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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+).

    http://www.insectscience.org/http://www.insectscience.org/http://www.insectscience.org/http://www.insectscience.org/
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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