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Seasonal parasitism and biologicalcharacteristics of Habrobraconhebetor (Hymenoptera: Braconidae)– a potential larval ectoparasitoid ofHelicoverpa armigera (Lepidoptera:Noctuidae) in a chickpea ecosystemHem Saxena a , Duraimurugan Ponnusamy a & Mir Asif Iquebal ba Division of Crop Protection , Indian Institute of Pulses Research ,Kanpur , Indiab Division of Biometrics and Statistical Modelling , IndianAgricultural Statistics Research Institute , New Delhi , IndiaAccepted author version posted online: 16 Jan 2012.Publishedonline: 13 Mar 2012.

To cite this article: Hem Saxena , Duraimurugan Ponnusamy & Mir Asif Iquebal (2012) Seasonalparasitism and biological characteristics of Habrobracon hebetor (Hymenoptera: Braconidae) – apotential larval ectoparasitoid of Helicoverpa armigera (Lepidoptera: Noctuidae) in a chickpeaecosystem, Biocontrol Science and Technology, 22:3, 305-318, DOI: 10.1080/09583157.2012.656579

To link to this article: http://dx.doi.org/10.1080/09583157.2012.656579

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RESEARCH ARTICLE

Seasonal parasitism and biological characteristics of Habrobraconhebetor (Hymenoptera: Braconidae) � a potential larval ectoparasitoid

of Helicoverpa armigera (Lepidoptera: Noctuidae) in a chickpeaecosystem

Hem Saxenaa*, Duraimurugan Ponnusamya and Mir Asif Iquebalb

aDivision of Crop Protection, Indian Institute of Pulses Research, Kanpur, India; bDivision ofBiometrics and Statistical Modelling, Indian Agricultural Statistics Research Institute, New

Delhi, India

(Received 28 September 2011; final version received 6 January 2012)

Seasonal parasitism of Habrobracon hebetor (Say) on Helicoverpa armigera(Hubner) in chickpea was studied for three consecutive years. Parasitism byH. hebetor on larvae of H. armigera reached 12.3%. The parasitoid maintainedreproductive activity on H. armigera from February to April coinciding with podformation and maturation stages of the crop. In laboratory assays, we investigatedthe suitability of larval instars of H. armigera to the parasitoid H. hebetor. Thisparasitoid attacked third to sixth instars, though fourth and fifth instar larvaewere found most suitable with 100% parasitism and development to adults.Parasitoid developmental time was longest in fifth instar (9.1 days) compared toother instars (8.1�8.9 days). Fifth instar larvae resulted in highest numbers ofcocoons and adult emergence. In addition, suitability of seven lepidopteranspecies to H. hebetor was investigated. Corcyra cephalonica, Galleria mellonellaand H. armigera were the most suitable hosts with 100% parasitism anddevelopment to adults. It was followed by Maruca vitrata and Autographanigrisigna with 60�76.7% and 40�70% parasitism and parasitoid developmentalsuccess, respectively. Though there was 23.3% parasitism, there was no parasitoiddevelopment in Spodoptera litura. No parasitism was recorded in Spilarctiaobliqua. Development of H. hebetor was most rapid in C. cephalonica (8.7 days),and longest in G. mellonella (9.3 days). Parasitoids that developed on these hostsresulted in highest numbers of cocoons and adult emergence. The parasitoid couldbe exploited for the biological control of H. armigera in a chickpea ecosystem.

Keywords: Habrobracon hebetor; Helicoverpa armigera; chickpea; host instar;host species; biological control

Introduction

Chickpea (Cicer arietinum L.) is the third most important grain legume in the world

after dry beans (Phaseolus spp.) and field pea (Pisum sativum L.). It is an important

source of protein, minerals, fibre and vitamins in the diets of millions of people in

Asia and Africa. Chickpea is cultivated on about 11 m ha adding 8.8 m tonnes to the

global food basket (Rao, Birthal, Bhagavatula, and Bantilan 2010). There are many

factors which influence the production of chickpea among which are insect pests,

*Corresponding author. Email: hem_saxena@yahoo.com

Biocontrol Science and Technology,

Vol. 22, No. 3, March 2012, 305�318

ISSN 0958-3157 print/ISSN 1360-0478 online

# 2012 Taylor & Francis

http://dx.doi.org/10.1080/09583157.2012.656579

http://www.tandfonline.com

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particularly the gram pod borer Helicoverpa armigera (Hubner) (Lepidoptera:

Noctuidae) (Rao et al. 2010).

Among the natural enemies of H. armigera recorded in chickpea ecosystem,

Campoletis chlorideae Uchida (Hymenoptera: Ichneumonidae) is an important larval

endoparasitoid that causes up to 50% parasitisation under natural conditions (Nema

2010). However, activity of the parasitoid occurs only during November to February,

coinciding with the vegetative stage of the crop. In North India, during March to

April, H. armigera damage coincides with the fruiting stage of chickpea causing

heavy losses (Sachan and Katti 1994). In a survey conducted to explore a potential

parasitoid coinciding with the fruiting stage of chickpea, we recorded a gregarious

larval ectoparasitoid Habrobracon (Bracon) hebetor (Say) (Hymenoptera: Braconi-

dae) on H. armigera in chickpea fields in Kanpur district, Uttar Pradesh (Saxena and

Duraimurugan 2009). Therefore, the present study was aimed at understanding the

seasonal parasitism of H. hebetor on H. armigera in chickpea ecosystems. We also

examined the suitability of H. armigera and six other lepidopteran species as hosts to

H. hebetor. Such information is essential for mass culture and utilisation of

H. hebetor as a major biological control agent of H. armigera.

Materials and methods

Test insects

Laboratory culture of H. armigera was established from larvae collected in chickpea

fields at the New Research Farm, Indian Institute of Pulses Research (IIPR), Kanpur

during November and December 2008. The larvae were maintained on a chickpea-

based semi-synthetic diet (Armes, Bond, and Cooter 1992) and reared in groups until

the early third instar. Henceforth, they were reared individually in plastic containers

(6 cm height�4 cm diameter). Air circulation in the container was ensured through

a hole (diameter 1 cm) in the lid, covered with nylon mesh. The container and diet

were replaced on alternate days and larvae were continuously reared until they

pupated. Four days after pupation, pupae were washed in running tap water, surface

sterilised by immersing in 0.5% sodium hypochlorite solution, followed by rinsing in

water and then placed on filter paper to dry. The pupae were transferred to a

40�40�40 cm emergence cage. Newly emerged adults were sexed and five pairs of

adults were transferred to plastic buckets (7 L capacity) maintaining the sex ratio of

1:1 for mating and oviposition. Adults were fed with 10% sugar solution enriched

with ABDEC vitamin solution. The plastic bucket was covered with sterile white

muslin cloth, which served as an oviposition substrate. Daily, the cages were checked

and the muslin cloth on which the eggs were laid was removed and replaced by a

fresh, sterile one. The sugar solution in the glass vials was also refilled daily. The

cages were kept in a culture room maintained at 90% RH, 278C with a photoperiod

of 14:10 (L:D). Newly hatched larvae from the eggs laid on muslin cloth were

transferred to plastic trays (30�15�5 cm) containing a 3 mm layer of semi-

synthetic diet. The tray was kept in an inverted position in dark after closing the lid

tightly. The larvae were allowed to grow until the early third instar stage followed by

rearing individually in plastic containers, as described earlier.

Field collected larvae of the tobacco caterpillar, Spodoptera litura (Fabricius)

[Lepidoptera: Noctuidae]; the Bihar hairy caterpillar, Spilarctia obliqua (Walker)

306 H. Saxena et al.

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[Lepidoptera: Arctiidae] and legume pod borer, Maruca vitrata (Geyer) [Lepidop-

tera: Pyralidae] (collected from mungbean during October 2008), the semilooper,

Autographa nigrisigna (Walker) [Lepidoptera: Noctuidae] (collected from chickpea

during December 2008) were continuously reared on their natural hosts. Thelaboratory hosts rice moth, Corcyra cephalonica (Stainton) [Lepidoptera: Pyralidae]

and greater wax moth, Galleria mellonella (Linnaeus) [Lepidoptera: Galleridae] were

obtained from the Department of Entomology, Narendra Dev University of

Agriculture and Technology, Faizabad were reared on respective natural hosts

broken maize and wax comb.

Parasitoid

A laboratory colony of H. hebetor was established from parasitised H. armigera

larvae collected from New Research Farm (IIPR, Kanpur) during March 2009.

H. hebetor was reared in the laboratory at 25928C, 6595% RH, and a 14:10 (L:D)

photoperiod using larvae of H. armigera as hosts. H. armigera larvae wereindividually placed in a plastic container (30�15 cm) and a pair of adult parasitoids

was released. A cotton swab soaked in 50% honey solution was kept in the container

for H. hebetor adults. The mouth of the container was covered with black muslin

cloth and fastened with rubber band. After 48 h, the parasitoid was removed and the

parasitised larvae were held until adult parasitoids emerged. These were then used

for the experiments.

Seasonal parasitism of H. hebetor on H. armigera in chickpea

Field studies were carried out on chickpea at New Research Farm (26827?N, 80814?E;

152.4 m), IIPR, Kanpur during post-rainy season over a period of three years (2007�2010). The chickpea seeds were sown in sandy loam soil with pH 8.16, EC 0.21 dS/m,organic carbon 0.24%, available P 11.88 kg/ha and available K 126 kg/ha. In all the

three years, the kabuli chickpea variety ‘JKG 1’ was sown during last week of

November with a spacing of 30�10 cm and plot size of 0.20 ha. A fertiliser of 20 kg

N and 50 kg P2O was applied. Recommended crop management practices were

adopted except that no insecticide was sprayed. To record the natural parasitism and

seasonal activity of parasitoids, the larval population of H. armigera was monitored

at weekly intervals beginning 15�21 days after the date of sowing and continued until

crop maturity. On each sampling date, observations were taken from 100 randomlyselected plants at four places (25 plants/place) selected diagonally across the field.

The plants were checked for the presence of H. armigera larvae and when collected,

were kept individually in a plastic container. The field-collected larvae were brought

back to the laboratory and reared on a chickpea based semi-synthetic diet (Armes,

Bond, and Cooter 1992) under laboratory conditions [25928C, 6595% RH, and a

14:10 (L:D) photoperiod] until the parasitoids emerged, or until H. armigera adult

emergence (Figures 1 and 2). Parasitoids were identified by Prof. M. Hayat, Emeritus

Scientist, Department of Zoology, Aligarh Muslim University, Aligarh, UttarPradesh, India.

A correlation coefficient was estimated to determine the relationship between

weather parameters and per cent parasitism (Schliserman 2001). For the analysis, the

mean maximum temperature, minimum temperature, relative humidity, wind speed,

Biocontrol Science and Technology 307

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Figure 1. Field collected healthy and parasitised larvae of Helicoverpa armigera in chickpea ecosystem.

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Figure 2. Different developmental stages of Habrobracon hebetor on Helicoverpa armigera.

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sunshine hours and rainfall during the sampling week and the corresponding per

cent parasitism were used.

Host instar suitability for the parasitoid

A no-choice test was conducted to determine the suitability of different larval instars

of H. armigera to H. hebetor under laboratory conditions. For studying the host

instar acceptance (paralysation, parasitisation and parasitioid developmental

success) by the parasitoid, newly-moulted larvae of each instar (first to sixth instar

larva) of H. armigera were placed individually in a plastic container (10�5 cm)

along with the diet. Larval instars were determined by checking the shed headcapsules. A single, four-day old, mated H. hebetor female, without prior access to

hosts, was released into each container along with diet. Forty-eight hours after their

introduction, the parasitoids were removed from the plastic container and the per

cent of the host instar larvae paralysed was assessed. For assessing parasitism, host

instar larvae were examined, and the presence of parasitoid eggs or larvae

determined. Parasitised host larvae were monitored daily and proportion of

parasitised hosts that successfully yielded live wasps (parasitoid developmental

success) was determined. For studying the host instar suitability for the parasitoid,

newly moulted third, fourth, fifth and sixth instars of H. armigera (host instars that

did not yield a live parasitoid in the acceptance test were discarded) were individually

kept in a plastic container together with artificial diet. Individual four-day old mated

female parasitoids, without prior access to hosts, were released into each plastic

container as described earlier. After 48 h, the parasitoid was removed and parasitised

larvae were allowed to develop. The parasitised larvae were checked at 12 h intervals

and the developmental time (egg to adult emergence), number of cocoons formed,

number of adult parasitoids emerged, sex ratio and longevity of adult parasitoids

were recorded. The emerged parasitoids were transferred to test tubes (5�1.5 cm)

containing 50% honey solution and adult longevity was calculated by observing daily

mortality. In all the experiments, 30 larvae for each host-instar (three replicates each

of 10 larvae) were used in completely randomised design.

Suitability of parasitoid on different hosts

Seven lepidopteran species (rice moth, Corcyra cephalonica; greater wax moth,

Galleria mellonella; tobacco caterpillar, Spodoptera litura; semilooper, Autographa

nigrisigna; legume pod borer, Maruca vitrata and Bihar hairy caterpillar, Spilarctia

obliqua; and gram pod borer, Helicoverpa armigera) were tested for acceptance and

suitability by the parasitoid in a no-choice test using plastic container (10�5 cm)

with a single host larva under laboratory conditions. A laboratory colony of

H. hebetor established from parasitised H. armigera larvae and cultured on

H. armigera as described earlier was used for the experiment. Newly moulted fifth

instar larvae of each host were individually placed in a plastic container along with

their natural hosts and a 4-day old mated female parasitoid was released as described

earlier. After 48 h, the female adult parasitoid was removed and the parasitised larva

was held in the container and allowed to develop. Observations on hosts paralysed,

parasitism and parasitoid developmental success were similar to the method

310 H. Saxena et al.

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described earlier for studying the influence of different larval instars of H. armigera

on the parasitoid.

Statistical analysis

The association between weather parameters and per cent parasitism were computed

using Pearson’s correlation coefficient using SPSS software. An analysis of variance

(ANOVA) was conducted on all data related to suitability of the parasitoid on host

instars of H. armigera and on different host species using SAS statistical softwareversion 9.2. Following ANOVA, differences between data-sets were determined using

Tukey-Kramer post hoc tests and the accepted level of significance was P50.05 in

all instances. Data are presented as means9standard error (SE), where means within

the same column and followed by different letters are significantly different

(P50.05; Tukey’s test).

Results

Seasonal parasitism of Habrobracon hebetor on Helicoverpa armigera in chickpea

The data on seasonal parasitism of H. armigera by H. hebetor in chickpea during the

post-rainy season of three consecutive years (2007�2010) are presented in Figure 3.

The occurrence and percentage parasitism varied between years. In all three years,

the parasitoid remained almost nil up to the third week of February and itsparasitism was observed only in the last week of February to third week of April,

coinciding with pod formation and maturation stage of the crop. Mean parasitism by

H. hebetor on larvae of H. armigera during all three years ranged from 0.9 (2010) to

12.3% (2009). Higher parasitism of 2.0�12.3% occurred between the last week of

February to second week of April. Adult emergence per parasitised larva of

H. armigera during these three years varied from 7.0 to 17.3 and the progeny sex

ratio varied across the standard meteorological weeks and years (Figure 4). Parasitic

activity did not show any significant correlation with abiotic factors.

Host instar suitability

Habrobracon hebetor paralysed all the developmental stages of H. armigera presented

under no-choice tests. However, significant differences were observed in theparasitism and parasitoid developmental success (egg to adult) by H. hebetor in

different larval instars of H. armigera (Tukey’s test, P50.05). In both cases, fourth

and fifth instar larvae were most suitable, representing 100% parasitism and

parasitoid development. Sixth instar larvae were the next most suitable for

parasitism (96.7%) and parasitoid development (95.0%) followed by third instars

(68.3% parasitism and 56.7% parasitoid development). There was no parasitism and

parasitoid development in first and second instars, though the parasitoid paralysed

these instars (Figure 5).Different instars of H. armigera greatly affected the biology and development of

the parasitoid (Table 1). When parasitism took place on fifth instars, parasitoid

developmental time (egg to adult emergence) was significantly longer (9.1 days) than

on larvae from other instars (8.1�8.9 days). Similarly, fifth instar larvae provided

Biocontrol Science and Technology 311

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Figure 3. Percentage of Helicoverpa armigera larvae parasitised by Habrobracon hebetor and

its association with weather parameters.

312 H. Saxena et al.

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higher numbers of cocoons (11.6) per host larva, adult emergence (98.7%) and

longevity of females (19.5 days) and males (9.6 days) than for parasitoids exposed to

other instars. The progeny sex ratio was male biased irrespective of host instar.

Suitability of parasitoid on different hosts

Among the larvae of seven lepidopteran species exposed to H. hebetor in no-choice

tests, 100% paralysation was recorded in all the species except S. obliqua (43.3%).

Significant differences were recorded in the parasitism and parasitoid developmental

0

5

10

15

20

25

30

35

9 10 11 12 13 14 15 16

Standard meteorological week

Female (2010)

Male (2010)

Female (2009)

Male (2009)

Female (2008)

Male (2008)

No.

of a

dults

em

erge

d pe

r la

rva

Figure 4. Mean number of adults emerged and sex ratio of Habrobracon hebetor from field

collected parasitised larvae of Helicoverpa armigera in chickpea.

0

20

40

60

80

100

I instar II instar III instar IV instar V instar VI instar

Per

cent

age

mea

n

% Paralyzation

% Parasitism

% Parasitoiddevelopmentalsuccess

Host instar

a c c a c c a b b a a a a a a a a a

Figure 5. Effects of host instar on per cent paralysation, parasitism and parasitoid

developmental success of Helicoverpa armigera host parasitised by Habrobracon hebetor in

no-choice test. Means followed by the same letter in the column are not significantly different

(Tukey’s test) at a�5% (p�0.05).

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success in different host species (Tukey’s test, P50.05). Among the seven host

species, C. cephalonica, G. mellonella and H. armigera were the most suitable hosts,

with 100% parasitism and parasitoid development. It was followed by M. vitrata and

A. nigrisigna with 60�76.7% and 40�70% parasitism and parasitoid development,

respectively. There was no parasitoid developmental success in S. litura, though there

was 23.3% parasitism. No parasitism was recorded in S. obliqua (Figure 6).

Different host species significantly affected the survival and development of the

parasitoid (Table 2). The developmental time of H. hebetor on G. mellonella wassignificantly longer than other hosts (9.3 days), and similar to H. armigera (9.0 days)

and M. vitrata (9.0 days). Most rapid parasitoid development was observed in

C. cephalonica (8.7 days), which was on par with A. nigrisigna (8.8 days). The

parasitoids that developed on G. mellonella and C. cephalonica gave the highest

number of cocoons per host larva (16.7 and 14.4, respectively). It was followed by

H. armigera and M. vitrata which recorded a higher number of cocoons per host larva

(11.1 and 7.9, respectively) as compared to A. nigrisigna (4.2). Emergence of adults

was highest on C. cephalonica (97.6%), H. armigera (97.3%) and G. mellonella (95.4%).Similarly, adult longevity of female and male parasitoid was highest on C. cephalonica

(21.3 and 13.7 days) and G. mellonella (20.8 and 12.7 days), followed by H. armigera

(19.3 and 9.3 days). In contrast, parasitoids developing on A. nigrisigna and

M. vitrata recorded lowest adult emergence and adult longevity. The development

of parasitoids in all host species showed a male-biased sex ratio in their progeny.

Discussion

Although a large number of parasitoids have been reported attacking various stages

of H. armigera, only a few parasitoids contribute to regulation of H. armigera

populations in the chickpea ecosystem due to presence of glandular and non-glandular trichomes on the surface of the calyxes and pods and also due to the acid

exudates (Romeies, Shanmower, and Gupta 1997). In North India, Campoletis

chlorideae is the most efficient parasitoid of H. armigera in chickpea, and it

preferentially attacks early instars (second and third instar larvae) which feed mostly

Table 1. Survival and development of Habrobracon hebetor parasitising host instars of

Helicoverpa armigera.

Mean9SE

Adult longevity (days)

Host instar

Egg to adult

emergence

(days)

No. of

cocoon per

larva

Percentage of

adult

emergence

Sex ratio

(M:F) Female Male

Third instar 8.190.25b 3.390.65c 67.8911.01b 0.8390.20a 16.991.16b 8.590.39b

Fourth

instar

8.390.14b 8.390.82b 96.792.95a 0.7190.14ab 19.490.38a 9.390.36a

Fifth instar 9.190.20a 11.691.22a 98.790.93a 0.7390.09ab 19.590.48a 9.690.41a

Sixth instar 8.990.43a 8.190.72b 94.693.86a 0.5590.12b 18.790.34a 8.790.20b

Note: Means followed by the same superscript letter in the column are not significantly different (Tukey’stest) at a�5% (p�0.05).

314 H. Saxena et al.

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on leaves (Dhillon and Sharma 2009). However, its occurrence and parasitism during

pod formation in March and April are very low (Yadava, Lal, Ahmad, and Sachan

1991). The braconid parasitoid, H. hebetor is known almost exclusively as a

parasitoid of pyralid moth larvae infesting stored grain (Eliopoulos and Stathas

2008). Previously, field parasitism of lepidopteran insects by H. hebetor was reported

in tea (Subbiah 1995), cotton (Gerling 1971) and coconut (Nasser and Abdurahiman

2001). However, no previous information is available on the seasonal occurrence of

the parasitoid on H. armigera in the chickpea ecosystem.

Seasonal occurrence and field parasitism of H. hebetor over three years indicated

parasitoid activity coinciding with the pod formation and pod maturation (February

to April) and mean percentage parasitism ranged from 0.9 to 12.3. Saxena (2007)

discussed the influence of climate change and development of large-seeded varieties

in chickpea on the feeding behaviour of H. armigera. She suggested that late instar

larvae prefer feeding on grain while completely within the pod, as compared to the

normal feeding habit of larvae as they feed with only their head inside the pod. This

behaviour may favour parasitism and population growth of H. hebetor on

H. armigera in chickpea. Interesting aspects of this parasitoid bio-ecology, that is,

occurrence in February to March and preference for late instar larvae of H. armigera,

indicate its non-competitive nature with C. chlorideae, which prefers early instar

larvae and occurs during November to February.

Many parasitoids exhibit a marked preference for a specific instar or larval stage

(Mackauer 1990; Mattiacci and Dicke 1995; McGregor 1996). We observed that late

instar larvae of H. armigera (fourth to sixth instars) were most suitable for successful

parasitism and development of H. hebetor. Parasitoid developmental rate is

0

10

20

30

40

50

60

70

80

90

100

Helicoverpaarmigera

Marucavitrata

Autographanigrisigna

Spodopteralitura

Spilarctiaobliqua

Corcyracephalonica

Galleriamellonella

Host species

Per

cent

age

mea

n

% Paralyzation % Parasitism % Parasitoid developmental success

a a a a b c a c d b c d a a a a a aa ab b

Figure 6. Effects of lepidopteran host species on per cent paralysation, parasitism and

parasitoid developmental success by Habrobracon hebetor in no-choice test. Means followed

by the same letter in the column are not significantly different (Tukey’s test) at a�5%

(p�0.05).

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frequently greater with older host larvae, presumably because more abundant

nutrients are available to support development of parasitoids in larger hosts (Vinson

and Iwantsch 1980; Lawrence 1990; Pennacchio, Vinson, and Tremblay 1993;

Harvey, Kadash, and Strand 2000). Higher numbers of cocoons, and greater adult

emergence and longer adult longevity of H. hebetor was recorded in the later instar

larvae (fourth to sixth instars) as compared to third instar larvae. This agrees with

Beckage and Templeton (1985), who found that maximum host larval size attracts

female oviposition and supports development of their progeny. The parasitoid,

Campoletis sonorensis (Hymenoptera: Ichneumonidae) develops faster in younger

H. virescens larvae and, specifically, total developmental time from oviposition to

adult emergence was significantly shorter when first or second instar hosts were

parasitised compared to later instars (Hu and Vinson 2000). Similarly, our results

showed that the developmental time of parasitoids was shorter on third and fourth

instar larvae as compared to fifth and sixth instars (Table 1).

Most parasitoids have the ability to determine host quality during oviposition

and will often accept or reject hosts on this basis (Charnov and Skinner 1985; Strand

and Pech 1995). The current study shows strong influence of different lepidopteran

host species on acceptance and survival of H. hebetor. Of the seven hosts presented to

H. hebetor, H. armigera, C. cephalonica and G. mellonella were the most suitable hosts

with 100% paralysation, parasitism and parasitoid development. M. vitrata, and A.

nigrisigna were least suitable with lower per cent parasitism (60.0�76.7%) and

parasitoid development (40.0�70.0%). Spodoptera litura and Spilarctia obliqua were

not suitable for the development of H. hebetor. This is similar to the findings of

Edwards, Weaver, and Marris (2001), who reported that failure to develop within a

given host may be due to the inability of the parasitoid to overcome their host

immune system. The parasitoid did not parasitise S. obliqua due to the presence of

hairs in the body, though it paralysed some of the larvae through the ventral body

Table 2. Survival and development of Habrobracon hebetor parasitising different lepidopteran

host species.

Mean9SE

Adult longevity (days)

Host species

Egg to adult

emergence

(days)

No. of

cocoon per

larva

Percentage of

adult

emergence

Sex ratio

(M:F) Female Male

Helicoverpa

armigera

9.090.25a 11.191.43b 97.392.33a 0.8690.18a 19.391.12b 9.390.73b

Maruca vitrata 9.090.23a 7.990.58b 83.1913.86ab 0.7990.27a 14.490.64c 8.390.60bc

Autographa

nigrisigna

8.890.52b 4.291.13c 77.2919.63b 0.7590.17a 11.890.16d 7.990.70c

Corcyra

cephalonica

8.790.31b 14.492.35a 97.693.83a 0.6890.05a 21.390.83a 13.791.26a

Galleria

mellonella

9.390.37a 16.793.08a 95.494.96a 0.6990.10a 20.890.48a 12.790.49a

Note: Means followed by the same superscript letter in the column are not significantly different (Tukey’stest) at a�5% (p�0.05).

316 H. Saxena et al.

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surface which is devoid of hairs. The offspring of hymenopteran parasitoids depend

on the host for their nutritional needs. The nutritional quality may be different in

different hosts (Harvey et al. 2000; Harvey and Strand 2002). The developmental

time and survival to adult eclosion for H. hebetor reared on different host species

may give some indication of the suitability of hosts for the parasitoid. In the present

study, the developmental time from egg to adult emergence was longer on

G. mellonella as compared to other hosts.

Our results suggest that late, rather than early instars of any one of the hosts

H. armigera, C. cephalonica and G. mellonella are preferable for mass rearing of

H. hebetor under laboratory conditions. Field releases of H. hebetor should coincide

with the occurrence of field populations of late instar larvae of H. armigera in March

and April to maximise parasitism of this pest infesting chickpea in India.

Acknowledgements

We thank Prof. M. Hayat, Emeritus Scientist, Department of Zoology, Aligarh MuslimUniversity, Aligarh, Uttar Pradesh, India for his kind identification of the parasitoid. Authorsthank Dr C. Chattopadhyay, Head (Crop Protection) and Dr N. Nadarajan, Director, IndianInstitute of Pulses Research, Kanpur for their expert advice and for providing facilities. Wethank Dr Y.S. Rathore, Principal Scientist and Dr Aditya Pratap, Senior Scientist for Englishlanguage editing. We thank the two referees for their valuable comments for improvement ofthis study.

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