Development of Spodoptera frugiperda on different hosts ... - UFRPE

<strong>Development</strong> <strong>of</strong> <strong>Spodoptera</strong> <strong>frugiperda</strong> on different
hosts and damage to reproductive structures in cotton
Eduardo M. Barros 1 , Jorge B. Torres 1 *, John R. Ruberson 2 & Martin D. Oliveira 1
1 Departmento de Agronomia ⁄ Entomologia, Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros
S ⁄ N, Dois Irmãos, Recife, PE 31794-900, Brazil, and 2 Department <strong>of</strong> Entomology, University <strong>of</strong> Georgia, Tifton,
GA 31794, USA
Accepted: 25 August 2010
Key words: fall armyworm, host suitability, landscape ecology, economic damage, color fiber cotton,
Lepidoptera, Noctuidae
Abstract The fall armyworm (FAW), <strong>Spodoptera</strong> <strong>frugiperda</strong> (J.E. Smith) (Lepidoptera: Noctuidae), is a widespread
pest species <strong>of</strong> various cultivated plants. The pest status <strong>of</strong> FAW in cotton in the Cerrado
region <strong>of</strong> Brazil has increased with the recent changes in cotton crop systems, such as double cropping
and the use <strong>of</strong> cover or winter crops with non-tillage cropping systems. In this study we investigated
the performance <strong>of</strong> FAW on three major crops cultivated in the Cerrado – soybean, corn, and cotton
– and millet which has been integrated into the landscape as a cover crop. Further, the damage to various
reproductive structures <strong>of</strong> cotton plants by FAW larvae was determined. Both studies were conducted
under field conditions. Survival <strong>of</strong> FAW larvae caged on millet plants was higher than on
other hosts. The FAW reared on millet also exhibited a net reproductive rate similar to that observed
on corn, which was considered the best host for FAW, and the highest intrinsic rate <strong>of</strong> increase and
lowest mean generation time compared to all other hosts. In cotton, the low availability <strong>of</strong> bolls during
the plant’s blooming stage resulted in higher square feeding, whereas infestation during the
plant’s boll stage resulted in higher loss <strong>of</strong> bolls and lower attack on squares. The number <strong>of</strong> adults
produced in a generation was higher when plants were infested in the boll stage. The results indicated
that FAW is a threat to cotton when bolls are available and can cause significant loss <strong>of</strong> reproductive
structures. In addition, based on the FAW performance feeding on millet, this cover crop can be
among the reasons <strong>of</strong> FAW increasing pest status in subsequent crops.
Introduction
The management <strong>of</strong> polyphagous and mobile insect herbivores
requires pest management systems to focus on areawide
cropping systems and not simply on the major season
crop in a single field or farm (Abel et al., 2007; Wu, 2007;
Herde, 2009). The exploitation <strong>of</strong> food resources <strong>of</strong>fered
in nearby crops and weeds in space, in crop rotations and
sequences in time play important roles in the population
dynamics and outbreaks <strong>of</strong> polyphagous herbivores. Thus,
managing polyphagous pests relies on understanding their
host use within and between crop seasons, and includes
*Correspondence: Jorge Braz Torres, Departmento de Agronomia
⁄ Entomologia, Universidade Federal Rural de Pernambuco, Rua.
Dom Manoel de Medeiros s ⁄ n, Dois Irmãos, 52171-900 Recife, PE,
Brazil. E-mail: jtorres@depa.ufrpe.br
DOI: 10.1111/j.1570-7458.2010.01058.x
cultivated and uncultivated plants that might serve as pest
reservoirs.
The fall armyworm (FAW), <strong>Spodoptera</strong> <strong>frugiperda</strong> (J.E.
Smith) (Lepidoptera: Noctuidae), is well known as a key
pest <strong>of</strong> corn in the Americas. Further, FAW is a polyphagous
species that uses important cultivated species <strong>of</strong> Poaceae
as hosts and can reach pest status on several <strong>of</strong> them
(e.g., rice, wheat, sorghum, and corn) (Luginbill, 1928;
Sparks, 1979; Cruz, 1995; Capinera, 2002). Despite the
preference for plants <strong>of</strong> the family Poaceae, FAW is
increasingly becoming a pest <strong>of</strong> important broadleaf crops
such as cotton and soybean in the Brazilian Cerrado, especially
when they are cultivated after corn. There are several
potential explanations for the increasing outbreaks <strong>of</strong>
FAW in these broadleaf hosts, including reduction <strong>of</strong> the
host-free window between crops (i.e., double cropping),
and the use <strong>of</strong> plant species as cover or winter crops, such
as millet, that serve as pest reservoirs. This last possibility
Ó 2010 The Authors Entomologia Experimentalis et Applicata 137: 237–245, 2010
Entomologia Experimentalis et Applicata Ó 2010 The Netherlands Entomological Society 237

238 Barros et al.
was under investigation in this study. Coordinated planting
to create a host-free period between crop seasons is recommended
as a preventive practice to manage pests.
However, in areas with irrigation and a favorable climate,
as is the case in the Brazilian Cerrado, corn, soybean, and
cotton can be double cropped. The revenue obtained per
area cultivated overcomes at first glimpse the risks
imposed by pest infestation, overcoming therefore the
benefits <strong>of</strong> adopting ‘sanitation windows’ or ‘host-free
periods’ between cropping seasons. As a result, polyphagous
species such as armyworm species may exploit a
diversity <strong>of</strong> hosts to build populations outside <strong>of</strong> crop
fields and migrate in high numbers into major crop areas
(Nagoshi et al., 2008).
Studies <strong>of</strong> FAW populations have shown that cropspecific
severity <strong>of</strong> FAW infestations is linked to host-related
strains: the corn strain and rice strain (Pashley et al., 1985;
Pashley, 1986; Busato et al., 2004; Meagher & Nagoshi,
2004). The corn strain, for which corn is the preferred
host, is the strain that also colonizes cotton fields (Martinelli
et al., 2007). Thus, FAW can migrate among fields <strong>of</strong>
corn and cotton and develop and reproduce in these unrelated
crops (Nagoshi, 2009).
The pest status <strong>of</strong> FAW is usually associated with specific
developmental stages <strong>of</strong> the host plant. In corn, FAW
initially colonizes plants during the vegetative whorl stage.
During this period, the larvae are protected while feeding
on the young leaves forming the leaf whorl. In host plants
other than Poaceae that do not <strong>of</strong>fer a whorl as a preferred
and protected feeding site for FAW, the reproductive
structures are targeted. Thus, in cotton plants the squares,
blooms, and bolls are the preferred location <strong>of</strong> FAW.
According to Ali et al. (1990), and our observations, newly
eclosed FAW larvae start feeding on underside leaf surface
<strong>of</strong> cotton, subsequently moving to squares and blooms,
and finally move downward within the plant canopy to
feed on bolls before pupating. Thus, the cotton plant
becomes a favorable host due to the abundance <strong>of</strong> flowering
and fruiting structures produced systematically from
ca. 40 to 120 days after emergence. Thus, although low
FAW densities occur in cotton fields, FAW is a very
destructive pest in cotton because it feeds directly on
reproductive structures rather than on leaves.
Thus, we can hypothesize that FAW colonizing cotton
fields at the blooming stage will complete a generation in
approximately 40–60 days after plant emergence, and
develop a second generation during the predominance <strong>of</strong>
boll production from 60 to 90 days, whereas a third generation
may occur during the boll maturation stage. The
development <strong>of</strong> a large FAW population would not be
expected early in the cotton season, as only leaves would
be available for feeding. Therefore, the largest outbreak is
expected to occur during the second ⁄ third generation
within cotton fields or from mass migration <strong>of</strong> adults from
nearby corn fields or from large populations generated
from winter ⁄ cover crops. Thus, this study had two objectives:
(1) to investigate the life history characteristics <strong>of</strong>
FAW fed corn [Zea mays L. (Poaceae)], millet [Pennisetum
glaucum L. (Poaceae)], cotton [Gossypium hirsutum L.
(Malvaceae)], and soybean [Glycine max L. Merril (Fabaceae)],
and (2) to characterize the damage to cotton reproductive
structures caused by FAW larvae during different
developmental stages <strong>of</strong> cotton.
Materials and methods
Insects
The FAW colony was initiated with larvae collected from
corn fields (8 o 1¢S, 34 o 57¢W) at the Universidade Federal
Rural de Pernambuco (UFRPE), Recife, Pernambuco
State, Brazil, and reared with corn leaves to pupation. The
emerged adults were used to establish a laboratory colony
reared with artificial diet adapted from Greene et al.
(1976). The larvae were reared using vials (2.5 cm in diameter
· 8.5 cm high) containing the artificial diet and
closed with cotton pads, and maintained at 25 ± 2 °Cand
L12:D12 photoperiod. The adults were reared using PVC
cages (15 cm in diameter · 22 cm high) with the inner
surface covered with paper as an oviposition substrate and
the upper opening closed with PVC plastic film. The cages
were placed on plastic plates (17 cm in diameter) lined
with paper towels. The adults were fed a 10% honey ⁄ water
(wt/vol) solution soaked on cotton pads <strong>of</strong>fered in small
plastic caps inside the cages and replaced every other day.
All insects used in the studies were reared on artificial diet
for more than five generations to avoid any potential
conditioning to a specific plant food.
Life history characteristics <strong>of</strong> FAW reared on different hosts in the
field
The development and reproduction <strong>of</strong> FAW were investigated
using corn, millet, cotton, and soybean plants cultivated
in microparcels in the field. The microparcels
consisted <strong>of</strong> cement rings (100 cm in diameter · 50 cm
high) filled with soil up to 5 cm below the upper edge.
Each microparcel was established with five plants <strong>of</strong> the
same host species. The plants were planted on different
dates to obtain plants <strong>of</strong> the desired ages that could be
infested at the same time. This procedure was adopted to
allow for the simultaneous infestation by FAW <strong>of</strong> the optimal
phenological stage <strong>of</strong> the three test plant species. Thus,
corn plants (variety BRS Caatingueiro and millet variety
ADR 500) were infested 40 days after planting, whereas
cotton plants (variety Deltapine Acala 90) were infested at

stage R4 (s<strong>of</strong>t bolls) and soybeans (variety BRS Sambaíba)
at stage R3 ⁄ R4 (pods appearing). The five plants in each
microparcel were confined using cylindrical cages
(95 · 100 cm) made with nylon mesh screen (2 mm
openings) fastened on a cylindrical iron structure set up
over the cement rings. A zipper 60 cm long was fixed along
the upper edge <strong>of</strong> the cage to allow access to the cages.
Fall armyworm larvae were released at a rate <strong>of</strong> 250 larvae
per cage (50 larvae per plant). The releasing procedure
consisted <strong>of</strong> placing 50 larvae on leaf disks <strong>of</strong> the respective
plant host. Then, the leaf disk was stapled onto the topmost
fully developed leaf <strong>of</strong> the plant. This number may
sound excessive, but one egg mass <strong>of</strong> FAW can produce
over 200 eggs (Cruz, 1995). These larvae were reared for
48 h on the respective hosts in the laboratory prior to
release to facilitate handling and counting the number <strong>of</strong>
larvae to be released. The outer border <strong>of</strong> the microparcels
was treated with tanglefoot BioStop Ò (Biocontrole, São
Paulo, SP, Brazil) to build a barrier against predators
inside the cages.
Evaluations were conducted on day 10 and day 18 after
FAW larvae were released. The relative developmental success
<strong>of</strong> FAW infesting the plants was determined by the
number and weight <strong>of</strong> larvae surviving on day 10 and
pupation rate on day 18. The day 10 evaluation consisted
<strong>of</strong> harvesting the plants and collecting the larvae, which
were then counted and weighed. During this evaluation
six, six, five, and eight microparcels (replications) cultivated
with corn, millet, cotton, and soybean, respectively,
were evaluated. The day 18 evaluation (pupation rate)
consisted <strong>of</strong> digging and sifting the soil in the microparcels
to collect the pupae. To facilitate collection <strong>of</strong> pupae, a
plastic 2 mm mesh was placed 15 cm below the soil surface,
encompassing the area <strong>of</strong> the cement ring. The mesh
was then covered with sifted soil prior to planting. Five
holes <strong>of</strong> 1cmindiameterweremadeinthemeshto
receive the seeds and to allow the main plant stem to
develop. On day 18, five microparcels (replications) were
evaluated for each host plant treatment. The pupae were
collected, separated by sex and divided into two groups <strong>of</strong>
male and female pupae: one group was reared in the laboratory
and the other group returned to the soil inside the
cages in the field to determine pupal viability in the field
(adult emergence rate). The group <strong>of</strong> pupae kept in the
laboratory was monitored to assess reproductive parameters.
Thus, in the laboratory 13 pairs (replications) <strong>of</strong> FAW
adults were reared for each host plant. They were kept in
PVC cages (10 cm in diameter · 15 cm high) lined with
paper as an oviposition substrate, fed 10% honey ⁄ water
solution and maintained in a climate chamber at 25 °C
and L12:D12 photoperiod. Because <strong>of</strong> accidental escapes,
data analyses were ultimately run on 13, 12, 11, and 13
Fall armyworm performance on different hosts 239
females from corn, millet, soybean, and cotton,
respectively. The cages were inspected daily to record
number <strong>of</strong> egg masses produced, eggs per egg mass, and
adult mortality.
Number and fresh weight <strong>of</strong> larvae on day 10, pupation
rate (number <strong>of</strong> pupae per 250 larvae released) evaluated
on day 18, adult emergence from field cages, preoviposition
period, female longevity, and number <strong>of</strong> eggs produced
were tested for normality (Kolmogorov D: normal
test) and homogeneity <strong>of</strong> variance (Bartlett’s test), and
square root (x + 0.5) or log(x + 1) transformations were
used when necessary; however, untransformed means are
presented in tables and figures. The results were submitted
to one-way analysis <strong>of</strong> variance (ANOVA) and Tukey’s
studentized range test, with Bonferroni’s corrections for
0.05 <strong>of</strong> significance level (a =0.05⁄ n, where ‘n’ represents
the number <strong>of</strong> means in comparison to hold the error level
equal or lower than 0.05; Abdi, 2007) using SAS s<strong>of</strong>tware
(SAS Institute, 2001).
Data on development and viability (rate <strong>of</strong> adult emergence
from field cages), adult reproduction and survival,
were used to estimate the net reproductive rate, mean generation
time, and intrinsic rate <strong>of</strong> natural increase, adapting
the procedure written by Maia et al. (2000) using SAS
s<strong>of</strong>tware (SAS Institute, 2001), which relies on a Jackknife
method to estimate confidence intervals and to allow comparisons
between host plants tested.
Loss <strong>of</strong> reproductive structures <strong>of</strong> cotton plants in different stages
caused by FAW infestation
Cotton plants (variety BRS Rubi) that produce light brown
fibers were cultivated in the field using microparcels as
describe above. In this assay, however, three plants were
grown per microparcel instead <strong>of</strong> five. All seeds were sown
on the same day, but with different FAW infestation dates.
Caging <strong>of</strong> plants in the microparcels followed the same
procedure as that used in the previous experiment and the
infestation rate was 50 neonate larvae per plant (i.e., 150
larvae per microparcel).
The experiment consisted <strong>of</strong> treatments evaluating the
effect <strong>of</strong> FAW colonization at two different cotton plant
stages (flowering and boll development). FAW colonization
<strong>of</strong> cotton fields can occur early in the blooming stage;
therefore, cotton plants are susceptible to FAW attack sufficiently
long to allow at least two FAW generations before
boll maturation. Thus, the experimental design was set up
to infest plants at the blooming stage and evaluated
20 days later. All released larvae had completed larval
development by this point (hereafter referred to as ‘blooming
stage and one immature generation = Blooming 1’).
The pupae evaluated were maintained in the same cage to
determine the entire immature period required to com-

240 Barros et al.
plete development in each host plant under field
conditions. The subsequent treatment consisted <strong>of</strong> infesting
the plants at the blooming stage and evaluating 40 days
later. Adults were allowed to emerge inside the cages and
lay eggs to initiate a second generation on the same plants,
so that a second larval generation was completed (hereafter
referred to as ‘blooming stage and two immature generations
= Blooming 2’). Finally, plants were infested at the
boll stage and FAW populations evaluated after pupation
(hereafter referred to as ‘boll stage and one immature generation
= Boll 1’). Pupae were allowed to complete development
in the same cage to evaluate the whole immature
period. The infestation <strong>of</strong> plants in the treatments during
the blooming stage took place 45 days after planting,
whereas infestation <strong>of</strong> plants in the boll stage took place
70 days after planting. Two control treatments were set up
to evaluate natural shedding: one to be evaluated simultaneously
with the Blooming 1 generation; and the second
control treatment to be evaluated simultaneously with the
Blooming 2 and Boll 1 treatments, as both were evaluated
at the same time. Each treatment was replicated five times
(each replicate consisted <strong>of</strong> microparcels with three plants)
except for Boll 1, which had 10 replications.
Evaluation consisted <strong>of</strong> harvesting the plants from each
microparcel and inspecting each whole plant to count
number <strong>of</strong> squares and bolls without damage, number <strong>of</strong>
bolls damaged, and number <strong>of</strong> squares and bolls dropped.
The cages were replaced on the microparcels to assess adult
emergence. Estimates were obtained for complete developmental
time, number <strong>of</strong> adults produced, and sex ratio.
These results were tested for normality (Kolmogorov D:
normal test) and homogeneity <strong>of</strong> variance (Bartlett’s test),
and square root transformation (x + 0.5) was used when
necessary; however, untransformed means are presented in
tables and figures. The results were submitted to one-way
ANOVA through Proc GLM <strong>of</strong> SAS and Tukey’s studentized
range test for mean comparisons after Bonferroni’s
corrections for appropriate significance level according to
the number <strong>of</strong> means compared (Abdi, 2007).
The cotton plants exhibit natural shedding <strong>of</strong> reproductive
structures, which can vary with plant variety and
environmental conditions. For instance, under the conditions
for the region and the variety, about 66% <strong>of</strong> produced
reproductive structures by cotton plants reach open
bolls (Arruda et al., 2002). Thus, to avoid mistaking natural
abscission exhibited by cotton plants for damage caused
by FAW larvae, we corrected the lost reproductive structure
counts observed in the microparcels <strong>of</strong> plants with
FAW infestation using their respective controls without
infestation. Therefore, the number <strong>of</strong> squares remaining
on the plant and those shed, and the number <strong>of</strong> undamaged
and damaged bolls in each treatment with FAW infestation
for each replication were adjusted to the difference
between treatments with and without FAW infestation.
Statistical significance on loss <strong>of</strong> cotton plants reproductive
structures in relation to FAW was determined using
the overlap rule for 95% CI <strong>of</strong> the treatment differences
(Di Stefano, 2005).
Results
Life history characteristics <strong>of</strong> FAW fed different hosts in the field
The survivorship <strong>of</strong> FAW larvae on day 10 post-infestation
was significantly higher for those caged on millet relative
to the other host plants (F 3,21 = 3.09, P = 0.049),
whereas results were similar among corn, soybean, and
cotton (Table 1). Likewise, the viability <strong>of</strong> the larval stage,
as determined by the number <strong>of</strong> pupae recovered <strong>of</strong> the
250 larvae initially released, differed significantly among
host plants (F3,16 = 5.21, P = 0.011), with higher recovery
on millet and soybean (Table 1). The weight gain <strong>of</strong> FAW
larvae after 10 days on the plants, however, did not differ
significantly among the tested host plants (F 3,21 =0.36,
P = 0.78) and ranged from 60 to 108 mg per larvae. Pupae
maintained in cages in the field exhibited similar rates <strong>of</strong>
adult emergence, ranging from 71 to 80%, with the sex
ratio varying from 45.7 to 47.4% <strong>of</strong> females.
Adults that emerged from the group <strong>of</strong> pupae collected
from the microparcels in the field and maintained
throughout the adult stage in the laboratory to evaluate
reproductive traits exhibited similar pre-oviposition periods
(F 3,41 = 0.53, P = 0.66) and egg viability (F 3,41 =2.76,
Table 1 Effect <strong>of</strong> host plant on survival and weight <strong>of</strong> <strong>Spodoptera</strong> <strong>frugiperda</strong> larvae on day 10 following release, pupation rate at day 18 following
release (250 48-h-old larvae caged on five plants <strong>of</strong> each plant species; cultivated in the field), and adult emergence. Mean temperature
27 °C (range 22.4–36.6 °C) and mean r.h. 84% (range 29.9–100%)
Host plants 1
Larval survival (%) Weight <strong>of</strong> larvae (mg) Pupation rate (%) Adult emergence (%)
Cotton 21.3 ± 4.05b 67.0 ± 26.0a 16.9 ± 0.99b 77.0 ± 4.70a
Millet 38.5 ± 6.83a 108.0 ± 54.0a 33.8 ± 6.37a 80.0 ± 6.40a
Corn 24.3 ± 4.20b 60.0 ± 32.0a 18.0 ± 3.33b 71.0 ± 4.50a
Soybean 20.5 ± 3.56b 91.0 ± 26.0a 32.5 ± 3.24a 72.0 ± 3.20a
1 Means (± SE) within columns followed by the same letter do not differ significantly (Tukey’s test: P>0.05).

Table 2 Adult life history characteristics <strong>of</strong> <strong>Spodoptera</strong> <strong>frugiperda</strong> caged on cotton, millet, corn, and soybean plants in the field. Conditions
for larval and pupal stages in the field: mean temperature 27 °C (range 22.4–36.6 °C) and mean r.h. 84% (range 29.9–100%)
Host plant No. eggs per female 1
Female longevity 1
P = 0.055), which ranged from 4.3 to 5.6 days and 49.6 to
70.5%, respectively. The number <strong>of</strong> eggs produced per
female, however, was significantly lower (F 3,41 =3.68,
P = 0.019) for females reared on cotton (1 144.7 eggs per
female) than females reared on the other three hosts
(Table 2). Likewise, longevity <strong>of</strong> females reared on cotton
was shorter than that <strong>of</strong> females reared on soybean
(F3,41 = 4.20, P = 0.011), whereas females reared on millet
and corn exhibited intermediate longevity not differing
from either cotton or soybean (Table 2).
The estimated life history characteristics based on data
from larval and pupal development determined in the
field, and egg production and egg viability in the laboratory
for adults from field reared on the four host plants,
resulted in higher rates <strong>of</strong> reproductive and intrinsic population
growth for individuals reared on millet than on
Fall armyworm performance on different hosts 241
R o ($ ⁄ $) 2
r m ($ ⁄ $*day) 2
T (days) 2
Cotton 1144.7 ± 132.7b 13.3 ± 1.11b 37.9 ± 4.39c 0.110 ± 0.007c 33.1 ± 1.45a
Millet 1574.1 ± 177.6a 17.5 ± 1.13ab 90.5 ± 10.21a 0.166 ± 0.010a 27.1 ± 1.10c
Corn 1604.2 ± 353.8a 15.5 ± 2.07ab 72.3 ± 15.95ab 0.141 ± 0.012b 30.3 ± 1.82b
Soybean 1590.8 ± 381.7a 19.1 ± 0.62a 51.2 ± 12.29bc 0.131 ± 0.014b 30.0 ± 1.50b
1 Means (± SE) within columns followed by the same letter do not differ significantly (Tukey’s test: P>0.05).
2 Means (± 95% confidence intervals) within columns followed by the same letter do not differ significantly through pairwise comparisons
after Jackknife method (Maia et al., 2000). R o = net reproductive rate, r m = intrinsic rate <strong>of</strong> population increase, and T = mean
generation time.
cotton plants, whereas those reared on corn and soybean
exhibited intermediate values (Table 2). For the mean generation
time, cotton plants produced the highest and millet
the lowest (Table 2).
Loss <strong>of</strong> reproductive structures <strong>of</strong> cotton plants under different
stages caused by FAW infestation
The infestation <strong>of</strong> cotton plants grown in the microparcels
with 48-h-old FAW larvae during the blooming stage and
allowed one immature generation caused significant loss
<strong>of</strong> squares (F 1,8 = 17.62, P = 0.003; Figure 1A). The mean
differences ( ± 95% CI) resulted in 7.7 ± 3.07 squares lost
per plant more than the natural shedding observed in the
control treatments at 20 days after infestation. In addition,
the infestation <strong>of</strong> FAW larvae allowing two immature
generations significantly increased the number <strong>of</strong> squares
Figure 1 Means [± 95% confidence intervals (CI)] for differences <strong>of</strong> (A) squares lost, (B) damaged bolls, (C) squares remaining, and (D)
undamaged bolls per plant between treatments (with infestation) and control treatment (without infestation) in the field following release
<strong>of</strong> 150 48-h-old <strong>Spodoptera</strong> <strong>frugiperda</strong> larvae on three cotton plants per microparcel at blooming stage and allowed one generation (Blooming
1), blooming stage with two FAW generations (Blooming 2), and boll stage and one FAW generation (Boll 1). CI not crossing the zero
line indicate significant differences between treatments with and without infestation <strong>of</strong> FAW.

242 Barros et al.
lost per plant (F 1,8 =17.62,P=0.003;Figure1C)with
5 ± 3.50 squares lost across the two generations. Moreover,
the loss <strong>of</strong> squares in the two-generation treatment
was greater than that in the treatment with one immature
generation during boll stage (F2,17 = 6.05, P = 0.010). On
the other hand, infestation <strong>of</strong> 48-h-old FAW larvae on cotton
plants at the boll stage and allowing one immature
generation did not result in significant loss <strong>of</strong> squares
(F 1,13 = 1.49, P = 0.24) when compared to natural shedding
found in the control treatments (mean ± 95% CI:
2 ± 2.62; Figure 1C).
All treatments with FAW infestation had damaged bolls
and there was greater loss <strong>of</strong> bolls with infestation at the
blooming stage and with two immature generations <strong>of</strong>
FAW (F 2,17 = 69.87, P

et al., 2004), we found lower larval survival and 44% lower
weight gain for larvae reared on corn compared to larvae
reared on millet under field conditions, indicating possible
competition among larvae reared on corn plants. Thus,
additional millet whorls possibly allow FAW larvae to
develop with less competition than occurs when several
larvae colonize a single corn plant. In addition, folds in the
millet leaves near the leaf collar <strong>of</strong>fer shelter to FAW larvae
– several larvae were found at this location on day 10 <strong>of</strong> larval
evaluation.
Soybean and cotton plants produce a larger foliage area
compared to corn, allowing larvae to be more diffuse and
reduce potential competition. Thus, the lower performance
<strong>of</strong> FAW larvae on cotton and soybean leaves is
related to the quality <strong>of</strong> leaves as food for early larval stages
colonizing these plants. According to Ali & Luttrell (1990),
the lower survival <strong>of</strong> nenoate FAW larvae fed cotton is
responsible for the lower success <strong>of</strong> FAW colonizing cotton
fields. Similarly, FAW larvae reared individually under laboratory
conditions and fed ad libitum with corn, millet,
soybean, or cotton leaves performed better on corn and
millet than on soybean or cotton (Sá et al., 2009; Barros
et al., 2010).
The lower performance <strong>of</strong> neonate FAW feeding on
either cotton leaves or bolls, when available, have some
possible explanations. First, cotton leaves contain several
antiherbivory secondary compounds such as gossypol, a
sesquiterpene aldehyde that confers resistance against
herbivory, delaying larval development, and reducing
weight gain and survival (Montandon et al., 1987; Stipanovic
et al., 2006). Second, the neonate larvae that avoid
feeding on leaves move to the bolls, where they feed on
bracts and try to bore into the bolls. However, young larvae
are unable to penetrate the boll walls, especially during
the maturation stage. In our field evaluation, we found
several bolls with destroyed bracts and external feeding
scars, but without entry openings. This indicates that as
the boll wall hardens with maturation it becomes increasingly
difficult for FAW larvae to bore into the boll. Ali
et al. (1990) and Luttrell & Mink (1999) observed that
FAW larvae fed on cotton leaves until the second instar,
when they moved to reproductive structures. The movement
required through the plant canopy seeking reproductive
structures may impose an energy use that also
affects their performance. It is important to highlight that
the FAW moths lay eggs on leaves in the plant top when
infesting species <strong>of</strong> Poaceae and the hatching larvae move
to the whorls where they complete the development. All
these conditions diminish the larval performance. For
instance, Luttrell & Mink (1999) estimated that only
0.07% <strong>of</strong> neonate FAW larvae successfully colonized cotton
plants in the field. S<strong>of</strong>t bolls, however, are suitable food
Fall armyworm performance on different hosts 243
for FAW larvae. When FAW larvae bore into s<strong>of</strong>t bolls they
exhibit development comparable to top host plants such as
corn and millet. Fall armyworm larvae fed only s<strong>of</strong>t bolls
performed significantly better than larvae fed only cotton
leaves or leaves plus mature bolls (Barros et al., 2010).
Life history characteristics estimate the instantaneous
population growth for a species under specific experimental
conditions (Maia et al., 2000; Greenberg et al., 2001).
Thus, under the microparcel conditions in the field, we
can conclude that millet, a cover or winter crop used in the
Cerrado, was the best host for FAW larvae based on the net
reproductive rate (Ro) and the intrinsic rate <strong>of</strong> population
increase (rm) (Table 2). Furthermore, cotton is capable <strong>of</strong>
sustaining the pest in the field, though not as productively
as host as millet and corn. This leads us to the observation
that FAW is a sporadic pest <strong>of</strong> cotton and that outbreaks
in cotton will depend on other environmental and biological
phenomena such as the temporary availability <strong>of</strong> preferred
hosts nearby (e.g., millet) that function as sources <strong>of</strong>
FAW populations for cotton fields (Johnson, 1987; Nagoshi
et al., 2008; Nagoshi, 2009). Based on our results and
those reported by Ali & Luttrell (1990) and Ali et al.
(1990), the low survival <strong>of</strong> neonate larvae and delayed larval
development on cotton are the main explanations for
the sporadic occurrence and unpredictable status <strong>of</strong> FAW
as a cotton pest, despite the large number <strong>of</strong> eggs (in
masses) that can be laid on cotton plants.
Loss <strong>of</strong> reproductive structures <strong>of</strong> cotton plants under different
stages caused by FAW infestation
According to the results, FAW larvae cause significant loss
<strong>of</strong> cotton squares only when plants are infested early in the
season and young bolls are available. The infestation <strong>of</strong>
cotton plants in the blooming stage resulted in losses <strong>of</strong>
squares that did not differ from natural abscission in
microparcels without infestation, indicating that FAW
preferred bolls over leaves or squares when they are available.
This is also verified by the number <strong>of</strong> squares remaining
on the plants infested at the boll stage, or at the
Blooming 2. These results suggest that during the second
generation <strong>of</strong> FAW larvae caged on plants, when bolls were
available, the larvae switched to feed on bolls, leaving the
new squares undamaged.
The infestation <strong>of</strong> FAW larvae in cotton plants at
blooming stage showed delayed development compared to
infestation at the boll stage or the average <strong>of</strong> two generations.
At blooming stage the larvae had access only to
leaves or squares. This confirms that young bolls are the
most suitable structures for FAW larval feeding in cotton.
The white mass <strong>of</strong> differentiating fiber in the interior <strong>of</strong>
bolls prior to boll maturity seems to be a suitable food for
FAW, in addition to the shelter that the boll affords to the

244 Barros et al.
larva. According to Meyer et al. (2004) young cotton bolls
before seed maturation do not contain gossypol, as the
seeds have not yet developed. Thus, FAW moths colonizing
cotton fields in early stages <strong>of</strong> boll development will
find suitable food for their larvae that survive and move to
the s<strong>of</strong>t bolls.
Although low performance is found for FAW larvae
infesting cotton plants in the blooming stage, development
and survival were sufficient to permit the population to
increase after completing two immature generations, only
one <strong>of</strong> which occurred when bolls were abundant. It is also
important to note that few bolls were available during the
infestation at Blooming 1 compared to the infestation at
Boll Stage or at Blooming 2. At the Blooming 2 stage, a second
immature generation occurred during the predominance
<strong>of</strong> s<strong>of</strong>t boll production by the plants.
Our results indicate that successful control <strong>of</strong> FAW in
the Brazilian Cerrado will depend on tracking the populations
across crop systems during and across seasons considering
the species <strong>of</strong> plants used for double cropping and
for cover crops in no-tillage planting systems. The use <strong>of</strong>
millet as a cover crop will <strong>of</strong>fer an excellent winter host for
FAW to build populations when not limited by winter
temperatures, from which FAW can colonize the major
summer crops such as corn, soybean, and cotton that compose
the Cerrado landscape. The timing <strong>of</strong> early maturation
<strong>of</strong> corn and soybean ( 90–110 days) overlaps with
the most favorable stage <strong>of</strong> cotton (pre-maturation boll
stage) for FAW. The need for area-wide and crop-system
management to deal with FAW is not a new concept
(Sparks, 1986). Polyphagous, mobile species all impose
similar needs to address management across landscapes.
This has been addressed for Helicoverpa armigera Hübner
in China and Australia (Wu, 2007; Herde, 2009), and
recently for plant bugs in the USA (Abel et al., 2007).
The slow development <strong>of</strong> FAW feeding only on cotton
leaves suggests that the outbreaks <strong>of</strong> FAW in cotton at the
boll stage will result from one to two previous generations
within cotton fields if only cotton is the source host. Otherwise,
the outbreak can be in advance from mass migration
<strong>of</strong> adults from nearby hosts during the maturation <strong>of</strong> other
crops and weeds that dominate the Cerrado landscape
(e.g., corn, soybean, and pasture). Egg production by FAW
was high irrespective <strong>of</strong> host used previously (Table 2),
which helps to compensate for low survival <strong>of</strong> young larvae
and, hence, the relatively high numbers <strong>of</strong> surviving larvae
are able to cause significant damage to available bolls. Possible
mass migration <strong>of</strong> adults seems to be an interesting
hypothesis testable by tracking larval population in the
crops and adult migration among the crops. Although
corn is considered the preferred host, FAW infests a large
number <strong>of</strong> cultivated and uncultivated plants that are
common in the Cerrado. These host plants can sustain
FAW populations and function as a reservoir between seasons.
Moreover, millet used as a winter cover crop provides
a highly suitable host for FAW, superior to corn based on
our results. Thus, FAW can find suitable developmental
hosts year-round in the Cerrado if temperature does not
impose developmental or survival limitations.
Acknowledgements
The authors acknowledge the support given, in the form <strong>of</strong>
research grants provided to the authors, by the agencies
FACEPE (Fundação de Amparo a Ciência e Tecnologia do
Estado de Pernambuco) and CNPq (Conselho Nacional
de Desenvolvimento Científico e Tecnológico), and
research funds provided by FINEP (Financiadora de Estudos
e Projetos).
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