1Department of Plant Protection,
College of Food and Agriculture Sciences, King Saud University, P.O. Box 2460, Riyadh 11451, Saudi Arabia
2Department of Entomology, University of Sargodha, 40100, Sargodha,
Pakistan
3Earth
and Life Institute, Biodiversity Research Centre, UCL, Belgium
4Department
of Entomology, Faculty of Agriculture and Environment
Sciences, The Islamia University of Bahawalpur, Pakistan
5Baba Guru Nanak University, Nankana
Sahib, Pakistan
*Correspondence
authors: khan87350@gmail.com
Insect pests are responsible for
damage to stored products such as nuts, dried fruits, oilseeds, legumes, and
cereals, which can suffer both qualitative and quantitative losses.
Post-harvest losses due to stored-product pests range from 5–10% in developed
countries such as the United States to 20% in developing countries (Adams 1977; Boxall 2001). Seed viability and
nutritional and market values can all decline as a result of insect
infestation. Among stored-grain insect pests, Coleoptera and Lepidoptera are
economically important orders, with approximately 600 species of beetles and 70
species of moths associated with damage to stored products worldwide (Cox and Bell 1991; Rajendran and Sriranjini 2008).
Pyralid moths including the Mediterranean flour moth Ephestia kuehniella Zeller
and the rice moth Corcyra cephalonica (Stainton) are usually proposed
for industrial rearing and are among the most destructive pests in milled
products. They are also widely considered destructive in stored products, with
larvae causing substantial losses through feeding and mold development (Ghimire and Phillips 2014).
Because insecticidal application
on stored food products comes with negative consequences for human health,
biological control is the preferred alternative for the management of
stored-product pests. However, successful release of natural enemies requires
mass rearing on alternative hosts to reduce the costs of production. Among
potential natural parasites, the highly polyphagous ecto-parasitoid idiobiont Bracon hebetor Say
(Braconidae: Hymenoptera) is a promising biological agent for controlling
members of the pyralid family in stored products. The pyralid moths, E.
kuehniella and C. cephalonica are considered potential hosts and
have been proposed for industrial rearing. They are widely used in many biological
control programs to rear both predators and parasitoids (Clercq et al. 2005; Kim and
Riedl 2005; Hamasaki and Matsui 2006).
The quality of the host used for
rearing influences the biological fitness traits of a parasitoid and its
efficacy in biological control (Khalil et al. 2016). The biological
parameters of B. hebetor reared on
different hosts including E. kuehniella and C. cephalonica were
studied from different countries (Faal-Mohammad-Ali
and Shishehbor 2013; Imam 2013; Farag et
al. 2015). But the biological and demographic parameters of B. hebetor reared on these host species
were not explored comprehensively in Pakistan. Therefore, we analyzed various
life-history traits such as immature
development, fecundity, and longevity in B.
hebetor living on E. kuehniella and C.
cephalonica to determine the most promising host for mass rearing under
laboratory conditions and for commercialized management of stored pests.
Materials and Methods
Insects and rearing
E. kuehniella and C. cephalonica colonies were cultured separately on wheat- and
rice-flour diets in plastic boxes (25 × 17 × 8 cm). E. kuehniella larvae were reared on a wheat (300 g) and maize (300
g) mixture while the C. cephalonica
colony was maintained on rice flour (600 g) for larval feeding. Both cultures
were maintained at a temperature of 25–26ºC and a relative humidity (RH) of
25–35%.
Three consecutive generations of B.
hebetor were reared on each of the two pyralid host species separately to
synchronize the populations prior to experimentation at the Earth and Life
Institute of the Biodiversity Research Centre, Université Catholique de
Louvain, Belgium. The initial B. hebetor culture was obtained from
parasitized larvae of the wax moth Galleria mellonella (L.) from infected honeybee combs at the College of
Agriculture, University of Sargodha, Pakistan. Infected larvae were transferred
to a clean sterilized plastic vial (7 × 3.5 cm in diameter) for adult
emergence. Species identity was confirmed on the basis of morphological characteristics
by utilizing Shaw and Huddleston (1991)
keys and further confirmed by DNA sequencing (Hajibabaei et al. 2006). After the
emergence of adult wasps, each pair was introduced to a separate plastic vial
with a droplet of 50% honey solution. After copulation, five host larvae of E.
kuehniella and C. cephalonica were separately introduced into the
vial for ovipositioning on a daily basis. The same procedure was following for
several generations of the parasitoids on their respective hosts’ larvae. All
insects were reared under laboratory conditions: 25 ± 1°C, 70 ± 5% RH and 16:8 h
light-dark photoperiod.
Life parameters of B.
hebetor from parasitized E.
kuehniella and C.
cephalonica
Ten freshly emerged B.
hebetor females (< 24 h old) were separately mated with a male and kept
in a separate plastic vial (7 × 3.5 cm in
diameter) containing five fully
grown fifth-instar larvae of each tested host species. This stage
was confirmed as the preferential stage for the parasitoid (Taylor 1988). Every day, a new set of five
fifth-instar larvae of each host was provided to replace previous larvae until
the female parasitoid died. We recorded daily ovipositioning per female,
numbers of larvae, pupae, sex ratios, dry mass, tibia size, and wing area of
adult parasitoids at emergence. The life table data were calculated from daily
observations of both immature and adult stages. The completely randomized
design (CRD) was used for the experiment and was replicated three times.
The emergence rate was used to
estimate larval-pupal mortality for each replicate. A parasitoid was considered
as surviving when it emerged completely from the pupae. To test for possible
variation in parasitoid longevity, 10 newly emerged females were kept at 25°C
with a 50% honey solution and survival was checked twice daily until the last
parasitoid died.
B.
hebetor fitness indicators (dry mass, wing area, tibia size) from parasitized E. kuehniella and C. cephalonica
From each day of emergence, five
males and females that appeared to be physically fit in appearance were
selected from both host species and collected in separate Eppendorf tubes
containing 70% ethanol prior to dry mass measurements. Adults were dried in an
oven at 60°C for 3 days and then weighed on a Mettler Me22 electro-balance
(sensitivity: 1 µg) to measure dry
mass (mg).
According to Godfray (1994), parasitoid standard size can be
estimated by measuring the length of the hind tibia. We therefore randomly
selected 10 adults (males and females) each day for measurements of tibia
length (mm) and wing area (mm2). A digital camera (SONY SSC-DC198P)
mounted on a stereomicroscope was used to photograph the tibia and wings. The
pictures were analyzed with ImageJ, version 1.46r (Wayne Rasband National
Institutes of Health, USA).
The mean number of eggs, larvae,
pupae, adults to emerge, egg-to-adult development time, percentage
survivorship, sex ratio and longevity were used as response variables to
evaluate the suitability of E. kuehniella and C. cephalonica
larvae for the reproduction and development of Table 1: Reproductive
and developmental parameters of B. hebetor reared on two hosts
Host species |
Oviposition period (days) |
Fecundity (eggs/female) |
Number of larvae |
Number of pupae |
Egg-adult development time (days) |
C. cephalonica |
21 ± 2.18 b |
158 ± 22.12 b |
122 ± 19.18 b |
102 ± 17.15 b |
12 ± 0.33 a |
E. kuehniella |
36 ± 2.88a |
429 ± 41.39 a |
363 ± 35.57 a |
332 ± 31.72 a |
11 ± 0.26 b |
Means in the column
followed by the same letters are not significantly different (LSD, P ≤ 0.05)
Table 2: The adult emergence of B. hebetor and egg-adult survivorship (%) on two hosts
Host species |
Number of adults emerged |
Number of males |
Number of females |
M:F ratio |
Female longevity (days) |
Egg-adult survivorship |
C. cephalonica |
87 ± 13.13 b |
59 ± 7.83 b |
29 ±3.49 b |
2:1 |
27 ± 2.01 b |
55 ± 2.68 b |
E. kuehniella |
278 ± 23.39 a |
155 ± 10.49 a |
124 ± 8.25 a |
1:1 |
46 ± 1.82 a |
65 ± 1.59 a |
Means in the column
followed by the same letters are not significantly different (LSD, P ≤ 0.05)
Table 3: Mean (± SEM) weekly production of immature stages of B.
hebetor on two hosts
Weeks |
Number of
eggs/female |
Number of larvae |
Number of pupae |
|||
|
C. cephalonica |
E. kuehniella |
C. cephalonica |
E. kuehniella |
C. cephalonica |
E. kuehniella |
Week 1 |
4.39 ± 0.49 b |
7.57 ± 0.64 c |
3.25 ± 0.40 b |
6.28 ± 0.58 d |
2.68 ± 0.35 b |
5.87 ± 0.58 c |
Week 2 |
7.13 ± 0.53 a |
11.69 ± 0.63 ab |
5.30 ± 0.48 a |
9.97 ± 0.60 ab |
4.40 ± 0.43 ab |
9.17 ± 0.60 ab |
Week 3 |
7.15 ± 0.83 a |
10.61 ± 0.75 b |
5.73 ± 0.75 a |
8.51 ± 0.64 bc |
4.67 ± 0.69 a |
7.94 ± 0.63 b |
Week 4 |
4.42 ± 0.94 b |
12.81 ± 0.85 a |
3.63 ± 0.85 ab |
10.91 ± 0.81 a |
3.28 ± 0.82 ab |
10.21 ± 0.81 a |
Week 5 |
5.47 ± 2.11 ab |
11.87 ± 0.86 ab |
4.47 ± 1.95 ab |
10.33 ± 0.79 ab |
4.00 ± 1.87 ab |
9.42 ± 0.74 ab |
Week 6 |
0.00 |
8.37 ± 0.84 c |
0.00 |
7.18 ± 0.79 cd |
0.00 |
5.98 ± 0.71 c |
Overall mean |
5.83 ± 0.36 B |
10.52 ± 0.32 A |
4.51 ± 0.32 B |
8.89 ± 0.30 A |
3.78 ± 0.29 B |
8.14 ± 0.29 A |
Means in the column
followed by the small similar letters are not significantly different (LSD, P ≤ 0.05)
Means in the row
followed by the capital similar letters are not significantly different (LSD, P ≤ 0.05)
B. hebetor. Analysis of variance was used to calculate the average responses of
the parasitoid on the two host species at different days and a least
significant difference test was used for mean separation (Stell et al.
1980). Regression and correlation was also used to study the average
change in dry mass, tibia size, and wing area of B. hebetor at different
days on E. kuehniella and C. cephalonica. The life table
parameters of all individuals were analyzed according to a method described by Farag et al.
(2015). Intrinsic rates of increase were estimated using the iterative
bisection method from the Euler-Lotka formula, Σ 𝑥=0𝑒− (𝑥+1) 𝑚𝑥 = 1.
Results
The mean oviposition periods of B.
hebetor females on fully grown fifth-instar larvae of C.
cephalonica and E. kuehniella were 20.6 and 36 days,
respectively. Mean lifetime egg production of B. hebetor was
higher on E. kuehniella (429.4 eggs) compared with C. cephalonica larvae
(157.5 eggs). The egg-adult development time on E. kuehniella was 10.85 days and on C.
cephalonica 12.11 days (Table 1).
The mean number of adult progenies
produced by B. hebetor females over their lifetimes on parasitized E.
kuehniella larvae was higher than on C. cephalonica. A significantly
higher longevity of 46.4 days was recorded for females on E. kuehniella
compared with C. cephalonica. Host species greatly influenced
egg-to-adult survivorship of B. hebetor progeny, with the percentage
survival greater on E. kuehniella larvae (64.81%) than on C.
cephalonica (55.37%) (Table 2).
The highest daily mean fecundity
on E. kuehniella was observed in week 4 (12.81) followed by C.
cephalonica at weeks 2 and 3 (7.13 and 7.15, respectively). A similar trend
was observed in parasitoid larval and pupal development stages, with highest
larval (10.91) and pupal (10.21) numbers observed at week 4 on E. kuehniella.
For C. cephalonica, the highest larval population was observed at weeks
2 (5.3) and 3 (5.73), respectively, and a significantly higher pupal population
was observed at week 3 (4.67) (Table 3).
Significant numbers of B.
hebetor adult progeny were produced at week 4 (8.69) on E. kuehniella compared
with C. cephalonica at week 3 (4.14). A similar trend was observed for
the emergence of male parasitoids from both host species at week 4 (4.99) and
week 3 (3.65). Variations were observed in female emergence, with maximum
progenies observed during weeks 2 (4.4) and 4 (3.7) on E. kuehniella,
while no significant female emergence was observed on C. cephalonica from
all five weeks (Table 4).
Life table parameters for B.
hebetor were notably superior for parasites on E. kuehniella in
terms of intrinsic rate of increase (0.14), finite rate of increase (1.14), net
reproductive rate (42.10), and generation time (34.56) compared with those of
parasites living on C. cephalonica (Table 5). A regression equation
showed a 0.0028% and 0.0013% change in female and male B. hebetor dry mass, respectively, with unit change in number of
days (Table 6).
Newly emerged B. hebetor male and female tibia size (mm) and wing
area (mm2) gradually increased each day for individuals on C. cephalonica while decreases were observed in those on E. kuehniella
(Fig. 1 and 2). A regression analysis showed
positive change in tibia size and wing area in both male and female B.
hebetor adults from C. cephalonica compared with E. kuehniella, with unit change in number of days. B. hebetor female and male adult dry masses were
significantly higher on E. kuehniella compared with C. cephalonica (Fig. 3).
Table 4: Mean (± SEM) weekly production of adults of B.
hebetor on two hosts over six weeks period
Weeks |
Number of adults
emerged |
Number of males |
Number of females |
|||
|
C. cephalonica |
E. kuehniella |
C. cephalonica |
E. kuehniella |
C. cephalonica |
E. kuehniella |
Week 1 |
2.28 ± 0.32 b |
5.10 ± 0.53 de |
1.88 ± 0.25 c |
2.49 ± 0.25 c |
0.39 ± 0.11 a |
2.61 ± 0.36 c |
Week 2 |
3.69 ± 0.40 ab |
8.56 ± 0.55 ab |
3.34 ± 0.32 ab |
4.16 ± 0.30 ab |
0.34 ± 0.14 a |
4.40 ± 0.46 a |
Week 3 |
4.14 ± 0.62 a |
7.10 ± 0.60 bc |
3.65 ± 0.52 a |
4.21 ± 0.37 ab |
0.48 ± 0.14 a |
2.89 ± 0.34 bc |
Week 4 |
2.84 ± 0.71 ab |
8.69 ± 0.75 a |
2.28 ± 0.56 bc |
4.99 ± 0.49 a |
0.56 ± 0.22 a |
3.7 ± 0.43 ab |
Week 5 |
3.11 ± 1.49 ab |
6.64 ± 0.63 cd |
2.16 ± 1.09 bc |
4.30 ± 0.45 ab |
0.95 ± 0.45 a |
2.34 ± 0.32 c |
Week 6 |
0.00 |
4.55 ± 0.62 e |
0.00 |
3.52 ± 0.51 bc |
0.00 |
1.03 ±0.25 d |
Overall mean |
3.23 ± 0.26 B |
6.82 ± 0.26 A |
2.77 ± 0.21 B |
3.95 ± 0.17 A |
0.46 ± 0.07 B |
2.87 ± 0.16 A |
Means in the column
followed by the small similar letters are not significantly different (LSD, P ≤ 0.05).
Means in the row
followed by the capital similar letters are not significantly different (LSD, P ≤ 0.05).
Table 5: Life table parameters of B. hebetor reared on C.
cephalonica and E. kuehniella under laboratory conditions
Host species |
Intrinsic
rate of natural increase (rm) |
The
finite rate of increase (𝜆) |
Net
reproductive rate (R0) |
Mean
generation time (T) |
E. kuehniella |
0.14 |
1.14 |
42 |
35 |
C. cephalonica |
0.13 |
1.14 |
25 |
29 |
Table 6: Influence of C.
cephalonica and E. kuehniella hosts on fitness consequences of
female B. hebetor parasitoids
Parameters |
Sex |
C. cephalonica |
E. kuehniella |
||||
|
|
Intercept |
Day |
R2 value |
Intercept |
Day |
R2 value |
Tibia size (mm) |
M |
0.72*** |
0.002 |
0.13 |
0.80*** |
−0.002*** |
0.40 |
|
F |
0.77*** |
0.0003 |
0.01 |
0.82*** |
−0.002* |
0.15 |
Wing area (mm2) |
M |
0.83*** |
0.004** |
0.27 |
0.99*** |
−0.003* |
0.13 |
|
F |
0.98*** |
0.0001 |
0.0002 |
1.08*** |
−0.001 |
0.02 |
Dry mass (mg) |
M |
0.24*** |
−0.00003 |
0.00003 |
0.23*** |
0.001 |
0.06 |
|
F |
0.33*** |
−0.0019 |
0.09 |
0.29*** |
0.003* |
0.15 |
Significance at ***
0.001; ** 0.01; * 0.05
Fig. 1: Influence age-related factors of female parasitoids
on newly emerged adult B. hebetor size, expressed as change in tibia
length (mm) from C. cephalonica and E. kuehniella, respectively
Fig. 2: Influence age-related factors of female parasitoids
on newly emerged adult B. hebetor size, expressed as change in wing area
measurement (mm2) from C. cephalonica and E. kuehniella,
respectively
Fig. 3: Influence age-related factors of female parasitoids
on newly emerged adult B. hebetor dry mass (mg) from C. cephalonica and
E. kuehniella, respectively
Discussion
The current study showed that
host species significantly influenced the reproductive and developmental
parameters of B. hebetor. Although this species is a well-known
generalist parasitoid, all hosts are not equivalent in terms of population
growth potential. The results of the present study are in accordance with those
of Ghimire and Phillips (2014), in which
the shortest egg-to-adult development time and reduced larval and pupal
development period of B. hebetor progeny was observed on E.
kuehniella. The developmental time of B. hebetor on E. kuehniella
in the present study was in
agreement with those of previous reports, including 10.83 days (Amir-Maafi and Chi 2006), 12.85 days (Eliopoulos and Stathas 2008), 10.2 days (Ghimire and Phillips 2010), and 9–12 days (Faal-Mohammad-Ali and Shishehbor 2013). E. kuehniella was the most preferred host of B.
hebetor, possibly because of less vigorous defensive behavior or provision
of more nourishment to developing parasitoids compared with other host species (Saadat et al.
2014a, b,
2016).
Similarly, average life-time
fecundity of B. hebetor females and all immature production were significantly
higher in individuals on E. kuehniella than on C. cephalonica. Overall the B. hebetor
female oviposition period was significantly higher on E. kuehniella (36
days) than on C. cephalonica (20.6 days). Significantly more adults
(male and females numbers)/female, female longevity, and egg-adult survivorship
of B. hebetor was observed on E. kuehniella (278.3 adults/female,
46.4 days, and 64.81%, respectively) than on C. cephalonica (87.2
adults/female, 27 days, and 55.37%, respectively). These results follow the
pattern reported by Ghimire and Phillips (2014),
with significantly higher oviposition periods, female longevity, and egg-adult
survivorship, and immature-stage populations observed on E. kuehniella compared
with C. cephalonica. According to Imam
(2013), similar trends were observed in the biological and developmental
parameters of a closely related species, Bracon brevicornis (Wesmael), on Ephestia cautella (Walker).
B. hebetor longevity approaches 60.3 days,
according to Ghimire and Phillips (2014). Contrary to our results, Nikam and Pawar
(1993) reported the mean longevity (37.5 days), oviposition period (34.5
days), total progeny development (258.9 adults/female) and sex ratio (1.9:1) of
B. hebetor from parasitized C. cephalonica. This difference may
be due to variations in experimental protocols, temperature, RH, or host
density, age, size, strain, and host diet used to carry out the experiment (Harbison et al.
2001; Rohne 2002; Milonas 2005). In the present result, Bracon
females’ mean oviposition periods, larval and pupal stages, longevity, and male
and female emergence and survival percentages of immature individuals favored Ephestia
species, which may be attributable to the fact that Ephestia is the
natural host of Bracon.
Results for weekly oviposition
and immature stages were also in accordance with Ghimire and Phillips (2014), in which overall B. hebetor
age-specific daily fecundity and immature-stage numbers were higher during the
first five weeks and then decreased with the increasing age of parasitoid
females until reproduction ceased. The highest mean fecundity was observed at
week 5 for both E. kuehniella and C. cephalonica species,
compared with our study, which week 4 on E. kuehniella and weeks 2 and 3
on C. cephalonica produced the highest fecundity. According to Ghimire and Phillips (2014), the largest
numbers of adult progeny of B. hebetor were produced in week 4 on C.
cephalonica followed by E. kuehniella in week 5. These results
showed little variation from our results, in which C. cephalonica adult
progeny production was significantly higher at week 3 (4.14 adults/female),
compared with week 4 (8.69 adults/female) for E. kuehniella. The
egg-adult developmental parameters of B.
hebetor were significantly higher on E.
kuehniella parasites, largely at week 4.
In the present study, the intrinsic rate of natural
increase and finite rate of increase of B. hebetor parasites on both C. cephalonica and E. kuehniella hosts
were similar, with little variation, while the net reproductive rate and mean
generations time were significantly higher on E. kuehniella. Similarly, Amir-Maafi and Chi (2006) reported an rm
value of 0.14 on E. kuehniella fed
wheat flour. In contrast to our results, the rm for B.
hebetor was higher on C. cephalonica fed sorghum flour (Nikam and Pawar 1993) compared with C.
cephalonica fed wheat (rm = 0.21), maize ( rm
= 0.21), sorghum (rm = 0.19), and rice flour (rm
= 0.15) (Singh et al. 2006). Eliopoulos and
Stathas (2008) reported rm values of 0.121, 0.163,
0.191, and 0.185 on 1, 5, 15 and 30, E. kuehniella densities,
respectively, for B. hebetor. Faal-Mohammad-Ali
and Shishehbor (2013) estimated an rm of 0.291 for B.
hebetor on E. kuehniella. These results suggest that E. kuehniella larvae are the more suitable
host in terms of population increase.
Various studies have reported
that insect size at emergence is an important life-history variable that is
closely associated with fitness. In parasitoids, numerous fitness indicators,
such as fecundity and longevity, exhibit a positive correlation with size (Cloutier et al.
1981; Visser 1994; Ellers et al.
2001). Host age–related quality greatly affects the fitness of
parasitoids (Kouamé and Mackauer 1991; Colinet et al. 2005), and our results
indicated that tibia size and wing area of B.
hebetor adults (males and females) were
reduced on E. kuehniella but increased gradually on C. cephalonica with
the passage of time. The most likely reason for this phenomenon is that
competition among the plentiful numbers of immature B. hebetor on E. kuehniella ultimately resulted in a decrease in adult size compared with those on
C. cephalonica (Saadat et al. 2016). In our study, a linear decrease in adult B.
hebetor dry mass was observed at 25ºC on C. cephalonica with the passage of time compared with those on E. kuehniella. Similarly, Saadat et al. (2014b) reported the highest dry mass of B. hebetor individuals
reared on E. kuehniella compared with those reared on C. cephalonica. According to Colinet et al.
(2007) a linear decrease resulting from an increase in rearing
temperature was observed in the dry mass of B.
hebetor.
Conclusion
In
conclusion, E. kuehniella is a more suitable host than C. cephalonica for rearing B. hebetor parasites with superior biological
attributes for industrial purposes. In the future, it would be interesting to establish a phylogenetic approach that links host preference and suitability with
a history of parasitism. Our hypothesis is that E. kuehniella is
likely a primary host of B. hebetor with
a potential for diversification.
Acknowledgments
The authors extend their appreciation to the
Deanship of Scientific Research, College of Food and Agriculture Research
Centre at King Saud University for funding this work. The
authors also thank the Deanship of Scientific Research and RSSU at King Saud
University for their technical support. The authors are also highly thankful to Dr.
Jureerat Rattanatip for providing her technical support.
Author
Contributions
MSK carried out research work and written original
draft of the manuscript. ABMR, MA and MAA supervised the work. HK helped in
carried out research work. NA improved and edited the final manuscript. Thierry
Hance supervised and technically improved the final manuscript.
Conflicts
of Interest
None declared.
Data Availability
All the related data reported in the manuscript will be
available as requested.
Ethics Approval
The authors declare that the research
was in accordance with all ethical standards.
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