Consensus recommendation:

Managing Western C orn R ootworm R esistance to Bt on the F ringe

Submitted to the EPA

- FIFRA Scientific Advisory Panel Scientific Uncertainty Associated with CRW Resistance Monitoring for Bt Corn PIPs 2 December, 2013

This document is s upported by the following field crops entomologists:

Chris DiFo nzo, (corresponding author) Michigan State University

288 Farm L ane, East Lansing, MI
difonzo@msu.edu

Tracey Baute, Ontario Ministries of Agriculture and Food & of Rural Affairs Ridgetown, Ontario, Canada

Ron Hamm ond, The Ohio State University OARDC, Wooster, Ohio

Chris tian Krupke, Purdue University West Lafayette, Indiana

Andy Michel, The Ohio Stat e University OARDC, Wooster, Ohio

Art S chaafsma, University of Guelph Ridgetown, Ontario, Canada

Elso n Shields, Cornell University Ithaca, New York

Jocelyn Smith, University o f Guelph Ridgetown, Ontario, Canada

John Tooker, Pennsylvania State University State College, Pennsylvania

The first Bt corn targeted for rootworm control was commercially marketed in the U.S. in 2003. The Bt toxin in this corn, Cry3Bb1, was originally sold as Yieldgard Rootworm,

then combined with corn borer B t toxins and/or herbicide tolerance genes in YieldGard Plus, VT T riple, and Genuity VT TriplePro. Beginning in 2010, Cry3Bb1 wa s also available as part of a two

- toxin pyramid for rootworm control (with Cry34/35Ab1) incorporated into the SmartStax platform. The introduction of pyramids resulted in a reduction in refuge percentage from 20% to 5%, and a change of refuge placement from

structured to in

- the

- bag. Adoption of Bt traits by producers has been high. When all of the currently available trait packages are considered, the Cry3Bb1 toxin is expressed in the majority of Bt hybrids targeting rootworms in North America.Performance problems (i.e. fields exhibiting excessive root damage and lodging) with

Cry3Bb 1 hybrids were first reported in southern Minnesota and eastern Iowa in 2009. Registrants classified f ields with unexpected levels of root damage and high beetle

numbers as product performance inquiries. The number of problem fields in Iowa and

Minnesota has increased since that time , and additional reports have since come from Colorado, Illinois, Kansas, Missouri, Nebraska, South Dakota, and Wisconsin

. Using a combination of field and laboratory studies over multipl e field seasons, Gassmann et al.

showed that weste rn corn rootworm larvae from problem fields in Iowa survived better on Cry3Bb1 corn than larvae from fi elds without unexpecte d damage. C orn entomologists in the Midwest now agree that this, and several other ongoing research efforts, demonstrate evidence of field

- evolved resistance to Cry3Bb1 by western corn

rootworm . Further, analysis of field populations in Iowa now suggest s resistance to another toxin, mCry3A, and cross

- resistance between this toxin and Cry3 B b 1

.

Suspected Resistance in the Focus Area Agricultural production in the focus area for r ootworm resistance is characterized by

intensive corn cultivation coupled with low crop and landscape diversity. Rootworm

resistance in this focus area appears to have ar isen independently in single field s ( point

- source s )

. In hindsight, the original problem fields a ll share d the common characteristic s of planting to multiple years of continuous corn

, with the same (Cry3Bb1)

Bt trait . Continuous corn fields typically have high rootworm pressure , which maximizes the opportunity for resistance evolution because s election pressure is applied to a large

roo tworm population over a large area, year

- after

- year. Any alleles for Bt resistance

- even if rare

– are likely present in rootworm populations across the Corn belt. The pattern of problem fields to date suggest s that resistance to Cry3Bb1 evolved independe ntly

, in multiple locations across multiple states (as opposed to spreading from a single point source), often in areas of intensive production of continuous corn expressing the same Bt toxin. Local spread of beetles from point sourc es could then

contribute to widespread ‘neighborhood’ failures.

The registrant of Cry3Bb1, Monsanto

, responded to reports of performance issues with

a set of recommendations to manage Bt resistance, start ing with crop rotation to a non

host (typically soybeans) . Howeve r, the limited crop diversity in the central Corn Belt

, a direct need for grain for livestock, and highly favorable economics for corn production

, make crop rotation an unpalatable option for many producers. Furthermore, resistance in the focus area is so widespread that crop rotation would have to be practiced on a massive, coordinated scale to halt the spread of resistance to new areas

. As an alternative to rotation, Monsanto recommends using a differen t Bt trait targeting rootworms, alone or as part of a pyramid

, or applying a granular or liquid insecticide in

combination with a conventional or Bt hybrid. In practice, this usually has resulted in growers planting the SmartStax pyramid (Cry3Bb 1 + Cry 34/35 Ab1 ), often with a soil

insecticide. Use of an insecticide over

- top a Bt hybrid is not recommended by corn entomologists in the Midwest; insecticides alone should provide satisfactory control in most cases, without the associated economic costs of the Bt trait. Insecticides may also mask a resistance problem. Except for crop rotation

, most options listed above haveone primary shortcoming

– they continue to exert selection pressure. Resistance

arises when selection pressure (i.e. Bt toxin) is consistently applied to a pest population. There is little utility in continuing to apply the same pressure when resistance is present

, or at risk of occurring.

Suspected Resistance in the Fringe Area Production practices differ in important ways across the corn

- growing regions of North

America. In contrast to the central and western areas of the Corn Belt , agricultural production in the eastern Corn Belt is characterized by high er crop and landscape

diversit y, more crop rotation

, lower levels of irrigated corn, and smaller field and farm

sizes. Thus far, r ootworm resistance to Bt corn in this ‘F ringe A rea’ ( Indiana, Michigan, New York, Pennsylvania, Ohio, Ontario) is rare; only a handful of fields with unexpected damage have been re ported to two of us , in central Michigan (DiFonzo) and in New

York State (Shields)

. However, it is prudent to assume that the genetic basis for Cry3Bb1 resistance is present in the corn rootworm population across the Fringe region

, as in the Focus area. It follows that resistance is likely to arise in fields planted to

continuous corn with the same Bt rootworm trait

. Predictably , the fields in 2013 with unexpected damage in Michigan and New York were continuous corn fields in areas of heavy livestock production

, planted to either Cry3Bb1 or mCry3A hybrids for multiple

seasons

.

T he current status o f Bt

- resistant rootworm in the F ringe is somewhat analogous to the

movement of an invasive species from an established infested zone into a new area. Current examples in the Great Lakes region include emerald ash borer, which established and spread from Detroit, and the gypsy m oth, which is still moving from east

to west into Wisconsin and Minnesota. For both of these insects, ‘Slow

- the

- Spread’ programs involving education, monitoring, and remedial action were put in place to delay pest population movement. Beyond the ran ge of the established infe station, the

remedial action often involves eradicat ing isolated hot spots. In the case of rootworm resistance to Cry3Bb1, our goal is to use similar principles to slow any spread of resistance from the focus areas, and in particular to reduce the development of new resistant populations within the Fringe. T he goal is to preserve the usefulness of Cry3Bb1 and other Bt traits for as long as possible.

Recent history suggests that suspected resistance to Cry3Bb1 Bt hybrids (characterized by high levels of rootworm feeding upon roots and/or lodging of plants) , and to other Bt

toxins like mCry3A

, will be reported in additional areas of the corn belt in the near

future. Therefore, t he c orn entomologists on the F ringe have taken the following actions:

* Discover isolated point sources early . Growers, extens ion personnel and agribusiness representative s servicing the fringe area are being informed of the potential for Bt

resistance and urged to report suspect fiel ds to companies and the authors of this

document . Specific at

- risk areas or producer s (for example, dairy producers w ho typically plant high levels of continuous corn ) are particularly targeted for education focusing on detecting, reporting, and managing point sources of rootworm resistance. Infact, such targeted education efforts by two university entomologists directly resulted in

the reporting of the suspect fields in Michigan and N ew York.

Further, random sampling of adult beetles for resistance monitoring in the Fringe does not seem particularly efficient, given what we know about where and how resistance

arises. We thus recommend that i ndustry target high risk fields (continuou s corn)

, farms (livestock and dairy production ) , and areas (high rates of Bt adoption, based on seed

sales data ) for their monitoring efforts . Such direct efforts are more proactive and may detect shifts in susceptibility sooner than a random program.

* Respond and document isolated point sources

. When a suspected case of resistance is found, every attempt is made by us to document field history, plant damage, and beetle populatio n levels

, and to confirm Bt expression . If possible, a sample of adult

beet les is taken for eventual egg collection and resis tance testing

. For example, in
2013, eggs were sent to the University of Guelph

- Ridgetown for testing in 2014. Adjacent corn field s are also sampled with permission. The following season, this point

source and surrounding fields should continue to be monitored for beetle emergence and damage.

* Eliminate point sources. For fields with suspected resistance, our recommendation

– the sole recommendation

– is rotation the next season to a non

- host crop . Rotation

must be coupled with early and complete control of volunteer corn with a grass herbicide

. Rootworm eggs that hatch in a pr oblem field the following year exhibit 100% mortality if no hosts are present, making rotation the single

- most effective measure to

r educe the spread of resistance. The goal is to eliminate all offspring of resistant beetles, effectively wiping out the point

- source of genetic material for resistance to spread

. Note that in some areas in the Fringe (Indiana and southwest Michigan ), western corn rootworm females may lay eggs in non

- host crops, resulting in some rootworm pressure in first

- year corn. This behavioral modification is k nown as the soybean variant. The variant does not change our recommendation. R otation to a no n

host crop is still the single

- most powerful and robust method of reducing populations over a large area

– no rootworm larvae will survive and develop without corn in the field. Bearing this behavior in mind

, and to enhance resistance management further, w e also

rec ommend that a djacent at

- risk fields be rotated. If this cannot be done, then adjacent fields should at least be monitored the following year, and rotated as soon as p ractical as a precaution ary step

.

When there is absolutely no option to rotate a suspect or adjacent at

- risk field out of corn the following season, then the field should not be planted to a hybrid expressing the failing toxin

, or to a toxin with demonstrated cross resistance (for Cry3Bb1, this is mCry3A)

- alone, with an insecticide, or in a pyramid. Instead, the field should be planted with a rootworm hybrid expressing a different Bt altogether, or to a conventional hybrid treated with soil insecticide. Although rootworm adults will still emerge under this scenario, there will be no add itional selection of the population by the failing toxin. The suspect field should then be rotated as soon as possible. No other practice trumps the

sole recommendation for rotation to deal with a ‘hot

- spot’ on the Fringe.The sole recommendation of rotat ion is more restrictive than the mult iple mitigation

strategies recommended in the focus area

. However , our collective knowledge of rootworm biology and behavior suggests that this approach will be extremely powerful. Rotation also offers the advantage of eliminating exposure of the problem population to Bt toxins or other insecticides, which have the potential to worsen the situation. The assumption that eradication of point sources (i.e. targeted rotation of problem fields) will reduce resistance spread h as not been tested in the field. But given the speed with which Cry3Bb1 resistance evolved and its widening distribution, common sense dictates taking a proactive approach in the east, i.e., targetin g the sampling for resistance to high risk areas and chan ging cropping practices where problems are detected. Most producers in the Fringe are ideally equipped and geographically situated to rotate to

non

- corn crops (typically soybeans, sometimes wheat or alfalfa ) with minimal disruption to cropping practices; t his represents an important competitive advantage compared with many of the areas where resistance ha s been reported to date.

Further Information :

 Gassman et al. 2011. Field

- evolved resistance to Bt maize by western corn rootworm. PLoS ONE 6(7): e22629. doi:10.1371/journal.pone.0022629

 Gassmann. 2012. Field

- evolved resistance to Bt maize by western corn rootworm: predictions from the laboratory and effects in the field. Journal of Invertebrate Pathology 110:287

- 293

 Gassman et al. 2013. Resistance of western corn rootworm to Bt corn: data from the laboratory and field. ESA National Meeting, Nov. 10, 2013, Austin TX.