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Abstract

Spanish

The fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) is a polyphagous pest species of cultivated plants. Changes in cotton crop systems are increasing the importance of this pest in cotton in the El Cerrado region of Brazil. This work aimed to evaluate resistance types of cotton (Gossypium hirsutum) varieties by non-preference to oviposition and feeding along with antibiosis to S. frugiperda in the laboratory (27±2°C, 70±10% R.H. and photophase of 14 h). Two tests were performed to evaluate the non-preference to oviposition and feeding, one with free choice in a randomized block design and another in a completely randomized design. Leaves of the cotton varieties DeltaOpal®, NuOpal®, FMX 993®, FMT 701®, FMX 910® and FMX 996® were offered daily to S. frugiperda larvae. The presence of antibiosis was evaluated by the duration of each instar and of the larval and pupal stages, larval and pupal biomass, and adult longevity and fecundity. The NuOpal® variety was the most resistant to S. frugiperda. Spodoptera frugiperda fed on non-Bt cotton had heavier pupae and larvae, shorter development time for the larval stage, longer adult longevity, and a higher rate of oviposition and total viability when compared to the Bt cotton varieties.

Keywords

Fall armyworm Plant resistance

Introduction

Insects damage can limit cotton (Gossypium hirsutum) production. The defoliator Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) is present in many countries and considered an important pest of cotton (Ramalho et al. 2011). This insect is of economic importance to many cropping systems, but few studies are reported for this species on cotton plants (Soares et al. 2006).

First and second instar to S. frugiperda feed together near the oviposition site on parenchyma and their feeding leads to leaves becoming necrotic and translucent. As larvae develop, they disperse and natural mortality occurs as they search for food and due to natural enemies (Luthy and Wolfersberger 2000). Developed larvae prefer to feed on the reproductive structures of cotton (Ali et al. 1990; Luttrell and Mink 1999; Ramalho et al. 2011).

Terpene and aldehydes, such as gossypol, heliocides and hemigossypolone, can help plants resistant feeding by different lepidopteran species (McAuslane et al. 1997) and they can be employed in management programs for S. frugiperda. Pilosity (Calhoun et al. 1994), presence or absence of extrafloral nectarines (Flint et al. 1992), type of bracts and leaves (Maredia et al. 1993) and allelochemicals content are factors that can contribute to cotton resistance (Mohan et al. 1996). Antixenose and/or antibiosis are the categories involved in cotton resistance to lepidopteran defoliators (Campos et al. 2012).

Genetically modified plants with genes of B. thuringiensis var. kurstaki (Bt) express lethal protein crystals (Cry) when ingested by lepidopteran larvae (De Polanía et al. 2009; Ramalho et al. 20011). However, cotton cultivars containing only CrylAc were not efficient in controlling S. frugiperda (Adamczyk Junior et al. 1998) and they increase tolerance of individuals feeding on the cultivar (Adamczyk Junior and Sumerford 2001).

Campos et al. (2012) evaluated different structures of the cotton plant and observed that leaves were the most attractive to S. frugiperda feeding compared to bracts, squares and carpel walls of the bolls. The Coodetec-410™ variety was more attractive and BRS Acala-90™, Fibermax-966™ and DeltaPenta™ were less attractive to S. frugiperda. BRS-Araça™ was most preferred for feeding and BRS-Cedro™, BRS Itamarati 90™, DeltaPenta™™, Coodetec-408™ e BRS-Aroeira™ were less preferred.

Therefore, the aim of this study was to evaluate the types of resistance in non-Bt and transgenic Bt varieties of cotton grown in the Cerrado region, Brazil for S. frugiperda.

Material and methods

This research evaluated the resistance of the commercial cotton varieties DeltaOpal™, FMX 701™, FMX 910 ™, FMX 993™ and FMX 996™ (No Bt) and NuOpal™ (transgenic Bt) to S. frugiperda. The experiments were performed at the Laboratory of Plant Resistance to Insects of the Department of Plant Protection, Faculty of Agriculture and Veterinary Sciences (FCAV) in Jaboticabal, São Paulo State, Brazil.

Cotton leaves for the bioassays were collected from cotton that was growing in the experimental plots at the Department of Plant Protection. Management practices as fertilizing, weeds control etc., were performed according to this culture needs, except insecticide application.

Spodoptera frugiperda rearing.

Spodoptera frugiperda was reared in cages of polyvinyl chloride (PVC) tubes (10 cm in diameter and 21.5 cm high) covered internally with white paper sheets as oviposition sites. The cages were covered with "voile fabric" to prevent moths from escaping (Campos et al. 2012; Jesus et al. 2014).

Cotton wads, soaked in 10% honey solution were provided as a food source for S. frugiperda moths. The food source was changed every two days. The white paper sheets with moth eggs were collected daily by cutting out the papers and placing them in 100 mL plastic cup with 5 g of artificial diet (Kasten Junior et al. 1978). These containers were covered and kept in a controlled room (25±2°C, RH of 50 ± 10% and photophase of 14 hours).

Second instar S. frugiperda caterpillars were separated (around 4 mm) to avoid their cannibalistic behavior and individually placed in 50 mL plastic cups with 5 g of artificial diet. These cups were closed with acrylic lids and placed in styrofoam stands with holes on the size of the cup. The cups were kept in a controlled room until the larvae reached the pupal stage and were then separated by sex. Seven pairs of moths were placed in each cage.

Non-preference test for feeding.

The attractiveness free choice test was performed in laboratory with six treatments and 2 third instar S. frugiperda caterpillars per variety and replication. Thirty days old leaves were collected from the plants in the field, washed and cut into 2.5 cm diameter disks and distributed in a circular manner in a Petri dish (14 cm in diameter) over a moistened filter paper. DeltaOpal™ variety was included as the susceptible control (Boiça Junior et al. 2012; Campos et al. 2012; Souza et al. 2012).

Two leaf disks (2.5 cmβ diameters) were removed equidistant from the leaves of cotton variety. One was offered to the insects and the other known as the aliquot was oven dried at 60 °C for 48 hours. The dry matter consumed by S. frugiperda larvae was determined by the difference between this rate and the remaining portion of the disk consumed.

The attractiveness of caterpillars to foliar disks of each variety was evaluated by counting the number of disk fed upon at 1, 3, 5, 10, 15, 30, minutes and 1, 2, 6 and 24 hours after releasing. Leaves of the six cotton varieties were collected in the field, washed, cut into disks of 2.5 cm diameter and individually placed in Petri dishes in the attractiveness in no choice test. One disk was placed per Petri dish (6 cm diameter) over a moistened paper filter. Two third instar caterpillars were used per replication in the tests of attractiveness and free choice.

An aliquot of each variety was also dried to determine the dry matter consumed based on its dry weight and that of the disks at the end of the tests. The difference between the two foliar disk was determined to be the dry mass consumed.

Test of non-preference for oviposition.

The non-preference in free choice test for oviposition was performed in a mesh (1.5 m x 0.6 m x 0.6 m) container with anti-aphid screen. Each container contained a terminal bud of each variety was put in a glass tube with water and 12 couples of S. frugiperda released per cage. The number of eggs per plant was evaluated at 72 hours after the release of the insects. This experiment had ten replications (cages) and six treatments (cultivars) in a randomized block design.

A couple of adults of S. frugiperda from the mass rearing was put per PVC cage (12 cm diameter and 20 cm of height) with a terminal bud of each variety placed in a glass tube with water for the non-preference of oviposition. Seventy-two hours after the release of the insects, the total number of eggs per plant was counted. This experiment had a complete randomized design with six treatments and ten replications (Barros et al. 2010; Boiça junior et al. 2013).

Antibiosis test.

Leaves for the study were collected from cotton varieties planted in the field. The study had a completely randomized design with six treatments (cultivars) and 50 replications, each with a Petri dish (6 cm in diameter) with moistened filter paper and leaves of one variety with a newly hatched caterpillar to obtain its biological cycle. The paper filter was changed daily and leaves replaced. Length of the larva and pupa stages, mass of 10-day old larvae and 24-hour old pupae, adult longevity and fecundity were obtained (Moreno et al. 2008; Boiça Junior et al. 2012; Campos et al. 2012; Cataño et al. 2014).

Statistical analysis.

Data were subjected to analysis of variance or Fisher's exact test followed by the Tukey's test at 5% probability, using the software SISVAR version 5.1 (Ferreira 2011). When necessary the means were transformed in ( $x + 0.5$ )^1/2 before analysis.

Results and discussion

Mass consumed per instar of S. frugiperda in the free choice test differed among treatments at 3, 5 and 30 minutes and at 2, 6 and 12 hours after insect introduction (Table 1). The FMX 993 (0.0 to 0.9) and FMX 910 (0.0 to 1.0) varieties were less attractive to S. frugiperda while DeltaOpal™ (0.5 to 1.1) and FMX 966™ (0.3 to 2.1) varieties were more attractive. The dry mass consumed showed lower values for the NuOpal™ variety (1.58), whereas, DeltaOpal™ (4.51) was the most preferred (Table 1).

Table 1.

Attractiveness and leaf mass consumption (LMC) (mean ± standard deviation) of third instar Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae on leaves of different cotton varieties in a free choice test. Jaboticabal, São Paulo State, 2008.

Varieties	Time in minutes¹
Varieties	1	3	5	10	22	30
DeltaOpal®	0.6±0.16	0.5±0.22 abc	0.7±0.30 ab	0.5 ± 0.22	0.5 ± 0.22	0.7±0.15 a
NuOpal®	0.6 ± 0.22	0.8±0.20 a	0.8±0.25 a	0.4 ± 0.22	0.4±0.16	0.3±0.21 abc
FMX 993®	0.2 ± 0.13	0.0 C	0.2±0.30 ab	0.3 ± 0.15	0.4±0.16	0.2±0.13 bc
FMT 701®	0.5 ± 0.17	0.5±0.17 abc	0.5±0.17 ab	0.1±0.10	0.2 ±0.13	0.3±0.15 abc
FMX 910®	0.4 ± 0.22	0.2±0.13 abc	0.1±0.10 b	0.1±0.10	0.0±0.00	0.3±0.15 c
FMX 966®	0.3 ± 0.21	0.7±0.26 ab	0.7±0.15 ab	0.5 ± 0.17	0.4±0.16	0.6±0.16 ab
C.V	31.95	29.04	30.64	30.49	30.44	28.22
F. (Tr.)	0.705^NS	2.42*	2.25*	1.17^NS	1.20^NS	2.34*

Varieties	Time in hours
Varieties	1	2	6	12	24	LMC (g)
DeltaOpal®	0.9±0.23 b	0.8±0.29 a	0.9±0.10 a	0.9 ± 0.23 a	1.1 ± 0.23	4.51±0.71 a
NuOpal®	0.4±0.22 b	0.4±0.22 ab	0.4±0.16 b	0.5±0.22 ab	0.8±0.20	1.58 ± 0.43 b
FMX 993®	0.1±0.10 b	0.1±0.10 b	0.1±0.10 b	0.9±0.31 a	0.6±0.22	2.57±0.47 ab
FMT 701®	0.3±0.15 b	0.4±0.22 ab	0.2±0.13 b	0.1±0.10 b	0.6±0.27	2.61±0.60 ab
FMX 910®	0.3±0.21 b	0.0±0.00 b	0.1±0.10 b	0.3±0.15 ab	1.0 ± 0.26	3.76±0.90 ab
FMX 966®	2.1 ± 0.86 a	0.4±0.22 ab	0.3±0.15 b	0.8±0.33 ab	0.9 ± 0.23	4.09±0.86 ab
C.V	42.60	34.84	23.97	35.76	51.80	0.20
F. (Tr.)	3.41*	1.78*	5.46**	1.87*	0.84^NS	2.76*

Means followed by the same letter are not different by Tukey's test at the 5% probability level. Data were transformed to (x + 0.5)^1/2) for analysis purposes.

Significant at 1% probability.

Significant at 5% probability.

NS Non-significant.

The attractiveness and dry mass consumed by S. frugiperda larvae in the no-choice test showed differences among treatments at 1 minute and 1, 6 and 12 hours after the caterpillars were released (Table 2).

Table 2.

Attractiveness and leaf mass consumption (LMC) (mean ± standard deviation) of third instar Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae on leaves of different cotton varieties in a no-free choice test. Jaboticabal, São Paulo State, 2008.

Varieties	Time in minutes¹
Varieties	1	3	5	10	15	30
DeltaOpal®	0.9±0.09 ab	0.9±0.09	0.9 ± 0.09	0.9 ± 0.09	0.8±0.11	0.8±0.11
NuOpal®	1.0±0.00 a	0.8±0.11	0.7 ± 0.12	0.9±0.09	0.9 ± 0.07	1.0 ± 0.00
FMX 993®	0.9±0.07 ab	0.8±0.11	0.9 ± 0.09	0.8 ± 0.11	0.7 ± 0.13	0.9 ± 0.09
FMT 701®	0.6±0.13 b	0.9 ± 0.09	0.7 ± 0.12	0.8±0.11	0.7 ± 0.12	0.7 ± 0.12
FMX 910®	0.9±0.09 ab	0.8 ± 0.11	0.9 ± 0.09	0.9±0.09	0.9 ± 0.09	0.9 ± 0.09
FMX 966®	0.7±0.13 ab	0.7 ± 0.12	0.7±0.13	0.6±0.13	0.6±0.13	0.7 ± 0.12
C.V	16.78	18.48	19.21	18.57	18.57	16.99
F. (Tr.)	2.70*	0.23^NS	0.68^NS	0.98^NS	0.98^NS	1.09^NS

Varieties	Time in hours
Varieties	1	2	6	12	LMC (g)
DeltaOpal®	1.0±0.00 a	0.9±0.09	1.0±0.00 a	0.5±0.13 b	2.47 ± 0.43
NuOpal®	1.0±0.00 a	0.9 ± 0.07	0.9±0.07 ab	0.2±0.11 b	2.31 ± 0.21
FMX 993®	0.8±0.11 ab	0.9 ± 0.09	0.9±0.09 ab	0.3±0.13 b	2.55 ± 0.53
FMT 701®	0.9±0.07 a	0.9 ± 0.09	0.9±0.09 ab	0.3±0.12 b	2.55 ± 0.36
FMX 910®	0.9±0.07 a	1.0 ±0.00	1.0±0.00 a	0.9±0.09 a	2.49 ± 0.45
FMX 966®	0.7±0.13 b	0.9±0.07	0.7±0.12 b	0.3±0.12 b	2.91 ± 0.39
C.V	13.33	12.73	13.03	25.52	64.54
F. (Tr.)	2.84*	0.53^NS	1.75^NS	4.46**	0.46^NS

Means followed by the same letter are not different by Tukey's test at the 5% probability level. Data were transformed to (x + 0.5)^1/2) for analysis purposes.

Significant at 1% probability.

Significant at 5% probability.

^NS Non-significant.

The FMX 966 variety (0.3 to 0.9) was less attractive and the DeltaOpal™ variety (0.5 to 1.0) was more attractive to S. frugiperda. The dry mass consumed by caterpillars S. frugiperda in the no choice test did not differed among the cotton varieties (Table 2).

Lower consumption of the NuOpal™ variety by S. frugiperda larvae might be explained by the presence of the Cry1Ac gene from Bacillus thuringiensis which induces endotoxin crystals formation in this variety (De Polania et al. 2009). Higher attractiveness of S. frugiperda to DeltaOpal™ variety may be due to kairomones (Macintosh et al. 1990; Adamczyk Junior et al. 1998; Adamczyk Junior and Gore 2004; Adamczyk Junior et al. 2008; Ramalho et al. 2011). The presence of these chemicals in these genotypes may increase its attractiveness.

The non-preference for oviposition in the free choice test showed that moths oviposited more frequently on FMX 966™ with 502.11 eggs and 4.0 egg masses and the NuOpal™ variety was the least preferred (321.8 and 2.9). In the no choice test, DeltaOpal™ had a higher number of eggs and egg masses (380.3 eggs and 3.3 egg masses) when compared to FMX 993™ (193.1 and 1.3) (Table 3).

Table 3.

Number of eggs and ovipositions (mean ± standard deviation) of Spodoptera frugiperda (Lepidoptera: Noctuidae) on different cotton varieties with and without free choice tests. Jaboticabal, São Paulo State, 2008.

Varieties	Free choice test		No choice test
	Number of eggs	Number of ovipositions	Number of eggs	Number of ovipositions
DeltaOpal®	348.9±125.5	2.7 ± 0.8	380.3±105.1	3.3±0.6 a
NuOpal®	321.8±170.8	2.9 ± 0.9	372.5 ± 103.1	2.7±0.7 ab
FMX 993®	339.6 ± 107.5	2.8±0.8	193.1 ± 81.9	1.3±0.4 b
FMT 701®	353.7 ± 102.5	2.6 ± 0.7	297.2 ± 91.0	1.9±0.5 ab
FMX 910®	335.0±91.2	3.2 ± 0.7	346.6 ± 148.9	1.6±0.4 ab
FMX 966®	502.9±113.1	4.0 ± 0.8	357.6±167.9	1.8±0.5 ab
C.V	59.11	33.13	71.76	33.93
F. (Tr.)	0.55^NS	0.62^NS	0.37^NS	1.74*

¹ Means followed by the same letter in column are not different by Tukey's test at the 5% probability level. Data were transformed to (x + 0.5)^1/2) for analysis purposes.

Significant at 5% probability.

^NS Non-significant.

The distribution of egg masses of S. frugiperda on Bt-cotton plants was also different from that of non-Bt plants, which suggests that moths do not show an ovipositional preference between Bt-cotton and non-Bt plants (Pitre et al. 1983; Ali et al. 1989; Hardke et al. 2012).

Reproductive parameters (except fecundity) of S. frugiperda differed among treatments (Table 4). Larval and pupal masses were higher in FMX 910 (169.9 and 225.29) and lower in the NuOpal™ (55.49 and 164.02) variety, which indicates that NuOpal™ is less suitable for development of this pest. Larval and pupal development periods were longer with NuOpal™ (30.05 days and 11.7 days) and shorter with the FMX 910™ (24.0 days) and FMX 993™ (24.9 days) varieties. The pupal period with FMT 701™ variety (10.1 days) was short among the varieties, thus demonstrating that they are more suitable for the development of this insect.

Table 4.

Caterpillar mass, pupae mass, larval period, pupal period and adult longevity with and without food and fecundity (mean + standard deviation) of Spodoptera frugiperda (Lepidoptera: Noctuidae) on different cotton varieties. Jaboticabal, São Paulo State, 2008.

Varieties	Parameters evaluated
Varieties	Caterpillar mass (mg)	Pupae mass (mg)	Larval period (days)	Pupae period (days)
DeltaOpal®	108.95±10.12 с	200.25±6.96 bc	27.2 ± 0.77 b	10.4±0.27 bc
NuOpal®	55.49±6.47 d	164.02±6.86 d	30.05 ± 0.96 a	11.7±0.33 a
FMX 993®	139.33 21.04 abc	212.65±8.12 ab	24.9 ± 0.38 c	11.1±0.23 ab
FMT 701®	128.85±13.22 bc	185.77±8.67 cd	25.9±0.81 bc	10.10.28 c
FMX 910®	169.94±12.98 a	225.29±8.54 a	24.0 ± 0.51 c	10.4±0.27 bc
FMX 966®	150.39 ± 11.34 ab	207.09 ±9.06 abc	25.1±0.72 bc	11.0±0.37 abc
C.V	9.03**	7.17**	9.08**	9.04**
F. (Tr.)	6.53	18.14	12.24	8.62

Varieties	Parameters evaluated
Varieties	Adult longevity without food (days)	Adult longevity with food (days)	Fecundity (number of ovipositions)	Fecundity (number of eggs)
DeltaOpal®	4.2±0.36 ab	7.8±0.71 ab	1.36±1.12 ab	288.9 173,20
NuOpal®	2.9±0.18 c	5.9±0.90 b	1.03 ±0.79 b	124.298.87
FMX 993®	3.9±0.18 ab	8.1±0.43 ab	1.41±0.79 ab	166.369.52
FMT 701®	3.5±0.22 bc	9.7 ± 1.16 a	1.46 ±2.26 ab	108.587.02
FMX 910®	4.8 ± 0.61 a	8.9±0.57 ab	2.13±1.43 a	243.9±7242
FMX 966®	3.9±0.23 ab	7.6±0.88 ab	1.86±1.91 ab	246.487.33
C.V	3.67**	2.53*	1.54*	0.76NS
F. (Tr.)	27.35	32.04	64.49	71.56

¹ Means followed by the same letter in column are not different by Tukey's test at the 5% probability level. Data were transformed to (x + 0.5)^1/2) for analysis purposes.

Significant at 1% probability.

Significant at 5% probability.

^NS Non-significant.

Duration of 24.0 to 30.05 days for larval period and 10.1 to 11.7 days for pupal period were close to the lower weight and larva and pupa survival of insects fed on Bt-cotton (Verissimo et al. 2009; Ramalho et al. 2011). This lower mass and longer larva period of S. frugiperda fed on Bt-cotton could be due to allocation of energy to regenerate the midgut epithelium damaged by endotoxin (Luthy and Wolfersberger 2000).

These results are similar to Ramalho et al. (2011) who observed a prolongation of 2.8 days in the lifecycle of S. frugiperda fed on Bt cotton compared to larvae fed on non-Bt genotypes. Cataño et al. (2014) observed a prolongation of 7.3 days when S. frugiperda fed on transgenic variety DP141 B2RF (Cry1Ac + cry2Ab2) compared to the non-Bt cotton DeltaOpal™.

The longevity of S. frugiperda adults with and without food showed lower values with the NuOpal™ for both parameters with 2.90 days longevity without food and 5.90 days with food while the FMX 910™ variety with food and FMT 701™ without food had insects with longer longevity, 4.8 and 9.7 days, respectively. Differences in adult longevity may be related to individual variation or ability to convert food during the juvenile stage, therefore affecting their longevity (Luginbill 1928).

The correlation between longevity, and larva and pupa mass showed that longer-lived adults originated from heavier larvae and pupae (Table 4).

Differences in instar duration showed different levels of resistance among the cotton varieties to S. frugiperda. The NuOpal™ variety exhibited the highest level of antibiosis. This variation of biological parameters of S. frugiperda fed on the cotton varieties may be due to the presence of chemicals of these plants interfering with the development of the insect (Bavaresco et al. 2004; Meagher et al. 2004). The chemical defenses of plants repel and reduce digestibility of herbivores. Tannins stored in plant leaves combined with proteins from leaves and digestive enzymes in the gut of insects can hinder digestion and thus negatively affecting their current and future generations (Mauricio and Rausher 1997). In the NuOpal variety the lower performance of S. frugiperda can be due the damage in the midgut epithelium caused by endotoxin (Luthy and Wolfersberger 2000).

Conclusions

The NuOpal™ variety was the most resistant with the development of the larvae and pupae being severely impacted. S. frugiperda fed on non-Bt cotton resulted in heavier larvae and pupae, shortened larval development times, increased longevity and fecundity rates of adults. S. frugiperda had a longer pupal development and shorter adult longevity and viability when fed on Bt-cotton.

Footnotes

Acknowledgements

We would like to thanks the "Coordenação de Aperfeiçoamento de Pessola de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support. Dr. Tiffany Heng-Moss from Department of Entomology to University of Nebraska - Lincoln for reading and suggestions and the anonymous reviewers for comments and corrections of this manuscript.

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Resistance of Cotton Varieties to Spodoptera Frugiperda (Lepidoptera: Noctuidae)

Abstract

Keywords

Introduction

Material and methods

Spodoptera frugiperda rearing.

Non-preference test for feeding.

Test of non-preference for oviposition.

Antibiosis test.

Statistical analysis.

Results and discussion

Conclusions

Footnotes

Acknowledgements

References