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European Journal of Applied Sciences – Vol. 12, No. 5
Publication Date: October 25, 2024
DOI:10.14738/aivp.125.17554.
Hegazi, E., Khafagi, W., El-Rahman, S. A., Hasaneen, M., Showiel, S., Shal, A. A., El Eryan, M., & Attia, M. (2024). Effects of Adult
Feeding Treatments on Longevity and Egg Maturation in Non-Ovipositing Broomrape Females, Phytomyza Orobanchia Kalt
(Diptera: Agromyzidae). European Journal of Applied Sciences, Vol - 12(5). 240-249.
Services for Science and Education – United Kingdom
Effects of Adult Feeding Treatments on Longevity and Egg
Maturation in Non-Ovipositing Broomrape Females, Phytomyza
Orobanchia Kalt (Diptera: Agromyzidae)
Esmat Hegazi
Faculty of Agriculture,
Alexandria University, Alexandria, Egypt
Wedad Khafagi
Plant Protection Research Institute,
Agricultural Research Center (ARC),
Research Center (ARC), Alexandria, Egypt
Safaa Abd El-Rahman
Mammalian Toxicology Department,
Central Agricultural Pesticide Laboratory (CAPL),
Agricultural Research Center (ARC), Alexandria, Egypt
Mervat Hasaneen
Plant Protection Research Institute,
Agricultural Research Center (ARC),
Research Center (ARC), Alexandria, Egypt
Sania Showiel
Plant Protection Research Institute,
Agricultural Research Center (ARC),
Research Center (ARC), Alexandria, Egypt
Amany Abou Shal
Faculty of Agriculture,
Alexandria Uniersity, Alexandria, Egypt
Mohamed El Eryan
Faculty of Agriculture,
Alexandria Uniersity, Alexandria, Egypt
Manal Attia
Bioassay Research Department,
Central Agricultural Pesticide Laboratory (CAPL),
Agricultural Research Center (ARC), Giza, Egypt
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Hegazi, E., Khafagi, W., El-Rahman, S. A., Hasaneen, M., Showiel, S., Shal, A. A., El Eryan, M., & Attia, M. (2024). Effects of Adult Feeding
Treatments on Longevity and Egg Maturation in Non-Ovipositing Broomrape Females, Phytomyza Orobanchia Kalt (Diptera: Agromyzidae).
European Journal of Applied Sciences, Vol - 12(5). 232-239.
URL: http://dx.doi.org/10.14738/aivp.125.17554
ABSTRACT
Orobanchaceae, is noxious root parasites, in Egypt. Some causing huge economic
losses to faba bean fields. So far, there are few detailed reports on the rearing
protocols of its biological control agent, Phytomyza Orobanchia Kalt. The effect of
food supplements on longevity and egg load in non-ovipositing Broomrape fly
Ph.Orobanchia ,is not well known. We investigated the effect of three feeding
regimes of the adult flies (supplement with sterile water or honey solution and
starvation) on its longevity, and egg load female fly. Adult longevity was affected
by feeding treatments, insect sex and hatching time. Under starvation, the
longevity and egg load of Ph. Orobanchia adults were significantly lower than
those with access to sterile water and a honey solution. Honey fed females of non
diapaused flies lived longer than diapaused ones. Egg loads were significantly
influenced by female age, feeding treatments and physiological state of the female.
Females emerged without mature eggs. For honey solution fed flies, egg load
increased until age of 3 d old (non-diapausing females) day 14 (diapausing
females), reaching respective maxima of 28.2± 1.2 and 16.4 ± 2.2 eggs/female.
Eggs load then declined with age. Non- diapausing females produce more eggs than
diapausing ones.
Keywords: Phytomyza Orobanchia Kalt., food supplements, adult longevity, egg load of
nonovipositing fly.
INTRODUCTION
Kaltenbach (1864) described Phytomyza orobanchia from flies bred from larvae on Orobanche
sp. Ph. Orobanchia Kaltenbach, 1864 is frequently cited and studied species which is used as
biological agents against very harmful plants, the multitude of parasitic Broomrape species.
The larvae of Ph. Orobanchia consume the fruits and seeds of its host plant, thus reducing the
dissemination of those pest species. The preferred food of Ph. orobanchia are the Orobanche- seeds, but larvae also mine the epidermis of the shoots. Damage to the shoots produces
premature desiccation of the seed capsules (Spencer, 1973). Development starts in spring,
when temperature and photo-period trigger the end of diapause of overwintering pupae. As
Ph. orobanchia depends on its host, it is adapted to the summer vegetation period. Hegazi et al
2024, reported that, the fly is long lived adult and may stay alive in the field up 2 months
(unpublished data) waiting for its host plant. It is a short-day species with a pupal summer -
winter diapause. Depending on the specific climatic conditions there are 1–6 generations per
year (Klein & Kroschel, 2002). Several technical, vegetable and fodder crops are damaged by a
harmful flowering parasite– the Broomrape (Orobanche L., 1753, Orobanchaceae). Parasitic
weeds of the genus Orobanche pose a tremendous threat to European agriculture (Joel 2000).
These weeds considerably damage crop plants due to withdrawal of water, minerals and
organic compounds. The growth of the hosts is retarded and yield losses range from 5 to
100% depending on the region and the crop (Sauerborn, 1991). A detailed literature overview
on Orobanche was published by Pieterse (1979). This genus [sensu lato] includes 140–200
species worldwide of which O. crenata, O. cumana, O. minor, and Phelipanche ramosa are the
most noxious ones. In Egypt, parasitic weed species, O. crenata is noxious root parasites which
seriously constrain the production of many crops, including Leguminosae and Solanaceae
families (Hegazi et al 1981, Parker & Riches, 1993, Al-Eryan et al.2011). The larvae of
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European Journal of Applied Sciences (EJAS) Vol. 12, Issue 5, October-2024
Ph.orobanchia mine Orobanche shoots and feed on immature seed capsuples. For faba bean
season in Egypt, the onset of pupal diapause was in February increases in March and reached
maximum in April. Large proportion of diapausing puparia of 1year old, hatched in January,
decreased gradually, reaching its minimum in April. The live pupria that did not emerge after
April, were assumed to be prepupae-pupae in diapause for more longer period (2-3years).
The Ph.orobanchia fly has prolonged diapause of different diapause intensities. The
polymorphism in the intensity of prolonged diapause split population of adult’s flies of a
single population to emerge in different years(2-3years) (Hegazi et al., 2024). So we have
different categories of Ph.orobanchia populations: non-diapaused and diapaused flies. So far,
knowledge about the effect of food supplementation on fly quality of Ph.orobanchia is still
scarce.
In the present work we investigated the effect of three feeding regimes on longevity and egg
load of non-diapaused and diapaused fly.This study provides knowledge for the effect of
feeding treatments of adults Ph.orobanchia fly which is important to improve fly effectiveness
as biological control agent and mass-rearing of the fly .
MATERIALS AND METHODS
Insects
The larvae of Ph.orobanchia mine Orobanche shoots and feed on immature seed capsules.
Pupation takes place in the plant capsules but most frequently in the stem base near the
ground. The Ph. orobanchia fly, is hard to rear in the laboratory for several generations, So all
Ph Orobanchia adults were from field collected puparia. Several visits were paid to faba bean
fields to collect monthly of Orobanche shoots infested by Ph.orobanchia fly, from January 1st to
end April of the seasons of 2023. Several samples of O.crenata shoots were successively
collected from 4 faba bean farms in Nubaria area , Alexandria governorate. The field
temperature during the sampling date was 12-15, 13-15,14-17 and 18-19°C, in January,
February, Mach and April, respectively. By dissecting the 7443 of infested Orobanche shoots
large numbers of Ph.orobanchia puparia were collected ,monthly. The Puparia (n=150-250/
sample) were kept in glass vials provided with wet pieces of cotton and covered with muslin
kept in position. To identify the diapausing pupraria, each sample was held for more than five
weeks, to allow sufficient time for the non-diapausing flies to complete their life cycles and
emerge. The emerged adults were counted, sexed and removed to use as non-diapaused flies.
When adult emergence was discontinued, the puparia that did not emerge after five weeks,
were assumed to be puparia containing prepupae-pupae in diapause. The numbers of flies
entering diapause and relevant notes were recorded and used as hatched flies from diapaused
Ph.Orobanchia flies. Each sample of diapausing or non-diapausing flies were counted, dated
and allowed to develop under controlled conditions. The diapausing flies were monitored
every day for eclosion. Monthly mean emergence Ph. orobanchia of diapaosing puparia was
recorded. At emergence, they were sexed by the slightly protruding ovipositor of the female.
Feeding Regimes, Adult Longevity, and Egg-load
Two different supplements were provided to adult flies to study the effect on adult longevity
and egg-load, i.e., high temperature-sterilized water (i.e., sterile water) and with honey water
solution (20%). The adult flies under starvation or fed on water served as the control group.
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Hegazi, E., Khafagi, W., El-Rahman, S. A., Hasaneen, M., Showiel, S., Shal, A. A., El Eryan, M., & Attia, M. (2024). Effects of Adult Feeding
Treatments on Longevity and Egg Maturation in Non-Ovipositing Broomrape Females, Phytomyza Orobanchia Kalt (Diptera: Agromyzidae).
European Journal of Applied Sciences, Vol - 12(5). 232-239.
URL: http://dx.doi.org/10.14738/aivp.125.17554
For the longevity experiments, seven sets of newly emerged adult flies, were used, three for
non-diapaused flies and four for diapausing flies. A total of 30 female adults/set of each non- diapaused flies and diapaused were tested in glass vials (2.5 x 10 cm) covered with an
organdie cloth to allow ventilation, in each treatment and for each time period. The water and
honey solution were offered as droplets on small pieces of oleander leaves. The food was
changed and renewed daily. Mortalities were recorded daily till the death of all adults The
overall experiment was repeated 3 times.
For the egg-load experiments, one newly emerged unmated female and one newly emerged
male were randomly paired in glass vials (2.5 x 10 cm) covered with an organdie cloth to
allow ventilation. Each treatment was replicated 30 times. Ten sets of newly emerged adult
flies, each composed of 40 individuals, were selected. Five of these sets were non-diapaused
flies, while the other five sets were adult flies hatched from diapaused puparia. Each set was
distributed into 4 glass vials (2.5 x 10 cm) as above at rate of 5 males and 5 females per vial.
All of these groups were fed on honey. For control, another six sets were prepared. The first
three sets were deprived of any kind of food or water, while the other three sets were fed only
with water.
To determine total egg numbers, adult female flies in each time period were killed by freezing
and dissected in Ringer’s solution (0.75 g of NaCl, 0.035 g of KCl and 0.021 g of CaCl2 in
100mL of distilled water) under a stereo-zoom microscope (model #S111; Olympus, Japan) at
a magnification of ×60 to ×90. Using two size #0 insect micropins, the abdomen of each female
was teased apart and the ovaries were removed. The numbers of eggs present deemed to be
mature eggs were counted by teasing the tissues apart so that the individual eggs were
released.
The ovaries were pressed with a needle until the eggs were expulsed, and fully matured eggs
were counted. Eggs with a full shape were regarded as mature eggs. Since the longevity of
wasps was less than 69h without feeding with carbohydrate-rich diet, there were 24, 48 and
72 h observations in the two treatments, i.e., those fed with only water and deprivation. The
experiments were carried out at 25 ± 1°C in incubators (type Hann, Munden, Germany), under
photoperiod 12:12 (light: dark), RH 75% and light intensity 8000 Lx. Light was measured
with an available Weston light meter (Weston Electrical Instrument Company, Newark, NJ),
located in a controlled room. Also, all adult females tested were non-ovipositing females.
Insects were neither anesthetized nor child prior to the test
RESULTS
Feeding Regimes and Adult Longevity
Table 1 shows the longevity of non-diapausing Ph. orobanchia adults under different feeding
conditions. The lowest life span was among the fasting adults. The adults survived starvation
for an average of 3.7±0.1 and 3.9 ± 0.2 days for males and females, respectively. However, no
significant increase in the average was found when the adults were fed on water. The honey- fed groups of the flies differed significantly in their life span compared with those fed on
water or fasted. They survived for 11.4 ±1.2 and 16.9 ±2.4 days, respectively for males and
females, when they were fed on of honey. The adults survived starvation or water-feeding for
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few days, while they significantly lived longer (F = 24.8; d.f. = 2,27; P < 0. 05) when non- diapausing adults they fed on honey (Fig. 1).
Table 1: Longevity of non-diapausing, non-ovipositing female and male Ph. orobanchia
for water, no food and honey treatments.
Treatments Longevity (days± SE)
Male Female
Range Average ± SE Range Average ± SE
Fasting 3 – 5 3.7 ± 0.1 3 - 5 3.9 ± 0.2
Water 3 - 6 3.9 ± 0.2 3 - 8 5.0 ± 0.23
Honey 5 - 36 11.4 ± 1.2 5 - 39 16.9 ± 2.4
Figure 1: Effect of feeding treatments on longevity of non-diapausing Ph. orobancia females.
In a separate experiment, we compared the longevity in diapausing Ph. orobanchia
flies that hatched in different months during faba bean season and reared on honey
(Table 2). The longevity of Orobanchia diapaused females that emerged in different time of
the season varied significantly (F = 6.8; d.f. = 3,36; P < 0. 05). Its longevity was emergence
date dependent. The shortest longevity was for females emerged in January when the number
of parasitic weeds was low. The longest one was for those emerged in February where the
parasitic weed population was high (Figs.2). Honey fed females of non diapaused flies did not
significantly lived longer than diapaused ones.
Table 2: Longevities of honey-fed diapausing Ph. orobanchia emerged in different
months
Month Longevity (days)
Male Female
Range Average ± SE Range Average ± SE
Jan. 4 - 22 7.2 ± 1.3 4 - 14 7.1 ± 1.6
Feb. 4 - 58 17.5 ± 1.5 4 – 32 16.4 ± 2.4
Mar. 4 - 44 13.8 ± 2.1 4 - 14 8.0± 0.8
Apr. 7 - 33 11.5 ± 2.4 7 - 24 14.2 ± 2.3
A
B
B
0
5
10
15
20
25
Honey Water Fasting
Longevity (days
± SE)
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Hegazi, E., Khafagi, W., El-Rahman, S. A., Hasaneen, M., Showiel, S., Shal, A. A., El Eryan, M., & Attia, M. (2024). Effects of Adult Feeding
Treatments on Longevity and Egg Maturation in Non-Ovipositing Broomrape Females, Phytomyza Orobanchia Kalt (Diptera: Agromyzidae).
European Journal of Applied Sciences, Vol - 12(5). 232-239.
URL: http://dx.doi.org/10.14738/aivp.125.17554
Figure 2: Longevities of honey-fed adult females Ph. orobanchia diapaused in 2022 season and
emerged in different months of 2023 season. The different letters above the error bars
indicate significant differences between months (ANOVA, P˂ 0.05)
Feeding Regimes and Egg-load in Non-diapausing and Diapausing Females
The adult female of Ph. orobanchia has two ovaries, each with 9-11 ovarioles. At eclosion, the
number of mature eggs in either diapaused or nondiapaused flies was zero, i.e the ovigeny
index (OI) (Jervis & Peter Ferns 2005), was = 0.0, (Fig. 3 a). The numbers of eggs present
deemed to be mature eggs were counted by teasing the tissues apart so that the individual
eggs were released. The ovaries were pressed with a needle until the eggs were expulsed, and
fully matured eggs were counted (Fig 3b).
Figure 3: Ovaries of Ph. orobanchia in (a), newly emerged female (b) 24h-after emergence.
Eggs with a full shape were regarded as mature eggs. The mean length of an egg in the 24-h.
old ovariole measures 399.8 ± 30.7 um. Table 4 shows the dynamics of egg production in
honey fed non-diapausing and diapausing females of Ph. orobanchia the results suggest that
the non-diapausing females significantly (F = 7,4; d.f. = 4,20; P < 0. 05)produce more eggs
than diapausing females (F = 4,9; d.f. = 4,20; P < 0. 05) (Fig.4). In non-diapausing females
egg production reached up to16.6 ± 1.5 eggs/female in the first day of life. When these
females stay deprived from hosts the egg production increase reaching its maximum on the
3rd day, then decreased to 19.4 ± 1.4egge/female for females of 28 days old, showing that
some of eggs were absorbed during aging. The same trend with the time was observed among
diapausing females, but the number of egg production was lesser compared with those
observed in non-diapausing females (Table 4, Fig.4). At 24 h after emergence, egg load of
B
A
B
A
0
5
10
15
20
25
Jan. Feb. Mar. Apr.
Longevity (Days
± SE)
Months
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honey solution fed flies increased significantly until age of 3 d old (non-diapausing females), d
14 (diapausing females) reaching respective maxima of 28.2± 1.2 and 16.4 ± 2.2 eggs/female
(Table 4, Fig. 4). Eggs load then declined with age. Non- diapausing females produce more
eggs than diapausing ones.
Table 3: Mean number of mature ovarian eggs in non-fed and water-fed Ph. orobancia
lived for four days.
Table 4: Dynamics of egg production in honey fed non-diapausing and diapausing
females of Ph. Orobanchia fly
Ovary Female age (days ± SE)
1 3 7 14 28
Non-diapausing females
Ovary 1 8.9 ± 0.8 14.5 ± 0.5 14.3 ± 1.14 12.2 ± 1.5 11 ± 2
Ovary 2 7.7 ± 0.75 13.7 ± 0.7 12.7 ± 0.94 10.8 ± 0.7 8.5 ± 0.5
Total 16.6 ± 1.5 28.2 ± 1.2 27 ± 2.0 23 ± 2.2 19.4 ± 1.4
Diapausing females after emergence
Ovary 1 6.5 ± 0.4 7.4 ± 0.4 7.5 ± 0.4 9 ± 2.1 5 ± 1
Ovary 2 7.3 ± 0.4 7.0 ± 0.5 7.1 ± 0.5 7.4 ± 1.3 4.4 ± 0.5
Total 13.8 ± 0.7 14.4 ± 0.8 14.6 ± 0.8 16.4 ± 2.2 9.4 ± 1.5
Figure 4: Mature egg-load of honey- fed non-diapausing and diapausing Ph. orobancia fly. For
each set the different letters above the error bars indicate significant differences between
female ages
c
a a
b
bc
A A A
A
B
0
10
20
30
40
NO.
1 3 7 14 28
of matyre eggs/ female
± SE
Age of females (days after emergence)
Non-diapausing female
Ovary Female age (days ± SE)
1 3 4
Non-fed females
Ovary 1 9.4 ± 0.6 10.7 ± 1 8.9 ± 0.8
Ovary 2 9.6 ± 0.6 9.5 ± 0.9 7.8 ± 1
Total 19 ± 0.8 20.2 ± 1.9 16.7 ± 1.8
Water- fed females
Ovary 1 3 ± 0.4 19 ± 0.3 11 ± 0.4
Ovary 2 6 ± 0.5 15 ± 0.4 12 ± 0.4
Total 9 ± 0.9 34 ± 0.7 23 ± 0.8
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Hegazi, E., Khafagi, W., El-Rahman, S. A., Hasaneen, M., Showiel, S., Shal, A. A., El Eryan, M., & Attia, M. (2024). Effects of Adult Feeding
Treatments on Longevity and Egg Maturation in Non-Ovipositing Broomrape Females, Phytomyza Orobanchia Kalt (Diptera: Agromyzidae).
European Journal of Applied Sciences, Vol - 12(5). 232-239.
URL: http://dx.doi.org/10.14738/aivp.125.17554
Figure 5: Egg-load of non-fed and water-fed Ph. Orobanchia females lived for four days
Table 3 shows the mean number of mature ovarian eggs in non-fed and water-fed Ph.
orobancia lived for four days. Water fed females significantly produced more eggs than non –
fed females (Fig.5, for water fed F = 349.2; d.f. = 2,27; P < 0. 05; for non-fed (F = 3.79; d.f.
= 2,27; P < 0. 05). In non-fed females the total number of mature eggs 19 ± 0.8 ,20.2 ± 1.9
eggs were developed in day 1 and 3, but decreased to 16.7 ± 1.8egges/female in day 4. For
water fed females they developed total of 9 ± 0.9eggs in day1, 34 ± 0.7eggs in day 3, decreased
to 23 ± 0.8 eggs/female in day 4. In both cases of feeding conditions, the female absorbed
some of their eggs in day 4.
DISCUSSION
The effect of food supplements on longevity and egg load of the Broomrape fly. Ph. orobanchia
is not well known. We investigated the effect of three feeding regimes of the adult flies
(supplement with sterile water or 20% honey solution and starvation) on its longevity, and
egg load. The nutritional requirements of the Phytomiza adults assume a considerable
importance in biological control, i.e, the convenient factor, increases the ability of adult female
to search for its host, enables it to attack a large number of hosts (Flanders, 1950), increases
its longevity and fecundity (Allen & Smith, 1958). The Ph. orobanchia adults survived
starvation or water-feeding for few days, while they lived longer when non-diapausing adults
they fed on honey the longevity of Orobanchia diapaused females was emergence date
dependent. The longest one was for those emerged in February where the parasitic weed
population was high. Honey fed females of non diapaused flies lived longer than diapaused
ones. The adults survived starvation or water-feeding for few days, while they lived longer
when non-diapausing adults they fed on honey the longevity of Orobanchia diapaused females
was emergence date dependent. The longest one was for those emerged in February where
the parasitic weed population was high. Honey fed females of non diapaused flies lived longer
than diapaused ones.
Both the ovigeny index (OI) − defined as the proportion of the potential lifetime complement
of eggs that is mature upon female emergence, and the egg load − defined as the number of
mature eggs carried by a female at a given moment in her lifetime, have been identified as
significant fitness variables in insects (Papaj, 2000; Jervis & Ferns, 2005). It can play an
a
a
b
C
A
B
0
10
20
30
40
NO.
1 3 4
of mature eggs/ female ± SE
Age of female (days after emergence)
Non- fed
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important role in the ecology and evolution of insect foraging and ovipsion behavior (Richard
& Casas, 2012). At eclosion, the number of mature eggs in either daiapaused or nondiapaused
of Ph. Orobanchia flies was zero, i.e the ovigeny index (OI) (Jervis & Ferns, 2005), was = 0.0.
The egg load at any time is the result of a number of physiological, behavioral and ecological
variables, including rates of pre-and post-eclosion egg maturation, oviposition, and egg
resorption as well as adult nutrition and temperature (Jervis et al., 2008). Non- diapausing
females produce more eggs than diapausing ones.
CONCLUSIONS
Overall, our study shows that additional water and honey to the Ph. orobanchia significantly
increased the longevity and egg load. Adult longevity was affected by feeding treatments,
insect sex and hatching time. Honey fed females of non diapaused flies lived longer than
diapaused ones. Both diapaused or non-diapaused females emerge without mature eggs. Non- diapausing females produce more eggs than diapausing ones.
Egg loads were significantly influenced by female age, feeding treatments and physiological
state of the female. Egg resorption occurs in non-ovipositing females’ life. The supply of honey
solution is a better food substitution when releasing is planned for Ph. Orobanchia for some
environment-friendly pest control tactics such as the parasitic weed species, O. crenata.
Dietary sugars increase longevity and enhance reproductive parameters of Bracon
ACKNOWLEDGMENTS
We express our sincere thanks to Alexander von Humboldt Foundation for scientific donation
used in this work. This work was funded by the zeroparasitic, project –PRIMA (PRIMA S2
2018)
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Hegazi, E., Khafagi, W., El-Rahman, S. A., Hasaneen, M., Showiel, S., Shal, A. A., El Eryan, M., & Attia, M. (2024). Effects of Adult Feeding
Treatments on Longevity and Egg Maturation in Non-Ovipositing Broomrape Females, Phytomyza Orobanchia Kalt (Diptera: Agromyzidae).
European Journal of Applied Sciences, Vol - 12(5). 232-239.
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