biology and feeding behaviour iran
TRANSCRIPT
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ournal of Insect Science: Vol. 10 | Tavadjoh et
Journal of Insect Science | 1
Biology and feeding behaviour of ladybird,Clitostethus arcuatus, the predator of theash whitefly, Siphoninusphillyreae, in Farsprovince, Iran
. Tavadjoh1! ". "a#$eh$arghani2%! ". Ale#ansoor&! J.
'halghani( and A.Vi)ra#*
1+e,art#ent of -nto#olog! Science and /esearch a#,us of Isla#ic A$ad niversit!Tehran! Iran 1(1**
(3&&2+e,art#ent of 4lant 4rotection! Shira$ niversit! 5adjgah!Iran! 61(((7*187&/esearch enter of 9atural /esources and Ani#al "usandr of ;ars ,rovince Shira$!Iran 61***716 and for#er facult of /esearch enter of 9atural /esources and Ani#al"usandr of ;ars ,rovince Shira$! Iran61***716(-vin 4lant +isease and 4est /esearch Institute!
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ournalof Insect Science: Vol. 10 | Tavadjoh et
www .in s e ctscien c e . o r g 2
$arghan i sh ira$u .ac.ir! %orres,onding author AssociateEditor:
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www .in s e ctscien c e . o r g &
ournal of Insect Science: Vol. 10 | Tavadjoh et
Introduction
hiteflies feed heaily on plant sap and
produce stic/y honeydew. Ash whitefly(Siphoninus phillyreae) (Halliday)
(Hemiptera: Aleyrodidae) is a small white
sap suc/ing insect that occurs in both
temperate and 0editerranean climates.
1ymphs and adults of this pest cause
economic damage on the host plants mainly
by feeding on plant sap from late 0ay to
mid ecember (Alemansoor and
2allah3adeh #44"). !he highest population
density of this pest occurs on ash trees, butmore than seenteen other host plants
(including apple, pears, apricot, acer, and
plum) are reported under its host range in
2ars -roince of Iran (Alemansoor and
2allah3adeh #44"). It can also be found on
many small trees and shrubs during
outbrea/s (Caon and de 5arro +666). Heay
infestations of S. phillyreae can cause stress
to apple and pear trees, resulting in
premature leaf drop, wilting, and smallerfruit si3e in 7urope (Caon and de 5arro
+666). 8utbrea/s of S. phillyreae fre9uently
occur when their natural enemies hae been
disturbed or destroyed by pesticides or
other factors (2lint #44#).
S. phillyreae has seeral natural enemies
that can control its population to leels
under the economic threshold. !hese
natural enemies include predators such asClitostethus arcuatus (Rossi) (Coleoptrea:
Coccinellidae), Menochilus spp., and
Scymnus pallidivestis and parasites such as
Coccophagus eleaphilus, Encarsia gautieri,
Encarsia inaron, Encarsia partenopea,
Encarsia siphonini, Encarsia
pseudopartenopea Eretmocerus siphonini,
and Eretmocerus corni (1guyen and
Hamon Aas #444).
Among arious parasitoids, predators and
pathogens reported on S. phillyreae, the
ladybird beetles hae long been used as
biological control agents (8nillon +664
8bryc/i and ;ring +66'). In their recent
studies, Alemansoor and 2allah3adeh
(#44") reported C. arcuatus as a good
candidate for controlling the pest in 2ars.
!his ladybird beetle belongs to the
subfamily ), -ortugal (0agalhaes +6'4), Africa
(2ursch +6'$), Italy (?argani +664), the
=) (2igure +).
!he predator prefers Aleyrodid species
(0ills +6'+) and has been used to control S.
phillyreae in California. It preys on other
species of Homoptera (5untin and !ama/i
+6'4) including Trialeurodes
vaporariorum, Bemisia tabaci (?erling et
al. #44+),Dialeurodes citri (Age/yan +6$$
5asiri et al. #44"), Aleurotrahelus jelinekii
(0ills +6'+), and Aleurodes proletella
(5athon and -ietr3i/ +6'). In addition it
also feeds on the eggs of Tetranychus
urticae (Biotta et al. #44&) as well as aphids
(?erling et al. #44+).
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A decline in the population of S. phillyreae
was obsered in all locations in 7gypt after
the release of the predator C. arcuatus. !he
population of C. arcuatus increased in all
eperiments following its release (Abd*Rabou #44). !he population of C.
arcuatus spread oer a wider area all the
way from the northwest of Iran to coastal
lines of -ersian ?ulf. 5athon and -ietr3i/
(+6') reported the coloni3ation of the
predator in the warmest regions of Central
7urope. Although C. arcuatus is widely
distributed in Iran, only a few studies hae
been conducted on the biology of this
predator. !he obectie of this study was toinestigate the biology and feeding
behaiour of C. arcuatus as one of the
potentially important biological control
agents of S. phillyreae.
"aterials and"ethods
Rearing of C. arcuatus
Adults of the whitefly S. phillyreae werecollected from trees in nature, and a stand
of &4 young ash trees in + mm polystyrene
-etri dishes under laboratory conditions.
!he predators were additionally fed with
syrup of honey made by adding one
teaspoonful of honey in +44 ml water.
Rearing containers were /ept under
laboratory conditions at #$ D +E C, &' D #%RH, and a photoperiod of +:' B:
photoperiod.
Biological studies conducted in the
laboratory
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Figure #$ +istriution of Clitostethu. arcuatus in Iran. "igh >ualit figures are availale online.
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dishes to estimate the egg to adult mortality
rate. !he incubation period of the eggs and
the lifetime of different laral stages, pre*
pupae, pupae, and the adults were also
recorded, with a difference for the latter inwhich only si pairs of adults were used.
!he mean duration of & pre*copulation
times (the time between emergence of the
adults and their first copulation) were
recorded for twele pairs of C. arcuatus.
!he time re9uired for a copulated female to
lay her eggs was also determined. 8ne
hundred pupae were collected from ash
trees, and the number of males and females
were recorded to determine the se ratio.
Biological studies conducted in the field
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&rowth "ini'u' "a*i'u' "ean+E" "ortality
-gg & ( &.66F0.06 2.7
1st larva 2 & 2.(3F0.03 7.2
2nd larva & ( &.(7F0.03 *
&rd larva & ( &.&(F0.08 2.6
(th larva ( * (.27F0.08 1.2
4re,u,a 1 2 1.27F0.08 0.*
4u,a & ( &.83F0.07 2.6
-gg to Adult 16 21 13.07F0.16 22.6
;e#ale longevit 60 66 6&.*F1.07
min (between 6:">
and +4:44 am) eery wee/ from spring until
late autumn in order to estimate the
population density. !he area around the
host plants that were used for the fieldeperiments was chec/ed during winter to
determine C. arcuatus hibernation sites.
Feeding behaviour of C. arcuatus
aily and the oerall feeding of each actie
stage (laral and adult) of C. arcuatus were
measured by placing #4 newly emergent
samples of each stage in separate -etri
dishes. !en adults were randomly selected
and placed in separate -etri dishes toinestigate staration tolerance and daily
mortality of C. arcuatus adults. aily
obserations were recorded from each adult
without feeding them. !o study the feeding
behaiour, +> adults were randomly
selected from a population of C. arcuatus
that had preiously been stared for #"
hours and then eposed to +#4 S. phillyreae
eggs as a food supply. D 4.+, &.> D 4.+, &." D 4.+, ".& D 4.+),
and &.6 D 4.+ days, respectiely (!able #).
!he adults of C. arcuatus suried for #*
$& days, and the predator lifetime underlaboratory conditions was +6.+ D 4.# days.
!he highest mortality rate was recorded for
the first laral instar (.#%) and the
mortality from egg to adult was ##.$%
(!able #). -re*copulation time aeraged &.'
days, and the mean length of copulation
time was $.+ minutes. !he results showed
that the mated females laid their eggs after
+.' D 4.& days. !he females laid their eggs
indiidually on the lower side of the leafsurface among S. phillyreae eggs. !he C.
-able #$ +ail ovi,osition and total eggs of Clitostethus arcuatus ,er fe#ale at 26F1G CSEM:
Replication"ini'u'daily
"a*i'u'daily
.ailyoviposition
-otaleggs per
1 1 7 2.26F0.26 18*
2 1 ( 2.06F0.27 160
& 2 * 2.&6F0.26 13&
( 1 * 2.26F0.23 180
* 2 7 2.(&F0.27 136
7 1 ( 2.1&F0.20 177
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Replicatio"ini'u'
daily"a*i'u'
daily.aily
oviposition-otal eggs
per
1 2 7 2.86F0.(7 136
2 2 ( 2.(6F0.(* 181& 1 * 2.68F0.(7 20(
( 1 7 2.86F0.(8 132
* 1 & 2.*3F0.(* 208
7 2 ( 2.7&F0.&3 166
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0adybird
active
"ini'u'
daily
"a*i'u'
daily
.aily feeding
("ean+E")
-otal
feeding("ean+E
1st larva & 27 12F2. 27F0.7
2nd larva 1( (3 &2F&. *1F2.&
&rd larva 26 6* (3F*. 6*F(.2
(th larva 28 10* 78F8. 106F(.8
min aftereclosion of the first laral instar, and the
adults can consume an egg in +>*#4 s.
1ewly hatched +st
instar C. arcuatus larae
were relatiely immobile and fed on S.
phillyreae eggs and nymphs oer a limited
leaf surface area. !he #nd
, &rd
and "th
laral
instars of C. arcuatus moed rapidly on the
leaf surface and fed on all nymphal stages
of the host while showing a preference for
eggs. !otal feeding by lara of C. arcuatusamounted to #>6 D & S. phillyreae eggs !he
total number of eggs consumed by males
and females of C. arcuatus was #4#" D &6
and "4#& D $", respectiely (!able >).
!he adults of C. arcuatus suried
staration for a maimum period of " days.
!he greatest loss of adult C. arcuatus due to
staration occurred in the second day
(2igure "). !o assess feeding rate of thepredator, +> adult C. arcuatus were
randomly selected from a population that
had preiously been stared for #" hours
and eposed to +#4 S. phillyreae eggs as a
food supply. !he consumption of eggs was
recorded hourly for the first h after
feeding and again at +# h, +' h, and #" h
after feeding. !he results showed thathighest and lowest feeding actiity occurred
in the #nd
and >th
hours, respectiely. !here
was a sharp increase in feeding in the #nd
hour after feeding followed by a steady
decline until the >th
hour where the feeding
rate dropped to its minimum and began to
increase slowly to reach to a second smaller
pea/ at +# hours after feeding, which was
followed by a less steep increase. !he
differences obsered between feeding ratesof stared predators at different hours after
feeding were highly significant (2igure >).
.iscussion
5iological studies on C. arcuatus showed
that the mean duration of egg deelopment,
laral and pupal stages were &.', ++." and
&.6 days, respectiely. 7gg incubation timewas relatiely shorter than the alue
reported by Age/yan (+6$$), which might
be attributed to the fact that the host
Dialeurodes citri, was different. 2rom our
-able 1. The longevit CdaD and #ortalit CHD of different growth stages of Clitostethus arcuatusunder field conditionsCSEM: Standard -rror of
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studies C. arcuatus adults suried for #*
$& days on S. phillyreae eggs, which is
considerably lower than the surial of C.
arcuatus on Aleurodes proletella, which
was reported to be approimately +>4 days(Biotta +6'+). !he longeity of females ($&
days) is was higher than males (# days),
which is consistent with the results of other
studies (5ellows et al. +66#).
!he first laral instar had the highest
mortality rate, and the mortality of egg to
adult was ##.$%, which is consistent with
results from 5ellows et al. (+66#), who
reported egg to adult surial of $'%
(!able ). A higher mortality rate for the
first laral instar is conceiable because thisinstar is the most ulnerable stage for C.
arcuatus followed by the #nd
, &rd
and "th
instars. 0ortality of C. arcuatus stabili3es
after the #nd
instar. Immature instars of
higher stages surie aderse
enironmental conditions better and
accordingly hae a lower mortality rate.
Figure 1$ +ail losses in adults of Clitostethus arcuatus during the starvation ,eriod. Valuesare the #eans of four re,licatesE error ars re,resent standard error of the #ean. "igh>ualit figures are availale online.
Figure 2$ ;eeding ehaviour of Clitostethus arcuatus in a 2(h ,eriod. Values are the #eans offour re,licatesE error ars re,resent standard error of the #ean. "igh >ualit figures are availale
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online.
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Al3Alafet al$
Bellows
et al$ #55%
Bathon and
6ietr7i8,
Age8yan,#5;;
0iotta,#59#
6resen
t
9u#erofgeneratio
& ( (
@ength ofegg! larval!and ,u,alStages
*! 1&1(! (* Con
Dialeurodes &.8! 11.(!
9u#er ofeggs
consu#ed the
(((Con5e#isi
*((F183ConAleurodes , to 270
. days and that the aerage surial
ability of the females was '# days. !he
results of the eperiments were produced
under laboratory conditions (#$ D +E C, &' D
#% RH and +:' B:) which was close to
the optimum temperature (#'.#E C) for the
deelopment, surial, and fertility of C.arcuatus reported by 5ellows et al. (+66#).
8ur studies reported a lower se ratio
(+:+.&') for C. arcuatus as compared to the
se ratio (+:+) reported by 5ellows et al.
(+66#).. In addition, the mean number of
eggs laid per day per female in present
eperiments was #.& D 4.&, with a total of
+'# D > eggs per female throughout its
entire lifetime, which is lower than the #4#eggs per day per female reported by
5ellows et al. (+66#) (!able ).
?enetic heterogeneity of the local
populations of C. arcuatus added to the
inherent demographic stochasticity of C.
arcuatus indiiduals and possibly the use of
S. phillyreae as prey may account for minor
inconsistencies between our results and
other findings. C. arcuatus is normallyactie for eight months, from April to
ecember, in the
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A. proletella in central 7urope where each
lara consumes about >"" D +'6 eggs
during its lifetime (5athon and -ietr3i/
+6'). C. arcuatus larae are reported to
consume an aerage of """ whitefly eggson B. tabaci (Al*Alaf et al. #44+). 7ach
male and female consumes about #$." and
4.$ whitefly eggs per day, respectiely
(5athon and -ietr3i/ +6'). Age/yan
(+6$$) obsered that C. arcuatus has a
preference for eggs and +st
instar nymphs of
S. phillyreae. Bower consumption rates of
the eggs of B. tabaci (approimately """)
C. arcuatus larae (Al*Alaf et al. #44+)
may be accounted for by host differencesand differential egg consumptions by males
and females, which are #$." and 4.$ eggs
of A. proletella per day, respectiely
(5athon and -ietr3i/ +6'). 2urther
research on this will certainly be re9uired to
clarify the host effect on the biology and
feeding behaiour of C. arcuatus (!able ).
In this study, the laral and adult stages of
C. arcuatus showed cannibalisticbehaiour. !he larae fed on conspecific
eggs, younger instars, and een pupae,
while the adults fed mainly on the eggs.
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Age/yan 1?. +6$$. Clitostethus arcuatus
Rossi (Coleoptera, Coccinellidae) * A
predator of citrus whitefly in Ad3haria.
Entomologicheskoe#$bo%renie >(+): &+*
&&.
Al*Alaf 1!, Ali AA, A*Adil ;0. #44+.
Integration of the I?R ApplaudJ
and the
predators, Clitostethus arcuatus (Rossi) and
$rius albidipennis Reut., for controlling the
whiteflyBemisia tabaci ?en. in Ira9.Arab
!ournal o" &lant &rotection +6(#): ++6*+#".
Alemansoor H, 2allah3adeh 0.#44".
5ioecology of ash whitefly Siphoninus
phillyreae (Halliday) (Hom. Aleyrodidae)
in the 2ars -roince, Iran.&ajouhesh#va#
Sa%andegi #: "*$4.
5asiri ?H, Allahyari 0, 2asihi 0!. #44".
-arsaitoids and predators of citrus
aleyrodids in south of Iran.pp. "",
-roceeding of the +th
Iranian -lant
-rotection Congress #' August*+
++*&".
5untin BA, !ama/i ?. +6'4. 5ionomic of
Scymnus marginicollis (Coloptera:
Coccinellidae). Canadian Entomologist
++#($): $>*'4.
Caon ?, e 5arro -.+666. Ash hitefly*A
1ew -est.)ursery *ndustry Association o"
Australia. Aailable from:
http:KKwww.ngia.com.auKpublicationLresour
cesK1-L-dfK1-L+666*4$.pdf.
elrio ?, 8rtu !7
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Biotta ?. +6'+. 8ssera3ioni bio*etologiche
su Clitostethus arcuatus (Rossi)
(Coleoptera: Coccinellidae) in .
Biotta ?, Agro A, -into 0B. #44&.
5iological control in citrus groes in the
last >4 years: !hree successful cases in
estern .Aleurothrius "loccosus(0as/.) in