April	3,	2013

Comments	for

FIFRA	Scientific	Advisory	Panel

Scientific	Uncertainties	Associated	with	Corn	Rootworm	Resistance	Monitoring	for	Bt	Corn	

Plant	Incorporated	Protectants	(PIPs)

Docket:	EPA-HQ-OPP-2013-0490

by	Center	for	Food	Safety

Emailed to:

Fred	Jenkins,	DFO,	Office	of	Science	Coordination	and	Policy	(7201M)

Environmental	Protection	Agency

1200	Pennsylvania	Ave.,	NW

Washington,	DC	20460-0001

Jenkins.fred@epa.gov

Summary of	Comments

CFS	generally	agrees	with	EPA’s	proposed	changes	to	corn	rootworm	(CRW)	resistance	

monitoring.		However,	such	changes	will	not	significantly	deter	further	emergence	of	Btresistant	CRW	unless	they	are	accompanied	by	a	substantial	strengthening	of	the	resistance	

prevention components	of	insect resistance	management	(IRM).

Monitoring	has	revealed	declines	in	susceptibility	to	all	of	the	commercial	rootworm	toxins	

since	2005;	and	escalating	emergence	of	Cry3Bb1-resistant	CRW	since	no	later	than	2009.		

First	identified by	independent	scientists	in	Iowa	and	Illinois,	resistant	CRW	are	likely

present	in	multiple	regions	of 11	states	based	on	reports	of	unexpected	damage	to	Bt	corn	

reviewed	by	EPA	(see	section	II.A).		This	rapid	emergence	of	resistance	is	attributable	to	

several	factors:	

1) Increased	continuous	corn	cultivation	that	has	been	facilitated	by	Bt	corn	and	

encouraged	by	its	developers	(see	II.D);

NATIONAL	OFFICE : 660	Pennsylvania	Ave.,	S.E.,	Suite	302,	Washington,	D.C.	20003 phone: 202-547-9359 fax: 202-547-9429

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2) Sharply	reduced	availability	and	planting	of	conventional	(or	non-Bt)	corn	seed,	a	

key	IRM	measure	(see	II.C);

3) The	rise	of	resistance-promoting,	volunteer	Bt	corn	as	a	weed,	made	more	difficult	

to	control	when	stacked	with	herbicide-resistance	traits	(see	II.E);	and

4) Most	importantly,	EPA’s	irresponsible	reductions	in	refuge	size	requirements	to	

levels	much	lower	than	are	needed	to	dilute	resistance	genes	and	deter	resistance	

(see	II.B).

EPA’s	failure	to	stem	resistance	in	CRW	can	be	explained	in	several	ways (see	generally	IV).		

First,	there	has	been	misplaced	application	of	IRM	for	lepidopteran	Bt	corn	to	the	very	

different	resistance	challenges	presented	by	rootworm-active	Bt	corn.		Second,	an	overly	

stringent	definition	of	resistance	has	resulted	in	numerous	false	negative	findings	and	thus	

delayed	effective	remedial	action	for	years (I:	Questions	4	and	6).		Finally,	EPA	has	relied	

excessively	on	industry	views	and	assessments	that	are	skewed	by	financial	self-interest;	

and	rejected	the	unbiased	analysis	and	recommendations	of	independent	experts,	as	seen	

most	clearly	in	refugia	requirements	that	are	much	too	low	to	dilute	resistance	genes	and	

forestall	resistance (II.B).

CFS	recommends	that	EPA:

1) Make	publically	available	the	monitoring	data	reported	to	EPA	re:	unexpected	

damage	to	Bt	corn,	and/or	provide	complete	descriptions	of	it	in	relevant	

documents	released	to	the	public	(II.A)

2) Establish	a	simple,	single-criterion	definition	of	resistance	along	the	lines	discussed	

in	section	I,	Question	4

3) Increase	refuge	requirements	for	all	rootworm-active	Bt	corn	events	to	50%	for	

single-toxin	Bt	corn	and	20%	for	pyramids	(II.B)

4) Establish	mandatory	IRM	involving rotation	away from	rootworm	Bt	corn	(IV)

5) Increase	the	role	of	independent	scientists	and	reduce	that	of	seed	firms	in	every	

aspect	of	IRM	in	light	of industry’s	failure	to	successfully	detect	and	notify	EPA	of

the	emergence	of	resistant	CRW	(IV)
Comments

Center	for	Food	Safety	(CFS)	appreciates	the	opportunity	to	comment	on	the	growing	

resistance	of	corn	rootworm	to	Bt	toxins	and	EPA’s	proposals	to	improve	monitoring	for	

resistance	and	remedial	action.

CFS	generally	agrees	with	EPA’s	proposed	changes	to	corn	rootworm	(CRW) resistance	

monitoring.		However,	while	these changes would	perhaps	deliver marginal	improvements,	

they	would	not	significantly	deter	further	rapid	emergence	of	Bt	toxin-resistant	CRW.		To	

achieve	this	would	require	more	thoroughgoing	reform	of	the	insect	resistance	

management	plans.		In	these	comments,	we	first	address	the	specific	charge	questions,	

followed	by a	discussion	of	issues not	addressed	by	EPA	and	of	measures	that	do	have	the	

potential	to	significantly	deter	further	emergence	of	CRW	resistance.

I. Comments	on	Charge	Questions

Question	1:	Annual	Corn	Rootworm	Sampling	to	Assess	Bt	Susceptibility

CFS	agrees	with	EPA that	IRM	monitoring	should	involve	more	intensive	and	focused

sampling.		This	approach	would	seem	to	be	more	consistent	with	the	primarily	shortdistance	dispersal	patterns	of	CRW	adults,	as	well	as	the	observed	emergence	of	resistant	

CRW	populations	primarily	in	localized	hot	spots.		However,	corn	rootworm	has	shown	the	

capacity	for	fairly	rapid	dispersal	over	long	distances.		First,	CRW expanded	eastward	

across	the	Corn	Belt	in	the	1960s	and	1970s at	rates	ranging	from	20	to	200	km/year,	

depending	in	part	on	the	direction	of	prevailing	winds	and	storm	fronts.		Second,	rotationresistant	CRW	has	expanded	its	range	from	its	origins	in	eastern	Illinois	in	1987	to	infest	

parts	of	seven	states	in	2007,	just	20	years	later.		Finally,	CRW	first	discovered	in	Europe	

near	Belgrade	in	1992	was	found	in	20	European	countries	just	15	years	later	in	20071

(Gray	et	al	2009,	see	maps below).		Thus,	EPA	must	not	neglect	the	potential	for	longerdistance	dispersal	of	resistant	CRW	from	numerous	hot	spots,	which	is	likely	already

leading	to	rapid	emergence	of	area-wide	resistance.		Random	sampling	is	better	suited	to	

detect emergence	of	area-wide	resistance,	and	should	remain	part	of	annual	monitoring	

together	with	more	intensive	and	focused	sampling.

Current	monitoring	involves	random	sampling	of	just	12-15	populations	each	year	in	three	

states.		Clearly,	many	more	populations	will	have	to	be	sampled	with	incorporation	of	the	

intensive,	focused	sampling	approach.		The	number	of	CRW	populations	that	are	sampled	

should	increase	in	proportion	to	the	number	of	unexpected	Bt	damage	reports,	and	

intensive	sampling	should	be	focused	in	those	areas.

																																																							 1 CRW’s	expansion	in	Europe	is	due	to	some	combination	of	multiple	introductions	from	the	U.S.	(at	least	3)	

and	subsequent	range	expansion	from	these	foci.	
4

Source:	Gray	et	al	(2009)

Source: Gray	et	al	(2009)
5

Source: Gray	et	al	(2009).

Question	2:	Corn	Rootworm	Sampling	in	Response	to	Damaged	Bt	Fields

EPA	recommends	use	of	field	damage	ratings	based	on	root	node	injury	for	investigations	

of	CRW	populations	causing	damage	to	Bt	corn.		The	triggers	suggested by	EPA	are:	1.0	for	

single-toxin	Bt	products	and	0.5	for	pyramided	Bt	products.		CFS	recommends	that	EPA	

utilize	the	0.5	rating	for	both	categories.		This	would	be	consistent	with	the	expert	

recommendation	of	the	2002	Scientific	Advisory	Panel	(SAP)	that	advised	EPA	on	insect	

resistance	management	for	Cry3Bb1-expressing	MON863 corn.		This	SAP	advised	that	CRW	

root	damage	“approaching	a	0.5	(node-injury	scale)”	on	MON863	roots,	coupled	with	a	

history	of	MON863	cultivation,	was	sufficient	to	regard	a	CRW	population	as	“suspected	

resistant”	(SAP	2002,	pdf	p.	652).

It	is	unclear	why	greater	damage	should	be	needed	to	deem	a	CRW	population	resistant	or	

suspected	resistant	in	the	case	of	single-toxin	plants.		For	example,	at	present	Cry34/35Ab1	

																																																							 2 Pdf	page	numbers (e.g.	page	65	of	71)	are	cited	for	this	SAP	report	because	it	does	not	have	printed	page

numbers.
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appears	to	be	the	only	commercial	rootworm	PIP	that	remains	largely	uncompromised	by	

resistant	CRW,	in	light	of	the	strong	evidence	for	cross-resistance	between	Cry3Bb1	and	

mCry3A (BPPD	2013c,	p	24).		It is	thus	extremely	important	that	its	efficacy	be	preserved;	

and	its	effectiveness	must	be	safeguarded	as	fully	when	deployed	in	a	single-toxin	plant as	

when	deployed	in	a	pyramid	(e.g. SmartStax	corn).	 This	is	true	not	only	for	Cry34/35Ab1;

it	applies	more	generally.		EPA	should	establish the	same	damage	trigger	– 0.5	node	injury	

– for	single-toxin	and	pyramided	seeds	in	resistance	assessments.

In	the	charge	question,	EPA	notes	that	some	unidentified	party	or	parties	has	raised	a	

concern	that	sampling	for	adult	CRW	directly	in	damaged	Bt	fields,	specifically	in	the	

vicinity	of	the	damage,	“may	be	biased	relative	to	surrounding	areas and	not	representative	

of	the	overall	CRW	population.”		Some	such	concern	may	well	have	been	well	have	been	

what	motivated	Monsanto	to	propose	a	sampling	plan	in	response	to	damage	reports	in	

which	CRW	were	collected	as	far	as	one	to	two	miles	from	failed fields (BPPD	2011,	p.	2).

This	concern,	however,	is	entirely	misplaced,	based	on	a	misunderstanding	of	the	nature	of	

CRW	resistance	and	the	purpose	of	this	part	of	the	monitoring	program.

First,	because	CRW	resistance	to	Bt	toxins	is	likely	to	arise	(at	least	initially)	in	numerous	

confined	areas,	collecting	CRW	samples	far	away	from	damaged	Bt	corn	would	introduce	a	

clear	bias	tending	towards	false	negative	results.		As	EPA	noted	with	respect	to	the	

Monsanto	plan	mentioned	above:	“this	proposal	is	insufficient	if	the	goal	is	to	determine	

whether	Bt	failure	is	due	to	resistance	of	the	CRW	population”	(BPPD	2011,	p.	2).		CFS	

agrees.

Second,	the	primary	purpose	of	sampling in	response	to	damage	reports	is	damage	control	

– rapid	assessment	of	probable	resistance,	followed	by	strong	and	effective	remedial	action	

to	contain	and	extirpate	it,	as	needed.		The	purpose	is	not	– as	it	has	been	with	annual	

sampling – to	provide	early	indications	of	evolving	resistance	on	an	area-wide	basis,	in	

which	case	broader	sampling	would	make	more	sense.		However,	as	discussed	above,	CFS	

agrees	with	EPA	that	annual	monitoring	should	incorporate	more	intensive	and	focused	

sampling.

For	both	of	these	reasons,	sampling	of	CRW	adults	in	response	to	unexpected	damage	

should	be	focused	directly	in	the	damaged	area	of	Bt	fields	and	the	immediate	vicinity	as	

much	as	possible.		

Question	3:	Diagnostic	Assays

CFS	supports	EPA’s	recommendation	that	diagnostic	on-plant	assays	be	the	primary	

resistance	detection	tool	for	corn	rootworm.		CFS recommends	use	of	the	Gassmann	assay,	

which	has	proven	itself	capable	of	detecting	resistance	where	diet	bioassays	have	

(perhaps)	failed.3 As	EPA	notes	in	its	white	paper,	neither	the	instar	development	nor	body	

																																																							 3 We	say	“perhaps	failed”	because	in	EPA’s	white	paper (page	16), it	is	stated	that	field	populations of	CRW

that	meet	a	key	resistance	criterion	(LC50s	exceeding	the	upper	limit	of	the	95%	confidence	interval	of	the	

control	population)	have	been	identified	with	use	of	diet	bioassays,	apparently	for	all	three	CRW	Bt	toxins,
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size	criteria employed	in	the	sublethal seedling	assays	(e.g.	Nowatzki	et	al	2008) has	been	

validated	as	a	reliable	marker	of	resistance.		

“BPPD	notes	there	is	no	evidence	demonstrating	that	resistant	corn	

rootworm	need	to	have	greater	body	mass	or	head	capsule	widths	for	

development	than	their	susceptible	counterparts.	 Hence,	this	significance	

criterion	is	likely	too	stringent	and	would	potentially	result	in	false	

negatives.”	(White	paper,	p.	17)

Whenever	diagnostic	assays	involve	comparisons	to	susceptible	CRW	populations	

(whether	contemporary	or	historical	data),	care	should	be	taken to	ensure	that	the	

susceptible	standard	of	comparison	represents	truly	susceptible	CRW	prior	to	any	selection	

pressure from	exposure	to	Bt	rootworm	toxins.		EPA	notes	that	“[i]n	some	cases,	lower	

susceptibility	has	been	observed	in	field	populations	relative	to	the	laboratory	colonies”	

(White	Paper,	p.	15);	and	similarly:	“CRW	populations	in	the	field	have	experienced	

selection	to	Bt	corn	over	the	past	decade	and	likely	have	obtained	some	degree	of	tolerance	

to the	toxins	(Cry3Bb1,	mCry3A,	and	Cry34/35)”	(White	paper,	29).		Use	of	“less	

susceptible”	or	partially	tolerant	CRW	for	control	purposes	in	resistance	assessments	is	to	

be	avoided	whenever	possible;	or	if	not	avoidable,	accounted	for in	resistance	assessments	

by,	for	example, reducing	the	resistance	ratio	or	other	comparative	metric	required	for	

diagnosis	of	resistance.

Question	4:	Defining	Resistance

EPA’s	ostensible	goal	is	to	make	resistance	monitoring	proactive	rather	than	reactive.		To	

that	end,	the	Agency recognizes	that	resistance	must	be	defined	such	that	an	“actionable	

threshold”	is	met	before	resistance	is	widespread (White	paper,	p.	22). If	resistance	is	not	

defined	in	this	way;	if	timely	regulatory	action	is	not	possible	due	to	an	excessively	

stringent	definition	of	resistance;	then	IRM	completely	fails to	serve	its	intended	purpose;	

the	Bt	toxin’s	value	is	lost	or	eroded;	and	chemical	insecticide	use	rises,	with	associated	

toxicity	to	human	health	and	the	environment. In	EPA’s	terms,	“population	suppression	

(e.g.	chemical	insecticide	use)	may	be	the	only	alternative	for	managing	resistance”	(White	

paper,	p.	22).		

Results	of	a	prospective	survey	conducted	by	University	of	Illinois	entomologist	Michael	

Gray	show	that	in	2013,	nearly 50%	of	Illinois	corn	growers	expected	to	use	both	Bt	corn	

with	rootworm-active	toxin(s) AND	chemical	insecticides (Jongeneel	2013).		University	of	

Minnesota	entomologist	Ken	Ostlie	expected	similarly	high	use	of	insecticides,	both	on	

continuous	corn	and	rotated	corn:

"At	winter	meetings	with	ag	professionals,	they	indicated	more	than	50	

percent	of	corn-on-corn	would	end	up	with	an	insecticide	overlay	of	traits,"	

																																																																																																																																																																																		

“although	none	of	the	populations	have	been	deemed	resistant	by	registrants...		[p]resumably	...	due	to	the	

difficulty	of	interpreting	and obtaining	accurate	LC50	values.”	 Thus,	the	problem	may	lie	less	with	the	type	of	

assay	than	with how	it	is	interpreted,	and	who	is	doing	the	interpreting.		Below,	we	discuss	how	corporate	

financial	interests	may	be	skewing	the	science	and	regulation	of	IRM.	
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says	Ostlie.	"About	25	to	30	percent	of	rotated	corn	with	no	threat	of	

resistance	was	expected	to	receive an	overlay.	 I	suspect	final	percentages	of	

both	were	higher." (Ruen	2013)

This	evidence	shows	that	resistance4 is	already	prevalent	enough	to	be	driving	up	the	use	

of	insecticides	substantially.

Despite	EPA’s	goal to	make	IRM	proactive,	however,	its	current	and	proposed	definitions	of	

resistance	ensure	its continuing	failure	for	corn	rootworm.		As	EPA	itself	concedes:

“All	of	the	proposed	procedures	are	likely	to	detect	resistance	only	if	it	is	

complete	(i.e.,	CRW	develop	and	survive	on	Bt corn	at	the	same	levels	as	

isoline	corn).	 Comparisons	of	field	populations	on	Bt	and	non-Bt	corn	

require	statistical	equivalence	to	make	a	positive	resistance	determination.	

This	statistical	approach	would	exclude	cases	of	incomplete	resistance,	in	

which	a	field	population	is	more	fit	than	a	control	colony	on	Bt	plants	but	not	

as	fit	as	a	population	with	complete	resistance.”	(White	Paper,	p.	29)

The	definition	of	resistance	must	be	revised	to	encompass partial	resistance.		This	is	

particularly	important	given	the	ongoing	emergence	of	resistant	CRW	populations	under	

the	more	stringent	definitions	used	hitherto.		Because	more	stringent	definitions	of	

resistance	have	demonstrably	enabled	resistant	CRW	to	emerge	without	triggering	

remedial	action	plans,	these	definitions must	be	loosened	to	enable	more	timely	response	

at	earlier	stages	of	resistance.		Otherwise,	IRM	has	little	chance	of	stemming	the	tide	of	

resistant	CRW.

To	this	end,	criteria	that	require	demonstration	of	complete	resistance	should	be	

eliminated.		CFS	supports	the	first	criterion	of	the	Single	On-Plant	Assay	Option	2	(White	

paper,	p.	28)	as	a	fully	sufficient	definition	of	confirmed	resistance.		

“Using	a	single	on-plant	assay	(e.g.,	Gassmann	et	al.	2011	or	similar	

methods),	a	corn	rootworm	population	is	said	to	be	resistant	when:	The	

percent	survival	observed	of	the	field	population	on	Bt	corn	exceeds	the	

percent		survival	of	the	susceptible	population	on	Bt	corn	(statistically	

significant;	P-value	<0.05).”

The	second	criterion	relates	to average	weight: “The	average	weight	of	the	survivors	from	

the	field	population	on	Bt	corn	is	equal	to	(no	statistically	significant	difference)	or	greater	

than	the	average	weight	of	the	susceptible	colony	on	isoline	corn.“

This	second	criterion	should	be eliminated	for	several	reasons.		First,	as	noted	by	EPA,	it is	

not	independent	from	the	first (White	paper,	28-29).		Second,	average	larval	weight	has	not	

																																																							 4 More	accurately,	one	should	say	some	unknown	mix	of	actual	resistance	and	fear	of	resistance,	with	use	of	

chemical	insecticides	to	either	control	resistant	CRW	or	as	a	prophylactic	measure	to	forestall	or	prevent	the	

spread	of	resistance.
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been	validated	as	a	measure	of	resistance	(Ibid,	p.	17).		Finally,	to	the	extent	that	weight	

does	prove	to	correlate	with	percent	survival,	the	criterion	demands	a	showing	of	complete	

resistance,	when	as	argued	above	the	definition	must	include	incomplete resistance.

If	EPA	does	choose	to	use	either	instar	development	or	body	size/weight	as	a	criterion	in	

resistance	definitions,	it	should	only	be	used	as	a	possible	alternative measure to	survival,	

not	as	an	independent	criterion.		This	is	how	it	appears	to	function	in	the	first	criterion	of	

the	proposed	On-Plant	Assay	Option	1:

“A	statistically	significant	difference	in	measures	of	either

lethality/mortality	or	sublethal	effects	(growth/development)	between	the	

field	population	and	the	control	population	on	Bt	corn”	(White	paper,	p.	28,	

emphasis	added).		

In	a	similar	context,	EPA’s	BPPD	IRM	team	recommended	a	definition	of	confirmed	

resistance	to	Cry3Bb1	based	on	a	single	criterion	(survival):

“On-plant	assays	with	“suspected	resistant”	field	populations	demonstrate	

increased	survival	of	field	populations	on	Bt	compared	to	non-selected	lab	

colonies.”	(BPPD	2012,	p.	20).

Likewise,	when	presented	with	a	possible	definition	of	resistance	that	involved	meeting	

both	of	two	independent	criteria	(LC50	and	proportion	of	root	nodes	destroyed),	the	2002	

SAP	mentioned	above,	which	included leading	experts	on	Bt	resistance,	recommended	that	

meeting	a	single	criterion	sufficed	for	confirmation of	resistance:

“The	Panel	also	agreed	that	rather	than	require	both	clauses,	either	clause	

would	be	sufficient	to	demonstrate	confirmed	resistance.”	(SAP	2002,	pdf	p.	

66)

Question	5:	Determining	Remedial	Action	Areas

No	comment.

Question	6:	Containment/Mitigation	of	Resistance

The	most	effective	measures to	mitigate	resistant	CRW	populations	will	be	those	that	deny	

CRW	a	food	source.		It	is	well	known	that	CRW	infestations	are	much	more	likely	– and	

more	severe	when	they	occur	– in	continuous	corn.		Indeed,	one	of	many	benefits	of	

rotating	corn	(e.g.	with	soybeans)	is	to	forestall	CRW	infestations.

5		Thus,	rotating	away	

from	corn	to	a	non-CRW	host	crop	is	clearly	the	most	effective	mitigation	measure,	and	is	

especially	important	in	view	of	the	sharp	rise	in	in	acres	planted	to	continuous	corn	over	

																																																							 5 A	corn/soybean	rotation	provides	good	protection	against	CRW	in	parts	of	the	Corn	Belt,	but	is	of	less	value	

in	areas	(e.g.	Illinois	and	Indiana)	where a	rotation-resistant	variant has	become prevalent.		However,	even	in	

these	areas	entomologists	have	recommended	that	growers	“continue	rotating	as	a	second	line	of	defense”	to	

soil	insecticides	and/or	rootworm	active	Bt	toxins	(Michael	Gray,	as	quoted	in	Ruen	(2013)).
10

the	past	decade	(addressed	further	below).		EPA	should	consider	mandating	such	crop	

rotations	as	part	of	remediation	plans.

Any	mitigation	that	involves	continuous	corn	is	of	less	value.		But	of	measures	that	involve	

corn-on-corn,	planting	of	non-Bt	corn	eliminates	all selection	pressure	for	evolution	of	

resistance	to	any rootworm-active	PIP	and	is	thus the	most	desirable (Porter	et	al	2012).		

This is	particularly	true	given	the	inadequate	refuge	size	requirements	for	all	corn	

rootworm-active	PIPs	(see	section	II.B	below).		Rotation	to	corn	that	expresses a	different	

PIP	or	PIP	combination	should	be	the	last	recommendation.	

CFS	finds	EPA’s	distinction	between	“hot	spot”	and	“area-wide”	resistance	somewhat	

misleading (White	paper,	34-36).	 While	probably	not	intended	by	EPA,	the	labels	suggest	

that	the	operative	distinction	is	total	area	infested	with	CRW	– little	for	“hot	spot”	

resistance	and	much	more	for	area-wide	resistance	– and	that	the	former	is	thus	less	

problematic	and	merits	less	intervention	than	the	latter.		This	is	not	the	case.		

As	EPA	acknowledges,	reports	of	unexpected	CRW	damage	to	Bt	corn	are	rising	

dramatically,	indicative	of	expanding	resistance	(see	section	II.A).		EPA	finds	that	the	most	

likely	scenario	is	evolution	“in	many	different	hot	spots	simultaneously	from	ubiquitous	

management	practices	favoring	resistance”	(scenario	2)	rather	than	widespread	dispersal	

of	resistant	CRW	from	one	or	a	few	hot	spots	(scenario	1).		As	EPA	concedes,	the	end	result	

of	these	two	scenarios	is	not	likely	to	be	distinguishable;	they	are	merely	different	paths	to	

“area-wide	resistance.”

What	distinguishes	these	scenarios is	the	relative	importance	of	the	evolution of	resistance	

versus	the	spread of	resistance,	once	evolved,	rather	than	the	geographic	extent	of	

resistance.	 EPA	is	probably	right	that	scenario	2	predominates.		Resistance	evolution	is	not	

a	rare,	but	rather	a	frequent event,	resulting	in	numerous	“hot	spots”	due	to	“widespread	

agricultural	practices	employed	across	the	Corn	Belt	(i.e.	continual	planting	of	corn	for	feed	

or	ethanol	production,	lack	of	crop	rotation,	etc.)	and	the	non-high	dose	nature	of	the	

rootworm	Bt	toxins”	(White	paper,	p.	35).		EPA	leaves	out	one	of	the	most	important	

causative	factors,	however,	which	is	its	own	setting	of	entirely	inadequate	refuge	size

requirements for	all	corn	events	expressing	rootworm	PIPs (see	section	II.B).

The	“many	little	hot	spots”	mode	of	CRW	resistance	emergence	has	further	implications	not	

addressed	by	EPA.	 CRW	adults	are	capable	of	sustained,	high-altitude	flight,	and	can	take	

advantage	of	prevailing	winds	and	storm	fronts	to	move	considerable	distances	(Isard	et	al	

2004). Extreme	weather	is	becoming	more	common	with	climate	change.		All	other	things	

being	equal,	the	likelihood	that	storms will	transport	resistant CRW	moderate	to	long	

distances	increases	with	the	geographic	range and	number	of	hot	spots	across	the	Corn	

Belt.	 It	is	greater	with	EPA’s	scenario	2	than	scenario	1.		To	illustrate	this,	imagine	just	one	

large	population	of	resistant	CRW	(scenario	1)	vs.	50	hot	spots	scattered	across	the	Corn	

Belt	(scenario	2),	where	the	total	area	occupied	by	resistant	CRW	is	the	same	in	both	

scenarios.	The	likelihood	of	unusual	weather	events	spreading	resistant	CRW	in	scenario	1	

is	small,	equivalent	to	the	probability	that	such	a	weather	event	will	occur	(and	occur	at	the	

appropriate	CRW	life	stage)	in	just	one	area.		In	scenario	2,	the	probability	of	CRW-
11

transporting	weather	events	is	much	greater – somewhat less	than	the	sum	of	the	

probabilities	of	occurrence	in	50	different	areas.6

Thus,	some	proportion	of	resistant	CRW	populations	in	numerous	confined	areas will	spill	

beyond	their	local	boundaries	during	extreme	weather,	an	additional	mode	of	resistance	

spread	that	EPA	must	consider.		Most	importantly,	however,	frequent	emergence	of	

resistance	in	numerous	localized	areas	points	directly to the	glaring	weaknesses	in	the	

resistance	prevention component	of	EPA’s	IRM	plans,	to	which	we	now	turn.

II. Comments	on	Issues	Not	Addressed	by	EPA

A. Prevalence	of	CRW	Resistance

EPA’s	white	paper	and	charge	questions	focus	narrowly	on	technical	issues	associated	with	

monitoring	for	resistance	and	give	no	overall	impression	of	the	prevalence	and	seriousness

of	the	problem,	which	22	corn	entomologists	recently	told	EPA	requires	action	“with	a	

sense	of	some	urgency”	(Porter	et	al	2012).		Corn	rootworm	resistance	to	Bt	toxins	has	

risen	dramatically	in	the	decade	since	the	first	rootworm-active	Bt	corn	event	was

approved	in	2003,	but	precise	data	are	lacking.	

EPA	must	make	publically	available	much	more	complete	resistance	monitoring	data	so	

that	farmers,	extension	agents,	entomologists	and	the	public	are	better	informed	about	the	

extent	of	CRW	resistance	to	Bt toxins.		The	BPPD’s	reviews	of	monitoring	data	(e.g.	BBPD	

2011)	contain	some	useful	information,	but	lack	basic	components	such	as	total	number	of	

unexpected	Bt	corn	damage	reports	each	year,	broken	down	by	state	and	county.	 Fuller	

and	standardized	reporting	of	such	data is	necessary	to	keep	stakeholders	informed.7

Monitoring	data	provided	by	Monsanto	to	EPA	shows	a	clear	trend	of	declining	

susceptibility	to Cry3Bb1	since	2005 (BPPD	2011,	Tables	5	and	6).		Entomologists	in	

Nebraska	have	observed	moderate	to	severe	rootworm	damage	to	Cry3Bb1	corn	beginning	

no	later	than	2008,	and	in	Minnesota	since	2009 (Ibid,	p.	5),	likely	indicative	of	resistance.		

CRW	sampled	from	a	damaged	Bt	field	in	Iowa	in	2009	were	confirmed	as	resistant	in	2011	

(Gassmann	et	al	2011),	and	resistant	CRW	have	been	confirmed in	Illinois	as	well	(Gray	

2012).

Between	2009	and 2012,	there	were reports	of	heavy	corn	rootworm	damage	to	Cry3Bb1	

corn	in	at	least	23	counties	of	6	states	in	the	Corn	Belt	(NE,	IA,	SD,	MN,	WI,	IL)	(BPPD	2012,	

p.	2).		The	BPPD	IRM	team	believes	that	these	damaged	Cry3Bb1	fields	may	also	be	due	to	

Cry3Bb1	resistance.

																																																							 6 “Somewhat	less	than”	because	weather	patterns	in	different	regions	of	the	Corn	Belt	are	of	course	not	

entirely	independent.	

7 Ironically,	perhaps,	University	of	Illinois	entomologist	Joseph	Spencer	expressed	the	hope	that	seed	

companies would	provide	this	information	to	help	farmers	make	planting	decisions	(see	Smith	2013).		

Farmers	and	scientists	should	not	be	dependent	on	the	good	will	of	seed	firms	(which	in	some	cases	have	

denied	resistance	even	exists,	see	Philpott	2011)	for	this	information.		It	is	EPA’s	responsibility	to	provide	it.
12

Figure	above	excerpted	from	BPPD	(2012),	p.	17,	report	dated	Oct.	11,	2012.

Figure	above	excerpted	from	BPPD	(2013c),	p.	21,	report	dated	Sept.	26,	2013.		New	areas	compared	to	Oct.

2012	map	above	include	western	KS,	eastern	CO,	central	NE,	western	2/3	of	Iowa, eastern	Illinois and	

Oklahoma.		As	noted	in	text,	heavy	damage	to	Cry3Bb1	fields also	reported	in	MI and	MT	(not	shown	on	map).
13

An	update	to	the	aforementioned	report	one	year	later	shows	additional	areas	of	heavy	

CRW	damage	to	Cry3Bb1	corn	in	several	new	regions	(central	NE,	the	western	2/3	of	Iowa,	

eastern	Illinois	and	in	two	new	states	(CO	and	KS),	for	8	states	altogether	(BPPD	2013c,	

Figure	5,	p.	21).		Additional	though	apparently	less	frequent	reports	of	unexpected	damage	

to	Cry3Bb1	corn	came	from	three	additional	states:	Michigan,	Montana	and	Oklahoma	

(BPPD	2013c,	p.	16).		Thus,	CRW	have	caused	heavy	damage	to	Cry3Bb1 corn	in	at	least	11	

states,	and	most	of	these	cases	likely	represent	CRW	that	have	evolved	resistance	to	

Cry3Bb1.		On	the	preceding	page,	two	maps	are	reproduced	from	the	EPA	reports	cited	

above	that	portray	this	development.

And	there	are	also	signs	of	resistance	evolving	to	the	other	two	commercially	available	

rootworm	toxins	– Cry34/35Ab1	and	mCry3A	– in	the	form	of	LC50	values	in	field	

populations	that	substantially	exceed	those	of	control	populations:

“A	number	of	field-collected	populations	have	shown	LC50s	exceeding	the	

upper	limit	of	the	95%	confidence	interval	of	the	control	population	(see	data	

reviewed	in	BPPD	2011,	2012,	2013a,	b,	c),	although	none	of	the	populations	

have	been	deemed	resistant	by	registrants”	(White	paper,	p.	16)8

The	rapid	emergence	of	Cry3Bb1-resistant	corn	rootworm	throughout	the	Corn	Belt,	and	

signs	of	evolving	resistance	to	the	other	toxins,	raise	several	serious	questions	for	EPA.		

First	and	most	obviously,	why	are	EPA’s	IRM	plans	for	corn	rootworm	failing	so	

dramatically	and	so	rapidly?		

B. Deficient	Refuge	Requirements

All	of	EPA’s	charge	questions	relate	to	changes	in	the	monitoring	program.		Yet	by	far	the	

most	important	reason	for	the	expanding	failure	of	IRM	is	to	be	found	in	the	thoroughly	

inadequate	refuge	size	that	EPA	has	set	for	rootworm-active	Bt	corn	events.

All	Bt	corn	hybrids	targeting	corn	rootworm	produce	relatively	low	doses	of	Bt	toxin,	

violating	EPA’s	preferred	high-dose	strategy	that	is	met	by	all	or	most	Bt	events	for	major	

lepidopteran	pests.		EPA	guidelines	for	a	high	dose	require	that	such Bt	plants	kill	≥99.99%	

of	susceptible	target	insects	in	the	field (SAP	1998,	pp.	4-5),	equivalent	to	a	survival	rate	of	

≤0.01%.	 The	various	rootworm	Bt	events	not	only	do	not	meet	this	standard,	they	do	not	

even	begin	to	approach	it.		The	survival	rate	of	susceptible	CRW	on	corn	expressing	

Cry3Bb1,	averaged	over	three	studies,	is 2.6%,	or	260-fold	higher	than	the	maximum	

0.01%	survival	rate	that	defines	high-dose	Bt	events.		Similar	CRW	survival	rates	are	found	

for corn	expressing	Cry34/35Ab1 (4.2%)	and	mCry3A	(3.6%) (Tabashnik	&	Gould	2012,	

Figure	2).

																																																							 8 BPPD	2011,	2012	and	2013c	are	EPA	reviews	of	monitoring	data	and	field	reports	on	unexpected	damage	to	

Cry3Bb1-expressing	corn;	BPPD	2013a	and	BPPD	2013b	are	similar	reviews	for	Cry34/354Ab1	and	mCry3A	

corn,	respectively.
14

These high	survival	rates are	indicative	of	nonrecessive	inheritance	of	resistance,	which	is	

predicted	to	dramatically	accelerate	evolution	of	resistance	relative	to the	recessive	

resistance	to	Bt	toxins	like	Cry1Ab	seen	in	lepidopteran	pests	such	as	European	corn	borer.		

In	fact,	survival	rates	in	this	range	represent	a	worst-case	scenario	for	resistance	evolution	

(Tabashnik	&	Gould	2012,	p.	769).

A	large	refuge	is	required	to	compensate	for	the	resistance-promoting	effects	of	the	low

doses of	rootworm-active	Bt	toxins.		Below,	we	focus	on	Cry3Bb1,	as	both	the	first	

rootworm	Bt	toxin	and	the	one	to	which	CRW	resistance	is	most	advanced.		But	similar	

considerations	apply	to	the	others	as	well	given	their	similarly	low	doses.

In	2003,	EPA	convened	a	Scientific	Advisory	Panel	(SAP)	to	advise	it	on	insect	resistance	

management for	Cry3Bb1-expressing	MON863,	the	first	Bt	corn	event	targeting	corn	

rootworm.		A	clear	majority	of	the	SAP	(11	of	14	members) recommended	that	at	least	a

50%	refuge	be	mandated	for	MON8639 (Knight	2003). This	SAP,	which	included	some	of	

the	world’s	leading	experts	on	pest	resistance	to	Bt	toxins,	found	that	“modeling	suggested	

that	a	50%	refuge	would	net	at	least	twice	the	time	to	resistance	as	the	proposed	20%	

refuge” (SAP	2002). EPA	ignored	the	SAP’s	recommendation	and	instead	complied	with	

Monsanto’s	request,	establishing	a	20%	refuge (Knight	2003).		It	appears	that	EPA	took	this	

action	on	the	basis	of	information	submitted	to	it	by	Monsanto	after the	SAP	meeting	took	

place	(Pollack	2003),	information	that	was	thus	unavailable	for	critical	review	by	the SAP.

In	contrast	to	Bt	resistance	experts,	EPA	claimed	then	that	its	modeling	projected	that even	

if	Cry3Bb1-producing	corn	were	planted	all	over	the	U.S.,	it	would	take	7	to	16	years	for	

resistance	to	become	a	problem (Knight	2003):	that	is,	not	until	2009	to	2018.	 With	the	

much	less	extensive	plantings	projected	by	Monsanto,	resistance	would	presumably	take	

much	longer	to	emerge.		As	it	turned	out,	MON863	plantings	in	fact	represented	just	17%	of	

aggregate	corn	plantings	from	its	introduction	in	2003	to	2009.10		Despite	this	limited	

acreage,	resistance	emerged	no	later	than	2009	(Gassmann	et	al	2011),	the	earliest	date	

that	EPA	had	predicted	for	its	“worst-case”	scenario	of	nationwide	coverage	with	MON863.

EPA’s	ostensible	reasons	for	acceding	to	Monsanto’s	request	for	a	20%	refuge	were:

1) The	registration	being	considered	was	interim,	lasting	only	one year with	

probable	extension	to	three	years	(Pollack	2003); and	even	with	a	refuge	as	

small	as	20%,	resistance	was	not	likely	to	evolve	in	three	years,	after	which	time	

the	refuge	size	requirement	could	be	re-evaluated	and	changes	made	as	

necessary (Knight	2003);

2) Growers	would	be	confused	by,	and	not	comply	with,	a	refuge	as	large	as	50%,	

while	their	familiarity	with	a	20%	refuge	(from	Bt corn	targeting	European	corn	

																																																							 9 A	majority	favored	50%;	a	couple	of	panel	members	supported	a	refuge	of	greater	than	50% (Tabashnik	&	

Gould	2012,	p.	770). 10 Based	on	Monsanto	biotechnology	trait	acreage	figures	calculated	from	Monsanto	(2009)	and	USDA	NASS	

data	on	total	corn	plantings.		Cry3Bb1-expressing	corn comprised 1%,	2%,	5%,	13%,	22%,	35%,	and	36%	of	

U.S.	corn	plantings	from	2003	to	2009,	respectively.
15

borer)	would	increase	compliance (SAP	2002,	pdf	p. 58,	expressing	the	views	of	

a	minority	of	SAP	members,	3	of	14).

In	making	these arguments,	EPA	essentially	ignored	the	majority	of	its	scientific	advisers,	

who	“concluded	that	there	was	no	practical	or	scientific justification	for	establishing	a	

precedent	for	a	20%	refuge”	for	MON863 (SAP	2002,	pdf	p. 57,	emphasis	added).

As	for	EPA’s	first	reason, the	SAP	warned	that	while	the	20%	refuge	was	not	likely	to	result	

in	field	failures	due	to	resistance	during	this	three-year	period:

“[i]t	could,	particularly	in	local	areas,	lead	to	a	significant	increase	in	

resistance	allele	frequencies	over	this	time.		This	increased	frequency	would	

limit	future	options	for	resistance	management	relative	to	Cry3Bb1	and	any	

other	toxin	for	which	there	was	cross-resistance	with	Cry3Bb1.		Panel	

members	indicated	that	the	choice	of	a	20%	refuge	for	the	interim	plan	was	

likely	to	limit	choices	of	refuge	size	in	the	future	because	farmers	and	

companies	would	not	desire	to	increase	refuge	size.” (SAP	2002,	pdf	p.	57)

The	SAP’s	majority was	correct	on	both	scientific	and	practical	grounds.		As	noted	above,	

CRW	survival	rates	and/or	the	amount	of	toxin	required	to	kill	or	impair	growth	have	

generally	increased	over	time	for	all	of	the	rootworm-active	Bt	toxins,	including	Cry3Bb1,	

indicating	a	rise	in	resistance	allele	frequency.		A	50%	refuge	would	have	diluted	resistance	

genes	and	delayed	resistance	much	better	than	the	unscientific	20% refuge	that	EPA	

actually	implemented.		As	noted	above,	the	SAP	found	that	a	50%	refuge	would	have	at	

least	doubled	the	time	to	emergence	of	resistance	relative	to	the	20%	refuge.

Neither	did	EPA	(to	the	best	of	our	knowledge)	make	any	attempt	to	re-assess	its	interim	

decision	or	increase refuge	size	at	any	of	the	three	decision	points	on	extending	the	

registration	of	Cry3Bb1-expressing	corn	(MON863	or	its	successor	MON88017) in	2004,	

2006	or	2010.11

EPA	presented	no	empirical	evidence	in	support	of	its	second	reason regarding	grower	

compliance,	while	ignoring	evidence that	undermined	it.		First	of	all,	in	the	five	years	

preceding	introduction	of	MON863,	U.S.	corn	farmers	applied	insecticides	to	control	CRW	

on	just	14	to	18	million acres	of	corn	each	year,	representing	18%	to	23%	of	total	corn	

acres	(EPA	2005).		If	CRW	infestations justified	spraying	on	just	one-fifth	of	national	corn	

acres,	it	is	difficult	to	understand	how	permitting	50%	of	corn	(over	twice	as	much)	to	be	

“treated”	with	Cry3Bb1 would	result	in	massive	non-compliance	with	a	50%	refuge	

requirement.12

																																																							 11 The	EPA	initially	(2/24/03)	issued	a	time-limited	registration	for	MON863	corn	that	was	renewed	for	two	

years	on	4/23/04;	then	for	four	additional	years	on	7/27/06.		In	September	2010,	the	registration	for	

MON863’s successor, MON88017, was	extended	for	five	years	and	now	expires	on	9/30/15	(EPA	2010a,	

Regulatory	History,	pp.	9-18). 12 While	the	proportion	of	corn	acres	sprayed	for	CRW	would	of	course	vary	greatly	at	the	on-farm	level	

depending	on	CRW	pressure	in	various	regions,	the	fact that	only	20%	of	corn	acres	were	sprayed	for	CRW	

nationally	suggests	at	least	that	the	pest	afflicts	a	clear	minority	of	corn	at	economic	injury	levels	in	any	given	
16

Second,	EPA	completely	ignored the	precedent	of	insect	resistant	management	(IRM)	for	Bt	

cotton	in	Australia,	which	was	discussed	and	cited	as	a	precedent	by	the	SAP	(SAP	2002,	

pdf	pp.	57-58).		There,	government	regulators	successfully	implemented, and	farmers	

complied	with, a	comprehensive	IRM	plan	that	included	a 50%	refuge	requirement	and	

involved	a	host	of	other	measures	as	well (Fitt	2004,	Table	1	and	p.	17):

1) Sliding	cap	on	the	proportion	of	national	cotton	acreage	that	could	be	planted	to	

single-toxin	(Cry1Ac)	cotton,	which	increased	in	stages	from	just	8%	in	1996/97	

to	a	maximum	of	30%	in	2001/02;13

2) Refuge	requirements	stipulating	that	up	to	50%	of	a	Bt	cotton	farmer’s	fields	be	

planted	to	non-Bt	cotton;14

3) Defined	planting	window	to	avoid	late	planted	cotton	that	could	serve	as	host	for	

H.	armigera late	in	the	season;

4) Mandatory	cultivation	of	Bt	cotton	to	destroy	overwintering	pupae	of	H.	

armigera and	mandatory	removal	of	volunteer	Bt	plants	in	subsequent	seasons;

5) Three	audits	per	year	for	each	farm	growing	Bt	cotton	to	check	on	compliance	

with	refuges;	among	other	requirements	(Fitt	2004).

Australian	regulators	established this	stringent	IRM	plan	because, vis-a-vis the	chief	

Australian	cotton	pest	(H.	armigera)	“Inguard	cotton	varieties	expressing	a	single	Cry1Ac	

gene	clearly	do	not	express	a	high	dose	and	heterozygote	mortality	is	unlikely	to	be	high	

except	perhaps	when	plants	are	quite	young...”	(Fitt	2004).		This	mirrors	precisely	the	

situation	EPA	faced	with	MON863 and	corn	rootworm.		While	Australian	regulators	

followed	the	science	and	have	thus	far	succeeded	admirably	in	forestalling	resistance,	EPA	

rejected	the	science	in	favor	of	entirely	unfounded	speculation	about putative	farmer	noncompliance and	thus	set	the	stage	for	today’s	rapidly	emerging	CRW	resistance.

As	the	reports	of	unexpected	damage	to	Cry3Bb1	corn	and	hence	the	incidence	of	CRW	

resistance	escalate,	EPA	has	responded,	incredibly,	by	sharply	reducing the	already	

inadequate	20%	refuge	requirement.		EPA’s	rationales	for	doing	so	– refuge	in	a	bag	and	

pyramided	Bt	corn	products	– have	no	more	scientific	merit	than	its	decision	to	set	a	20%	

refuge.

Refuge	in	a	bag	(RIB)	or	blended	refuge	is	a	seed	mixture in	which	the	non-Bt seed15 is	

mixed	together	with	the	Bt	seed;	the	“refuge”	is	then	comprised	of	the	non-Bt	corn	plants	

																																																																																																																																																																																		

year; and	that	constraining	the	minority	of	corn	farmers	with	economic	CRW	infestations	to plant	half	their	

fields	to	non-Cry3Bb1	corn	would	have	been	a	reasonable	requirement	striking	a	scientifically	sound	balance	

between	current	benefits and	long-term	sustainability.	 13 Australian	regulators	worked	with	industry	to	orchestrate	a	planned	transition	from	single-toxin	Cry1Ac	

cotton	to	dual-toxin	Bollgard	II	cotton,	which	took	place	in	the	2003/04	season,	the	only	season	in	which	both	

single	and	dual-toxin	varieties	were	planted.	The	national	cap	was	eliminated	at	this	time,	though	other	IRM	

measures	remained	in	effect. 14 Refuge	requirements	varied	by	refuge	crop	and	management	practice.		A	refuge	of	50%	was	required	if	the	

non-Bt	cotton	refuge	was	sprayed	for	CRW.		Refugia	could	be	smaller	if	unsprayed.
17

growing	uniformly	intermixed	with	the	Bt	plants.		The	other	form	of	refuge	is	the	block	or	

structured	refuge,	where	the	non-Bt	plants	are	planted	together	in	a	plot	or	plots	adjacent	

to	the	Bt	corn.	 EPA	required	block	refugia	for	all	Bt	crop	varieties	until	2010,	when	it	

registered	the	first	refuge	in	a	bag	product,	Optimum	AcreMax,	which	consisted	of	90%	

Cry34/35Ab1	and	10%	non-rootworm	Bt	corn	(EPA	2010b).		This	90:10	ratio	for	RIB	

represented	half	the	refuge	required	for	the	same	Cry34/35Ab1	corn	in	a	structured	

context,	where	a	20%	refuge	is	required.

Once	again,	EPA’s	decision	was	directly	contrary	to	the	recommendation	of	its	expert

advisors.		A	Scientific	Advisory	Panel	convened	to	advise	EPA	on	this	very	question	was	

unequivocal:	“The	Panel	generally	agreed	that	data	presented	by	Pioneer	and	data	found	in	

the	public	literature	provide	no	compelling	evidence	to	reduce	the	proportion of	non-Bt	

plants	(either	as	a	seed	blend	or	spatial	refuge)	from	20%....”	(SAP	2009,	p.	6).		“[I]n	fact,	

the	Panel	recommended	that	the	proportion	of	non-Bt	plants	remain	at	20%	rather	

than	be	reduced	to	10%	as	proposed	by	BPPD.		The	recommendation	from	a previous	

FIFRA	Scientific	Advisory	Panel	was	for	a	50%	refuge.”	(SAP	2009,	p.	21,	emphasis	

added).

The	experts	on	this	Scientific	Advisory	Panel	were	not	alone.		Most	agronomists	and	

entomologists	see	refuge	in	a	bag	as	a	decidedly	“mixed	bag”	that	has	some	advantages	

over	the	traditional	block	refuge	as	well	as	some	disadvantages.		Thirteen	agronomists	who	

evaluated	the	issue	found	that	“neither	blocks	nor	refuges	are	clearly	superior” (Onstad	et	

al	2011;	see Table	1	from	that	paper,	reproduced	below),	making	it	very	unclear	whether	

RIB	justifies	any	reduction	in	refuge	size	at	all.		What	is	clear,	however,	is	that	any	effect	

that	RIB	might have	in delaying	resistance	should	not	be	undercut	by	slashing	the	refuge	

size,	given	the	continuing	rapid	emergence of	CRW	resistance	throughout	the	U.S.

Pyramided	Bt	products	incorporate	two	or	more	Bt toxins	that	act	on	the	target	pest(s)	

with	differing	modes	of	action,	thereby	reducing	the	likelihood	of	resistance	evolving	to	

either	one.		In	2009	and	2011,	EPA	registered	Cry3Bb1	+	Cry34/Cry35Ab1	corn	and	

mCry3A	+	Cry34/Cry35Ab1	corn,	respectively.		For	these	products,	EPA	slashed	the	

prevailing	20%	refuge	requirement	for	single-toxin	Bt	seed	by	75%,	from	20%	to	just	5%	

(Tabashnik	&	Gould	2012,	Table	1).

																																																																																																																																																																																		 15 As	used	here,	“non-Bt seed”	means	seed	that	does	not	contain	a	rootworm-active	Bt	toxin;	it	may	be	either	

conventional	seed	or	contain	one	or	more	Bt	toxins	targeting	lepidopteran	pests.
18

Source:	Onstad	et	al	(2011).		

Similar	arguments	apply	here	as	to refuge	in	a	bag	(even	though	pyramids	more	clearly	

provide	at	least	a	modest resistance	prevention	boost	versus RIB).		With	resistance	to	

Cry3Bb1	on	the	rise	due	to	a	clearly	inadequate	20%	refuge,	it	was	reckless	of	EPA	to	

squander	the	resistance-fighting	effects	of	the	pyramid	through a	resistance-promoting	

reduction	in	refuge	size.		The	first	pyramid	cited	above	acts	as	a	single-toxin	product	for	the	

large	and	growing	number	of	CRW	that	are	rapidly	evolving	resistance	to	Cry3Bb1

throughout	the	Corn	Belt.		In	those	resistance-ridden	areas where	this	pyramid	is	most	

likely	to	be	grown,	there	is	next	to	no	refuge	corn	(only	5%)	to	dilute	the	Cry34/35Ab1

resistance	alleles	that	can	be	expected	to	rapidly	accumulate	in	Cry3Bb1-resistant	CRW.		

The	expected	result	is	rapid	evolution	of	CRW	resistant	to	both	toxins.

The	situation	may	be	somewhat	better	for	the	second	pyramid,	but	rather	uncertain	due	to	

the	close	amino	acid	sequence	similarity	and	likely	cross-resistance	between	Cry3Bb1	and	

mCry3A.		Only	time	will	tell	the	magnitude	of	the	cross-resistance	risk.		If	it	is	small,	then	

this	pyramid	has	the	potential	to	be more durable;	if	on	the	other	hand	resistance	to	

Cry3Bb1	frequently	confers	resistance	to	mCry3A (and	vice	versa),	then	similarly	to	the	

first	pyramid, an	increasing	number	of	CRW	already	resistant	to	the	Cry3 toxins will	

experience	intense	selection	pressure	to	evolve	additional	resistance	to	Cry34/35Ab1.

EPA’s	BPPD	IRM	team	summarizes	the	situation	well:

“BPPD	is	concerned	with	these	preliminary	reports	of	cross-resistance	

between	Cry3Bb1	and	mCry3A	and	the	planting	of	CRW	pyramided	corn	

expressing	Cry3-Bt	toxins	in	areas	with	Cry3Bb1	resistant	corn	rootworm	

populations.	 Such	pyramids	are	effectively	reduced	to a	single	toxin	

product	deployed	with	a	much	lower	refuge	(5%). There	are	currently	

four	registered	corn	rootworm	toxins,	two	of	which	(mCry3A	and	Cry3Bb1)	
19

would	be	ineffective	in	corn	rootworm	resistant	areas.	 The	selection	

pressure	in	these	regions	on	the	remaining	toxin,	Cry34/35,	will	be	

tremendous	if	deployed	in	a	pyramid	with	Cry3Bb1	and	a	reduced	refuge	

of	5%.” (BPPD	2013c,	p.	24,	emphasis	added)

It	is	also	concerning	that	the	Cry3Bb1	+	Cry34/Cry35Ab1	pyramid	(sold	commercially	as	

SmartStax)	does	not	have	anywhere	near	the	lethality	that	one	would	expect	if	the	two	

toxins	acted	independently.		The	predicted	survival	rate	assuming	independent	action	is	

just	0.145%;	yet	the	observed	survival	rate	is	12	times	that,	or	1.8%,	≥	180	times	the	

≤0.01%	survival	rate	that	defines	a	high-dose	event (Tabashnik	&	Gould	2012).		The	fact	

that	the	SmartStax	pyramid	delivers	only	a	marginally	higher	dose	than	its	constituent	

single-toxins,	and	is	still	a	low-dose	event, represents	another	argument	against	EPA’s	

irresponsible	reduction	in	refuge	requirements	to	a	miniscule	5%.

In	light	of	these	and	similar	considerations,	two	of	the	world’s	leading	experts	on	Bt	

resistance,	Drs.	Bruce	Tabashnik	and	Fred	Gould,	recently	recommended that	EPA	establish	

a	50%	refuge	for	all	single-toxin	Bt	corn	products,	and	a	20%	refuge	for	pyramided	

products (Tabashnik	&	Gould	2012).		These	sensible	recommendations	– which	logically	

propose	that	increasing CRW	resistance	be	countered	by	strengthening IRM	– is	

thoroughly	at	odds	with	EPA’s	inexplicable	actions	that	dramatically	weaken it.		If	short	

supplies	of	non-Bt	seed	make	immediate	establishment	of	these	refugia	requirements

unworkable,	increases	in	refuge	percentage	could	be	phased	in	over	years	to	give	seed	

firms	time	to	multiply	the	needed	seeds.	

C. Declining	Availability	of	High-Quality	Conventional	(Non-Bt)	Corn	

Endangers	IRM

The	discussion	above	suggests that	an	adequate	supply	of	high-quality,	non-Bt	corn	seed	is	

an	indispensible	element	of	any	successful	IRM	plan.		With	a	large	majority	of	U.S.	corn	

acreage	planted	to	varieties	with	Bt	toxins (76%	in	2013),

16 refugia	represent	by	far	the	

biggest	source	of	demand	for	non-Bt	corn	seed	today.		An	indirect	effect	of	EPA’s	reckless	

slashing	of	refuge	requirements	is	a	corresponding	decline	in	demand	for	non-Bt	corn seed,	

accompanied	by	a	reduction	in	the	diversity, quality	and	volume	of	non-Bt	offerings.		The	

paucity	of	non-Bt	corn	seed	in	turn	undermines	integrated	pest	management (IPM).			

Growers	who	would	like	to	periodically	grow	conventional corn as	part	of	their	overall	IPM	

strategy	find	it	increasingly	hard	to	do	so.		IRM	is	reduced	to	a	dangerously	narrow	set	of	

transgenic	options:	switching	among different	Bt	modes	of	action	or	(more	commonly)	

combining	them	in	pyramids (Gray	2011).

Numerous	agronomists	have	warned	of	these	intertwined	problems	of	declining	

availability	of	non-Bt	seed	and	the	demise	of	IPM.		In	a	2010	survey,	University	of	Illinois	

																																																							 16 Up	sharply	from	67%	in	2012,	likely	reflecting	the	increased	use	of	RIB	with	5%-10%	refuge	requirements.		

See	http://www.ers.usda.gov/data-products/adoption-of-genetically-engineered-crops-in-theus.aspx#.Upyxd6VXaa4.		Add	figures	for	“insect-resistant”	and	“stacked”	corn	(stacked	corn	by	definition	

includes	traits	for	both	herbicide- and	insect-resistance).
20

entomologist	Michael	Gray	found	that	fully	40%	of	Illinois	corn	farmers	did	not	have	access	

to	elite	varieties	of	non-Bt	corn	seed	in	2009	(Gray	2011,	Table	2).		Onstad	et	al	(2011)	also	

find	that	the	pool	of	nontransgenic	corn	hybrids	is	shrinking,	giving	growers	fewer	choices

to	eliminate	selection	pressure	by	growing	conventional	corn.	

Twenty-two	public	sector	corn	entomologists,	many	with	extension	responsibilities	and	

hence	familiarity	with	the	challenges	farmers	face, warned	EPA	that	declining	availability	of	

high-yielding	non-Bt	corn varieties leads	to	prophylactic	or	entirely	superfluous	

deployment	of	Bt	toxins,	and	hence	needless	selection	pressure	for	resistance.		This	in	turn

erodes an	essential	tool	in	the	fight	against	further evolution	of	CRW	resistance to	Bt	

toxins:

“Rootworm-protected	Bt	corn	is	being	used	prophylactically	in	areas	with	little	or	

no	need	for	it.		This	unwarranted	use occurs	in	part	because	genes	to	produce	

rootworm	Bt	toxins	(and	toxins	active	against	Lepidoptera)	are	incorporated	into	

elite	germplasm	with	the	highest	yield	potential.		Thus	growers	often	have	few	

options	other	than	to	plant	stacks	and	pyramids	if	they	wish	to	use	the	hybrids	with	

best	yield	potential.		When	growers	do	not	want	to	use	Bt	corn,	many	report	

increasing	difficulty	in	obtaining	non-transgenic	seed.		Scarcity	of	non-Bt	seed	may	

become	more	acute	as	the	seed	industry	transitions	to	a	refuge	“in	the	bag”	

approach	for	resistance	management.

Planting	non-Bt corn	can	be	profitable	and	should	be	one	of	the	IPM	tools	to	

maintain	susceptibility	to	rootworm-protected	transgenic	corn.		After	all,	

whether	used	in	conjunction	with	soil-applied	insecticides	or	not,	conventional	

hybrids	cause	no	selection	for	resistance	to	any	Bt	toxin.		It	is	ironic	that	the	

decreasing	availability	of	non-Bt	hybrids	erodes	the	ability	of	producers	to	move	

to	a	more	integrated	system	of	corn	rootworm	management,	one	that	protects	

the	value	of	Bt	hybrids.		As	a	component	of	effective	IPM	for	corn	rootworms,	

attention	should	be	given	to	increasing	the	supply	of	elite hybrids	that	do	not	

contain	Bt” (Porter	et	al	2012,	emphasis	added)

It	is	noteworthy	that	“refuge	in	a	bag,”	an	innovation	that	EPA	has	used	to	justify	the	refuge	

reductions	(e.g.	20%	block	to 10%	RIB	for	Cry34/35Ab1	corn)	desired	by	industry,	is	cited	

by	these	corn	entomologists	as	a	prime	driver	of	non-Bt	corn	scarcity, and	hence	

superfluous	selection	pressure that	accelerates	CRW	resistance	to	rootworm	toxins.		Gray	

(2011)	makes	a	similar	point.

Thus,	EPA’s	unjustified	reductions	in refuge	requirements	exacerbate rootworm	resistance	

in	two	ways:	1)	Directly,	by	shrinking	the	pool	of	susceptible	insects	for	dilution	of	

resistance	alleles;	and	2)	Indirectly,	by	reducing	demand	for	non-Bt	corn,	which	leads	to	

declining	availability	and	planting	of	non-Bt	seeds	that	are	urgently	needed	to	lessen

selection	pressure	for	rootworm	resistance	to	Bt	toxins.		

Monsanto	wanted	a	20%	rather	than	a	50%	refuge	requirement	because its	makes	more	

profit	selling	biotech vs.	conventional	seeds;	and	seeds	with	more	vs.	fewer	traits. Related	

to	this,	the	20%	refuge	requirement	matched	the	existing	one	for	Bt	corn	targeting	
21

lepidopteran pests.		Having	the	same	refuge	requirements	for	rootworm	and	lepidopteran	

Bt	corn	greatly	facilitated	Monsanto’s	profit-driven	“biotech	trait	penetration”	strategy	of	

combining	both	Bt	traits	in	the	great	majority	of	their	corn	varieties,	and	sharply	reducing	

single	Bt	offerings	of	either	sort.		This	trend	is	reflected	in	Monsanto’s	biotechnology	trait	

acreage	figures,	which	show	that	U.S.	acreage	planted	to	Monsanto	single-Bt	corn	(of	either	

sort)	peaked	at	34	million	acres	in	2004,	declining	to	7.9	million	acres	by	2009;	while	

plantings	of	Bt	corn	targeting	both	CRW	and	lepidopteran	pests	increased	from	0	to	31.3	

million	acres	over	the	same	period	(Monsanto	2009).

If	EPA	had	followed	the	science	and	established	a	50%	refuge	requirement,	it	would	not	

only have	dramatically	slowed	evolution	of	resistance.		It	would	have	had	the	additional	

beneficial	effects of	encouraging	Monsanto (and	other	seed	firms) to	offer more

conventional	and/or more	single-toxin-Bt	corn	lines.17		This	increased	diversity	of	seed	

offerings	would	have	better	met	farmers’	needs	and	reduced	the	“unwarranted	use”	of	Bt	

toxins	mentioned	above	by	farmers	who	are	presently	constrained	to	buy	them	even	

though	they	have	no	agronomic	need	for	them.

Industry	and	EPA	often	place	the	blame	for	resistance	on	farmers	for	not	always	complying	

with	refuge	requirements.		The	analysis	presented	above	suggests	that	seed	firms	are	as	or	

more	culpable.	 Farmer	non-compliance	with	refuge	requirements	is	at	least	partly	

attributable	to	the	dearth	of	locally	adapted,	high-yielding	conventional	(non-Bt)	varieties

on	offer.

18

D. Increasing	Corn	Monoculture

U.S.	corn	acreage	has	increased	a	substantial	31%	since	1990,	to	a	near	historical	high	of	

96.9	million	acres	in	2012.		The	19%	increase	in	corn	acreage	since	the	year	2005	in	

particular	is	attributable	largely	to	ethanol	demand,	which	has	driven	up	corn	prices	and	

made	corn more	profitable	to	grow	than	most	other	crops.		The	portion	of	U.S.	corn	

production	utilized	for	ethanol	rose	from	just	14%	in	2005	to	roughly	40%	in	2012.	 This	

rise	in	overall	corn	acreage	has	meant	more	acres	planted	to	corn	continuously,	year	after	

year.

A	recent	assessment	that	utilized	satellite	imagery	to	determine	cropping	patterns	in	the	

central	U.S.	found	that	corn	monoculture	has	increased	sharply	over	the	past	decade

(Plourde	et	al	2013).		From	2003	to	2010,	the	land	area	planted	to	corn	two	years	in	a	row	

increased	by	22%.		Still	more	striking,	the	amount	of	corn	in	quadruple	planting	(four	years	

of	corn	in	a	row)	doubled	– from	4%	to	8%	of	total	corn	acres	– from	the	first	half	of	the	

period	2003-2006	to	the	second	half	of	the	2007-2010	time	period.

																																																							 17 Especially	single-toxin	Bt	for	lepidopteran	pests,	since	these	could	be	used	to	meet	the	50%	refuge	

requirement	and	would	be	more	profitable	than	conventional	lines.	 18 A	related	reason	for	non-compliance	has	been	farmer	anticipation	of	refuge-in-a-bag,	which	led	many to	

believe	that	structured	refuge	requirements	(and	hence	compliance	with	them)	were of	little	importance,	

since	soon	to	be	replaced	by	RIB	(Gray	2011).
22

Cultivation	of	corn	continuously	on	the	same	fields	over	years	is	associated	with	several	

adverse	impacts	relative	to	corn	grown	in	rotation	(e.g.	with	soybeans):	lower	yield; higher	

per	acre	fertilizer	use	in	an	attempt	to	compensate for	reduced	yield;	greater	disease	

pressure; corn	rootworm	infestations;	and,	if	the	corn	expresses	a	rootworm-active	Bt	

toxin,	accelerated	evolution	of	resistance.

Nearly	all	reports	of	Cry3Bb1-resistant	CRW	have	been	in	fields	planted	continuously	to	

Cry3Bb1-producing	corn.		For	instance,	the	first	published	paper	on	resistant	CRW	

(collected	in	2009)	noted	that	all	fields	harboring	them	had	been	planted	to	Cry3Bb1	corn	

for	at	least	three	consecutive	years:

“In	all	cases,	fields	experiencing	severe	rootworm	feeding	contained	Cry3Bb1	

maize.	Interviews	with	farmers	indicated	that	Cry3Bb1	maize	had	been	

grown	in	those	fields	for	at	least	three	consecutive	years.	There	was	a	

significant	positive	correlation	between	the	number	of	years	Cry3Bb1	maize	

had	been grown	in	a	field	and	the	survival	of	rootworm	populations	on	

Cry3Bb1	maize	in	bioassays.”	(Gassmann	et	al	2011)

The	same	team	found	that	2010	CRW	populations	determined	to	be	resistant	“came	from	

fields	with	a	history	of	continuous	maize	production	and	between	3	and	7	years	of	Cry3Bb1	

maize	cultivation”	(Gassmann	et	al	2012).

While	continuous	corn	is	nothing	new,	it	has	always	represented	a	minority	of	corn	acres.		

Most	farmers	have	been	reluctant	to	plant	corn	in	successive	years	because	of	the

heightened	risk	of	rootworm	infestations and	the	other	problems	mentioned	above:	

reduced	yield,	greater	fertilizer	use,	and	disease	issues.	 Bt	corn	targeting	corn	rootworm	

has	been	a	major	factor	in	eroding	that	reluctance,	and	thus	an	important	factor	facilitating	

the	rise	of	corn-on-corn discussed above.

19		Understanding	this	dynamic,	seed	firms	have	

actively	promoted	Bt	corn	for	this	use.

According	to	Wyffels	Seed	Company:

“With	the	advent	of	seed	technology	that	puts	rootworm	protection	in	the	

plant,	growing	corn-on-corn	has	become	much	easier.		Selecting	hybrids	

with	Agrisure®	3000GT,	Herculex®	XTRA,	Genuity®	SmartStax®,	

Genuity®	VT	Triple	PRO®	or	YieldGard	VT	Triple®	technologies	is	a	great	

way	to	go.”20 (Wyffels	Hybrids	undated)

Monsanto	goes	so	far	as	to	offer	farmers	“Corn-On-Corn	Clinics,” which	it	describes	as	

follows:

																																																							 19 While	ethanol	is	driving	the	demand	for	more	corn	and	hence	more	continuous	corn	by	driving	up	corn	

prices,	some	and	perhaps	many	farmers	who	did	in	fact	transition	to	“corn-on-corn”	would	not	have done	so	

because	of	the	associated	risk	of	major	losses	from	CRW	infestations	if	they	had	not	had	access	to	a	tool	(Bt	

corn	for	rootworm)	that	for	a	time	at	least	prevented	those losses.	 20 http://www.wyffels.com/agronomy/continuous-corn/,	last	visited	12/3/13.
23

“The	Corn-On-Corn	Clinics	are	a	series	of	events	across	the	country	

featuring	a	panel	of	industry	experts,	academics	and	local	growers	speaking	

on	a	variety	of	corn	topics,	including	fertility	management,	insect	

management,	disease	management	and	residue	management.		Control	pests	

in	your	corn-on-corn	acres	with	the	help	of	Genuity® SmartStax® RIB	

CompleteTM” corn	blend.” (emphasis	added)21

Monsanto understands	that	most	growers	have	reservations	about	continuous	corn.		Those	

reservations	are	eroded	by	holding	“clinics”	in	which	experts	from	Monsanto	and	academia	

persuade	these	farmers	that	with	proper	“scientific”	management,	corn-on-corn	can	be	

good	or	at	least	acceptable	agronomic	practice,	when	of	course	there	are	few	practices	

more	agronomically	or	environmentally	detrimental.22		The	chief	facilitator	of	continuous	

corn	is	Bt	seed	– in	this	case,	SmartStax,	which	is	Monsanto’s	most	expensive	and	profitable	

product.	 Monsanto	even	entices	farmers	to	attend	its	“Corn-On-Corn	Clinics”	by	offering	

attendees	the	chance	at	a	$500	gift	card.

Interestingly,	Monsanto’s	2012	“corn-on-corn	clinics”	were	all	held	in	areas	where	CRW	

resistance	to	Monsanto’s	Cry3Bb1	is	prevalent	(see	map	on	next	page),	and	thus	where	

SmartStax	often	acts	as	a	single-toxin	product	with	a	paltry	5%	refuge.		There	is	no	better	

recipe	for	rapid	evolution	of	resistance	to	the	sole	Bt	toxin	that	(at	present)	remains	largely	

uncompromised	(Cry34/35Ab1).

																																																							 21 http://www.genuity.com/corn/Pages/Corn-on-Corn-Clinics.aspx,	last	visited	12/3/13. 22 Aside	from	fostering	CRW,	increased	acreage	planted	to	continuous	corn	is	likely	a	major	factor	in	the	

record	rates	of	inorganic	nitrogen	fertilizer	applied	to	corn,	since	as	noted	above	N	use	is	normally	boosted	in	

continuous	corn	to	compensate	for	reduced	yield	relative	to	corn	in	a	corn/soybean rotation.		In	2010,	the	

last	year	for	which	USDA	data	are	available,	an	average	of	140	lbs./acre	of	nitrogen	fertilizer	were applied	to	

corn,	the	highest	rate	since	1964	(although	matched	in	1985).		See	“Table	10.		Nitrogen	used	on	corn,	rate	per	

fertilized	acre	receiving	nitrogen,	selected	States,”	accessible	from:	http://www.ers.usda.gov/dataproducts/fertilizer-use-and-price.aspx#.Up40LqVXaa4.n.		Corn	is	by	far	the	biggest	N	using	crop,	and	N	runoff	

generates	dead	zones	in	coastal	waters	while	N	fertilizer	also	contributed	substantially	to	global	warming	

through	conversion	to	nitrous	oxides,	potent	greenhouse	gases.	
24

Figure	5.	 2013	Updated	map	showing	the	general	areas	in	the	US	Corn	Belt	that	have	had	Cry3Bb1	fields	with	

heavy	damage	and/or	resistant	western	corn	rootworm	populations	(2009-2012).		Map	excerpted	from	BPPD	

(2013c).		CFS	has	amended	EPA’s	map to	show	(in	red)	towns	in	which	Monsanto	gave	“corn-on-corn	clinics”	

in	the	summer	of	2012.		See	http://www.genuity.com/corn/Pages/Corn-on-Corn-Clinics.aspx.

E. Volunteer	Herbicide-Resistant	Corn

Volunteers	are	crop	plants	that	sprout	from	unharvested	seed	to	infest	the	following	

season’s	crop	grown	on	the	same	field.		Harvesting	equipment	always	leaves	some	

proportion	of	the	crop	seed	in	the	field.		For	instance,	storms	and	plant	disease	often	cause	

corn	plants	to	topple,	leading	to	ears	of	corn	on	or	near	the	ground	that	are	then	missed	by	

harvesters.		Some	proportion	of	this	seed	will	find	conducive	conditions	to	sprout,	so	some	

level	of	volunteer	presence	is	an	inescapable	fact	of	farming.		Corn volunteers	can	be	a	

troublesome	weed	in	the	following	season’s	crop,	especially	soybeans,	dry	beans,	sugar	

beets	and	subsequent	corn	crops	(Bernards	et	al,	2010;	Davis,	2009;	Johnson	et	al,	2010;	

Stewart,	2011).		Two	to	four	volunteer	corn	plants	per	square	meter	can	reduce	yields	in	

soybeans	by	20%	(Morrison	2012).		

Volunteer	corn	not	only	reduces	yields,	it	can	act	as	a	host	plant	for	corn	rootworm	in	years	

when	corn	is	not	grown.		In	the	common	corn/soybean	rotation,	volunteer	corn	provides	a	

bridge	for	rootworm	populations	to	persist	in	the	soybean	years.		If	the	volunteer	corn	is	Bt	

Burlington,	CO

Norfolk,	NE

Spencer,	IA

Cascade,	IA
25

for	CRW,	it	could	also	accelerate	the	evolution	of	resistance,	especially	when	stacked	with	

an	herbicide	resistance	trait.

Krupke	et	al	(2009)	examined	volunteers	of	stacked	glyphosate-resistant/insect-resistant	

corn	emerging	in	follow-on	glyphosate-resistant	soybeans.		They	found	that	65%	of	the	

volunteers	tested	positive	for	Cry3Bb1,	and	that	60%	tested	positive	for	both	glyphosateresistance	and	Cry3Bb1.		Surprisingly, Cry3Bb1-positive	corn	volunteers	exhibited	the	

same	degree	of	root	damage	from	larval	rootworm	feeding	as	volunteers	that	tested	

negative	for	the	Cry3Bb1.		They	hypothesized	that	these	volunteers	produce	lower,	nonlethal	levels	of	Cry3Bb1	due	to	deficient	nitrogen	in	soybean	fields	that	are	not	amended	

with	this	nutrient (as	corn	fields	are).		Whatever	the	reason,	exposure	of	corn	rootworm	to	

low	levels	of	Cry3Bb1	in	corn	volunteers	has likely	accelerated evolution	of	resistance	and	

helped	undermine insect	resistance	management	efforts.

Corn	volunteers	have	become	an	increasingly	problematic	weed	in	their	research	area	

(Indiana)	and	throughout	the	Corn	Belt	because	glyphosate-only	weed	control	programs	

with	Roundup	Ready	soybeans	fail	to	control	glyphosate-resistant/Bt	corn	volunteers	in	

common	soy/corn	rotations.		Krupke	et	al	conclude	that	“weedy	volunteer	corn	plants	

stacked	with	GR	[glyphosate-resistance]	and	Bt	traits	may	accelerate	the	development	of	

Bt-resistant	WCR	[western	corn	rootworm]	populations,	circumventing	the	current	[Bt	

insect-resistance]	management	plans.”		In	continuous	GR/Bt	corn managed	with	

glyphosate,	GR/Bt	corn	volunteers	producing	lower,	resistance-promoting	levels	of	

rootworm	toxin	would	be	still	more	likely	to	escape	control than	in	soybeans,	since	harder	

to	distinguish	as	volunteers	in	a	field	of	corn.

In	2013,	only	5%	of	U.S.	corn	acres	were	Bt	only,	versus	71%	stacked	with	both	Bt	and	

herbicide	resistance,23 giving	a	sense	of	the	scope	of	this	problem.		And	the	CRW	resistance	

risks	posed	by	volunteer	corn	will	only	increase	with	the	introduction	of	multiple	

herbicide-resistant/Bt corn	varieties that	are	still	more	difficult	to	control	than	those	with	

the	Roundup	Ready	trait	alone.		Already,	SmartStax	corn	volunteers	(which	incorporate	

both	glyphosate	and	glufosinate	resistance)	have	been	noted	as	more	problematic	weeds	

than	GR	corn	volunteers,	especially	in	corn-on-corn	rotations	(Brooks	2012,	Morrison	

2012).	 Recommended	control	practices	for	such	dual-HR	corn	volunteers	are	a	preemergence	application	of	a	paraquat-atrazine	mixture,	or	post-emergence	use	of	inter-row	

cultivation	(USDA	APHIS	2013,	p.	37).		Neither	paraquat	(applied	to	just	1%	of	corn	acres	in	

201024)	nor	inter-row	cultivation	are	used	much	in	corn;	thus	many	growers	would	likely	

leave	such	volunteers	uncontrolled.	

Dow	AgrosSciences	is	awaiting	deregulation	of	GE	corn	resistant	to	2,4-D	and	“fops”	grass	

herbicides,	which	would	be	stacked	with	glyphosate-resistance.

25		Monsanto	is	developing	

																																																							 23 See	http://www.ers.usda.gov/data-products/fertilizer-use-and-price.aspx#.Up40LqVXaa4. 24 USDA	National	Agricultural	Statistics	Service	data,	accessible	at	

http://www.nass.usda.gov/Data_and_Statistics/PreDefined_Queries/2010_Corn_Upland_Cotton_Fall_Potatoes/index.asp. 25 Dow’s	corn	is	engineered	to	produce	an	aryloxyalkanoate dioxygenase-1	enzyme	(AAD-1)	that	confers	

high-level	resistance	to	both	phenoxy	auxin	herbicides	like	2,4-D	as	well	as	the	aryloxyphenoxyproprionate	
26

corn	resistant	to	the	herbicides	dicamba,	glufosinate and	glyphosate,	as	well	as	“FOPSTolerant	corn”	that	would	also	be	resistant	to	glyphosate.26		“Fops”	herbicides	like	

quizalofop	are	often	used	to	kill	volunteer	corn	in	soybeans;	that	option	would	be	

eliminated	with	these new	multi-herbicide-resistant	crops.		Big	Biotech	firms	frequently	

cross-license	their	traits,	which	could	easily	lead	to	corn,	and	hence	volunteer	corn,	with	

resistance	to	four	or	more	different	classes	of	herbicide.		For	example,	USDA	recently	

deregulated	a	DuPont-Pioneer	GE	corn	with	dual	resistance	to	glyphosate	and	glufosinate.		

DuPont-Pioneer	suggested	it	might	be	combined	with	Dow’s	2,4-D	and	”fops” resistance	for	

quad-resistant	corn (DuPont-Pioneer	2012,	pp.	78-79).		A	patent	awarded	to	DuPont	

envisions	corn	and	other	crops	resistant	to	seven	or	more	different	classes	of	herbicide

(DuPont-Pioneer	2009,	par.	33).

Volunteer	corn	control	options	diminish	as	the	number	of	herbicide-resistance	traits rises.		

Corn	volunteers	with	multiple	resistance	to	glyphosate,	glufosinate,	dicamba,	“fops”	and/or	

other	herbicides	would	be	more	likely	to	survive,	and	if	stacked	with	rootworm	Bt,	select	

for	CRW	resistance	to	the	Bt	toxin.		While	Krupke’s	work	involved	Bt	corn	expressing	

Monsanto’s	Cry3Bb1,	it	is	quite	possible	volunteers	of	other	HR/Bt	corn	types	would	

express	similarly	low	levels	of	rootworm	toxin	and	also	foster	resistance.	

III. Conclusion

EPA	is	rightly	proud	of	the	mandatory	insect	resistance	management	plans	it	established	

for	cultivation	of	Bt	crops	targeting	lepidopteran	pests.		The	Agency	heeded	the	warnings	

and	recommendations	of	independent	entomologists,	and	prevailed	over	considerable	

opposition	from	industry.		IRM	for	Bt	crops	represented	the	first	time,	to	our	knowledge,	

that	EPA	imposed constraints	on	the	use	of	a	class	of	less	harmful	pesticides to	preserve	

their	efficacy	and	so	forestall	the	use	of	more	toxic	pesticides that	would	ensue	in	the	event	

that	resistance	to	the	former	emerges.		Because	IRM	for	this	class	of	Bt crops	has	been	

scientifically	sound,	it	has	succeeded	in	largely	forestalling	any	significant	resistance	in	

above-ground	pests.

In	contrast,	EPA’s	IRM	for	rootworm	Bt	has	been	thoroughly	ineffective.		CFS	sees	several	

reasons	for	EPA’s	failure.

The	IRM	concepts	and	modeling	that	EPA	and	entomologists	developed	for	lepidopteran	Bt	

are	in	many	respects	inapplicable	to	rootworm	Bt,	yet	EPA	appears	unwilling	to	fully	accept	

the	implications.		Lepidopteran	Bt	corn	delivers a	high	dose	to	kill	over	99.99%	of	pests	

that	exhibit	recessive,	high-level	resistance	to	Bt	toxins.		Corn	rootworm	Bt	delivers	a	low	

dose	to	kill	a	relatively	low	percentage	of	pests	that	exhibit	non-recessive,	lower-level	

																																																																																																																																																																																		

(“fops”)	class	of	ACCase	inhibitor	herbicides,	such	as	quizalofop	and	cyhaolfop.		For	more	on	this	crop,	see	CFS	

comments	to	EPA	at	http://www.centerforfoodsafety.org/files/cfs-24-d-comments-to-epa-final-6-22-12.pdf.		

Dow’s	corn	is	pending	deregulation	(approval for	commercial	cultivation)	by	USDA.		See	petition	09-233-01p	

at	http://www.aphis.usda.gov/biotechnology/petitions_table_pending.shtml

26 See	http://www.monsanto.com/products/Pages/corn-pipeline.aspx,	last	visited	12/3/13.
27

resistance	to	Bt	toxins.	 While	the	difference	between	resistance	and	susceptibility	to	Bt	

toxins	is	a	“bright	line”	in	European	corn	borer, the	distinction	is	muddier	for	CRW.		

Industry	has	exploited	the	less	clear-cut nature	of	Bt	resistance	in	CRW	to deny	the	obvious	

fact	that	it	has	developed (Philpott	2011), and	so	avoid	serious	remedial	actions	that	might	

involve	reduced	sales	of	its	products.

EPA	must	adopt	a	more	expansive	definition	of	resistance	that	aims	foremost	at	reducing	

the	current	high	rate	of	false	negative	resistance	assessments	that	are in	large	part	

responsible	for	emerging	resistance.		The	definition	must	include	“partially	resistant”	CRW.		

We	remind	EPA	that	with	its	current	IRM	plans,	it	has	failed	to	stem	resistance; and	so	

failed	to	fulfill	its	statutory	mandate	of	preventing	the	unreasonable	adverse	effects	on	the	

environment	that	are	caused	by	sharply	increased	use	of	organophosphate	insecticides	to	

kill	Bt-resistant	CRW.

EPA’s	failure	is	due	in	large	part	to	undue	reliance	on	industry.		In	contrast	to	its	

formulation	of	IRM	plans	for	lepidopteran Bt	corn,	EPA	has	consistently	privileged	industry	

assessments	and	views	over	independent	science	in	developing	IRM	for	corn	rootworm.		As	

noted	above,	on	at	least	two	occasions	EPA	has	explicitly	rejected	the	recommendations	of	

Scientific	Advisory	Panels	(SAP	2002,	SAP	2009)	and	instead	allowed	itself	to	be	led	by	

faulty	industry	assessments	biased	by	self	interest (in	setting	deficient	refuge	

requirements).		EPA	has	also	flaccidly	accepted	industry’s	“blame-the-farmer”	excuses	for	

resistance.		EPA	made	a	major	regulatory	blunder	(20%	refuge	for	Cry3Bb1	corn)	based	in	

part	on	industry-inspired	speculation	that	farmers	wouldn’t	comply	with	a	50%	refuge,	and	

like	industry	has	often	used	putative	farmer	“non-compliance”	as	an	excuse	for	rejecting	

scientific	IRM	in	favor	of	expedient	but	ineffective	IRM	plans.

EPA	must	fully	comprehend	that	seed	firms	have	not	been	good-faith	partners in	IRM	

efforts,	and	act	accordingly.		Since	effective	IRM	must	involve	reducing	selection	pressure,	

which	entails	reduced	product	deployment,	sales	and	hence	profits,	industry’s	financial	

self-interest	is	directly	opposed	to	IRM. This	self-interest	skews	industry	science,	making	it	

unreliable	as	the	basis	for	regulatory	decision-making.		This	is	demonstrated	by	the	bottom	

line	measure	of	rapidly	emerging	resistance	that	has	occurred	with	use	of	industryfashioned	IRM	plans.		One	may	also	refer	to	the	lengthy	critique	of	Lefko	et	al	(2008) – a	

study	by	DuPont-Pioneer	scientists	that	formed	the	basis	of	DuPont’s	request	for,	and	EPA’s	

grant	of,	reduced	refuge	requirements	for	an	RIB	version	of	Cry34/35Ab1	corn	– by	

independent	scientists	in	SAP	(2009).		Neither	have	seed	firms	proven	reliable	in	terms	of	

IRM	practice,	as	evidenced	by	the	many	deficiencies	in	Monsanto’	resistance	monitoring	

(BPPD	2011).		EPA	should	return	to	its	former	course	of	accepting	and	following	the	

recommendations	of	its	independent	experts.

Bt	corn	developers	have	consistently	opposed	and	weakened	resistance	prevention efforts,	

but	have	understandably	proven	much	more	willing	to	engage	in	profitable	forms	of	

resistance	management.		For	instance,	Monsanto	prevailed	upon	EPA	to	set	a	thoroughly	

inadequate	20%	refuge	for	MON863,	substantially	accelerating	evolution	of	Cry3Bb1	

resistance	in	CRW.		Now	that	resistance	has	emerged,	Monsanto	is	eagerly exploiting it	as	

an opportunity	to	market	SmartStax corn,	particularly	as	a	tool	to	facilitate the	resistance-
28

promoting	and	generally	detrimental	agronomic	practice	of	corn-on-corn;	continuous	

SmartStax	corn,	however,	will	accelerate	the	evolution	of	additional	resistance	(to	

Cry34/35Ab1).	 While	eager	to	promote these	profitable	forms	of	short-term	resistance	

management,	industry	makes	less	profitable	but	more	effective	tactics	(e.g. periodic	use	of	

non-Bt	corn)	much	more	difficult	for	farmers	to	implement	by	slashing	their	offerings	of	

high-quality	conventional	corn	seed.		Resistance	prevention must	take	center	stage	as	EPA	

moves	to	reform	IRM.

None	of	this	is	inevitable.		While	biotech-seed	firms	(like	most	others)	will	normally	act	to	

maximize	their	financial	self-interest,	it	is	not	inconceivable	that	they	might	pursue	more	

responsible	paths	that	sacrifice	some	profit	if	prodded	by	proactive	regulators.		In	this	

context, seed	firms should	implement	a	mandatory	resistance	management	plan	for	all	lowdose	rootworm-active	Bt	corn	events	(which	includes	today’s	pyramids)	as	part	of	the	

technology	use	agreement	that	farmers	sign	upon	seed	purchase.		The	IRM	plan	would	

require	that	farmers	grow	the	Bt	corn	in	rotation	with	another	crop	(e.g.	soybeans)	or	with	

non-Bt	corn.		The	Bt	corn	would	have	to	be	rotated	every	other	year,	or	perhaps	(to	permit	

greater	flexibility) planted no	more	than	two	years	of	every	four.		Seed	firms	should	also	

drop	their	efforts	to	zero	out	refuge	requirements,	and	scale	up	production	of	high-quality	

conventional	seeds.

There	is	precedent	for	such	an	approach.		As	part	of	its	stewardship	program	for	its	

herbicide-resistant,	Clearfield	wheat,	BASF	requires	that	growers	abstain	from	growing	it,	

and	from	applying	the	associated	herbicides	(imidazolinones),	more	than	two	of	every	four	

years	(OSU	2010).		The	goal	is	to	deter	the	emergence	of	resistant	weeds	and	so	prolong	

the	effective	life	of	the	herbicide-resistance	trait	through	restraints	on	its	use27 – precisely	

analogous	to	the	purpose	of	IRM	for	Bt	crops.

There	is	also	precedent	for	a	proactive	regulatory	stance	by	EPA.		One	model	is	the	

comprehensive	IRM	program	for	Bt	cotton	that	was	successfully	implemented	by	

Australian	regulators	in	collaboration	with	industry.		With	more	respect	for	science	and	

law,	and	the	requisite	political	will,	EPA	could	even	now	redress	the	huge	deficiencies	in	its	

IRM	program.	 If	decisive	action	is	not	taken	soon,	however,	EPA	and	industry	will	have	

squandered	the	valuable	resource	of	rootworm-active	Bt	toxins.

																																																							 27 This	example	should	not	be	misconstrued	as	CFS	endorsement	of	Clearfield	wheat,	only	the	concept	of	

reducing	selection	pressure	for	resistance	through	restraints	on	use.		CFS	opposes	herbicide-resistant	crops	

(however	they	are	developed,	via	genetic	engineering,	mutagenesis	or	conventional	breeding)	because	they	

foster	greater	use	of	and	dependence	on	often	harmful	pesticides,	and	increase	selection	pressure	for	

resistant	weeds.		In	the	case	of	Clearfield	wheat,	one	clear	harm	of	the	associated	class	of	herbicides	

(imidazolinones)	is	that	they	increase	the	risk	of	bladder	and	_____	cancer	in	farmers	exposed	to	them.
29

IV. Recommendations

1) Establish	a	simple,	single-criterion	definition	of	resistance	along	the	lines	

discussed	above	(comments	on	Question	4)	that	reduces	as	much	as	possible	the	

potential	for	false	negative	resistance	assessments

2) Increase	refuge	requirements	for	all	rootworm-active	Bt	corn	events	as	

recommended	by	Tabashnik	&	Gould	(2012)	– 50%	for	single-toxin	Bt	corn	and	

20%	for	pyramids	– with	phase-in	as	needed	allow	for	seed	firms	to	multiply

sufficient quantities	of	needed	seeds

3) Mandatory	IRM	involving	rotation	away from	rootworm	Bt	corn

4) EPA	should	increase	the	role	of	independent	scientists	and	reduce	that	of	seed	

firms	in	every	aspect	of	IRM	– for	instance,	resistance	monitoring,	diagnostic	

assays,	definition	of	resistance,	and	setting	of	refuge	size	requirements	– in	light	

of	seed	firms’	failure	to	successfully	detect	and	notify	EPA	of	the	emergence	of	

resistant CRW.

5) EPA	should	make	publically	available	the	resistance	monitoring	data	reported	to	

it by	industry,	and/or	provide	complete	and	standardized	descriptions	of	it	in	

relevant	documents	released	to	the	public,	in	particular	the	number	of	

unexpected	damage/resistance	reports	broken	down	by	state	and	county.

V. References

Bernards,	M.,	Sandell,	L.,	&	Wright,	B.	(2010).	Weed	Science:	Volunteer	Corn	in	Soybeans.	

University	of	Nebraska-Lincoln	Extension,	Lincoln,	NE.

BPPD (2011).	 BPPD	Review	of	Reports	of	Unexpected	Cry3Bb1	Damage,	Monsanto’s	2009	

Corn	Rootworm	Monitoring	Report,	and	Revised	Corn	Rootworm	Resistance	Monitoring	

Plan	for	MON	88017,	MON	88017	x	MON	810,	MON	863,	MON	863	x	MON810,	MON	89034	

x	TC1507	x	MON	88017	x	DAS-59122-7,	and	MON	89034	x	MON	88017.	 Memorandum	

from	J.C.	Martinez	to	M.	Mendelsohn,	dated	November	22,	2011.

BPPD (2012).	 BPPD	IRM	Team	review	of	Monsanto’s	2010	corn	rootworm	monitoring	

data,	unexpected	damage	reports	for	Cry3Bb1	expressing	Bt	Corn	and	academic	reports	of	

Cry3Bb1	field	failures	as	well	as	corn	rootworm	resistance.	 Memorandum	from	J.C.	

Martinez	and	A.	Reynolds	to	A.	Sibold,	dated	October	11,	2012.
30

BPPD (2013a).	 Review	of	Corn	Rootworm	Resistance	Monitoring	Submissions	and	Data	for	

Bt	corn	products	containing	Cry34/35Ab1.	Memorandum	from	A.	Reynolds	to	A.	Sibold,	

dated	March	20,	2013.

BPPD (2013b).	 Review	of	Corn	Rootworm	Resistance	Monitoring	Submissions	and	Data	for	

Bt	corn	products	containing	mCry3A.	Memorandum	from	A.	Reynolds	to	A.	Sibold,	dated	

May	15,	2013.

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