Physiological Effects of Gibberellic Acid on the Reproductive Potential of Locusta migratoria migratoria
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Physiological Effects of Gibberellic Acid on the Reproductive
Potential of Locusta migratoria migratoria
Khemais Abdellaoui, Monia Ben Halima-Kamel, and Mohamed Habib Ben Hamouda,
Département des Sciences Biologiques et de la Protection des Végétaux, Institut Supérieur
Agronomique de Chott-Mariem, 4042, Sousse, Tunisia
__________________________________________________________________________
ABSTRACT
Abdellaoui, K., Ben Halima-Kamel, M., and Ben Hamouda, M.H. 2009. Physiological effects of
gibberellic acid on the reproductive potential of Locusta migratoria migratoria. Tunisian Journal
of Plant Protection 4: 67-75.
The effects of gibberellic acid (GA3) on the reproductive potential of Locusta migratoria migratoria
(Orthoptera, Acrididae) were investigated by exposing freshly emerged male and female adults to 10 µl
doses, applied either topically or injected into the oesophagus every 2 days for six days after
emergence, of one of six concentrations: 125, 625, 3125, 4125, 5125 and 6125 µg/ml. Application of
GA3 showed a significant adverse influence on the reproductive potential of this insect. The
assessment for reproductive potential was made on the basis of reduction in fecundity and fertility and
measured as sterility in females and shortening of the ovipositional phase. GA3 was responsible for
prolonging the pre-ovipositional phase and the egg laying rhythm, delaying the development of ovaries
and so reduced the length of terminal oocyte. The most developed oocytes were observed in ovaries of
untreated control females. The maximum reduction in fecundity and fertility rates was observed with
6125 µg/ml. It may be concluded that this plant growth regulator has severe adverse effects on
reproductive potential of L. migratoria migratoria.
Keywords: Gibberellic acid, Locusta migratoria migratoria, reproduction.
__________________________________________________________________________
In recent years, interest in the description of natural compounds capable
development of natural insecticides has of interfering with the processes of
increased because of disadvantages to the development and reproduction of the
use of synthetic insecticides, such as target insects (13). Much attention has
environmental pollution, development of been devoted to the use of plant
insecticide resistance, insecticide-induced constituents that have an insecticidal
resurgence of insect pests and adverse effect as “biocides” (17). The use of plant
effects on non-target organisms (16, 2, products to control pest populations is the
19). Alternative pesticides are becoming new approach which has captured world
increasingly important. New approaches wide attention.
to the development of insect control Plants contain an enormous diversity
agents have been revealed through the and quantity of secondary metabolites,
some of which are toxic and deterrent to
herbivores and pathogens. Plants have
Corresponding author: M. Ben Halima-Kamel always been rich source of natural
Kamonia_tn@yahoo.fr
compounds that are insecticidal (nicotine,
rotenone and pyrethrins) and have diverse
Accepted for publication 24 March 2009 modes of action (hormonal, neurological,
Tunisian Journal of Plant Protection 67 Vol. 4, No. 1, 2009enzymatic or nutritional) (12). Many distilled water respectively. In the control
examples in recent years have shown that experiment (C0), the insects received the
plant extracts exert insecticidal activity on same quantity of the solvent used for
locusts, e.g. the leaves of Olea europea preparing the solutions of GA3.
(5, 6) and the leaves of Cestrum parquii The freshly emerged male and female
(3, 8, 9, 10). Among the natural imagoes, procured from the stock culture,
compounds produced by plants, the were sexed and treated topically or by
growth regulatory compounds appear to forced ingestion by applying respectively
directly or indirectly influence the 10 µl of GA3 solution on their dorsum
patterns of growth and reproduction of with a micro-applicator or in their
associated phytophagous insects (14). oesophagus with an insulin syringe during
There are several reports in the literature the pre-oviposition phase (every 2 days
demonstrating an influence on these until 6 days after emergence). For forced
parameters when growth regulators are ingestion, GA3 solution in the digestive
added to the diet or applied exogenously system of the insect was achieved using
on the insects, e.g. gibberellic acid an insulin syringe with a needle onto
(GA3), abscisic acid (ABA), kinetin, etc which we fixed a 10 cm length of 0.5 mm
(5, 15). Some researchers have even diameter catheter; the later being
recommended the use of plant growth stretched at its end. This catheter was
regulators like GA3, coumarin and introduced into the oral cavity of the
indole-3-acetic acid as successful insect until reaching the oesophagus, then
chemosterilants against some insect pests the substance was injected.
(18). The present investigation is an Females deposited their egg batches
attempt to explore the effects of various into sterile sand held in plastic cups (5 cm
concentrations of gibberellic acid (GA3) in diameter and 10 cm long). Egg
on the reproductive potential of Locusta deposition was checked daily until the
migratoria migratoria. death of the females. The number of pods
per female (NP/F), the total number of
MATERIALS AND METHODS eggs per female (TNE/F), as well as the
Insects. The insect L. migratoria weight of a sample of five eggs, and the
migratoria used for testing came from a egg laying rhythm (ELR) were noted in
gregarious stock, which had been reared the control and the treated insects. The
according to Abdellaoui et al. (1). data were also tabulated for pre-
oviposition phase period (POP), fecundity
Reproduction. The effects of GA3 rate (total number of eggs per female) and
(Sigma-Aldrich Chemie GmbH) on the fertility rate ((number of hatched eggs per
reproductive potential of the Asiatic pod)/(number of deposited eggs per
migratory locust L. migratoria pod)x100). The remaining eggs of the pod
migratoria were investigated by exposing were left in the sand and incubated in
the freshly emerged (0-1 day old) male darkness at 33°C. The rate of hatching
and female adults to six concentrations was assessed on day 17th after egg
125, 625, 3125, 4125, 5125 and 6125 deposition (eggs normally hatch on days
µg/ml, denoted respectively as C1, C2, 12 to 13). The corrected sterility rate was
C3, C4, C5, and C6. Groups of five also calculated by applying the following
control and five experimental males and formula:
females were used. The pure substance of (% fertility in control - % fertility in
GA3 used was dissolved in acetone and treatment)/(% fertility in control)x100.
Tunisian Journal of Plant Protection 68 Vol. 4, No. 1, 2009To determine the effects of GA3 on treatment with GA3 significantly reduced,
the ovaries, five control and treated in a dose-dependant manner, the fresh
females, ten days after adult emergence, body weight and the fresh ovarian weight
were weighted and dissected. Ovaries in female adults compared with those of
were dissected from these insects in the control (Fig. 1). However the insects
Ringer’s solution under a binocular presented differences in sensitivity
microscope and the length of several according to the method of treatment used
terminal oocytes in each ovary was and the concentration tested. The
measured. After removing the excess of maximum reduction in body and ovarian
Ringer’s solution, the freshly dissected fresh weight, independently to the method
ovaries were weighed on an analytical of treatment, were observed with the
balance. highest concentration tested (6125
µg/ml). The ratio of fresh ovarian
Statistical analyses. Results are weight/fresh body weight was reduced to
expressed as means ± standard deviation about the half with the concentration of
(SD). The significance between control 6125 µg/ml (11.7 ± 1.22% and 10.97 ±
and treated series was estimated using 1.93%) compared with the control (19.96
Student-Newman-Keuls test at 5% level. ± 4.83% and 20.21 ± 2.14%) for the
All data were statistically analyzed in forced ingestion and the topical
SPSS (Version 13.0). application, respectively. The influence of
GA3 on the body and ovarian fresh
RESULTS weight increased as its concentration was
Analysis of the data for body and raised.
ovarian fresh weight revealed that
2,5 a
a
ab C0 C1 C2 C3 C4 C5 C6
2 b bc
cc
Weight (g)
c d
1,5 e
dd e
1
a ab
0,5 bcc
cc c cd
e ee
0
Forced Topical Forced Topical
ingestion application ingestion application
Weight (g)
Fig. 1. Effect of different concentrations of GA3 on body and ovarian fresh weight of female adults (ten
days after emergence) after forced ingestion and topical application to imagoes of L. migratoria migratoria
(Bar = Standard Deviation). C0, C1, C2, C3, C4, C5, and C6 are 0, 125, 625, 3125, 4125, 5125, and 6125
µg of GA3/ml, respectively. Bars with the same letter are not significantly different (P < 0.05).
Tunisian Journal of Plant Protection 69 Vol. 4, No. 1, 2009The results reported in table 1 showed groups, even at the lowest concentration
a significant adverse influence of GA3 on tested. In the same way, a significant
the reproductive potential and the ovarian difference was noted between the
development of L. migratoria migratoria. different concentrations tested while
Both fecundity and fertility were reduced comparing the total number of eggs
when the 0-1-day old adults were treated deposited by female.
with different concentrations of GA3. The Results in Fig. 2 suggested that GA3
maximum reduction in total number of also disrupted growth and development of
eggs, fecundity rate, fertility rate and an oocytes by significantly affecting the
increase in corrected sterility rate were length of the terminal oocyte. In treated
observed with the highest concentration adult females, the mean of length of the
tested (6125 µg/ml). Fecundity was terminal oocyte was significantly reduced
reduced to 6.36±1.14% with 41.85 ± compared to the control. In the same way,
6.39% fertility and to 43.33 ± 8.29% with we can deduce that forced ingestion had a
55.54 ± 9.62% fertility with the forced greater effect on the development of the
ingestion and the topical application, oocyte than did topical application ten
respectively, compared with the untreated days after adult emergence. The length of
control insect. The corrected sterility rate the terminal oocyte in the control ovaries
reached 49.09 ± 6.98% and 32.8 ± was 6.08 ± 0.27 and 6.15 ± 0.24mm,
11.64% respectively to the forced respectively, for the forced ingestion and
ingestion and the topical application the topical application. At a concentration
(Table 1). An effect of GA3 was observed of 6125 µg/ml these values became 3.4 ±
even for the treatment with the lowest 0.22 and 2.96 ± 0.14 mm, respectively. A
concentration tested (125 µg/ml). significant difference was observed even
Therefore, GA3 was responsible of with the lowest concentrations tested (125
prolonging the pre-ovipositional phase µg/ml).
and the egg laying rhythm of L. The analysis of data in Fig. 3 shows a
migratoria migratoria. The treatment significant difference in the fresh weight
appeared to influence the pattern of egg of eggs laid by control females of L.
deposition by delaying ovarian migratoria migratoria compared to those
maturation and thereby disrupting the treated with different concentrations of
egg-laying cycle. Also, the period gibberellic acid. The highest weight was
between laying the first and the second observed with the untreated control
egg pods averaged 10.1 ± 2.07 and 6.39 ± insect. The mean fresh weights noted in
0.87 days, respectively, for the females control groups were 13.08 ± 0.67 and
treated by forced ingestion and topical 13.98 ± 0.96 mg, respectively, for the
application with the high concentration forced ingestion and topical application.
tested (6125 µg/ml). In the control The weights of fresh eggs deposited by
groups, this period was 3.39 ± 0.44 and treated females (at 6125 µg/ml) were 5.54
3.17 ± 0.39 days, respectively, for the two ± 0.32 and 7.31 ± 1.21 mg, respectively,
methods of treatment. for the two methods of GA3 application.
The number of pods per female was The significant effect started with the first
also significantly higher in untreated concentration tested (125 µg/ml).
control insects compared to the treated
Tunisian Journal of Plant Protection 70 Vol. 4, No. 1, 2009Table 1. Effect of two modes of application of different concentrations of GA3 on the reproductive activity of L. migratoria migratoria
Application Treatment POP (in days) ELR (in days) NP/F TNE/F Fecundity (%) Fertility (%) CS (%)
method
C0 10.4±1.14a 3.39±0.44a 6.8±1.64a 475±44.3a 100 82.11±3.64a -
C1 14.4±0.54b 4.66±0.62ab 5.8±1.48ab 361±96.81b 74.94±8.87 64.45±3.26b 21.29±6.8
Forced C2 14.8±0.83b 6.6±2.09b 3.8±1.3bc 187.2±46.26c 41.62±11.83 52.8±6.94c 35.47±9.82
ingestion C3 15.8±0.44bc 8.01±1.59cd 2.8±0.83c 146.6±83.67cd 32.29±15.16 49.86±5.25c 39.12±7.72
C4 17±1.41bc 9.98±1.23d 1.8±0.44c 98.2±16.48cd 21.22±5.6 46.45±9.76c 43.62±10.22
C5 16.8±2.48bc 9.08±1.71d 2.2±1.3c 58.8±10.75cd 12.88±4.45 51.43±11.27c 37.39±13.03
C6 19.2±4.54c 10.1±2.07d 1.8±0.83c 28.2±13.06d 6.36±1.14 41.85±6.39c 49.09±6.98
C0 11.8±1.09a 3.17±0.39a 6.6±1.51a 480.6±9.68a 100 86.07±5.02a -
C1 13±0.7ab 3.84±1.12ab 6.2±0.4ab 416.4±34.78b 86.63±6.79 80.91±5.76ab 2.1±0.97
Topical C2 14.4±1.3abc 4.13±1.29ab 5.2±0.8ab 351.2±15.67c 73.1±3.71 76.23±3.01b 7.76±3.64
application C3 15.8±1.48bc 5.45±1.98bc 4.6±2.5ab 313±45.85cd 65.15±9.71 73.27±6.62bc 11.34±8.01
C4 16.8±1.64c 6.3±1.13c 3.8±2.16b 272.2±69.6cd 56.75±14.98 64.26±4.73c 22.25±5.72
C5 16.5±3.2bc 5.2±0.95abc 4.2±2.3ab 316.8±32.93d 65.94±6.95 65.84±2.45c 20.33±2.96
C6 17.2±2.94c 6.39±0.87c 3.8±0.83b 208.2±39.7e 43.33±8.29 55.54±9.62d 32.8±11.64
* CS: Corrected sterility rate; ELR: Eggs laying rhythm; NP/F: Number of pods per female; POP: Pre-ovipisition period; TNE/F: Total number of eggs per female; C0:
control experiment; C1: 125 µg/ml; C2: 625 µg/ml; C3: 3125 µg/ml; C4: 4125 µg/ml; C5: 5125 µg/ml; C6: 6125 µg/ml.
* Means within a column and application methods followed by different letters are significantly different (P < 0.05).
Tunisian Journal of Plant Protection 71 Vol. 4, No. 1, 20097 a a Forced ingestion
6
b c
b c Topical application
5 d
c d
Lengh (mm)
4 cd e de e
e
3
2
1
0
C0 C1 C2 C3 C4 C5 C6
Concentration (ppm)
Fig. 2. Effect of two modes of application of different concentrations of GA3 on the length of terminal
oocyte of L. migratoria migratoria, 10 days after adult emergence (Bar = Standard Deviation). C0, C1, C2,
C3, C4, C5, and C6 are 0, 125, 625, 3125, 4125, 5125, and 6125 µg of GA3/ml, respectively. Bars with the
same letter are not significantly different (P < 0.05).
Forced ingestion
16 ab
a a ab Topical application
14
b
Fresh weight (mg)
12 b bc
10 c cd cd
cd
d d
8 d
6
4
2
0
C0 C1 C2 C3 C4 C5 C6
Concentration (ppm)
Fig. 3. Effect of treatment of the freshly emerged male and female imagos of L. migratoria migratoria by
different concentrations of GA3 on the weight of fresh laid eggs (Bar = Standard Deviation). C0, C1, C2,
C3, C4, C5, and C6 are 0, 125, 625, 3125, 4125, 5125, and 6125 µg of GA3/ml, respectively. Bars with the
same letter are not significantly different (P < 0.05).
Tunisian Journal of Plant Protection 72 Vol. 4, No. 1, 2009DISCUSSION observed in Spodoptera littoralis (15).
Analysis of the results revealed that Moreover, some workers have even
gibberellic acid (GA3) significantly recommended the use of plant growth
reduced, in a dose dependent manner, regulators like GA3 as successful
both fecundity and fertility of L. chemosterilants against some insect pests
migratoria migratoria, thereby inducing (18). Many examples in recent years have
partial sterility in females. Therefore, illustrated that plant growth regulators
GA3 was responsible of prolonging the play a vital role in the patterns of
pre-oviposition period and the eggs laying reproduction of associated phytophagous
rhythm, delaying the development of insects. Kaur and Rup (15) demonstrated
ovaries and so reduced the length of a significant reduction in the reproductive
terminal oocyte and the weight of fresh capacity of B. cucurbitae following
laid eggs. topical application of kinetin and
Similarly, a reduction in the coumarin even at very low concentrations
reproductive potential following the (25 and 125 ppm). Isman and Rodriguez
application of GA3 has been reported in (14) showed that natural phytoregulator
Ceratitis capitata (5). Indeed, Barbouche extracted from the Parthenium plant is
and Ben Hamouda (5) showed that GA3 capable of reducing by 88 % the
reduced the synthesis of vitellogenin in population of Heliothis when provided in
the fat body of C. capitata and decreased food at a concentration of 3 mg/kg of
the absorption of vitellin in the oocytes. food. Elsayed and Al-Otaibi (11) showed
While comparing the number of mature that the storage of certain compounds,
oocytes in the ovaries of control females notably gibberellins and monoterpenoids
to those treated with the concentration of in senescent vegetation may lead to
2500 ppm, these authors showed a delayed maturation of desert locusts
significant difference between the two Schistocerca gregaria.
groups of insects. They noted that 75 to Ovarian development, which includes
80% of oocytes completed vitellogenesis oocytes growth and vitellogenesis, is
among the control flies, whereas only 50 known to be under hormonal control. The
to 62% of young oocytes reached adverse effects of gibberellic acid on the
maturity in the ovaries of the treated reproductive potential of L. migratoria
females. They also showed that GA3 migratoria has been attributed to the
significantly reduced the fecundity of C. chemical configuration of GA3, which is
capitata in a dose-dependent manner. a terpenoid compound; it was thought that
Indeed, with a concentration of 5000 GA3 interfered in the endocrinal
ppm, the fecundity can be reduced to metabolic process involved in
50%. reproduction (5). Since GA3 derived from
In the same way, Kaur and Rup (15) the mevalonic acid similarly to a juvenile
reported a reduction in the reproductive hormone (JH), the researchers presumed
potential of Bactrocera cucurbitae that GA3 might interfered in the
following topical application of GA3 metabolic pathways regulated by
given to freshly emerged male and female endogenous JH and affected the
adults. Corroborating influence of GA3 vitellogenesis (4, 15).
on reproductive potential has been
Tunisian Journal of Plant Protection 73 Vol. 4, No. 1, 2009__________________________________________________________________________
RESUME
Abdellaoui K., Ben Halima-Kamel M. et Ben Hamouda M.H. 2009. Effets physiologiques de
l’acide gibbérellique sur le potentiel reproductif de Locusta migratoria migratoria. Tunisian
Journal of Plant Protection 4: 67-75.
Les effets du GA3 sur le potentiel reproductif du criquet migrateur asiatique Locusta
migratoria migratoria sont étudiés suite à l’exposition des imagos mâles et femelles à 10 µl
du GA3, chaque 2 jours jusqu’à 6 jours après émergence, soit par application topique ou
introduit directement dans l’œsophage en utilisant six concentrations: 125, 625, 3125, 4125,
5125 et 6125 µg/ml. Les résultats montrent que l’application du GA3 diminue de façon
significative le potentiel reproductif de cet insecte. L’estimation de l’activité reproductive est
faite d’après la réduction de la fécondité et la fertilité et exprimée comme stérilité chez les
femelles et raccourcissement de la phase d’oviposition. Le GA3 a provoqué un prolongement
de la période de préoviposition et du rythme de ponte, un retard du développement des
ovaires et également une diminution significative de la longueur de l’ovocyte terminal. La
plupart des ovocytes développés ont été observés dans les ovaires des femelles non traitées.
Les réductions maximales des taux de fécondité et de fertilité ont été notées avec la
concentration de 6125 µg/ml. On peut conclure que ce régulateur de croissance de plantes a
des effets néfastes sévères sur le potentiel reproductif de L. migratoria migratoria.
Mots clés: Acide gibbérellique, L. migratoria migratoria, reproduction
__________________________________________________________________________
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__________________________________________________________________________
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Tunisian Journal of Plant Protection 75 Vol. 4, No. 1, 2009Tunisian Journal of Plant Protection 76 Vol. 4, No. 1, 2009
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