Evaluation of Foliar Damage by Spodoptera frugiperda (Lepidoptera: Noctuidae) to

Genetically Modified Corn (Poales: Poaceae) in Mexico

Author(s): Luis A. Aguirre , Agustín Hernández-Juàrez , Mariano Flores , Ernesto Cerna , Jerónimo
Landeros , Gustavo A. Frías and Marvin K. Harris
Source: Florida Entomologist, 99(2):276-280.
Published By: Florida Entomological Society
DOI: http://dx.doi.org/10.1653/024.099.0218
URL: http://www.bioone.org/doi/full/10.1653/024.099.0218

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 Evaluaion of foliar damage by Spodoptera frugiperda
(Lepidoptera: Noctuidae) to geneically modiied corn
(Poales: Poaceae) in Mexico
Luis A. Aguirre1,*, Agustín Hernández-Juàrez1, Mariano Flores1, Ernesto Cerna1,
Jerónimo Landeros1, Gustavo A. Frías1, and Marvin K. Harris2

Abstract
The fall armyworm, Spodoptera frugiperda Smith & Abbot (Lepidoptera: Noctuidae), is a key pest of corn, Zea mays L. (Poales: Poaceae), in Mexico.
The development of geneically modiied (GM) corn hybrids for resistance to this insect, with the inclusion of several genes coding for proteins
Cry1Ab, Vip3Aa20, and mCry3A of Bacillus thuringiensis Berliner (Bacillales: Bacillaceae) (Bt), ofer an alternaive to convenional insecicides to con-
trol this pest. Resistance to fall armyworms of the GM corn hybrids Agrisure 3000 GT, Agrisure Viptera 3110, and Agrisure Viptera 3111 was evaluated
in 4 locaions at Sinaloa for a 3 yr period. Damage evaluaion showed that the maize hybrids with the Bt gene inserion were not afected by the fall
armyworm as compared with their respecive isolines, which were seriously damaged. The results reairm the insect control beneits provided by
this technology and provide a baseline for resistance management.

Key Words: Bacillus thuringiensis; δ-endotoxin; fall armyworm; leaf damage

Resumen
El gusano cogollero Spodoptera frugiperda Smith & Abbot (Lepidoptera: Noctuidae), es la plaga de mayor importancia económica del maíz Zea mays
L. (Poales: Poaceae) en México. El desarrollo de híbridos de maíz genéicamente modiicados para resistencia a este insecto, con la inserción de
diversos genes que codiican para las proteínas Cry1Ab, Vip3Aa20 y mCry3A de Bacillus thuringiensis Berliner (Bacillales: Bacillaceae) (Bt), ofrecen
una alternaiva a los insecicidas convencionales de control de esta plaga. Se evaluó durante tres años, el daño foliar del gusano cogollero en maíz
GM con los híbridos Agrisure 3000 GT, Agrisure Viptera 3110 y Agrisure Viptera 3111 en cuatro localidades del estado de Sinaloa. La evaluación del
daño demostró que el maíz con la inserción de genes de Bt son eicaces para contrarrestar o no ser afectado por el daño provocado por la plaga,
en comparación con sus respecivas líneas convencionales que fueron seriamente dañadas. Los resultados reairman los beneicios del control de
insectos que ofrece esta tecnología y proporciona una línea base para el manejo de la resistencia.

Palabras Clave: Bacillus thuringiensis; δ-endotoxina; gusano cogollero; daño foliar

The fall armyworm, Spodoptera frugiperda Smith & Abbot (Lepi- The development of new control techniques led to the elabo-
doptera: Noctuidae), is indigenous to the American coninent (Sena ration of genetically modified corn hybrids expressing a Bacillus
et al. 2003) and has been reported to infest 186 host plant species in thuringiensis Berliner (Bacillales: Bacillaceae) (Bt) crystal protein
North and Central America (Casmuz et al. 2010). Corn, Zea mays L. that, when consumed by lepidopterous larvae, proved fatal to the
(Poales: Poaceae), is the primary host of economic importance wher- European corn borer, Ostrinia nubilalis Hübner (Lepidoptera: Cram-
ever it is grown in Mexico (Sena et al. 2003). Tropical and subtropical ar- bidae), the southwestern corn borer, Diatraea grandiosella Dyar
eas are most seriously afected (Ortega 1987; Rodríguez & Marín 2008) (Lepidoptera: Crambidae), the sugarcane borer, Diatraea sacchara-
with losses incurred from post-emergence to maturity (Ortega 1987). lis (F.) (Lepidoptera: Crambidae), the corn earworm, Helicoverpa
Yield losses over 30% are common (Herrera 1979; García-Guiérrez et zea Boddie (Lepidoptera: Noctuidae), and S. frugiperda (Abel et al.
al. 2012), and in some cases total crop loss occurs (Silva-Aguayo et al. 2000; Castro et al. 2004). A pyramided strategy that combines 2
2010). or more Bt genes deployed in the same corn plant is now used to
A reliance on chemical control to manage pest populaions has conserve insecticidal efficacy (Burkness et al. 2010; Niu et al. 2013;
become increasingly inefecive as S. frugiperda now expresses resis- Yang et al. 2013). Genetically modified corn (GM) hybrids with Bt
tance to several toxicological groups of insecicides (Georghiou & Mel- genes have also been developed to resist a wider range of pests
lon 1983; Yu 1991; Pacheco-Covarrubias 1993; Morillo & Notz 2001; within Lepidoptera and Coleoptera (Buntin et al. 2004a,b; Buntin
Yu et al. 2003). 2008; Duan et al. 2008; Hardke et al. 2011). These hybrids support a

1
Universidad Autónoma Agraria Antonio Narro, Departamento de Parasitología, Calzada Antonio Narro 1923, Buenavista, Salillo, Coahuila, 25315, México
2
Texas A&M University, Department of Entomology, College Staion, Texas 77843, USA
*Corresponding author; E-mail: [email protected]

276 2016 — Florida Entomologist — Volume 99, No. 2

Aguirre et al.: Leaf damage by Spodoptera frugiperda in Bt corn 277
pest management strategy in modern agriculture (Fernandes et al. avoid cross-pollinaion with non-GM hybrids in accordance with gov-
2007), although concerns from an economic, scientific, and social ernment regulaions for ield tests with GM corn (Halsey et al. 2005;
standpoint remain in Mexico. LBOGM 2005).
Mexico is the center of origin of over 61 naive races of corn (Reyes Three Bt corn hybrids (AgrisureTM 3000 GT with Cry1Ab and mCry3A
1990; Matsuoka 2005; CONABIO 2006; Kato et al. 2009), and there is proteins; Agrisure® VipteraTM 3111 with Cry1Ab, Vip3Aa20, and
concern that GM corn could jeopardize those races (Kato-Yamakake mCry3A; and Agrisure® VipteraTM 3110 with Cry1Ab and Vip3Aa20)
2004; Serratos-Hernández et al. 2004; Turrent et al. 2010); however, were used in this research and compared with their respecive non-GM
Baltazar et al. (2015) suggest that measures such as spaial isolaion isolines provided by Syngenta Agro S.A de C.V. de México (San Lorenzo
could minimize contaminaion risks. More informaion is needed in 1009, Primer Piso, Colonia Del Valle, 03100, México, D.F.). The irst two
Mexico to validate if the Bt Cry proteins of GM corn are efecive in hybrids are resistant to Lepidoptera and Coleoptera and the last one is
controlling the crop pests under various environmental condiions be- resistant to Lepidoptera.
yond those reported by Aguirre et al. (2015a) to control corn earworm A randomized complete block design was used in each locality and
in the state of Sinaloa and by Aguirre et al. (2015b) to control S. frugi- date. In 2011, Agrisure 3000 GT and Agrisure Viptera 3110, plus their
perda in the state of Tamaulipas. Thus, the objecive of this study was isolines, were planted at Oso Viejo. In addiion, each variety had a cor-
to evaluate foliar damage in corn hybrids with Cry1Ab, Vip3Aa20, and responding treatment that included a foliar insecicide control (see
mCry3A toxins from B. thuringiensis to control S. frugiperda larvae in Table 1). There were 4 replicate blocks per treatment, and they were
Sinaloa, Mexico, during 3 growing seasons. planted on 28 Jan. In 2012, Agrisure Viptera 3111 and Agrisure 3000 GT
hybrids, with and without insecicide treatments, were planted on 15
Feb at Navolato. Agrisure Viptera 3111 was planted at El Dorado on 19
Materials and Methods Feb, also with and without insecicide applicaions (see Table 1). Only
3 replicates were planted in these areas. In 2013, Agrisure Viptera 3111
Research was conducted at Oso Viejo, El Dorado, and Camalote was planted at Camalote and Oso Viejo on 14 and 15 March, respec-
in the city of Culiacan and the city of Navolato, both in the state of ively, with 3 treatments (GM hybrid, isoline, isoline plus insecicide)
Sinaloa, during the 2011–2013 fall–winter growing seasons. Plots were and 4 replicates (see Table 1). In addiion, experimental plots during
planted under biosafety condiions, isolated at least 500 m from com- the 3 yr period received an insecicide treatment for S. frugiperda if
mercial corn plots and planted at least 21 d later than recommended to plants less than 20 cm tall reached a 10% infestaion level, or plants 20

Table 1. Insecicide treatments used to evaluate leaf damage by fall armyworms in geneically modiied (GM) corn during 2011–2013 fall–winter growing seasons
in localiies of Culiacan and Navolato, Sinaloa, Mexico.

Year Hybrida Locality Insecicideb,c

2011 Agrisure 3000 GT Oso Viejo without insecicide applicaion
Agrisure 3000 GT + ic Oso Viejo permethrin—lambda cyhalothrin—emamecin benzoate
Isoline + ic Oso Viejo permethrin—lambda cyhalothrin—emamecin benzoate
Isoline Oso Viejo check
Agrisure Viptera 3110 Oso Viejo without insecicide applicaion
Agrisure Viptera 3110 + ic Oso Viejo permethrin—lambda cyhalothrin—emamecin benzoate
Isoline + ic Oso Viejo permethrin—lambda cyhalothrin—emamecin benzoate
Isoline Oso Viejo check
2012 Agrisure Viptera 3111 El Dorado without insecicide applicaion
Agrisure Viptera 3111+ ic El Dorado permethrin—lambda cyhalothrin—emamecin benzoate
Isoline + ic El Dorado permethrin—lambda cyhalothrin—emamecin benzoate
Isoline El Dorado check
Agrisure Viptera 3111 Navolato without insecicide applicaion
Agrisure Viptera 3111 + ic Navolato permethrin—lambda cyhalothrin—emamecin benzoate
Isoline + ic Navolato permethrin—lambda cyhalothrin—emamecin benzoate
Isoline Navolato check
Agrisure 3000 GT Navolato without insecicide applicaion
Agrisure 3000 GT + ic Navolato permethrin—lambda cyhalothrin—emamecin benzoate
Isoline + ic Navolato permethrin—lambda cyhalothrin—emamecin benzoate
Isoline Navolato check
2013 Agrisure Viptera 3111 Camalote without insecicide applicaion
Isoline + ic Camalote emamecin benzoate
Isoline Camalote check
Agrisure Viptera 3111 Oso Viejo without insecicide applicaion
Isoline + ic Oso Viejo emamecin benzoate
Isoline Oso Viejo check
a
ic = insecicide control
b
check = isoline without insecicide applicaion
c
Insecicides were applied at the following rates: permethrin, 400 mL/ha; lambda cyhalothrin, 500 mL/ha; emamecin benzoate, 200 mL/ha.
278 2016 — Florida Entomologist — Volume 99, No. 2
cm or taller reached a 20% infestaion level, at the rate of 2 applica- insecicide treatment, showed litle foliar damage (<1.4 on the Davis
ions per year (Table 1). scale) and few injured plants, with some plants with pinholes and only
Each experimental plot consisted of 10 rows, each 5 m long, 13.3% of plants injured in the Agrisure 3000 GT treatment. The isolines
with 0.8 m between rows with a 40 to 50 seed planting density. The of the GM hybrids were signiicantly diferent, with 52.2 to 81.1% of
seedlings were later thinned to 34 plants per row. The experimental plants injured and plant damage that varied from 2.89 to 4.97 on the
plot was surrounded with a buffer area of 6 rows of convention- Davis scale, including large holes and long leaf lesions (Table 3).
al corn, and other buffer areas were planted between replicates, In 2013, Agrisure Viptera 3111 did not show feeding signs by S.
which were planted the same time as the experimental material frugiperda at any of the test sites, whereas the isolines were heavily
as required by official regulations. Agricultural management of the infested including those in which chemical control was applied. Foliar
plot followed the technical guide for corn growers developed by the injury was 1.72 to 3.22 on the Davis scale and 35.8 to 74.2% of plants
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecu- injured, including large lesions (Table 4).
arias (INIFAP 2010).
Foliar damage under natural infestaion by fall armyworms was
evaluated by sampling 10 plants randomly in the 4 central rows at V6– Discussion
V8 (2011), and V2–V4, V6–V8, and V10–V12 (2012 and 2013) pheno-
logical stages of the plant. A numerical scale (1–9), also known as the
Agrisure 3000 GT, Agrisure Viptera 3110, and Agrisure Viptera 3111
Davis scale, was used to evaluate foliar feeding damage (Davis et al.
hybrids were resistant to S. frugiperda as compared with their severely
1989, 1992; Mihm 1983) ranging from 1 = no foliar damage (highly
injured respecive isolines during the 3 yr research study in the Sinaloa
resistant) to 9 = severe foliar damage (totally suscepible).
corn-growing areas. These results are similar to those found by Aguirre
PROC ANOVA and Tukey’s muliple rank test (P < 0.05) were used to
et al. (2015b), tesing the same Bt hybrids in the state of Tamaulipas.
compare among treatments. SAS/STAT (SAS version 9.0; SAS Insitute,
Also, Piña & Solleiro (2013) indicated that experimental tests of GM
Cary, North Carolina) sotware was used to analyze the percentage of
corn in various areas of Mexico are consistently eicacious in control-
injury to plants injured and the damage raings (Davis scale).
ling key pests.
This research showed that use of GM Bt corn hybrids provides
Results season-long protecion from S. frugiperda. In contrast, chemical con-
trol only protects the plant when the insecicide residue is present,
Geneically modiied hybrids at Oso Viejo in 2011 did not show sig- and a failure in iming of applicaion(s) represents a risk in control
niicant (P > 0.05) damage by fall armyworms. The isolines with inseci- eicacy. Piña & Solleiro (2013) reported that protecing non-Bt corn
cide treatment also had low damage scores, 1.85 and 1.22 (Davis scale) in several areas of Mexico from infestaions of corn earworms and fall
for Agrisure 3000 GT and Agrisure Viptera 3110, respecively, with only armyworms required from 3 to 5 insecicide applicaions per season,
some pinhole feeding marks on leaves and no signiicant diferences and from 720 g to 3.6 kg of acive ingredient per ha. In addiion, re-
between treatments (P > 0.05). In contrast, isolines without chemical searchers in other countries reported similar results of Bt corn with
treatment had an average of damage score of 4.20 in both hybrids, the Cry1Ab toxin for controlling the fall armyworm with respect to
which possessed large holes and long lesions on leaves. Spodoptera convenional hybrids with and without insecicide control (Bunin et
frugiperda did not damage Agrisure Viptera 3110 and Agrisure 3000 al. 2001, 2004a,b; Bunin 2008; Hardke et al. 2011; Huang et al. 2011;
GT with insecicide treatment, and 5.0% of plants were damaged in Ríos-Díez et al. 2012).
the later without treatment. The non-GM hybrids displayed damaged Hybrids with the Bt toxin used in this research consistently demon-
plants from 15.0 to 90.0%, including those in which chemical control strated reducion in foliar damage. However, in all areas tested, Agri-
was used (Table 2). sure 3000 GT displayed more injured plants and larger lesion size than
At El Dorado and Navolato in 2012, results were similar to those in Agrisure Viptera 3110 and Agrisure Viptera 3111. The higher level of
2011. Agrisure Viptera 3111 and Agrisure 3000 GT, including those with damage is thought to be due to Agrisure 3000 GT having only 1 Bt toxin
(Cry1Ab) for Lepidoptera control, whereas the other tested hybrids
have 2 pyramided Bt genes. Muliple genes for resistance are thought
Table 2. Foliar damage and percentage of plants injured by fall armyworms on to provide beter resistance to the pest. Agrisure Viptera 3110 and
the geneically modiied hybrids Agrisure 3000 GT and Agrisure Viptera 3110 Agrisure Viptera 3111 have 2 toxins (pyramid events) for Lepidoptera
and their respecive isolines at Oso Viejo, Culiacan, Sinaloa, in 2011.
control, the δ-endotoxin Cry1Ab and the vegetaive insecicide protein
Vip3Aa20, which provide excellent protecion to the crop, not only
Hybrida Leaf damageb,c Plants injured (%)c
from S. frugiperda but also from other Lepidoptera (Burkness et al.
Agrisure 3000 GT 1.10 a 5.0 a 2010; Niu et al. 2013; Yang et al. 2013).
Agrisure 3000 GT + ic 1.00 a 0.0 a Planing dates of experimental plots were at least 21 d later than
Isoline + ic 1.85 a 30.0 b the recommended date in Sinaloa. This requirement was imposed by
Isoline 4.20 b 82.5 c regulatory authoriies in order to avoid cross pollinaion with conven-
F = 17.33*** F = 38.58*** ional corn in the area. This condiion put the experimental plots in this
Agrisure Viptera 3110 1.00 a 0.0 a research under high pest pressure, which came from surrounding corn
Agrisure Viptera 3110 + ic 1.00 a 0.0 a ields and sorghum ields. Despite this high level of pest pressure, the
Isoline + ic 1.22 a 15.0 b Bt toxin in the crop reduced the infestaion level and damage. If these
Isoline 4.20 b 90.0 c GM hybrids were planted on the recommended planing date under
F = 13.22*** F = 297.00*** opimal condiions to the crop, these Bt hybrids could be expected to
a
ic = insecicide control perform well. Such a corn pest management program would reduce
b
Mean numerical scale the use of chemical insecicides, allow the crop to beter express its
c
Geneically modiied hybrids and their respecive isolines followed by the same leter
do not difer signiicantly (ANOVA and Tukey’s test; P > 0.05). *** Indicates signiicant F geneic potenial, and conserve yield and grain quality by decreasing
value at P < 0.001, df = 3,15. foliar damage.
Aguirre et al.: Leaf damage by Spodoptera frugiperda in Bt corn 279
Table 3. Foliar damage and percentage of plants injured by fall armyworms on the geneically modiied corn hybrids Agrisure Viptera 3111 and Agrisure 3000 GT
and their respecive isolines at El Dorado and Navolato, Sinaloa, in 2012.

Hybrida Locality Leaf damageb,c Plants injured (%)c

Agrisure Viptera 3111 El Dorado 1.00 a 0.0 a
Agrisure Viptera 3111 + ic El Dorado 1.00 a 0.0 a
Isoline + ic El Dorado 3.53 b 64.4 b
Isoline El Dorado 2.89 b 56.7 b
F = 10.35*** F = 16.54***
Agrisure Viptera 3111 Navolato 1.07 a 1.1 a
Agrisure Viptera 3111 + ic Navolato 1.07 a 1.1 a
Isoline + ic Navolato 3.20 b 52.2 b
Isoline Navolato 4.90 c 81.1 c
F = 11.52*** F = 14.99***
Agrisure 3000 GT Navolato 1.34 a 13.3 a
Agrisure 3000 GT + ic Navolato 1.13 a 7.8 a
Isoline + ic Navolato 3.87 b 66.7 b
Isoline Navolato 4.97 b 77.8 b
F = 9.65*** F = 10.39***
a
ic = insecicide control
b
Mean numerical scale
c
Geneically modiied hybrids and their respecive isolines followed by the same leter do not difer signiicantly (ANOVA and Tukey’s test; P > 0.05). *** Indicates signiicant F value
at P < 0.001, df = 11,35.

Table 4. Foliar damage and percentage of plants injured by fall armyworms on the geneically modiied corn hybrid Agrisure Viptera 3111 and its respecive isoline
at Camalote and Oso Viejo, Culiacan, Sinaloa, in 2013.

Hybrida Locality Leaf damageb,c Plants injured (%)c

Agrisure Viptera 3111 Camalote 1.00 a 0.0 a
Isoline + ic Camalote 1.72 b 35.8 b
Isoline Camalote 3.22 c 74.2 c
F = 48.92*** F = 58.44***
Agrisure Viptera 3111 Oso Viejo 1.00 a 0.0 a
Isoline + ic Oso Viejo 1.80 b 39.2 b
Isoline Oso Viejo 2.63 c 62.5 c
F = 35.46*** F = 27.38***
a
ic = insecicide control
b
Mean numerical scale
c
Geneically modiied hybrid and the respecive isoline treatments followed by the same leter do not difer signiicantly (ANOVA and Tukey’s test; P > 0.05). *** Indicates signiicant
F value at P < 0.001, df = 8,35.

Acknowledgments low in maize: implicaions for isolaion requirements and coexistence in

Mexico, the center of origin of maize. PLoS One 10: e0131549.
Bunin GD. 2008. Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm
The authors would like to thank Syngenta Agro S.A de C.V. de Méxi- and corn earworm (Lepidoptera: Noctuidae) management in ield corn for
co for providing the geneic material that made this research possible. grain producion. Florida Entomologist 91: 523–530.
Bunin GD, Dewey LR, Wilson DM, McPherson RM. 2001. Evaluaion of Yieldgard
transgenic resistance for control of fall armyworm and corn earworm (Lepi-
References Cited doptera: Noctuidae) on corn. Florida Entomologist 84: 37–42.
Bunin GD, All JN, Lee RD, Wilson DM. 2004a. Plant-incorporated Bacillus
thuringiensis resistance for control of fall armyworm and corn earworm
Abel CA, Wilson RL, Wiseman BR, White WH, Davis FM. 2000. Convenional (Lepidoptera: Noctuidae) in corn. Journal of Economic Entomology 97:
resistance of experimental maize lines to corn earworm (Lepidoptera: Noc- 1603–1611.
tuidae), fall armyworm (Lepidoptera: Noctuidae), southwestern corn borer Bunin GD, Flanders KL, Lynch RE. 2004b. Assessment of experimental Bt events
(Lepidoptera: Crambidae), and sugarcane borer (Lepidoptera: Crambidae). against fall armyworm and corn earworm in ield corn. Journal of Economic
Journal of Economic Entomology 93: 982–988. Entomology 97: 259–264.
Aguirre LA, Hernández A, Flores M, Frías GA, Cerna E, Landeros J, Harris MK. Burkness EC, Dively G, Paton T, Morey AC, Hutchison WD. 2010. Novel Vip3A
2015a. Geneically modiied maize resistant to corn earworm (Lepidoptera: Bacillus thuringiensis (Bt) maize approaches high-dose eicacy against He-
Noctuidae) in Sinaloa, Mexico. Florida Entomologist 98: 821–826. licoverpa zea (Lepidoptera: Noctuidae) under ield condiions. GM Crops 1:
Aguirre LA, Hernández A, Flores M, Pérez-Zubiri R, Cerna E, Landeros J, Frías 337–343.
GA. 2015b. Comparación del nivel de daño de Spodoptera frugiperda (Lepi- Casmuz A, Juárez ML, Socías MG, Murúa MG, Prieto S, Medina S, Willink E,
doptera: Noctuidae) en plantas de maíz genéicamente modiicado y con- Gastaminza G. 2010. Revisión de los hospederos del gusano cogollero del
vencional en el Norte de México. Southwestern Entomologist 40: 171–178. maíz, Spodoptera frugiperda (Lepidoptera: Noctuidae). Revista de la Socie-
Baltazar BM, Castro EL, Espinoza BA, de la Fuente MJM, Garzón TJA, González dad Entomológica Argenina 69: 209–231.
GJ, Guiérrez MA, Guzmán RJL, Heredia DO, Horak MJ, Madueño MJI, Scha- Castro BA, Leonard BR, Riley TJ. 2004. Management of feeding damage and sur-
paugh WA, Stojšin D, Uribe MHR, Zavala GF. 2015. Pollen-mediated gene vival of southwestern corn borer and sugarcane borer (Lepidoptera: Cram-
280 2016 — Florida Entomologist — Volume 99, No. 2
bidae) with Bacillus thuringiensis transgenic ield corn. Journal of Economic LBOGM (Ley de Bioseguridad de Organismos Genéicamente Modiicados).
Entomology 97: 2106–2116. 2005. Diario Oicial de la Federación, 18 marzo 2005, México.
CONABIO (Comisión Nacional para el conocimiento y uso de la Biodiversidad). Matsuoka Y. 2005. Origin maters: lessons from the search for the wild ancestor
2006. Elementos para la determinación de centros de origen y centros de of maize. Breeding Science 55: 383–390.
diversidad en general y el caso especíico de la liberación experimental de Mihm JA. 1983. Eicient Mass-Rearing and Infestaion Techniques to Screen for
maíz transgénico al ambiente en México. Documento base preparado por la Host Plant Resistance to Fall Armyworm, Spodoptera frugiperda. Interna-
Coordinación Nacional de la CONABIO para la Secretaría de Medio Ambiente ional Maize and Wheat Improvement Center (CIMMYT), México, D.F.
y Recursos Naturales (SEMARNAT) y la Secretaría de Agricultura, Ganadería, Morillo F, Notz A. 2001. Resistencia de Spodoptera frugiperda (Smith) (Lepi-
Pesca y Alimentación (SAGARPA). México, D.F. htp://www.biodiversidad. doptera: Noctuidae) a lambdacihalotrina y metomil. Entomotropica 16:
gob.mx/genes/pdf/Doc_CdeOCdeDG.pdf (last accessed 10 Nov 2014). 79–87.
Davis FM, Williams WP, Wiseman BR. 1989. Methods used to screen maize for Niu Y, Meagher Jr RL, Yang F, Huang F. 2013. Suscepibility of ield populaions
and to determine mechanisms of resistance to the southwestern corn borer of the fall armyworm (Lepidoptera: Noctuidae) from Florida and Puerto Rico
and fall armyworm. In Proceedings, Toward Insect Resistant Maize for the to puriied Cry1F and corn leaf issue containing single and pyramided Bt
Third World. Internaional Symposium on Methodologies for Developing genes. Florida Entomologist 96: 701–713.
Host Plant Resistance to Maize Insects, 9–14 Mar 1987, Internaional Maize Ortega AC. 1987. Insectos nocivos del maíz: una guía para su ideniicación en
and Wheat Improvement Center (CIMMYT), México, D.F. el campo. Centro Internacional de Mejoramiento de Maíz y Trigo (CIMMYT),
Davis FM, Ng SS, Williams WP. 1992. Visual raing scales for screening whorl- México.
stage corn for resistance to fall armyworm. Mississippi Agricultural & For- Pacheco-Covarrubias JJ. 1993. Monitoring insecicide resistance in Spodoptera
estry Experiment Staion. Technical Bullein 186. frugiperda populaions from the Yaqui Valley, Son., Mexico. Resistant Pest
Duan JJ, Teixeira D, Huesing JE, Jiang C. 2008. Assessing the risk to nontarget Management, Newsleter 5: 3–4.
organisms from Bt corn resistant to corn rootworms (Coleoptera: Chryso- Piña S, Solleiro JL. 2013. México, pp. 341–408 In Solleiro RJL, Castañón IR [eds.],
melidae): ier-I tesing with Orius insidiosus (Heteroptera: Anthocoridae). Introducción al ambiente del maíz transgénico: Análisis de ocho casos en
Environmental Entomology 37: 838–844. Iberoamérica, México. AgroBio México y CambioTec, México.
Fernandes OA, Faria M, Marinelli S, Schmidt F, Ferreira CV, Moro G. 2007. Short- Reyes CP. 1990. El maíz y su culivo. AGT-EDITOR S.A., México.
term assessment of Bt maize on non-target arthropods in Brazil. Scienia Ríos-Díez JD, Siegfried B, Saldamando-Benjumea CI. 2012. Suscepibility of
Agricola (Piracicaba, Brazil) 64: 249–255. Spodoptera frugiperda (Lepidoptera: Noctuidae) strains from central Co-
García-Guiérrez C, González-Maldonado MB, Cortez-Mondaca E. 2012. Uso de lombia to Cry1Ab and Cry1Ac entotoxins of Bacillus thuringiensis. South-
enemigos naturales y biorracionales para el control de plagas de maíz. Ra western Entomologist 37: 281–293.
Ximhai 8: 57–70. Rodríguez DLA, Marín AJ. 2008. Insectos plaga y su control, pp. 29–46 In Rodrí-
Georghiou GP, Mellon RB. 1983. Pesicide resistance in ime and space, pp. 1–46 guez MR, De León C [eds.], El culivo del maíz. Temas selectos 1. Colegio de
In Georghiou GP, Saito T [eds.], Pest Resistance to Pesicides. Plenum Press, postgraduados, Mundi Prensa, México.
New York, New York. Sena Jr DG, Pinto FAC, Queiroz DM, Viana PA. 2003. Fall armyworm damaged
Halsey ME, Remund KM, Davis CA, Qualls M, Eppard PJ, Berberich SA. 2005. maize plant ideniicaion using digital images. Biosystems Engineering 85:
Isolaion of maize from pollen-mediated gene low by ime and distance. 449–454.
Crop Science 45: 2172–2185. Serratos-Hernández JA, Islas-Guiérrez F, Buendía-Rodríguez E, Berthaud J.
Hardke JT, Leonard BR, Huang F, Jackson RE. 2011. Damage and survivorship of 2004. Gene low scenarios with transgenic maize in Mexico. Environmental
fall armyworm (Lepidoptera: Noctuidae) on transgenic ield corn expressing Biosafety Research 3: 149–157.
Bacillus thuringiensis Cry proteins. Crop Protecion 30: 168–172. Silva-Aguayo G, Rodríguez-Maciel JC, Lagunes-Tejeda A, Landeral-Cázares C,
Herrera AJ. 1979. Principales Plagas del Maíz. Boleín Especial de la Dirección de Alatorre-Rosas R, Shelton AM, Blanco CA. 2010. Bioacivity of boldo (Peu-
Agricultura y Ganadería del Perú. mus boldus Molina) (Laurales: Monimiaceae) on Spodoptera frugiperda (J.
Huang F, Andow DA, Buschman LL. 2011. Success of the high dose/refuge re- E. Smith) and Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae). South-
sistance management strategy ater 15 years of Bt crops in North America. western Entomologist 35: 215–231.
Entomologia Experimentalis et Applicata 140: 1–16. Turrent FA, Cortés FJI, Espinosa CA, Mejía AH, Serratos HJA. 2010. ¿Es ventajosa
INIFAP (Insituto Nacional de Invesigaciones Forestales, Agrícolas y Pecuarias). para México la tecnología actual de maíz transgénico? Revista Mexicana de
2010. Centro de Invesigación Regional del Noreste (CIRNO). Campo Experi- Ciencias Agrícolas 1: 631–646.
mental Valle de Culiacán (CEVACU). Maíz, pp. 41–47 In Guía técnica para Yang F, Qureshi JA, Leonard BR, Head GP, Niu Y, Huang F. 2013. Suscepibility of
el área de inluencia del Campo Experimental Valle de Culiacán. Culiacán, Louisiana and Florida populaions of Spodoptera frugiperda (Lepidoptera:
Sinaloa, México. Noctuidae) to pyramided Bt corn containing Genuity® VT Double ProTM and
Kato TA, Mapes C, Mera LM, Serratos JA, Bye RA. 2009. Origen y diversiicación SmartStaxTM traits. Florida Entomologist 96: 714–723.
del maíz: una revisión analíica. Universidad Nacional Autónoma de México Yu SJ. 1991. Insecicide resistance in the fall armyworm, Spodoptera frugiperda
(UNAM), Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (J. E. Smith). Pesicide Biochemistry and Physiology 39: 84–91.
(CONABIO), México. Yu SJ, Nguyen SN, Abo-Elghar GE. 2003. Biochemical characterisics of inseci-
Kato-Yamakake TA. 2004. Variedades transgénicas y el maíz naivo en México. cide resistance in the fall armyworm, Spodoptera frugiperda (J. E. Smith).
Agricultura, Sociedad y Desarrollo 1: 101–109. Pesicide Biochemistry and Physiology 77: 1–11.