2 documenting its changes to the CRW resistance management program for Bt corn Pl ant Incorporated Protectants (PIPs)

.

EPA ’s new framework for Corn Rootworm Resistance Management and Bt Corn ( he reafter referred to as ‘framework’) is consistent with the recommendations received from the SAP and expert corn rootworm entomologists

, and addresses comments received from the public

. T he final

, implemented framework includes new obligations of registrants that distinguish it from the previous resistance management program [ 5 ] :

• Proactive Integrated Pest Management (IPM) : Each Bt technology provider must develop and implement an educational outreach program that will help the company’s customers develop and implement a multi

- year CRW management plan when using Bt corn, consistent with good IPM practices. The use of IPM is important as a means to reduce the likelihood of resistance, particularly with an insect like CRW that readily adapts to control efforts. IPM tech niques for CRW encouraged in the educational outreach
program include the rotation of fields to non

- Bt corn crops (e.g., soybean) every few
years , which should greatly reduce resi stant corn rootworm populations.

• Responses to Cases of Unexpected Damage (UX D) to Bt Corn Fields: CRW damage to Bt corn fields may be an early indicator of developing resistance. A proactive and effective response to such cases may lessen (or eliminate) the impact of resistance in the CRW population if the damage is in fact due to resistan ce

. As part of the new framework, Bt corn c ompanies are required to investigate reports of damage and conduct tests to determine whether CRW are resistant to Bt corn. Companies must also implement “Best Management Practices” (BMPs), which are I PM

- based strategies designed to reduce CRW popul ations in the affected field(s) and noti fy affected companies, neighboring
customers , extension specialists, and crop consultants in areas where populations are found to be resistant.

• Enhanced Mitigation Strategies for Cases of Confirmed Resistance: When testing of CRW from UXD fields confirms resistance to Bt corn, companies are required to implement a response strategy to limit (or eliminate) the resistan t population

. Companies

are re quired to take the following actions : notify affected parties (customers, extension specialists, and crop consultants) in areas with resistant populations ; impose restrictions

on t he use of the Bt corn product with resistance in the affected area ; and encourage growers to implement steps to reduce or eliminate the resistant population, such as crop rotation to soybean

.

• Additional information on the new CRW resistance management framework can be found on EPA’s web page at http://www.epa.gov/regulation

- biotechnology

- under

- tsca

and

- fifra/framework

- delay

- corn

- rootworm

- resistance

. See also the specific terms and conditions of registration specific to corn rootworm being imposed on these products.
In developing the framework, EPA considered all comments received by growers, grower and agricultural groups, stakeholders, CRW experts, non

- governmental organizations

, and other government entities in refining the original proposal

. EPA believes the new framework addresses

concern s raised by a number of commenters that the changes to the CRW resistance management program as initially propo sed in 2015 could be too prescriptive and not responsive to the needs3 of growers. The final framework allows flexibility for growers

, while incorporating sound scientific standards to improve the old resistance management paradigm for CRW and Bt corn

.
The intention of EPA’s framework is to extend the viability of Bt corn and future new CRW PIP products that reduce exposure to conventional pesticides in the environment and to humans

. Though resistance to some currently available CRW Bt toxins has been documented, EPA maintains that the framework should function well in areas inside and outside of the Corn Belt where resistance to these PIPs is not as prevalent

. In areas with CRW resistance to Bt traits , the framework encourages growe rs to utilize sound IPM tools (e.g., rotating to a non

- corn rootworm host) to manage corn rootworm populations

. The framework also provides a strong incentive for registrants to encourage rotation to non

- host crops such as soybean , which is the preferred and most effective method for managing resistance development in a field [ 6 ] [ 7 ]

. Most importantly

, the f ramework implements a program for future technologies and ensures that these management tools are in place to delay resistance in corn rootworm a t the onset of a new commercial PIP registration

. While the framework is legally binding for the biotech nology companies selling the Bt seed , it permits flexibility for growers and help s to encourage a n adaptive multi

- year corn rootworm management plan that will fit individual grower’s needs. The refore, the burden on growers as a result of the new framework should be minimal

. In addition, the framework s eeks to preserve the benefits of Bt corn to growers for as long as possible.

B. Background on Corn R ootworm Resistance to Bt Corn

Academic researchers at the University of Iowa first documented in

- field r esistance to Cry3Bb1

, one of the Bt PIPs used to control CRW

, in 2009 [ 1 ] [8] [9] , six years after the first commercial release of Cry3Bb1. The researchers use d a novel on

- plant bioassay rather than the established diet bioassay approach to identify resistance in the populations collected from the unexpected damage (UXD) fields. Subsequently, in 2012 , resistance to Cry3Bb1 was also confirmed in parts of Illinois and Nebraska using the same assay approach [10 ] [11]

. A cademic r eports of cross

resistance between Cry3Bb1 resistant CRW populations and mCry3A were first published in 2014 ; these reports further heightened EPA ’s concerns . During this time, unexpected damage cases to mCry3A cornfields were also investigated and mCry3A resistance was confirmed [12]

. In addition, EPA received a letter signed by 22 corn rootworm entomologist s on March 7, 2012, containing recommendations to the Agency on how best to prolong the lifetime of the Bt CRW technology to which CRW were rapidly developing resistance [13]

. Despite these field and academic reports, r esistance to Bt toxins could not be confirmed using standard diet bioassay methodologies used by registrant s , required by EPA for resistance monitoring

, and described in the terms and conditions of registration for these PIP products . The

reasons are as follows :

• CRW are less sensitive to Bt than other insects and large amounts of toxin (or extrapolations from lower concentrations) are needed to obtain a 50% mortality (LC 50

–4 lethal concentration where 50% of the population dies ) in the assays. Large amounts of toxin are prohibitively expensive to produce

.

• EC 50 (effective concentration where 50% of the populati on is impacted) measures (more sensitive measure than LC 50 used in diet bioassays) are still too variable and not sensitive enough to make a definitive resistance conclusions;

• Historical comparisons between populations collected in different years using EC 50 data can also be limited if the testing methodology is modified or toxin lots are changed or sourced differently;

• No diagnostic concentrations are available to identify potentially resistant populations from susceptible ones ; and

• Differences in compan y used diets also affect the accuracy of diet bioassays and add further variability and uncertainty to the analysis of the data

.

T he resistance reports by academic research scientists in conjunction with the recommendations of public corn rootworm experts led the Agency to re

- evaluate the current CRW resistance management program , including the use of diet bioassays

. On September 27, 2013, the Agency released its white paper on corn rootworm resistance monitoring for Bt Plant

- Incorporated Protectants (PIPs) [ 2 ] listing a series of “scientific uncertainties associated with corn rootworm resistance monitoring for Bt corn Plant

- Incorporated Protectants (PIPs)” in preparation for a Scientific Advisory Panel meeting in December 2013 and proposed improvements for the CRW IRM program

.

C. Scientific Advisory Panel Meeting and Recommendations to the US EPA

The US EPA’s Office of Pesticide Programs (OPP) convened a Scientific Advisory Panel meeting on December 4

- 5, 2013 , in Arlington, Virginia, to discuss the scientific uncertainties and the Agency’s proposal to improve six major components of the corn rootworm resistance management program. The Agency’s charge posed to the SAP asked for guidance on the following identified topics:

1) An nual sampling to assess Bt susceptibility; 2) Sampling in response to damaged Bt fields; 3) Diagnostic assays; 4) Defining resistance; 5) Determining remedial action areas; and 6) Containment and mitigation of resistance.

Public commenters, consisting of growers, ABSTC (Agricultural Biotechnology Stewardship Technical Committee , a consortium of the Bt corn companies ) , and Non

- Government Organization ( NGO ) representatives made presentations to the Panel on issue s related to Best5 Management Practices (BMP), on

- plant assay methodology resistance purposes , and rootworm resistance monitoring and development of resistance

. EPA/OPP presented the SAP with an overview of CRW Insect Resistance Management ( IRM ) and current resistance issues, including the scientific uncertainties associated with the established resistance management program for CRW and Bt corn. EPA ’s charge questions and the SAP’s response and recommendations are summarized below. The full repor t can be accessed on EPA ’s website ( http://www.epa.gov/sap/meeting

- materials

- december

- 4

- 6

- 2013

- scientific

- advisory

panel ) and materials related to the SAP (e.g., public comments, Agency supporting materials

, etc

. ) can be accessed on regulations.gov (Docket: EPA

- HQ

- OPP

- 2013

- 0490).

1) Replacing a nnual sampling with focused sampling : The Panel agreed with EPA that focused population sampling of unexpected Bt damage fields was more likely to detect resistant corn
rootworm than random corn rootworm sampling in the Corn Belt

. 2) Damage thresholds and s ampling methodology in Bt fields with unexpected CRW damage ( UXD ) : The Panel recommended that no n

- random transect sampling through the damaged area should be used to obtain root samples to assess the extent of the damage . The Panel agreed with EPA ’s current practice of using Node Injury Scale (NIS) [14] scores as a threshold for unexpected damage in single trait Bt corn (>1.0 NIS) and pyramided Bt corn (>0.5 NIS). UXD fields that exceed these triggers are investigated for potential resistance. The panel recommended that r oot injury ratings be obtained with a non

- random transect sampling approach

. 3) Replacing diet assay with on

- plant assays : Th ough EPA has proposed switching to on

- plant assays for resistance determinations, th e Panel stated that there were benefits to keeping the diet bioassays to monitor for resistance . However, the panel indicated that these standard assays did not serve as a proactive resistance detection tool. The Panel recommended complement ing the

on

- plant assays with diet bioassays

. 4) Definin g r esistance : The Panel noted that s everal different measurements from on

- plant assays
may be needed to understand when a population is resistant. The Panel recommended the use of a resistant laboratory colony alongside the suspect ed field population as a point of comparison

. The Panel noted that r esistance allele freque ncies (perhaps the most direct way to assess resistance) cannot be used to make resistance conclusion s because the technology has not been developed yet for CRW

. 5) D efining a m itigation a ction a rea in c ase of c onfirmed r esistance : If CRW populations are determined to be resistant, t he Panel cited to the following methods as potential approaches to demarcate a mitigation action area: adapt from corn rootworm population genetic/hybridization research conducted in Italy ; model corn rootworm dispersal based on mark

- recapture study or

c olonization from Europe; use spatial

- temporal trends in bioassay data

, information from the spread of the rotation resistant variant in the US Corn Belt, and shifts in abundance of adults as a measure of the resistance pro blem; or develo p risk maps for fields and areas based on expert advice.

6) M itigation of resistance : The Panel agreed with EPA that the use of theoretical models was a proactive and powerful method to test mitigation approaches and manage resistance. The Panel6 recommended that m itigation tools (e.g. crop rotation, planting of pyramids, non

- Bt corn with SAI) should be used in a mosaic in the landscape and rotated on each field during each successive corn growing season , and noted that the s udden appeara nce of resistance in multiple locations should be an indication that resistance was high in CRW populations.

Other recommendations by the SAP : IPM should be used with Bt deployment and not as a mitigation approach after field failure had occurred; chemical pesticides should not be used in conjunction with planting Bt corn for the purpose of corn rootworm control and is not consistent with IPM; in cases of resistance, a compromised Bt trait should not be used together wit h insecticide applications (this will mask resistance in the population and contribute to spreading resistance) ; the use of chemical insecticides to control adult corn rootworm (adulticides) should be a last resort.

D. EPA’s Proposal for an Improved Corn Ro otworm Resistance Management Program

After having received the expert recommendations from the SAP, EPA developed a propos al [4]

to improve the current CRW resistance management program (proposal dated August 27, 2014) consistent with those recommendations

. Specifically, EPA identified the following elements as part of the proposal:

• Integrated Pest Management stewardship program for Bt corn targeting CRW ;

• A standardized and robust response to unexpected damage in Bt corn;

• A nnual random monitoring requirement to be replaced by focused adult collections in unexpected d amage sites;

• R eplacement of diet bio assay with more sensitive on

- plant assays that are more reflect ive of conditions in the field ; and

• A defined , specific remedial action plan to be implemented in case s where of CRW resistance has been confirmed

.

EPA outlined its proposal to ABSTC in fall 2014. To ensure transparency, o n January 2 8 , 201 5

, EPA open ed a public docket and initiate d a 45 day public comment period on the 2014 proposed framework for CRW and Bt corn. During the initial comment period, several public request s were received by the Agency to extend the comment period. In response, EPA added an additional 30 days to the comment period which close d on April 15, 2015.

Over the course of the public comment period, EPA received several requests from the public to provide additional explanations on the proposed f ramework

. I n the interest of transparency, the
agency held multiple discussions with stakeholders. For example, o n February 25, 2015, EPA provided a webinar overview of the corn rootworm proposal to the Pesticide Program Dialogue Committee ( PPDC ) (accessible at https://www.epa.gov/pesticide

- advisory

- committees

- and

regulatory

- partners/pesticide

- program

- dialogue

- committee

- february ) , a group that provides a forum for a diverse group of stakeholders to provide feedback to EPA on various issues related7 to pesticides

. OPP held a teleconference for EPA ’s Region 8 stakeholders (e.g., growers , crop consultants ) o n March 5, 2015 and met with representatives from the NAICC (National Alliance of Independent Crop Consultants) o n April 22, 2015 to discuss EPA’s proposal in more depth

.
In March 2015, EPA initiated discussions with the Bt corn companies (via the ABSTC consortium group) on the proposed framework

. Additional meetings with ABSTC were held throughout 2015 to further discuss changes to the terms and conditions of the CRW PIP registrations

. Minutes from the meetings are in the public docket. Based on input from stakeholders, EPA modified aspects of the framework to address various stakeholder concerns, including input received during the open comment period. EPA’s discussions with ABSTC ended with an agreement that was announced on February 18 , 2016 [14]

.

The fi nal agreement was incorporated into new t erms and c onditions for each “ single toxin” Bt

corn registration (i.e., those expressing one CRW trait) [ 5 ] , and companies have also committed to implementing the provisions of the terms and conditions for “pyramided” products that express multiple CRW Bt traits

. EPA will formally amend the terms and conditions of the pyramided products when they come up for renewal over the next several years.

Lastly, EPA is working with the companies to transition out of single trait products i nto pyramided products over a several year period, which offer s enhanced protection against resistance development.

E. Response to Public Docket Comments

EPA received a total of 87 c omments relating to the Agency’s August 27

, 2014 draft proposal to improve the resistance management program for corn rootworm and Bt corn. Of these comments, 71 specifically addressed the proposal

, four comments expressed general opposition to EPA ’s regulation of Bt corn, 11 voiced overall opposition to GMOs/agricultural biotechnology, and one was ambiguous. C ommenters represented a variety of groups, including

corn growers , state grower associations and farm bureaus , university extension entomolog ists, independent crop consultants, biotech nology compani es and their industry group ( ABSTC )

, non

governmental organizations (including environmental and advocacy groups)

, state departments of agriculture, and the United States Department of Agriculture ( U SDA )

. Comment ers addressed topics such as IPM s tewardship

, crop rotation, the use of s oil

- a pplied i nsecticide for CRW

, r esistance i nvestigations

, b ioassays to determine resistance , and m itigation strategies for cases of resistance

. In summary, EPA carefully reviewed and considered all public comments received and substantially revised its initial proposal to address those comments.

1) IPM Stewardship

Many of the comments received addressed the IPM stewardship aspect of EPA’s proposal

. C ommenters generally expressed support for IPM approaches for CRW resistance management (21 comments)

, while also expressing a need for grower flexibility within IPM
programs (32 comments). A number of commenters expressed opposition to “mandato ry” crop
rot ation (24 comments) and overly prescriptive IPM adoption targets (7 comments). Others noted that growers/industry were already implementing IPM programs for CRW (10 comments). A few8 commenters (4 comments ) cautioned that crop rotation would complicate IPM stewardship in areas with the rotation resistant corn rootworm variant. Additional comment er s (6 comments ) noted that there was limited or no availability of non

- Bt corn seed varieties available to growers.

Agency Response : EPA addressed some of these co ncerns in its ultimate decision by moving away from the proposed, prescriptive regional IPM adoption targets , which had specified certain levels of crop rotation for areas based on risk of CRW resistance

. The Agency believes that crop rotation with a non CRW host (such as soybean) is the most effective means of reducing the risk of CRW resistance development ; h owever, EPA also recognizes the need for grower flexibility and realizes that not all growers can rotate to soybean. To address these concerns, EPA’s new CRW framework requires ABSTC and its member companies to work with growers to implement best management practices as supported by good IPM with the deployment of Bt corn for the purpose of corn rootworm control

. The framework indicates that soybean rotation is strongly preferred as a BMP , but also provides additional options for other multi

- year management plan s including the use of pyramided Bt corn, rotati on of single Bt modes of action, and non

- Bt corn with conventional CRW control (insecticides)

. It should also be noted that growers are not obliged to adopt measures that are not compatible with their current farming practices. ABSTC is mandated under the new framework to monitor IPM adoption via anonymous th ird party surveys, which will be submitted to the Agency on an annual basis.

2) Use of Soil Applied Insecticides for Control of Corn Rootworm on Bt Corn

Forty

- eight comments addressed the soil

- applied insecticide (SAI) use prohibition language with Bt corn in EPA proposal . Specifically, commenters opposed restrictions on SAI use with Bt corn ( 4 5 comments ), while some were in support of EPA’s proposal (2 comments ). Those opposed to SAI restrictions cited the need to maintain all available CRW controls, additional pests controlled by insecticides, economic considerations, and the benefits of SAIs in buttressing the efficacy of Bt corn and providing higher yields

. The commenters recommend ing against the use of SAIs with Bt corn indicated it would hasten resistance to Bt , specifically if the Bt trait had previously failed in a field. One additional commenter stated that SAI use with single mode of action Bt corn could b e justified but that it should not be needed for pyramided Bt corn.

Agency Response : EPA recognizes the need to maintain available CRW management tools but remains concerned that SAI use with Bt corn can increase the risk of CRW resistance. Therefore, EPA changed the proposed language from a prohibition against the use of SAI in combination with Bt corn to a recommendation that growers not use SAI with Bt corn for CRW control “ except in limited situations and in consultation with extension, crop

consu ltants, and other local experts

. ” This language will be incorporated into the grower educational materials for the single Bt corn products and pyramided Bt corn products.

3) Resistance Investigation

Public commenters who addressed the resistance investigation aspect of EPA’s proposal were generally in agreement that a random resistance monitoring program was not needed and that focusing on unexpected damage sites instead was more effective (3 comments). Several

commen ts were supportive of scouting for unexpected damage in Bt corn using the Agency’s9 threshold criteria and implementing BMPs as a proactive response to unexpected damage to Bt

corn (7 comments ) . However, some commenters cautioned that resources for scouting were limited (3 comments )

, and there were privacy concerns with unexpected damage reporting (3
comments )

. Some commenters expressed the need to standardize BMPs across industry but to keep them as recommendations (5 c omments ). The Agency’s proposed scouting thresholds for single and pyramided Bt corn were thought to be too low ( 1 comment) or too high and not proactive enough (1 comment ).

Agency Response : Random sampling for CRW resistance monitoring purposes has proved ineffective; resistant corn rootworm populations were not detected with this approach but rather with sampling that occurred in UXD sites [1]

. Accordingly , t he Agency replaced the random sampling resistance monitoring program with a resistance monit oring program that focuses on unexpected Bt damage sites instead. EPA understands that cases of unexpected damage could be an indication of deve loping CRW resistance to Bt corn. Therefore, the Agency believes a standardized and proactive response to these cases is essential to early mitigation of potential resistance. Along these lines, EPA has adopted uniform root damage thresholds across industry for single Bt corn (>1.0 NIS , i.e., mo re than 1 node of roots removed) and pyramided Bt corn ( > 0.5 NIS, i.e., more than 1⁄2 node of roots removed ) as triggers for conducting investigations in damaged fields

. EPA has also required that companies recommend that growers implement BMPs the following growing season in response to unexpected damage. These BMPs incl ude tools for management of CRW, including crop rotation to soybean (preferred option) , use of pyramided Bt corn, rotati on of single Bt modes of action, use of non

- Bt corn, and conventional insecticide use

. Biotech companies will provide reports to the Age n cy on unexpected damage cases at the county level for each State

. To address potential privacy concerns, EPA has required that these reports not include any personally identifiable information related to growers. EPA also recognizes that scouting resources may be limited but has required the Bt companies to coordinate responses to unexpected damage cases.

4) Bioassays

Three commenters recommended that EPA continue the use of diet bioassays alongside on

- plant assays (3 co mments). O ne commenter preferred a complete switch to on

- plant assays. Several other commenters noted that bioassays for resistance determinations should meet criteria for successful resistance detection in terms of biological relevance, sensitivity, cons istency, appropriate baselines, and control colonies (2 comments).

Agency Response : As mentioned above, t he Agency replaced the random sampling resistance monitoring program with a resistance monitoring program that focuses on unexpected Bt damage sites instead

. Population collections will be obtained from the site of damage during the year of UXD or the field and surrounding fields (if unable to collect that year), and root node injury will be assessed with a transect

- sampling approach through the damag ed location in the field of concern. On

- plant assays are the Agency’s preferred approach for testing field collected populations for resistance to Bt because they can function as diagnostic tools (i.e., capable of clearly distinguishing resistant CRW popul ations from susceptible ones). EPA is concerned that current diet bioassay approaches lack the sensitivity to reliably detect resistance populations. Nonetheless, EPA is open to an10 improved diet bioassay that addresses the Agency’s goals of having a reliab le diagnostic test to determine resistance. As part of the final CRW framework, EPA established criteria for resistance detection assays and required companies to consult with EPA on their assay approach prior to its use . Industry may continue to pursue a diet

- based approach provided that improvements are made to the methodology and a resistant lab colony is used as a control to validate resistance conclusions

. 5) Remedial Action

Several commenters noted that mitigation of resistance was a more realistic goal then remediation (4 comments). One commenter proposed to make crop rotation the primary tool to mitigate a resistant population because other approaches would be less effective , while other commenters recommended that mitigation plans should be flexible and not overly prescriptive (3 comments)

. Six commenters noted that “ b eetle bombing ” (i.e., use of conventional insecticides to kill adult corn rootworm and prevent egg laying) is not a preferred IPM method

- especially not in resp onse to unexpected damage; overuse could lead to pyrethroid resistance (the insecticide of choice against CRW) . One commenter indicated that it was crucial for growers to obtain information regarding corn rootworm resistance developments. Additional commen ter s noted that there were uncertainties with defining remedial action areas based on corn rootworm dispersal (2 comments), while others cited concerns about the feasibility of including multiple farms in a defined remediation area (3 comments)

. Agency Res ponse : The Agency agree s that mitigation is a more appropriate description of the response strategy for resistant populations than remediation and has included the term in the revised framework . The Agency recognizes that crop (soybean) rotation is the most effective tool to mitigate a resistant corn rootworm population and has indicated that it is the preferred mitigation action tool in the final framework. Furthermore, the Agency has incentivized industry to work with growers to use cro p rotation in cases of unexpected damage to Bt corn so that the best mitigation action can occur before resistance is confirmed. EPA agrees with the comments about beetle bombing. In the finalized framework, beetle bombing is listed as the least preferred option to mitigate resistance because it can create resistance risks for conventional pesticides as well as environmental and human health effects.

Regarding the mitigation action area, EPA defined the scope of this area as the “grower’s farming operation up to a 1⁄2 mile radius from the damaged site that produced the resistant population.” This distance was based on the typical life

- time dispersal potential for CRW beetles. EPA recognizes the challenges of including multiple farming operations within this area. To address this concern, the agreed

- upon framework requires the company with the resistance issue to inform its customers within the mitigation action area, as well as

e xtension entomologists, crop consultants and other companies selling the same trait. In addition, EPA is looking to develop its own n otification system to report incidents of resistance as well as unexpected damage in Bt corn. EPA believes the timely disse mination of information to affected stakeholders will allow growers to make informed decisions regarding CRW management.11 6) Other Comments and Recommendations

A number of commenters recommended that EPA consider raising the refuge requirements for Bt corn to 50% for single traits (from the currently required 20%) and 20% for pyramided varieties (from the current 5%) (6 comments). Additional commenters urged EPA to increase grower education/training for growers (7 comments). Several commenters suggested that it may be too late to address IRM in the Corn Belt and that the Agency should instead focus on “fringe” areas of the Corn Belt where the Bt traits are still effective (2 comments). Others comments

r ecommended EPA incentiviz e crop rotation and IPM activities (2 comments), offer expanded crop rotation options (e.g., longer rotations with pyramids) (2 comments), and restrict the use of single trait Bt corn products (in favor of pyramids) (2 comments).

Agency Response : EPA believes that the finalized framework will greatly enhance the durability of Bt corn at the current refuge levels

. Nevertheless, EPA recognized the concern raised about the current refuge requirements and, in cases of confirmed resistance

, the framework requires that companies increase the refuge for any pyramids with the affected trait to 20% in the resistance mitigation action area.

EPA agrees that that grower education is an essential aspect of IRM. The registrant

implemented grower edu cation outreach will be a major component of the IPM stewardship program that is a required part of the finalized framework to improve CRW IRM. As part of the stewardship program, companies must encourage growers to engage in multi

- year crop rotation stra tegies designed to reduce sele ction pressure for resistance. These rotational strategies can include planting a non

- CRW host (e.g., soybean), pyramided Bt corn products, other Bt corn products with different modes of action, and/or

non

- Bt corn. EPA believ es the new framework establishes incentives for industry to promote crop rotation to a non

- host crop such as soybean in cases of u nexpected damage or resistance. If growers rotate to a non

- host crop in such cases, the affected area is considered “mitigated” and no further action will be required of the companies

.

F. Summary of Final Agreement between EPA and ABSTC

In response to evidence that corn rootworm has evolved resistan ce to some single trait Bt products, EPA announced the adoption of n ew, more protective requirements designed to delay corn rootworm resistance to g enetically engineered Bt corn on February 18, 2016 [ 5 ] [14]

. The final framework consists of several improvements to th e previous corn rootworm resistance management paradigm that were in part based on an independent science peer review, a letter to EPA from corn rootworm experts, as well as public comments to EPA’s docket. The se measures will be included as registration terms for Bt corn products and include the following :

1. IPM Stewardship Program
Companies supplying Bt corn are required to implement a stewardship program designed to reduce selection pressure by encouraging growers to implement a multi

- year crop rotation strategy with the use of corn rootworm protected Bt corn

. Implementation of the IPM strategy can include g rower education initiatives or incentives ; and o utreach to extension and consultant
groups

.12 To address c oncerns about the potential for SAI use with Bt corn to exacerbate resistance development, EPA is requiring that g rower educational materials provided as part of the stewardship program include language stating that SAIs with single Bt corn control is not recommended for the control of corn rootworm except under limited circumstances and in consultation with extension, crop consultants or other local experts” and , for pyramided products, SAI use should not be necessary for CRW control with pyramided CRW trait Bt corn products

. Each Company must submit a report to EPA annually documenting activities under the IPM stewardship program including an anonymous survey of grower practices, and adoption of various IPM tools such as crop rotation.

2. Investigation of Reports of Unexpected Damage (UXD) by Corn Rootworm: Performance Inquiries
When companies become aware of field failures, it is important to EPA that those fields and populations of rootworm are investigated to determine what caused the damage. EPA is requiring that c ompanies inves tigate “performance inquiries” from corn growers and determine if the damage is attributed to corn rootworm feeding and exceeds a root damage threshold based on Node Injury Score ( >1.0 for single Bt corn; >0.5 for pyramided Bt corn )

. If the NIS trigger is exceeded in a UXD field, companies must collect insect from the damaged site and test those insects for resistance using a bioassay approach described in detail in the terms and conditions

, and summarized in section 3 below

. For fiel ds meeting the criteria above, c ompanies must review the CRW management history with growers and provide corn rootworm management recommendations , including an assessment of corn fields with similar trait(s) adjacent to the affected corn field that are man aged by the same
grower . In those fields, companies should also discourage the use of single

- trait products containing the affected CRW trait and encourage the following recommended management options:

• P rimary option : R otation to a non

- host crop ( e.g., soybean);

• S econdary option s: Use of pyramided Bt corn with multiple CRW traits , use of a different single corn rootworm Bt trait, use of non

- Bt corn or non

- CRW protected Bt corn ( with conventional insecticides) ;

• T ertiary option : I f additional pest manag ement need is determined beyond the secondary option s, additional CRW control tools including soil insecticides, seed applied insecticides, and chemigation can be used

.
• If a UXD field is rotated to a non

- CRW host crop (e.g., soybean) , the area will be considered mitigated and no further actions will be required by the companies for the UXD case.
Each Company must submit an annual report detailing activities related to investigations of UXD fields from the most recent (previous) corn growing season

, fina l disposition of UXD fields from previous seasons , and bioassays results if crop rotation was not implemented. UXD reports must be submitted by county and state , but must exclude sensitive business and customer information.13 3. Investigation of Populations of Concerns: Resistance Detection Assays

In order to definitively determine whether populations of rootworm causing unexpected damage

are resistant

, EPA is requiring that these populations be collected, and also tested. EPA is requiring that c ompanies cond uct investigation of all CRW populations collected as part of the performance i nquiry process described above. These investigations must include the use of an EPA

- approved bioassay to determine if the sampled populations are resis tant. The employed assay must be able to function as a diagnostic tool capable of distinguish ing resistant populations from susceptible ones

. See the Terms and Conditions for additional details on the criteria for a population to be considered resistant.

EPA is requiring m itigation , as described in the next section below, for any corn rootworm population that meets the resistance criteria. If the results of the bioassays are inconclusive, companies must collect and assay populations from the UXD field/area for another year

.

4. Mitigation of CRW Populations Meeting EPA ’s Resistance Criteria

It is important to EPA that affected stakeholders be made aware of the detection of resistance and that measures are put in place to prevent documented resistance from spreading. Therefore, f or any resistant population, EPA is requiring that companies take the following steps ;

a) Inform EPA of the bioassay results; b) N otify state extension agents and crop consultants within the county where resistance was identified of resistance detection in their county and the trait(s) affected ; c) Within a 1⁄2 mile radius around the resistant site

, EPA is requiring that companies i. I nform affected growers and other registrants holding registrations for the affected trait prior to finalizing growers’ seed orders the following
year . The company must also inform neighboring growers if those
growers are also customers of the company. Information shar e d must include identification of the county in which resistance was detected and the trait(s) affected ; ii. D iscontinue sales and planting of single trait product containing the compromised trait until resista nce has been mitigated; iii. M onitor the resistant population until resistance is mitigated (as long as the grower remains a customer of the company) ; iv. R equire that pyramids containing the resistant trait and sold and planted in the area receive a 20% refuge until resistance is mitigated;

v. Encourage the use of “Mitigation Practices” including crop rotation, use pyramids, and other best management practices

.14 5. Annual Reporting

Each company must submit the following annual reports to allow EPA to review the status of this new CRW mitigation program :

a) IPM Stewardship Program: Activities conducted under the IPM stewardship program, including an anonymous survey of grower practices, adoption levels of the various crop rotation options (if employed) and other elements of the stewardship program, on or before January 31 st of each year.

Unexpected Damage Investigations: Activities related to investigations of unexpected damage (UXD), including number and location of UXD cases, insect sampling, bioassays, and final disposition of UXD fields from the most recent and previous corn growing seasons, on or before November 30 th of each year.

G. Transition Plan from Single

- Trait ed Bt Corn to Pyramided Bt Corn

The first s ingle trait Bt corn for the control of corn rootworm was registered in 2003, while the first pyramided Bt corn (expressing two or more traits to a pest) was approved by EPA in 2009. Research indicates that single Bt traits deployed concurrently with pyramided Bt products will hasten resistance development to pyramids [ 1 6 ]

. This is of concern to the Agency , especially in the context of present corn rootworm resistance to Cry3Bb1 and cross

- resistance between Cry3Bb1 and mCry3A expressing corn [12]

. EPA is further concerned because there are only a limited number of Bt traits available to growers to manage corn rootworm. The Agency views the st ewardship for pyramided PIP corn as a high priority to maintain the usefulness of these products for growers for as long as possible.

Although EPA and the biotech companies have reached an agreement on the i mproved framework for Bt corn targeting corn rootworm

, the improved stewardship program will be strengthened by limiting the planting of single Bt corn rootworm protected corn over time

. However, EPA also recognizes the needs of farmers and understands tha t growers rely on specific corn hybrids for which pyramided varieties may not be immediately available

. Therefore, EPA is working with the companies to transition out of single trait products over time into the pyramided products while taking into consider ation the needs of the farmers

. EPA has extended the registrations of the single trait products through 2019 with yearly reductions in acreage planted to allow time for the transition to occur and will consider f urther extensions of the single trait products on a case

- by case basis by imposing, for example, acreage caps

, geographic restrictions , and/or other IRM

- related mitig ation

. By 2020, almost all Bt corn targeting corn rootworm and planted in the US will be of the pyramided variety

.

H

. Con clusion

EPA firmly believes that t he new CRW resistance management framework will result in an improved stewardship and resistance monitoring program for Bt corn. The new framework is the result of a public and transparent process involving a wide range of stakeholders including15 academic researchers [ 8 ] [ 14 ] , a Scientific Advisory Panel [ 3 ] , public interest groups and the public [ 4 ]

. Its aim is to delay resistance in corn rootworm to Bt biotech traits for as long as possible, particularly for the pyramided products, allowing growers to effectively and safely manage corn rootworm with the help of these tools. The framework, therefore, provides benefits to agriculture and growers (reduced use of conventional pesticides and exposure to humans, en vironment, and

non

- target species) , biotech companies, and the public as well as the environment by extending the effectiveness of these beneficial products.

I. References

1. Gassmann, A. J., J. L. Petzold

- Maxwell, R. S. Keweshan, and M. W. Dunbar. 2011. Field

- evolved resistance to Bt maize by western corn rootworm. PLoS ONE e22629.

2. US EPA [United States Environmental Protection Agency] . 2013. White paper on corn rootworm resistance monitoring for Bt Plant

- Incorporated Protectants. Report from OPP’s IRM team to the 2013 Scientific Advisory Panel in the Biopesticide and Pollution Prevention Division. Docket number: EPA

- HQ

- OPP

- 2013

- 040; http://www.regulations.gov/#!documentDetail;D=EPA

- HQ

- OPP

- 2013

- 0490

- 0031

3. US EPA FIFRA [United States Environmental Protection Agency Federal Insecticide, Fungicide and Rode nticide Act] Scientific Advisory Panel. 2014. Transmittal of Meeting Minutes of the FIFRA Scientific Advisory Panel Meeting Held on December 4

- 6, 2013 on scientific uncertainties associated with corn rootworm resistance monitoring for Bt corn. Docket numbe r: EPA

- HQ

- OPP

- 2013

- 0490; http://www.regulations.gov/#!documentDetail;D=EPA

- HQ

- OPP

- 2013

- 0490

- 0044

4. Draft Proposal to ABSTC to Improve Insect Resistance Management for Bt Corn

. Docket number: EPA

- HQ

- OPP

- 2014

- 0805; http://www.regulations.gov/#!documentDetail;D=EPA

- HQ

- OPP

- 2014

- 0805

- 0002

5. Terms and Conditions of Bt Corn Registr ations. 2016. Docket number: EPA

- HQ

- OPP

2014

- 0805; http://www.regulations.gov/#!searchResults;rpp=25;po=0;s=EPA

- HQ

- OPP

2014

- 0805;fp=true;ns=true

6. Andow, D. A., S. G. Pueppke, A. W. Schaafsma, A. J. Gassmann, T. W. Sappington, L. J. Meinke, P. D. Mitchell, T. M. Hurley, R. L. Hellmich and R. P. Porter. 2015. Early detection a nd mitigation of resistance to Bt maize by western corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol ., Vol. 109(1): 1

- 12.

7. Martinez, J. C. and M. A. Caprio. 2016. IPM use with the deployment of a non

- high dose Bt pyramid and mitigation of resistance for western corn rootworm ( Diabrotica virgifera virgifera ). Env. Entomol., http://ee.oxfordjournals.org/ cgi/reprint/nvw015?16 ijkey=RSoVuMMLBzsAjrX&keytype=ref

8. Gassmann, A. J. 2012. Field

- evolved resistance to Bt maize by western corn rootworm: predictions from the laboratory and effects in the field. J. In v ertebr. Pathol ., Vol. 110: 287

- 293.

9. Gassmann, A. J., J. L. Petzold

- Maxwell, R. S. Keweshan, and M. W. Dunbar. 2012. Western corn rootworm and Bt maize: challenges of pest resistance in the field. GM Crops Food : 3: 235

- 244.

10. Gray, M. E. 2012. Continuing Evolution Confirmed of Field Resistance to Cry3Bb1 in Some Illinois Fields by Western Corn Rootworm. The Bulletin , No. 20(2).

11. Wangila, D. S., A. J. Gassmann, J. L. Petzold

- Maxwell, B. Wade French, and L. J. Meinke. 2015 . Susceptibility of Nebraska Western corn rootworm (Coleoptera: Chrysomeli dae) Populations to Bt corn events. J. Econ. Entomol ., Vol. 108(2): 742

- 751.

12. Gassmann, A. J., J. L. Petzold

- Maxwell, E. H. Cliffton, M. W. Dunbar, A. M. Hoffmann, D. A. Ingber, and R. S. Keweshan. 2014. Field

- evolved resistance by western
corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize. PNAS, Vol. 111(14): 5141

- 5146.

13. Porter P., E. Cullen, T. Sappington, A. Schaafsma, S. Pueppke, D. Andow, J. Bradshaw, L. Buschman, Y. J. Cardoza, and C. DiFonzo. 2012 . Comment submitted by Pat Port er North Central Coordinating Committee NCCC46 and other corn entomologists. https://www.regulations.gov/#!documentDetail;D=EPA

- HQ

- OPP

- 2011

- 0922

- 0013

14. US EPA [United States Environmental Protection Agency] . 2016. OPP Update: New requirements to address corn rootworm resistance. Released on February 18, 201 6

. https://www.epa.gov/pesticides/new

- requi rements

- address

- corn

- rootworm

- resistance

- bt

- corn

15. Oleson, J D, YL Park, T M Nowatzki, and J Tollefson. 2005. Node

- injury scale to evaluate root injury by corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol. , Vol. 98(1): 1

- 8.

16. Zhao, J. Z., J. Cao, H. L. Collins, S. L. Bates, R. T. Roush, E. D. Earle, and A. M. Shelton. 2005. Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc. Natl. Acad. Sci. ; Vol. 102(24): 8426

- 8430.