corn with western bean cutworms and other species in the field, but it does suggest a potential direction for future field research to determine the importance of intraguild competition in the recent range expansion ”... (emphasis added).

Given the limited conclusions of Then (2010), we believe that a specific response to each conclusion is necessary, and a comprehensive review of several other factors that also may influence western bean cutworm dynamics is warranted. Moreover, we are concerned that potential misinterpretation of selected quotes by western bean cutworm researchers could create confusion among future regulatory decision makers in the United States, Europe, and developing countries where registration of transgenic corn or other crops is requested. In this paper, we reexamine the pest replacement theory based on experimental evidence to date, and we discuss additional factors that may have contributed to the range expansion of western bean cutworm to the central and eastern U.S. Corn Belt.

Responses to Specific Conclusions of the Greenpeace Report

The following statements focus on discrepancies of fact and interpretation in the Greenpeace document (Then 2010), specifically as they relate to western bean cutworm, but are not designed to be all inclusive.

Title of the paper: “Agro-biotechnology: New plant pest caused by genetically engineered corn. The spread of the western bean cutworm causes massive damage in the U.S.” The western bean cutworm is not a new plant pest. It has been recorded in Idaho corn since 1954 (Douglass et al. 1957, Blickenstaff 1979). The insect was “observed seriously injuring dent corn ears in southwestern Nebraska” as early as 1960 (Hagen 1962, 1976). In addition, Crumb (1956) recorded the insect from Iowa, but not as a serious or persistent corn pest. In the summer of 1954, western bean cutworm was first observed damaging field corn and sweet corn across a swath of >100 miles (160 km) in southern Idaho (Douglass et al. 1957). Originally collected in Arizona (Smith 1887), the western bean cutworm was an economic pest of commercial pinto beans, Phaseolus vulgaris L., in Colorado by 1915 and in Idaho by 1941 (Hoerner 1948). By the mid 1950s, the insect had been recorded from across a large geographical area of the western and central Great Plains, plus the Rocky Mountains, which included nine states (Arizona, Colorado, Idaho, Iowa, Kansas, Nebraska, New Mexico, Texas, Utah), one Canadian province (Alberta), and Mexico (Hoerner 1948, Crumb 1956). Later, it was recorded from South Dakota and Wyoming (1970) and Oklahoma (1977) (Blickenstaff and Jolley 1982). The western bean cutworm spread throughout the western Great Plains and intermountain areas where corn and dry beans are produced. Blickenstaff and Jolley (1982) speculated this range establishment was related to “the development of intensified and modern agriculture.”

Little expansion occurred after the establishment of the insect in these regions until 1999 when it was recovered in southwestern Minnesota (O'Rourke and Hutchison 2000). Although the insect was previously documented from Iowa, it was not until 2000 that economic losses to corn were documented in the state, some fields with as much as 95% of the ears heavily damaged (Rice 2000). By 2004, the insect had expanded its range into northeastern Missouri and western Illinois, where it was detected in those states for the first time (Dorhout and Rice 2004). Over the ensuing 5 years, the range of the western bean cutworm continued to expand eastward. Adults were first captured in Pennsylvania, New York, and Quebec in 2009 (Michel et al. 2010). Because this range expansion coincided with increased use of transgenic (i.e., genetically modified) corn through this region, one might conclude that the recent expansion of the pest's range was “caused by genetically engineered corn” (Then 2010). However, we believe this conclusion is too simplistic. In Table 1, we summarize several additional and potentially interacting factors that also likely have influenced the recent range expansion of western bean cutworm (Table 1).

View this table:
Table 1

Table 1. Potential factors that have favored the recent range expansion of the western bean cutworm, S. albicosta, to the central and eastern U.S. during 1999–2009

FactorSpecific influenceReferences
Insect biologyThe species has a previous history of range expansions, for example, to Idaho, then to Nebraska. Moths in the family Noctuidae are capable of long-distance movement.Blickenstaff (1979), Hagen (1962), Lingren et al. (1994), Michel et al. (2010)
Insect and corn phenologyCloser synchrony of moth flight phenology relative to corn tasseling phenology (a stage of corn growth attractive for oviposition) as a result of increasing use of shorter maturity hybrids and earlier planting dates in the central U.S. Corn Belt (e.g., 100–110 days relative maturity).T. Hunt, G. Hein, University of Nebraska (unpublished data)
Reduced insecticide useWidespread planting of Bt corn that expresses the Bt Cry1Ab protein and the consequent impact of reduced insecticide use in Nebraska corn to control corn borers and corn rootworm adults may have resulted in increased survival of western bean cutworm, promoting an eastward expansion of its range.Pilcher et al. (2002), Wilson et al. (2005), Hunt et al. (2007)
Conservation tillageIncreasing trend for less tillage (e.g., no-till, min.-till corn production) throughout the U.S. Midwest (e.g., 66% of Midwest corn/soybean acres represent an area wide impact on _150 million acres _60.7 million ha_). Less tillage of corn stubble in the fall and less tillage before planting soybean in the spring favors survival of overwintering larvae and emergence of adults in the spring.CTIC (2006), Givens et al. (2009), O'Rourke and Hutchison (2000)
Alternatively, continued use of tillage in southern Minnesota (areas with clay soils), is one area where western bean cutworm populations (moths and larvae) have remained low since 2000.
Soil typeSandy soils favor overwintering success of western bean cutworm in Idaho, Colorado, Nebraska—insect can overwinter at greater depths, which minimizes mortality because of insulation from extremes in winter temperatures and reduction in effects from tillage. Recent reports of high infestations of western bean cutworm have come from sandy regions, including the central sands of Wisconsin, central Michigan, and Ontario, Canada.Baute (2011), G. Hein (unpublished data)
Glyphosate-resistant cropsGlyphosate-resistant crops (soybean, corn, cotton) encourage less tillage for weed management, which favors survival of overwintering larvae and emergence of adults (e.g., 88% of _76 million acres of soybean _30.8 million ha_ are planted to glyphosate-resistant soybean).Givens et al. (2009)
Pest replacementPest replacement hypothesis associated with the extreme reduction in European corn borer populations, which opens a niche for western bean cutworm (as discussed in present paper).Rice and Dorhout (2006), Catangui and Berg (2006), Eichenseer et al. (2008), Dorhout and Rice (2010)
Insect geneticsLack of a genetic “bottleneck” supports long-distance movement of western bean cutworms and consequent colonization eastward.Lingren et al. (1994), DiFonzo and Hammond (2008), Miller et al. (2009)
Insect pathogensPossible reduction in occurrence of Nosemaspecies (a microsporidium pathogen) in expanding western bean cutworm populations. However, previous research in Nebraska suggests this pathogen remains active.Helms and Wedberg (1976), Dorhout (2007), Dorhout et al. (2011)
Preexisting Insect population densitiesLow-level infestations of western bean cutworm in several states (1900–1970, e.g., Iowa and Kansas) may have preexisted in “newly infested” states. Moth flights detected recently may have resulted from one or more of the factors indicated in this table or may have been the consequence of an expanded, extensive monitoring network initiated in many additional states.Hoerner (1948), Crumb (1956), O'Rourke and Hutchison (2000)
Climate changeGradually warmer ambient winter temperatures in the central U.S. Corn Belt, may be facilitating improved survival.Diffenbaugh et al. (2008), Midwest Climate Center (2010)
  • Factors based on current knowledge of S. albicostabiology and additional agricultural production trends in the central U.S. Corn Belt. These factors also reflect potential areas for future research.

With respect to “massive damage ” referred to by Then (2010), although flights of adults have been documented via pheromone and light trap networks throughout the Corn Belt (Rice 2007, DiFonzo and Hammond 2008, Jesse et al. 2010, Michel et al. 2010), documentation of economically damaging larval infestations in field and sweet corn has been relatively limited considering the potential 85 million acres (34 millions hectares) of corn available to the pest each year (O'Rourke and Hutchison 2000, Catangui and Berg 2006, Eichenseer et al. 2008). To date, some of the more consistent infestations of western bean cutworm have occurred in dry beans in Michigan, where the tolerance for damage to bean pods is low (Michel et al. 2010). In field corn, in a multi-year study in five states (Colorado, Iowa, Nebraska, New Mexico, and Texas), Eichenseer et al. (2008) found >75% of non-Bt hybrids had western bean cutworm infestation rates >20%, but when yields were collected in Iowa, Minnesota, and South Dakota, the losses were “not massive” and estimated at 4.1–8.0 bushels/acre (256–501 kg/ha).

Summary, page 4: “This cutworm has historically been confined to very limited regions and did not cause any major problems in maize crops.” Major problems caused by western bean cutworm were recorded as early as 1962 in Nebraska (Hagen 1962) “where they destroyed as much as 40% of the kernels.” Further documentation of the historical importance of western bean cutworm as a pest of corn in Nebraska was the development of an integrated pest management (IPM) program that included an economic injury level (EIL) for larvae (Appel et al. 1993) and practical monitoring methods for the pest (Seymour et al. 2004). With respect to being confined “to very limited regions,” the distribution of western bean cutworm throughout the western Great Plains from Mexico to Alberta and the intermountian west were documented by Blickenstaff and Jolley (1982) and have been discussed previously.

Summary, page 4: “In 2009, maize plants affected by the western bean cutworm were even found in Canada for the first time.” The insect has previously been reported from Alberta in the mid 1950s (Crumb 1956) and more recently it was found in southern Ontario in 2008 (Baute 2008). That the insect was detected in Canada over 60 years ago, its recent occurrence in corn is not surprising.

Summary, page 4: “According to scientific publications, this new pest has been caused by the large-scale cultivation of genetically engineered plants expressing Cry1Ab ”... As noted previously, this insect has been a corn pest for decades (Michel et al. 2010); therefore, one cannot conclude that the recent expansion of the western bean cutworm was entirely “caused” by genetically engineered plants expressing the Cry1Ab protein. This statement also does not define “large-scale cultivation;” as noted in Hutchison et al. (2010), early adoption rates of Bt corn were quite gradual in many central Corn Belt states from 1996 to 2002, and nationally as of 2010, ≈35% of the corn in the United States continued to be non-Bt corn, for a variety of reasons, including non-Bt corn refugia for insecticide resistance management purposes.

Page 5: “In 2006, a scientific publication reported extensive damage in South Dakota (Catangui and Berg 2006). By 2004, there were similar reports from Iowa, Illinois and Missouri (Dorhout and Rice 2004).”Dorhout and Rice (2004) did not report “extensive damage;” rather, they reported the capture of 3 moths in Missouri and 5 moths in Illinois. With respect to the occurrence of western bean cutworm in Iowa, Dorhout and Rice (2004) stated, “it was not until 2000 that an economically damaging population (i.e., exceeding the economic threshold) was found in field corn. Since then, it has become a recurring economic pest in western Iowa.” However, the term “extensive damage” was never used to describe the Iowa situation, and the phrase “extensive damage” is a gross misinterpretation of the Illinois and Missouri data.

Page 6, footnote 3: “The western bean cutworm, so far only known as a pest in dry beans is on its way to become number one in the U.S. Corn Belt ”... This statement is inaccurate. In addition to being a pest of dry beans, the western bean cutworm has been a pest of corn since 1954 (Douglass et al. 1957, Blickenstaff 1979). In addition, there is no empirical evidence that the western bean cutworm will cause annual yield losses similar to the yield losses typically associated with major corn pests–western corn rootworm (Diabrotica virgifera virgifera LeConte), northern corn rootworm (Diabrotica barberi Smith and Lawrence), corn earworm, European corn borer, or fall armyworm (Spodoptera frugiperda (J. E. Smith)), across a broad geographical area.

Page 7, “This latter pest (corn earworm) feeds not only on corn but is also cannibalistic to other pest insects such as the western bean cutworm.” The corn earworm is not cannibalistic on other insects; it can cannibalize only individuals of its own species. However, it can be predaceous on other species, such as the western bean cutworm (Dorhout and Rice 2010).

Page 8, “Interaction between the western bean cutworm and the corn earworm was confirmed in 2010 (Dorhout and Rice 2010). It can without doubt be concluded that the spread of the western bean cutworm is in fact fostered by the cultivation of Bt corn MON810.” This statement ignores the last paragraph of Dorhout and Rice (2010) who defined the limits of the conclusions from their study. The last paragraph of that paper states: “This artificial laboratory experiment does not (our emphasis) answer the question of intraguild competition (that could cause pest replacement) in corn with western bean cutworms and other species in the field, but it does suggest a potential direction for future field research to determine the importance of intraguild competition in the recent range expansion of western bean cutworm.” The interaction between western bean cutworm and corn earworm that Greenpeace Germany claimed to have been confirmed was based on a laboratory study; intraguild competition has never been confirmed in field studies. Additionally, the phrase “without doubt” is flawed. Science always allows for rejection of a hypothesis; therefore, there can and should be doubt.

Moreover, and germane to understanding potential interactions between the two pests under field conditions, the corn earworm historically has not been a consistent pest of field corn in the central Corn Belt states, as it has been in the southern and eastern United States (e.g., Molina-Ochoa et al. 2010). Because the corn earworm cannot overwinter in the northern United States, most of the infestations in the central and Midwestern United States (e.g., latitudes >40 degrees) are associated primarily with migratory flights in late July through August when moths disperse northward from the southern states (e.g., Lingren et al. 1994). By the time corn earworm adults arrive in the Midwestern United States, most of the field corn in the central Corn Belt has pollinated and is much less attractive for oviposition (W.D. Hutchison, unpublished data). Consequently, most of the corn earworm moths arriving to the upper Midwest in late summer are attracted to sweet corn, which is actively silking. However, sweet corn accounts for a small proportion of the total corn acres in the Midwest (e.g., <1% of the 7.2 million acre corn landscape in Minnesota; Burkness et al. 2002, 2010). In addition, despite the predaceous behavior of corn earworm on European corn borer larvae in the laboratory, field data suggest that both species, under a wide range infestation levels, often co-infest the same corn ears. For example, additional analysis of the multi-state data from Burkness et al. (2002) indicated 50–70% of the sweet corn ears at harvest were infested with both corn earworm and European corn borer larvae (based on non-Bt hybrids for three planting dates, in Minnesota, Illinois, and Wisconsin). These data suggest that European corn borer larvae may avoid corn earworm predation within the ear by altering their feeding location (e.g., moving to the side or base of ear). The pest replacement hypothesis is interesting from an ecological standpoint, but in this context for lepidopteran larvae in corn, the hypothesis should be examined in more detail for European corn borer, western bean cutworm, and corn earworm, under field conditions. For example, one important variable to examine closely is the impact of differential timing of larval hatch near the corn ear, by each species, and how this alone might influence survival of western bean cutworm larvae.

Notably, and a curious theme throughout the Greenpeace Germany report, is that Then (2010) ignored the possibility of other influences on western bean cutworm range expansion (Table 1), including several ecological and agronomic factors. For example, Dorhout (2007) found that adult western bean cutworm populations across a geographical continuum from eastern Wyoming to western Indiana, a distance of 860 miles (1,384 km), had an infection rate of an unidentified Microsporidium that was substantially less in moths collected east of the Missouri River—an approximate geographical midpoint—compared with adults trapped west of the Missouri River. In other species, such as European corn borer, individuals with less pathogenic infection were able to lay more eggs and fly farther (Dorhout et al. 2011), both factors that enhance the spread of a species. This was overlooked by Greenpeace Germany as a possible factor influencing the spread of western bean cutworm. This and other factors that may have contributed to the eastward expansion of the western bean cutworm are reviewed in Table 1 and in the summary section of this paper.

Page 9, “It is widely expected that there will be a further increase in damage over the coming years. Not only can the regional expansion of the pest increase but also the intensity of the damage it causes.” This broad statement that economic damage is expected to get worse is not supported by the literature. An examination of Nebraska data shows that western bean cutworm populations fluctuate, often in 6- to 8-year cycles (Hagen 1976), as do many insect populations over time. Since 2008, western bean cutworm infestations in eastern Nebraska and western Iowa have been subeconomic (T. Hunt, unpublished data). As with the European corn borer (e.g., Hutchison et al. 2010), some of the cyclical fluctuation in western bean cutworm may also be attributed to infections by Nosema spp. (Helms and Wedberg 1976, Dorhout et al. 2011), as well as numerous additional biotic and abiotic factors. The western bean cutworm population in 2009 declined substantially from levels recorded during previous years across much of the Corn Belt (Jesse et al. 2010). One exception to this trend was the increased numbers of adults captured in Michigan and Ontario, Canada, where damaging infestations were found in some fields of dry beans and corn (Baute 2010, 2011; Michel et al. 2010). In summary, although western bean cutworm adults have been detected recently in many states for the first time, moth captures at many locations have been rather low (e.g., <200 per season/trap), numbers that likely will not result in economically damaging larval infestations in corn (Michel et al. 2010, Seymour et al. 2010).

Page 9, “Industry's solution: more genetically engineered corn, ... what happened came as a surprise to farmers.” Farmers and entomologists have coped with pest resurgence and pest replacement for many years, often associated with changing insecticide use patterns (Luck 1977, Pedigo and Rice 2008). It was not unexpected that placing insecticidal Bt proteins within a crop, particularly Cry1Ab, which is highly efficacious against European corn borer (Ostlie et al. 1997, Burkness et al. 2002), would reduce the use of chemical insecticides for control of the pest (Hunt et al. 2007), thereby creating changes within the insect pest complex of the U.S. Corn Belt; Ostlie et al. (1997) anticipated that some minor pests could become a new threat to corn production, including western bean cutworm.

Page 9, “Actually, the companies had a possible solution in readiness ... a further corn hybrid ... so-called Herculex Corn ”... Herculex I (corn that expresses the Cry1F Bt protein) was not developed in response to an outbreak of a new pest. It was tested initially for control of black cutworm (Agrotis ipsilon (Hufnagel)) and fall armyworm, as well as control of European corn borer, to compete commercially with corn that expresses the Cry1Ab protein. The trait was tested across a wider range of environments and spectrum of insects, which provided a unique opportunity to assess the level of protection against other caterpillar pests, including western bean cutworm. The initial hypothesis was that because western bean cutworm is in the same subfamily of Noctuidae as Agrotis species, Herculex I might provide some protection against western bean cutworm. The coincidence of western bean cutworm moving eastward and field testing across a wide geographical area was a result of observations at the right time and place (Catangui and Berg 2006, Eichenseer et al. 2008). Research and development of the trait started before western bean cutworm was noted as a pest east of the Missouri River and in the central and eastern Corn Belt (H. Eichenseer, Pioneer Hi-Bred International, personal communication).

Page 10, “Presumably, western bean cutworm larvae have differing levels of sensitivity.” It is well known that populations of pest species exhibit significant variability (or sensitivity) to a given toxin (Pedigo and Rice 2008), which is true for lepidopteran pests and Bt toxins (Pilcher et al. 1997, Horner et al. 2003). This is the primary reason proactive resistance management plans were initially promoted and mandated by the U.S. Environmental Protection Agency (EPA) when Bt corn was first approved in 1996 (e.g., Ostlie et al. 1997, Lewis and Portier 2001, Glaser and Matten 2003). The 20% non-Bt corn refuge area initially required by the EPA for European corn borer resistance management (e.g., Onstad et al. 2002, Glaser and Matten 2003), may have also assisted with minimizing the risk of western bean cutworm resistance to transgenic corn.

Page 11, “There is no mention that the problem might be considerably curbed if U.S. farmers were to stop growing corn expressing Cry1Ab ”... This is a critical statement in the report. Then (2010) extrapolated from the simplistic, single-factor assumption of “pest replacement” to recommend that the primary solution to stop the spread of western bean cutworm would be to stop planting corn that expresses the Cry1Ab protein. As shown in Table 1, there are many other factors that may influence the spread of western bean cutworm. Given the biology of western bean cutworm, along with one or more of these additional factors, it is likely that pest replacement is not the primary factor affecting range expansion of the western bean cutworm. Finally, given the success of area wide suppression of European corn borer throughout much of the central Corn Belt (Hutchison et al. 2010), current resistance management efforts for the pest and the continued availability of Bt corn hybrids for other insect pests, removing corn that expresses the Cry1Ab protein from the marketplace is neither a realistic nor rational solution.

Page 11, “Indeed, in some regions of Michigan, farmers were advised to spray insecticides to avoid damage in dry bean cultivation.” Again, this is not the first time farmers have been advised to spray insecticides for this crop. Dry bean production throughout the Midwest often involves the application of insecticides for other insect pests, including potato leafhopper (Empoasca fabae (Harris) (e.g., Michel et al. 2010). In fact, insecticides applied against Mexican bean beetle (Epilachna varivestis Mulsant) in Nebraska were considered one reason why western bean cutworm moth flights were lower in the area of dry bean production than in the production area dominated by corn (Hagen 1976).

Page 12, “... companies are pushing for the development of the armament of genetically engineered corn.” The development of pyramided Bt events has been underway for several years, long before the western bean cutworm began to expand its range in the central Corn Belt (e.g., Ostlie et al. 1997, Hutchison et al. 2010). In fact, one of the reasons to pursue the use of pyramided Bt events (e.g., SmartsStax) was to broaden the spectrum of control for the lepidopterans, simplify insect resistance management for growers, and further minimize the need for chemical insecticides (e.g., Burkness et al. 2010). Commercial use of genetically engineered Bt corn was expected to substantially reduce the use of chemical insecticides (Rice and Pilcher 1998). As indicated in several economic and environmental impact studies of Bt crops and farmer practice surveys (Pilcher et al. 2002, Wilson et al. 2005), reduced insecticide use continues to be a favorable outcome of transgenic corn technology (Naranjo 2005, Brookes and Barfoot 2008, Romeis et al. 2008, Carpenter 2010).

Page 12, “The U.S. insect resistance management (IRM) implies a high dose and refuge strategy.” As noted previously, the IRM plans mandated by EPA are well documented, and for Bt corn were initially developed with a focus on European corn borer and corn earworm. At the time of approval and commercialization of Bt corn hybrids, western bean cutworm was still considered to be a minor pest and limited to the western Corn Belt. To date, non-Bt corn refuges maintained in the central Corn Belt (e.g., Hutchison et al. 2010), still comprising ≈35% of U.S. corn, likely have assisted in minimizing evolution of Bt resistance in both European corn borer and western bean cutworm.

Pages 14–16, “Industry's solution: more hazardous insecticides.” Insecticides, applied in response to potentially economic infestations discovered during pest monitoring, have been the primary method of managing western bean cutworm since the 1950s in Idaho and since the 1960s in Colorado and Nebraska (Seymour et al. 2004). Considerable space in this section of the Greenpeace Germany paper is given to a review of some of the more well known concerns regarding nontarget impacts of insecticide-based strategies. These have been well documented for many years in the United States (Luck et al. 1977, Pedigo and Rice 2008), and have been the focus of considerable research on insecticide alternatives, including biological control, cultural control, and host plant resistance. In brief, as part of IPM programs for many U.S. crops, chemical insecticides generally are used only when other tactics such as biological control or host plant resistance cannot provide economic control (Radcliffe et al. 2009). For growers who prefer to plant non-Bt corn, liquid foliar-applied insecticides are available that are effective against western bean cutworm (e.g., CropWatch-Insect Management, 2009). Farmers and crop consultants are made aware of numerous chemical insecticides for control of western bean cutworms via Cooperative Extension Service recommendations in several states (e.g., Seymour et al. 2004, 2010; Peairs 2011). Growers in Nebraska and other Corn Belt states who prefer to plant non-Bt hybrids often hire crop consultants to monitor fields for western bean cutworm egg masses during peak moth flight to anticipate economic infestations (Seymour et al. 2004, 2010).

Pages 17–18, “Some points for discussion ”...Then (2010) stated that there is “a growing need to find alternatives to current practices,” and then generalized the principles of IPM as the solution. He suggested that crop rotation would add more stability to an ecosystem and prevent the adaption of pests to certain crops. Annual crop rotation of corn and soybean is a common practice in the U.S. Corn Belt where the two crops frequently are planted adjacent to each other. In addition, recent plantings of the two crops indicate that the ratio of corn to soybean is 53:47 on 165.6 million acres (67 million hectares) (NASS 2011). Crop rotation has numerous agronomic advantages. However, because female western bean cutworms are highly mobile and can fly 11.3 miles (18.4 km) in 12 hours (Dorhout 2007), and because the ratio of the two crops is nearly 50:50, crop rotation is not a realistic alternative method of control for this insect pest.

Another strategy suggested by Then (2010) was to produce corn plants with tight husks that allow (our emphasis) corn earworm to subsist on plants while at the same time controlling western bean cutworm. In principle, tight corn husks are known to be a useful host plant resistance strategy (with or without Bt) for some insect pests such as the European corn borer (e.g., Burkness et al. 2001). However, this approach is not feasible for western bean cutworm larvae given their frequent penetration of ear directly through the husk, when entering the middle or base of ear (Seymour et al. 2010). Moreover, the concept of allowing an economically damaging insect such as corn earworm to exist simply as a “potential predator,” is not sustainable or realistic, given the yield losses caused by corn earworm.

Lastly, Then (2010) proposed “using beneficial insect parasites,” but did not offer suggestions for potential parasitoid species that could be used to manage western bean cutworm, possibly because none are known. Michel et al. (2010), in their comprehensive review of western bean cutworm, did not list any parasitoids as biological control management options; they listed only predators and pathogens. Moreover, and applicable to Bt corn specifically, several recent meta-analyses have shown that Bt corn supports high numbers of generalist predators (e.g., Naranjo 2005, Romeis et al. 2008), many of which can be effective against the western bean cutworm.

Page 19, “Conclusions.”Then (2010) concluded that the “spread of western bean cutworm should be seen as part of a worrying development” on the future of sustainable agriculture and that farmers will end up buying “expensive seeds to grow multi-stacked Bt-plants and spraying hazardous insecticides.” First, American farmers are not forced to buy “expensive” seed, but many farmers realize the agronomic and pest management benefits provided by the technology and have embraced transgenic Bt corn. Sixty-three percent of the U.S. corn acres were planted to Bt corn technology in 2009 (ERS 2010). Second, survey results published by Hunt et al. (2007) do not support Then's (2010) prediction that corn producers will resort to “simultaneous additional spraying of hazardous pesticides.” Hunt et al. (2007) reported that the use of insecticides was lower in Bt corn than in non-Bt corn in Kansas and Nebraska.

Summary of Additional Factors That May Be Responsible for the Eastward Expansion of Western Bean Cutworm

In addition to addressing specific points in the Greenpeace Germany article, we discuss several factors, beyond pest replacement theory, that likely have had an impact on the eastward spread of western bean cutworm, which has now reached Long Island, NY (Baute 2010). Given what we have learned from the pest's history of range expansion, our knowledge of western bean cutworm biology, and current production practices in the U.S. Corn Belt, many factors may be responsible for the recent movement of western bean cutworm into the eastern United States (Table 1). It is instructive to review all possible factors and to realize that many of these factors may be working in tandem or interacting to facilitate the increasing geographical distribution of this insect. Many of these factors also reflect areas where new research is needed.

Pest Biology and Ecology

As a species within the family Noctuidae (Crumb 1956), western bean cutworm adults are expected to be good fliers and have a reasonably high potential for long-distance flight that would explain the gradual interstate movement and range expansion in the United States since 2000. One example that suggested long-distance movement occurred in 2007 when larval damage to corn was first observed in northwest Michigan (DiFonzo and Hammond 2008). Before 2007, moth flights had been monitored only in southern Michigan, near the known infestation area along the Indiana and Ohio border. However, in August 2007, cornfields in several northwest Michigan counties were infested with western bean cutworm larvae. Although pheromone traps were not yet in place that year, a nearby weather station recorded sustained winds at 191° to 281° (south-south-west to west) between 23 July and 3 August, a period when peak moth flights would be necessary for subsequent larval populations. The authors hypothesized that these winds carried and deposited large numbers of western bean cutworm adults in several northwestern counties near Lake Michigan; strong winds from the west also suggested potential movement of moths from Wisconsin, where the pest was well established by 2007 (Michel et al. 2010). In addition, a recent genetic analysis of western bean cutworm populations from Wyoming to Illinois indicated considerable homogeneity among populations and concluded that the lack of a “genetic bottleneck” (i.e., no apparent evolutionary population structuring or restriction) was supportive of an eastward range expansion (Miller et al. 2009).

Last-stage larvae (prepupae) of western bean cutworm overwinter in earthen cells as deep as 4–8 inches (≈10–20 cm) beneath the soil surface (Seymour et al. 2004, 2010). Larvae typically burrow deeper in sandy soils, which is thought to enhance survival, and in western Nebraska and eastern Colorado, western bean cutworm populations are largest in areas where very sandy soils are found (G. L. Hein, unpublished data). Two of the regions recently colonized by western bean cutworm are the central sands of Wisconsin and sandy-loam soils of western and central Michigan (Michel et al. 2010). These regions also are known to have relatively mild winter temperatures conducive to overwintering survival (Michel et al. 2010). By contrast, despite detection in 1999 in southern Minnesota, the western bean cutworm has not, thus far, become an economically important corn pest in the state (W.D. Hutchison, unpublished data). Most of the corn production in southern Minnesota is characterized by heavier clay soils and colder winters versus the sandy soil regions of Wisconsin and Michigan. Recent trends for warmer winter weather in the Midwest region (Midwest Climate Center 2010), along with increasing ambient temperatures expected from climate change models (Diffenbaugh et al. 2008) also may have facilitated western bean cutworm survival, and could contribute to long-term establishment.

Changes in Agronomic and Production Systems

Just before and since 2000, two important changes in the corn and soybean Midwest production system may have facilitated the range expansion of western bean cutworm: significant increases in conservation tillage (i.e., reduced or no tillage) (CTIC 2006) and the rapid adoption of glyphosate-resistant soybean (Givens et al. 2009). Generally, less deep-plowing minimizes mortality to insect pests that overwinter in the soil (e.g., Stinner 1990). For example, Gray and Tollefson (1988) found that survival of corn rootworm, Diabrotica spp. (Coleoptera: Chrysomelidae), eggs in the Midwest is greatly increased in no-till or chisel-plowed fields than in moldboard-plowed fields. Where moldboard plowing occurs, cold winter temperatures penetrate the soil profile more deeply, and mortality of corn rootworm eggs is greater. For corn earworm, tillage resulted in ≈75% mortality (Roach 1981). The areas of greatest risk from serious western bean cutworm infestations in Nebraska and eastern Colorado have very sandy soils, which requires no-till or minimal tillage. More research is necessary to assess overwintering survival of western bean cutworm, but given the depths at which the prepupae overwinter (Seymour et al. 2004, 2010; Baute 2011), it is conceivable that reduced tillage could have a positive impact on survival of the insects.

With respect to glyphosate-resistant soybean, Givens et al. (2009) found significant reductions in conventional tillage in most of the states surveyed. The corn-soybean rotation continues to be the most dominant cropping sequence throughout the Corn Belt. Consequently most cornfields will be followed with soybean the subsequent year. With glyphosate-resistant soybean, most growers wait until the soybean plants are 12 inches (≈30 cm) tall and the weeds have germinated before applying the herbicide. Because of the high level of weed control, there is less need in most soil types to apply much tillage after the corn is harvested, either in the fall or spring. Farmers can then plant glyphosate-resistant soybean directly into corn stubble in the spring, knowing that most weeds can be controlled with glyphosate, requiring less reliance on cultivation or tillage to manage weeds. Less tillage of corn in the fall and less tillage of soybean in the spring or summer create less disruption to western bean cutworms in the soil, with less impact on pupation and adult emergence.

Another possible reason for the range expansion of western bean cutworm during the past decade may have been the reduced use of foliar insecticides in corn in Nebraska (Hunt et al. 2007), particularly for control of European corn borer during the same period of expansion. The insecticide-vulnerable period for both European corn borer and western bean cutworm larvae can overlap. Reduction or elimination of foliar insecticide applications that target European corn borer, which has occurred with increased use of Bt corn, likely resulted in increased survival of western bean cutworm.

An additional trend for several Midwest states is to plant shorter-maturity hybrids (e.g., 100–110 days) at earlier dates so that corn pollination occurs before the onset of high temperatures and moisture stress in midsummer (Hicks and Thomison 2004) and to minimize harvest delays (T. Hunt, unpublished data). Because western bean cutworm females are highly attracted to late whorl (pretassel) stage corn (Seymour et al. 2010), a transition to corn hybrids with earlier maturities and earlier planting dates may have created enhanced synchrony of the host with moth emergence and oviposition.

In conclusion, although Then (2010) attempted to fault transgenic Bt corn for the geographical spread of western bean cutworm into eastern North America, historical records indicate that the insect had an extensive range west of the Missouri River, and considerable eastward spread had began before the widespread adoption of Bt corn. Many factors, operating alone or interacting (Table 1), may have played a role in this biological phenomenon. The evidence is conclusive—the western bean cutworm is neither a “new plant pest” nor “caused by genetically engineered corn” as stated by Greenpeace Germany.

Acknowledgments

We very much appreciate the comments and suggestions of two anonymous reviewers. Photographs of western bean cutworm and ear damage provided by M. E. Rice.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, providedthe original work is properly cited.

References Cited

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