Cyromazine Induced Effects on Larvae and Adults of Laboratory

Cyromazine Induced Effects on Larvae and Adults of
Laboratory Tunisian Strain of the Mediterranean Fruit Fly
Ceratitis capitata
Jouda Mediouni-Ben Jemâa and Emna Boushih, Laboratoire de Protection des
Végétaux, INRAT, Rue Hédi Karray, 2080 Ariana, Université de 7 Novembre à
Carthage, Tunisia
__________________________________________________________________________
ABSTRACT
Mediouni-Ben Jemâa, J. and Boushih, E. 2010. Cyromazine induced effects on larvae and adults
of laboratory Tunisian strain of the Mediterranean fruit fly Ceratitis capitata. Tunisian Journal
of Plant Protection 5: 213-224.
Cyromazine is an insect growth regulator insecticide mainly used to control dipteran insects. This work
aimed to assess cyromazine-induced effects on the second instar larvae and adults of the Tunisian
laboratory strain of Mediterranean fruit fly Ceratitis capitata. Effects were assessed through larvae and
adult mortality together with the evaluation of larval and pupal body deformities, female fecundity and
adult emergence rate. Cyromazine was respectively added to the larvae diet and adult nutrient solution
at three doses 0.05, 0.1 and 0.2 mg/l. Results indicated that cyromazine induced significant mortalities
to both larvae and adults. After 96 h of exposure and with the dose of 0.2 mg of cyromazine per liter,
91 and 69% of mortality were recorded respectively for larvae and adults. Moreover, females exposed
to different cyromazine doses exhibited significant reductions in their fecundity. The mean number of
eggs laid per female was 55 against 200 for the control at the highest dose. Additionally, a poisoning
effect expressed by the appearance of body deformities for larvae and pupae was observed. The
percentage of deformities was positively correlated to cyromazine doses. Furthermore, adult emergence
rate was strongly reduced compared to the control. Emergence rates were 83, 73.5, 2.5 and 2.02%
respectively for the control, 0.05, 0.1 and 0.2 mg of cyromazine per liter.
Keywords: Ceratitis capitata, cyromazine, emergence, fecundity, IGR (for Insect Growth Regulator)
__________________________________________________________________________
The Mediterranean fruit fly,
Ceratitis capitata (Medfly) was first
recorded in Tunisia in 1885 (23). Since
that, it became a serious pest causing
quantitative and qualitative losses to
several crops; mainly citrus. Presently,
chemical control, using broad-spectrum
insecticides, essentially belonging to
organophosphates class, plays a major
role in controlling this insect. However,
Corresponding Author: Jouda Mediouni-Ben Jemâa
Email: [email protected]
Accepted for publication 29 December 2010
Tunisian Journal of Plant Protection
insect resistance was recorded and control
failures have been reported in field
conditions during last years (4, 5).
Among the most used insecticides,
malathion has been declared an ozonedepleting substance and therefore, is
being phased out. Consequently, it has
been banned from annex I of the EU
directive 91/414/ EEC (26) since 2009.
In the past few decades, a
considerable interest has been paid to the
potential use of insect growth regulators
known as IGR in controlling insect pests
(2). Insecticides, acting as insect growth
regulator, affect growth and development
213
Vol. 5, No. 2, 2010
of the pre-adult life stages of insects, and
are effective against many insects (25).
Cyromazine,
N-cyclopropyl-1,3,5triazine-2,4,6-triamine, is an atypically
substituted s-triazine, which acts as an
insect growth regulator used as a chitin
synthesis inhibitor for fly control in cattle
manure, field crops, vegetables and fruits
(7, 34). It is an effective larvicide against
a number of dipteran and lepidopteran
species (20, 29). Cyromazine has a good
activity against many dipteran species,
especially when it is orally administered
to larvae which usually exhibit a wide
range
of
different
morphological
abnormalities (3, 15, 27, 35).
Cyromazine is characterized by a
rapid stiffening of the cuticle, affecting
mostly larvae of Diptera (9, 14, 18).
Reynolds and Blakey (29) have shown
that an early action of cyromazine leads
the cuticle to become less extensible
when subjected to simple constant load
extension tests. They have suggested that
the cyromazine-induced reduction in
cuticle extensibility may be responsible
for the other symptoms of poisoning and
hence may be the primary effect of the
insecticide.
Moreover,
cyromazine
induces gross deformities manifest in
larvae and pupae of dipteran insects (3,
9), and also reduces egg laying and egg
hatch when fed to Lucilia cuprina adult
(38). Moreover, Alam et al. (2) clearly
demonstrated that cyromazine, ingested
by female flies, is incorporated into eggs
and inhibits larval development in the
first generation.
Cyromazine is also effective as
foliar spray in horticultural crops against
leafminers (Liriomyza spp.) and various
other insects, including fleas, thrips, and
coleoptera (18, 32). It is reported to be a
main translaminar pesticide used to
control respectively the pea leafminer
Liriomyza
huidobrensis
and
the
serpentine leaf miners (L. trifolii) (13, 17,
Tunisian Journal of Plant Protection
30, 37). Cyromazine was used because it
is harmless to parasitoids (6, 31).
Recently, there is an increasing trend
among onion growers in New York to
manage onion
maggot using a
combination
of
cyromazine
seed
treatment and chlorpyrifos (Lorsban 4E,
Dow AgroSciences LLC) in furrow
treatments (28). The Medfly, C. capitata
was reported among the susceptible
species to cyromazine applications (35).
Larvae when reared on an artificial diet
supplemented
with
different
concentrations of cyromazine, suffer from
severe
developmental
disruption
depending on larval age and duration of
exposure (11, 36). Symptoms of
poisoning include body malformations,
such as swelling of the integument and
elongation of the larvae, as well as
inhibition of larval growth, increase of
larval mortality and a lower pupation and
adult emergence rate. Furthermore, Budia
and Viňuela (10) reported that the
delivery of cyromazine could affect the
reproduction and larval development of
C. capitata.
The present work aims to assess
cyromazine effects on larvae and adults
of Tunisian Medfly strain reared under
laboratory controlled conditions.
MATERIALS AND METHODS
Insect. Larvae of C. capitata were
reared on an artificial diet based on wheat
bran, sucrose and yeast (Table 1). The
wheat bran was first sterilized at 120°C
for two hours. After that, all solid
ingredients were weighed and mixed until
a homogenous consistency was reached.
Liquid yeast and hydrochloric acid were
then added. To avoid bacterial and fungal
contaminations, sodium benzoate and
nipagin were added to the diet.
The rearing culture was kept in a rearing
room at 27oC ± 1oC, 75 ± 5% R.H and
under continuous light.
214
Vol. 5, No. 2, 2010
Table 1. Composition of C.
quantities per 1000 g of diet (12)
Ingredient
Wheat bran
Sucrose
Sodium Benzoate
Nipagin
Yeast (liquid)
Hydrochloric acid
Insecticide. Cyromazine (registered
trademark
Trigard
75,
Syngenta
AgroServices AG, Switzerland) was
tested against C. capitata. Trials were
conducted on the second instar larvae and
new emerged adult flies. Trigard 75 WP
was dissolved in distilled water at
respective doses of 0.2, 0.1 and 0.05 mg/l.
Technical ingredient, cyromazine, was
orally administered in the drinking water
and incorporated into the diet respectively
to newly emerged adult flies and larvae.
For adult flies, experiments were carried
out into circular plastic boxes (∅ = 20
cm). Each box contains 50 adults (25♂ +
25♀). Trials were replicated 10 times to
improve precision. Ten cages with
untreated drinking water served as
control. For larvae, experiments carried
on with 20 larvae, were performed in
Petri dishes (∅ = 9 cm) containing 100 g
of diet. The experiment was replicated 10
times. Ten Petri dishes containing
untreated diet were used as control.
The effects of three doses of
cyromazine on larvae and adult
mortalities were assessed at 24, 48, 72
and 96 h after treatment. The dose 0.2
mg/l corresponded to the recommended
dose of Trigard 75 by the registration
pesticide service of the Tunisian Ministry
of Agriculture. Moreover, female
fecundity was determined at different
doses. In addition, body deformities of
larvae and pupae together with adult
emergence rate were evaluated.
Tunisian Journal of Plant Protection
capitata diet:
Quantité
550.0 g
340.0 g
2.5 g
2.5 g
1000 ml
20 ml
Statistical analyses. Adult and
larval mortalities were calculated at 24,
48, 72 and 96 h after treatment using
Abbott formula (1) expressed by
, where C = rate of Medfly
C−T
TR =
x 100
C
mortality in the control field, T = rate of
Medfly mortality in the treated field and
TR = rate of population reduction. Results
were expressed as percentage of
mortality.
Biological
parameters,
like
fecundity, body deformities of larvae and
pupae and adult emergence rate, were
subjected to analysis of variance
(ANOVA) using Statistica software (33).
Significant differences were identified by
least significant difference (LSD) test at
the probability level 0.05.
RESULTS
Cyromazine effects on second
instar larvae adult mortality. Whatever
cyromazine concentration, this active
ingredient was toxic both to second instar
larvae and to adults of C. capitata (Fig.
1). Moreover, larvae were more
susceptible than adults. Results showed
that insect mortality raises with the
increase of cyromazine concentration and
time after treatment.
The lowest dose of cyromazine
(0.05 mg/l) caused 8% mortality of C.
capitata larvae and 10% of adults after 24
h exposure (Fig. 1). At the highest dose
(0.2 mg/l), 91 and 69% mortality were
respectively recorded for larvae and
adults after 96 h of exposure.
215
Vol. 5, No. 2, 2010
100
100
96 h of exposure
72 h of exposure
80
Adults
Larvae
60
Mortality (%)
Mortality (%)
80
40
20
Adults
Larvae
60
40
20
0
0
0
0,05
0,1
Concentration (mg/l)
0,2
0
0,05
0,1
Concentration (mg/l)
0,2
Fig. 1. Percentage of mortality of C. capitata larvae and adults exposed for various periods of time to different
cyromazine doses.
Fig. 2. Fecundity of female C. capitata exposed to different cyromazine doses
Tunisian Journal of Plant Protection
213
Vol. 5, No. 2, 2010
Cyromazine effect on female
fecundity. Females exposed to different
cyromazine doses exhibited significant
reductions in their fecundity (Fig. 2). At
the highest dose, the mean number of
eggs laid per female was 55 against 200
for the control. Moreover, at this dose, no
more eggs were laid after the seventh day
after the treatment. At the dose 0.1 mg/l,
the mean number of eggs obtained at the
third day of laying was 6 and was
significantly different from the control.
Nevertheless, at the dose 0.05 mg/l, no
significant reductions were obtained
concerning the mean number of eggs laid
per female compared to the control.
Cyromazine effects on body
deformities of larvae and pupae.
Cyromazine incorporated to second instar
larvaee diet manifested a poisoning effect
expressed by the appearance of body
deformities on larvae and pupae. The
percentage of deformities was positively
correlated to cyromazine doses (Fig. 3).
Statistical analyses showed significant
differences in percentage of body
deformities of larvae
larv and pupae exposed
to different doses of the insecticide
compared to the control.
Fig. 3. Percentage of body malformations of C. capitata larvae and pupae exposed to different cyromazine doses.
Cyromazine effects on adult
emergence rate. Results showed that
emergence rate significantly depended on
cyromazine dose (Fig. 4). The emergence
rate was 2.02% at the dose 0.2 mg/l
compared to 2.5% for the dose 0.1 mg/l,
Tunisian Journal of Plant Protection
while it reached 73.5% at the dose 0.05
mg/l against 83% for the control (0
( mg/l).
No statistical differences were
observed between the control and the
lowest dose 0.05 mg/l. Similarly, no
statistical differences
difference
were obtained
between the two doses 0.1 and 0.2 mg/l.
213
Vol. 5, No. 2, 2010
a
Emergence rate (%)
100
a
80
60
40
20
b
b
0
0
0,05
0,1
0,2
Dose (mg/l)
Fig. 4. Emergence rate of C. capitata adults exposed to different cyromazine doses
DISCUSSION
In Tunisia, C. capitata has been a
serious pest of several fruit crops mainly
citrus and is found all around the year. It
may complete seven or eight generations
per year, five of them are during the
summer (16, 19).
Results reported in this work clearly
demonstrate that cyromazine ingested by
larvae and adults of C. capitata induced a
poisoning
syndrome
that
include
significant mortality of all developmental
stages, reduction in female fertility,
increase of percentage of body
deformities and decrease of adult
emergence rate.
Many studies have been reported on
the insecticidal activity of cyromazine
against C. capitata. Indeed, Viňuela et al.
(36) reported that C. capitata larvae
reared on an artificial diet supplemented
with
cyromazine
undergo
severe
developmental disruption depending on
their age and exposure duration.
Moreover, Viňuela and Budia (35)
indicated that Medfly larvae treated with
cyromazine (20 mg/Kg of diet) were
smaller, more elongate and considerably
Tunisian Journal of Plant Protection
less elastic than control. On the contrary,
when sub-lethal
sub
concentrations were
added to the larval rearing medium, no
body
alterations
were
recorded.
Furthermore, at the concentration of 20
mg/Kg of diet, larvae
larv
of C. capitata
develop severe symptoms, less than 20%
of them are able to pupate and none
emerge adults (36).
(
In addition,
cyromazine is known to affect dipteran
puparia with lethal outcome (8).
(
These
authors reported that cyromazine has an
effect on pupae
pu
cuticle of Musca
domestica Besides, Kayser and Palivan
domestica.
(22) reported that, when larvae of
dipteran species (M.
(
domestica, Lucilia
sericata,
Calliphora
vicina
and
Protophormia terraenovae)
terraenovae were feed
with diet added with cyromazine (0.25
mg/l), there is an important insecticidal
effect. In another context, Reynolds and
Blakey (29) have shown that an early
action of cyromazine is to cause the
cuticle to become less extensible when
subjected to simple constant load
extension tests. Additionally, the effect of
cyromazine on cuticle mechanical
properties occurred rapidly after exposure
214
Vol. 5, No. 2, 2010
of larvae to the treated diet (24).
against Medfly larvae and adults. Thus,
Moreover, Karras et al. (21) indicated
cyromazine could be suggested as an
that the active ingredient of cyromazine is
alternative chemical control method in
more efficiently utilized at lower doses.
Tunisian citrus orchards and could have
After this study, promising results
an effective contribution in Integrated
are obtained with cyromazine treatment
Pest Management programs.
___________________________________________________________________________
RESUME
Mediouni-Ben Jemâa J. et Boushih E. 2010. Effets induits de la cyromazine sur les larves et les
adultes d’une souche tunisienne de laboratoire de la mouche méditerranéenne des fruits Ceratitis
capitata. Tunisian Journal of Plant Protection 5: 213-224.
La substance active, cyromazine, est un régulateur de croissance des insectes principalement utilisé
pour la lutte contre les diptères. Ce travail a pour objectif d’évaluer les effets induits par la cyromazine
sur les larves du deuxième stade et sur les adultes d’une souche tunisienne de laboratoire de la mouche
méditerranéenne des fruits Ceratitis capitata. Les effets ont été évalués à travers la mortalité des larves
et des adultes, le taux de malformations corporelles des larves et des adultes, la fécondité des femelles
et le taux d’émergence des adultes. La cyromazine a été respectivement ajoutée au milieu d’élevage des
larves et à la solution nutritive des adultes à trois doses différentes 0,05, 0,1 et 0,2 mg/l. Les résultats
ont indiqué que la cyromazine a induit des mortalités significatives des larves et des adultes. A la dose,
0,2 mg/l, 91 et 69% de mortalité ont été respectivement enregistrés pour les larves et les adultes après
96 h suivant le traitement. De plus, les femelles exposées aux différentes doses de cyromazine ont
montré des différences significatives de leur fécondité. A la plus forte dose (0,2 mg/l), le nombre
moyen d’œufs pondus par femelle était de 55 contre 200 pour le contrôle. En plus, un effet
d’empoisonnement exprimé par l’apparition de malformations corporelles chez les larves et les adultes
a été également observé. Le pourcentage de malformations corporelles a été positivement corrélé avec
les doses de cyromazine. En outre, le taux d’émergence des adultes a été fortement réduit comparé au
témoin. Les taux d’émergence ont été respectivement 83, 73,5, 2,5 et 2,02% pour le témoin, la dose de
0,05, 0,1 et 0,2 mg/l.
Mots clés: Ceratitis capitata, cyromazine, émergence, fécondité, RCI (Régulateur de Croissance des
Insectes)
___________________________________________________________________________
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Tunisian Journal of Plant Protection
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Vol. 5, No. 2, 2010
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___________________________________________________________________________
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Tunisian Journal of Plant Protection
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