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COMPATIBILITY OF F1 STERILITY AND A PARASITOID, COTESIA
MARGINIVENTRIS (HYMENOPTERA: BRACONIDAE), FOR MANAGING SPODOPTERA
EXIGUA (LEPIDOPTERA: NOCTUIDAE): ACCEPTABILITY AND SUITABILITY
OF HOSTS
J. E. Carpenter, Hidrayani1 and W. Sheehan2
Insect Biology and Population Management Research
Laboratory
1Andalas University
2E&C Consulting Engineers, Inc.
Abstract
The potential for combining two alternative pest
management tactics, F1 sterility and a parasitoid, was examined
in the laboratory and in the greenhouse. Studies compared the
acceptability and suitability of progeny from irradiated (100
Gy) and nonirradiated beet armyworm, Spodoptera exigua (Hübner),
males as hosts for Cotesia marginiventris (Cresson). Results from
these studies revealed that progeny of irradiated S. exigua males
and nonirradiated S. exigua females are acceptable and suitable
hosts for C. marginiventris development. Cotesia marginiventris
females showed no oviposition preference for S. exigua progeny
from females paired with either irradiated or nonirradiated males.
Cotesia marginiventris and F1 sterility appear to be compatible
tactics that potentially could be integrated into a preventative
pest management program for S. exigua.
Key Words: Spodoptera exigua, Cotesia marginiventris,
F1 sterility, inherited sterility, biological control
Resumen
Fue examinado el potencial de la combinación
de dos alternativas de manejo de plagas, esterilidad de la F1
y un parasitoide, en el laboratorio y en un invernadero. Los estudios
compararon la aceptación de la progenie del gusano de la
remolacha, Spodoptera exigua (Hübner), irradiado y no irradiado,
como hospedante de Cotesia marginiventris (Cresson). Los resultados
revelaron que la progenie de machos irradiados y de hembras no
irradiadas de S. exigua constituye un hospedante aceptable y adecuado
de C. marginiventris. Las hembras de C. marginiventris no mostraron
preferencia ovoposicional por la progenie de S. exigua proveniente
de hembras pareadas con machos irradiados o no irradiados. Cotesia
marginiventris y la esterilidad de la F1 parecen ser tácticas
compatibles que potencialmente podrían ser integradas en
un programa preventivo de manejo de plagas para S. exigua.
The beet armyworm, Spodoptera exigua (Hübner),
is a serious pest in cotton in the southeastern United States,
especially during outbreak conditions (Smith & Freeman 1994).
Although many factors have contributed to the outbreaks of S.
exigua in cotton, an unusually high level of resistance to some
pesticides is implicated (Sprenkel & Austin 1994). Alternative
management strategies, such as conservation of natural enemies
(Ruberson et al. 1994), mating disruption with synthetic pheromone
(Wakamura & Takai 1992), and inherited sterility, are being
studied for their potential role in an integrated pest management
program for S. exigua.
The potential for using F1 sterility as a component
of regional management of lepidopteran pests has been suggested
by Knipling (1970) and LaChance (1985), and numerous laboratory
and cage studies on pests around the world have supported these
ideas (LaChance 1985, Anonymous 1993). The successful application
of the F1 sterility principle to a wild population of Helicoverpa
zea (Boddie) during a recent pilot test encouraged further development
of this pest control strategy (Carpenter & Gross 1993). However,
the high cost of rearing lepidopterans, relative to the cost of
rearing dipterans, has moderated researchers’ enthusiasm concerning
the use of F1 sterility for the control of lepidopteran pests.
Nevertheless, Carpenter & Gross (1993) revealed that even
a low irradiated:wild insect ratio could significantly reduce
the seasonal increase of H. zea. In addition, population models
(Knipling 1992, Carpenter 1993) have suggested that F1 sterility
would be more efficient if combined with other pest control strategies.
Therefore, recent studies have investigated the potential of integrating
F1 sterility and parasitoids for increased efficiency in suppression
of pest populations.
Mannion et al. (1994 & 1995) studied the compatibility
of F1 sterility in H. zea and the tachinid parasitoid, Archytas
marmoratus (Townsend). They found these two control strategies
to be compatible and suggested that combining the two strategies
may be useful for managing early season populations of H. zea.
However, caution should be exercised in the extrapolation of these
results to other lepidopteran pests, such as S. exigua. Parasite/host
relationships are highly variable as a result of the various reproductive
strategies of both host and parasite species. For example, H.
zea females lay individual eggs spaced some distance apart which
reduces mortality from larval cannibalism. Alternatively, S. exigua
females lay eggs in masses, and larvae feed gregariously, in a
patch, during their first two instars. Also, A. marmoratus larviposits
many maggots in the vicinity of late instar H. zea, whereas a
common parasitoid for S. exigua, Cotesia marginiventris (Cresson),
stings individual, early instars.
The objectives of the present laboratory and greenhouse
studies were: (1) to compare the acceptability and suitability
of progeny from irradiated (100 Gy) and nonirradiated S. exigua
males mated with nonirradiated females as hosts for C. marginiventris,
and (2) to relate these findings to the potential of combining
the F1 sterility technique with resident or released C. marginiventris
for managing populations of S. exigua.
Materials and Methods
Insects
Cotesia marginiventris and S. exigua were obtained
from laboratory colonies at the Insect Biology and Population
Management Research Laboratory, Tifton, GA. All S. exigua larvae
were reared in plastic cups (30 ml) containing a meridic diet
(Burton 1969) at 27 ± 1°C with a photoperiod of 14:10
(L:D) h. Cotesia marginiventris was reared on S. exigua larvae
at the same temperature and photoperiod regime.
F1 Sterility Technique
The “irradiation treatment” (I) larvae
were those S. exigua larvae resulting from the mating of a nonirradiated
female moth with an irradiated male moth. The “normal treatment”
(N) larvae originated from crosses between nonirradiated moths.
Larvae from both treatments were reared as above. Adult males
undergoing irradiation were <24 h old and were irradiated (100
Gy) at about 20°C with a well-type 60Co source (Gammarad
Irradiator, Model GR-12, U.S. Nuclear Division, Irvine, CA) delivering
about 65 Gy per min. Dose calibration with an X-ray monitor and
probe indicated a dose error of approximately ±5%.
Suitability of Progeny from Irradiated Males as Hosts
Spodoptera exigua larvae from both treatments (I
& N) were stung by C. marginiventris. After a single sting,
the host larva was transferred to a one-ounce, clear cup containing
diet. A cardboard lid was placed on the cup and the host was allowed
to complete its development. Hosts were scored as producing either
a pupa or a parasitoid cocoon. Comparisons between larval treatments
were made when host larvae were early 1st instars, late 2nd instars,
early 3rd instars, and mid 3rd instars. Percent parasitism was
calculated as the number of hosts in a treatment producing parasitoid
cocoons divided by the total number of hosts in a treatment, multiplied
by 100. Wasps developing from larvae stung as 2nd instars (n=7
for I larvae, n=9 for N larvae) were compared for time of development,
adult weight, fecundity, and longevity. Data were subjected to
an unequal n, unequal variance t-test (Steel & Torrie 1980)
to separate differences between larval treatments (a=0.05).
Acceptability of Progeny from Irradiated Males as
Hosts
A single C. marginiventris female was placed onto
a cotton leaf in a large, open petri dish. The leaf had feeding
damage from the previous night and 10 unstung S. exigua larvae.
The following behavioral events were recorded: (1) time before
flying off the ‘patch’ (area containing a group of feeding larvae);
(2) number of stings before flying off a patch (maximum = five);
(3) number of ‘walkbys’ (walking past an unstung host within one
half wasp body length); and (4) number of ‘rejections’ (antennating
unstung host without stinging). Comparisons between larval treatments
were made when host larvae were early 1st instars, late 2nd instars,
early 3rd instars, and mid 3rd instars. Behavioral responses from
these “no-choice” experiments were recorded from ten
wasps for each larval treatment and each host age. Comparisons
between treatments were made using the t-test (Steel & Torrie
1980).
Oviposition Preference Test for Cotesia marginiventris
Four cotton plants (2-3 months old, DPL 90) were
placed in a cage in the greenhouse. I and N larvae were used as
host treatments. A host “patch” for each treatment was
established by confining 40 1st instars in a circle (4 cm diam)
on the surface of a leaf and allowing the larvae to feed for one
day. Within the cage, there were two host patches for each treatment
and one patch per plant. Eight female C. marginiventris (2-3 days
old) were released in the cage and allowed to search for and parasitize
larvae for approximately 4 h. Host larvae were removed from the
cage and dissected to determine the number parasitized. This test
was replicated five times. Percent parasitism was calculated as
the number of hosts in a treatment containing one or more parasitoid
eggs divided by the total hosts in the treatment, multiplied by
100. Because there were no differences between the percent parasitism
among patches within each larval treatment, patches for each treatment
were pooled for analysis. Comparisons between larval treatments
were made using the pooled t-test (Steel & Torrie 1980).
Table 1. Days to emergence, adult weight, fecundity,
and longevity of Cotesia marginiventris developing in progeny
of irradiated (I) (100 gy) and non-irradiated (N) Spodoptera exigua
males crossed with normal females, parasitized as second instars.
Parent Cross of Host Larvae
1Means followed by the same letter are not significantly
different (P < 0.05) (t-test).
Results and Discussion
Suitability of Progeny from Irradiated Males as Hosts
Results from this study revealed that progeny of
irradiated male S. exigua were generally suitable hosts for C.
marginiventris. Wasps developing in progeny of irradiated males
had a mean weight that was significantly (P >0.05) lower than
wasps developing in progeny of nonirradiated males. However, parasitoid
development, longevity, and fecundity were not significantly influenced
by the host larval treatment (Table 1). First and second instars
of S. exigua were more suitable as hosts for C. marginiventris
than third instars, but host suitability within instars was not
significantly affected by the larval treatment (Table 2). The
percentage of stung larvae that produced C. marginiventris cocoons
was similar for both larval treatments, regardless of the host
age.
Table 2. Effect of larval age of progeny of irradiated
(I) (100 gy) and non-irradiated (N) Spodoptera exigua males crossed
with normal females and as suitable hosts for Cotesia marginiventris
Parental cross of host larvae
1There was no significant difference due to larval
treatment (P ² 0.05) (t-test).
Table 4. Cotesia marginiventris oviposition preference
between progeny of irradiated (I) (100 Gy) and non-irradiated
(N) Spodoptera exigua males crossed with normal females
Parental Cross of Host Larvae
1Means followed by the same letter are not significantly
different (P ² 0.05) (t-test).
Acceptability of Progeny from Irradiated Males as
Hosts
Host acceptability was not significantly affected
by the larval treatment (Table 3). The behavior of female C. marginiventris
foraging in larval patches was similar for both larval treatments,
regardless of the host age.
Oviposition Preference Test for Cotesia marginiventris
Cotesia marginiventris females showed no oviposition
preference between irradiated and nonirradiated male S. exigua
progeny. The mean percentage of larvae parasitized within N larvae
and I larvae patches did not differ significantly (Table 4).
Fully successful integration of F1 sterility and
parasitoids into a pest management approach can occur only if
parasitoid strategies do not negatively impact irradiated insects
and their progeny more than those of the wild population, and
if F1 sterility does not negatively impact the efficacy of parasitoids.
Results from these studies indicate that C. marginiventris and
F1 sterility in S. exigua are compatible control strategies. The
compatibility of these two strategies is congruent with the findings
of Mannion et al. (1994, 1995). Carpenter (1993) suggested several
scenarios in which the integration of compatible strategies such
as F1 sterility and parasitoids might be used to control lepidopteran
pest populations. For example, sterile S. exigua larvae could
be field-reared on early season host plants or nursery crops.
Cotesia marginiventris (native and/or released) could use these
sterile larvae as hosts and, thereby, increase the parasitoid’s
early season population. Other natural enemies of S. exigua may
also use these sterile hosts. Larvae that escaped the natural
enemies would produce sterile adult S. exigua that would reduce
the reproductive potential of the next generation of S. exigua.
Cotesia marginiventris is considered the dominant
parasitoid of S. exigua in the eastern half of the United States
(Tingle et al. 1978, Ruberson et al. 1994). This parasitoid is
part of a large natural enemy complex that has the capacity to
suppress S. exigua populations in cotton. However, S. exigua can
become a serious pest of cotton, especially when the natural enemy
complex has been disrupted (Ruberson et al. 1994). When S. exigua
populations escalate, growers often are reluctant to postpone
insecticide applications until the natural enemy complex has brought
the S. exigua population under control. Pedigo (1995) suggested
that the development of new integrated pest management programs
should provide a special focus on the identification of preventative
tactics. Ruberson (1994) emphasized the usefulness of conserving
natural enemies for effective suppression of S. exigua. Because
F1 sterility and C. marginiventris are compatible and may provide
synergistic effects, further studies are warranted to test the
practicality and efficacy of integrating these two tactics for
controlling S. exigua.
References Cited
Anonymous. 1993. Proc. Intl. symposium on management
of insect pests: Nuclear and related molecular and genetic techniques.
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Burton, R. L. 1969. Mass rearing the corn earworm
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and other pest management strategies for Helicoverpa zea: Status
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pests: Nuclear and related molecular and genetic techniques. Jointly
organized by the Intl. Atomic Energy Agency and the Food and Agric.
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pp. 363-370.
Carpenter, J. E., and Gross, H. R. 1993. Suppression
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the infusion of inherited sterility from released substerile males.
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by releasing partially sterile males: A theoretical appraisal.
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Knipling, E. F. 1992. Principles of insect parasitism
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LaChance, L. E. 1985. Genetic methods for the control
of lepidopteran species. USDA, Agric. Res. Serv. ARS. 28. 40 pp.
Mannion, C. M., J. E. Carpenter, and H. R. Gross.
1994. Potential of the combined use of inherited sterility and
a parasitoid, Archytas marmoratus (Diptera: Tachinidae), for managing
Helicoverpa zea (Lepidoptera: Noctuidae). Environ. Entomol. 23:
41-46.
Mannion, C. M., J. E. Carpenter, and H. R. Gross.
1995. Integration of inherited sterility and a parasitoid, Archytas
marmoratus (Diptera: Tachinidae), for managing Helicoverpa zea
(Lepidoptera: Noctuidae): Acceptability and suitability of hosts.
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Table 3. Effect of host age on the mean response
of Cotesia marginiventris to progeny of irradiated (I)(100 Gy)
and nonirradiated (N) Spodoptera exigua males crossed with normal
females
Behavioral Event1
1Walkby = walking past an unstung host within one-half
wasp body length. Rejection = antennating unstung host without
stinging
2There was no significant difference due to larval
treatment (P ² 0.05) (t-test).
Agricultural Research Service
U. S. Department of Agriculture
Tifton, GA 31793-0748
Padang, Indonesia
2175 Highpoint Road
Snellville, GA 30278
Mean (S. D.)1
Days To Emergence
Wasp Wt
(mg)
No. Eggs
Laid
Longevity
Days
N/ × N?
10.8 a
1.03 a
70.7 a
17.9 a
(0.68)
(0.08)
(30.1)
(1.8)
N/ × N?
11.2 a
0.91 b
94.0 a
16.7 a
(0.47)
(0.09)
(45.3)
(1.6)
Mean ± S.E. % Stung Larvae Producing a Cocoon (n)1
Early 1st
Instar
Late 2nd
Instar
Early 3rd Instar
Mid 3rd
Instar
N/ × N?
66.7 ± 11
90 ± 6
39 ± 9
30 ± 9
(18)
(29)
(28)
(30)
N/ × N?
83.3 ± 9
87.1 ± 6
44 ± 9
29 ± 9
(18)
(31)
(27)
(29)
n
Mean % Parasitism of Larval Patch (S.D.)1
N/ × N?
10
23.1 a
(12)
N/ × N?
10
31.4 a
(16)
N
Mean ± S.E. Response to Host Age and Larval
Treatment2
Early 1st Instar
Late 2nd Instar
Early 3rd Instar
Mid 3rd Instar
N
I
N
I
N
I
N
I
Time before flying off (min.)
10
-
-
1.9 ± 0.5
2.3 ± 0.3
3.5 ± 0.4
3.6 ± 0.4
2.1 ± 0.3
2.5 ± 0.4
No. of stings before flying off
(max. = 5)
10
4.5 ± 0.3
4.7 ± 0.2
5
5
3.2 ± 0.5
3.5 ± 0.4
2.3 ± 0.4
1.9 ± 0.7
Walkby
10
2.6 ± 0.4
2.4 ± 0.4
0.2 ± 0.1
0.2 ± 0.1
0
0
0.6 ± 0.3
0.5 ± 0.2
Rejection
10
0
0
0.5 ± 0.3
0.3 ± 0.2
0.5 ± 0.2
0.7 ± 0.4
0.8 ± 0.2
1.0 ± 0.5