Functional response and mutual interference of Diaeretiella rapae (Hymenoptera: Aphidiidae) on Brevicoryne brassicae (Homoptera: Aphididae)

2006·0.14 MB·

by  Yaghoub Fathipour

©EntomologicaFennica.16June2006
Functional response and mutual interference
of Diaeretiella rapae (Hymenoptera: Aphidiidae)
on Brevicoryne brassicae (Homoptera: Aphididae)
YaghoubFathipour*,AliHosseini,AliAsgharTalebi&SaeidMoharramipour
Fathipour,Y.,Hosseini,A.,Talebi,A.A.&Moharramipour,S.2006:Functional
response and mutual interference of Diaeretiella rapae (Hymenoptera: Aphi-
diidae)onBrevicorynebrassicae(Homoptera:Aphididae).—Entomol.Fennica
17:90–97.
Functionalresponseandmutualinterferencearethemostimportantbehavioural
characteristicsthatrevealdifferentaspectsofhost–parasitoidinteractions.Inthis
study, functional response and mutual interference of the parasitoid wasp,
Diaeretiella rapae (M’Intosh) attacking the cabbage aphid, Brevicoryne
brassicae(Linnaeus)wereinvestigated.Logisticregressionwasusedtodistin-
guishtheshapeofthefunctionalresponse(typeIIorIII).Nonlinearleast-square
regressionwasusedtoestimatetheattackrate(a)andhandlingtime(T).Nichol-
h
son’smodelandlinearregressionwereusedtodeterminepercapitasearchingef-
ficiencyandinterferencecoefficient,respectively.Logisticregressionsuggested
atypeIIresponseonB.brassicaenymphs.Thepercapitaparasitismdecreased
significantly from80.80(67.33%)to11.85(9.88%)asparasitoiddensitiesin-
creasedfrom1to8females.Consequently,thepercapitasearchingefficiencyde-
creasedsignificantlyfrom1.173to0.205asparasitoiddensitiesincreasedfrom1
to8.Therateofparasitismincreasedasthehostdensityincreasedfrom2to50,
andsubsequentlytheparasitoiddensitydecreasedfrom8to1.Therefore,differ-
enthost–parasitoidratioscouldaffecttheefficacyofD.rapae.
Y.Fathipour,A.Hosseini,A.A.Talebi&S.Moharramipour,DepartmentofEnto-
mology, Faculty of Agriculture, Tarbiat Modares University, P.O. Box 14115-
336,Tehran,Iran.*Correspondingauthor’se-mail:[email protected]
Received12January2004,accepted10March2005
1.Introduction tant aphid on Brassica as it renders the head as
unmarketable.Controloftheaphidiscommonly
Thecabbageaphid,Brevicorynebrassicae(L.)is achievedbyrepeatedapplicationofinsecticides.
apestofcruciferousplants, especially cabbage, Thedevelopmentofresistancetoinsecticidesand
occurringinvariouspartsoftheworld.Theaphid adverseeffectsonnaturalenemieshighlightsthe
causesdirectandindirectdamagebysuckingthe need for less insecticide-dependent methods of
sapofplantsandtransmittingplantviruses(Ellis pestcontrol(Verkerketal.1998).Oneofthecon-
et al. 1998, Blackman & Eastop 2000, Schliep- trolmeasures,whichcanbeusedforthecabbage
hakeetal.2000).B.brassicaeprefersfeedingon aphid,isbiologicalcontrol.Theaphidisattacked
youngerplanttissues,whichmakesitanimpor- bytheparasitoidDiaeretiellarapae(M’Intosh),
ENTOMOL.FENNICAVol.17 (cid:127) DiaeretiellarapaeonBrevicorynebrassicae 91
which tends to specialize on crucifer-feeding etal.1992,Yuetal.1993,Bernaletal.1994,Les-
aphids.However,attackonarangeofplantfami- ter&Holtzer2002)havebeencarriedoutonthe
liesbynumerousotherspeciesofaphidshasbeen functionalresponseofD.rapaetodifferentden-
reportedtoo(Dhiman&Kumar1987,Costello& sities of other aphids such as Myzus persicae
Altieri1995,Bernaletal.2001,Lester&Holtzer (Sulzer),Diuraphisnoxia(Mordvilko)andLipa-
2002). phiserysimi(Kalt.).Lessattention,however,has
Beforeusingaparasitoidinabiologicalcon- beenpaidtocabbageaphid,B.brassicae.Inmost
trolprogramme,itisessentialtoknowaboutthe availableliterature,thefunctionalresponseofD.
efficiencyoftheparasitoid.Oneoftheimportant rapaetodifferentdensitiesofaphidshasbeende-
methodstoassesstheefficacyofnaturalenemies terminedasthetypeII.Inthestudiesreportedby
isthestudyofbehaviouralcharacteristics,includ- Pandey et al. (1984) and Abidi et al. (1987),
ing foraging behaviour. Study of parasitoid be- D.rapaedisplayedfunctionalresponseoftypeIII
haviourisanimportantkeytounderstandinghow tomustardaphid(Lipaphiserysimi).Thetypeof
the insects live, how they influence the popula- functionalresponseandtheratesofitsparameters
tiondynamicsoftheirhosts,andhowtheyinflu- (attackrateandhandlingtime)areinfluencedby
ence the structure of the insect communities in differentfactorssuchasnaturalenemyandhost
whichtheyexist(Jervis&Kidd1996).Itisthusa species,physicalconditionsinthelaboratory,and
necessaryprerequisitefortheselectionofnatural thevarietyofthehostplant,etc.(Coll&Ridgway
enemies for biological control programmes and 1995, Messina & Hanks 1998, Fathipour et al.
fortheevaluationoftheirperformanceaftertheir 2001).
release(Luck1990). Aggregationbyparasitoidstohostpatchesis
Twoimportantbehavioursofparasitoidsare an integral component of models of host–
functional response and mutual interference. parasitoidpopulationdynamics.Indiscrete-time
Functionalresponseisthenumberofhostssuc- models,aggregationinspacetohostpatchessta-
cessfully attacked per predator (parasitoid) as a bilizesthehost–parasitoidinteractionbycausing
functionofprey(host)density(Solomon1949). searchingefficiencytodecreasewithincreasing
Itdescribesthewayanaturalenemyrespondsto parasitoid density (Godfray & Pacala 1992,
thechangingdensityofitsprey(host)bykilling Cronin&Strong1993a).Inversedensitydepend-
(parasitizing)moreorfewerindividuals,anditis ence in searching efficiency is known as para-
a commonly measured attribute of natural ene- sitoid interference or mutual interference (Bed-
mies of pests (Bazzocchi & Burgio 2001). dington1975).Thestudyofmutualinterference
Holling (1959) considered three types of func- wasinitiatedbyHassellandVarley(1969),who
tionalresponse.InthetypeI,thereisalinearrela- notedaninverserelationbetweentheparasitoid
tion between prey density and the number of searchingefficiencyandthedensityofsearching
preyskilled,whileinthetypeIIitiscurvilinear parasitoids.Sucharelationistobeexpected,be-
andsaturationlevelisreachedinagradualway. causeasparasitoiddensity increases, individual
ThetypeIIIisdescribedbyasigmoidrelationand parasitoidswillwasteanincreasingproportionof
consideredtobearegulatingfactorinthepopula- theirsearchingtimetoencounterotherconspeci-
tiondynamicsofthepestandthenaturalenemy. fics.Accordingtotheliterature,theparasitoidin-
Thefunctionalresponseofaparasitoidisacrucial terferencehasbeenreportedtooccurcommonly
factor in the population dynamics of host– inthelaboratory,butithasbeenhardlyeverre-
parasitoidsystems.Thisbehaviourcandetermine ported by field studies. Significant interference
ifaparasitoidisabletoregulatethedensityofits has been reported among populations of
hosts (Schenk & Bacher 2002). Functional re- parasitoidsbothinmanylaboratoryexperiments
sponsemodelshelptoevaluatetwovitalparame- and some field experiments (Cronin & Strong
ters, handling time (i.e. the time that it takes a 1993a,b).Significantmutualinterferencewasre-
parasitoid to encounter and parasitize a single portedamongD. rapaefemalesparasitizingLi-
host), and attack rate (i.e. the rate at which a paphis erysim (Pandey et al. 1986, Abidi et al.
parasitoid searches). Several studies (Pandey et 1989,Shuklaetal.1997).
al.1984,Abidietal.1987,Luetal.1992,Shukla In this study, the functional responses of
92 Fathipouretal. (cid:127) ENTOMOL.FENNICAVol.17
D. rapae to various densities of second instar hosts parasitized as afunction ofinitialdensity.
nymphsofB.brassicawereinvestigatedandthe The proportion of hosts parasitized declines
handlingtimeandtheattackrateoftheparasitoid monotonicallywithpreydensityinthetypeIIre-
wereestimated.Weexaminedtheeffectsofmu- sponse,butispositivelydensity-dependentover
tualinterferenceamongD.rapaefemalesonper some region of host density in the type III re-
capitaparasitismandsearchingefficiency. sponse (De Clercq et al. 2000). The sign of the
linearcoefficientestimatedbythelogisticregres-
sion(negativeorpositive)canbeusedtodistin-
2.Materialsandmethods guishtheshapeofthefunctionalresponsecurve
(typeII or typeIII, respectively) (Juliano 1993,
2.1.Parasitoidandhostcultures Messina&Hanks1998,DeClercqetal.2000).In
thesecondstep,boththediscequation(Holling
Diaeretiella rapae used in this study was origi- 1959)(Eq.[1])andtherandomparasitoidequa-
nally collected from mummified aphids (Brevi- tion(Royama1971,Rogers1972)(Eq.[2])were
corynebrassicae)inaninfestedcabbagefieldat used to obtain estimates for handling time (T)
h
the College of Agriculture of Tarbiat Modarres andsearchingefficiencyorattackrate(a).Forthe
University(Tehran)inMay2002.Thefirstlabo- typeIIresponse,theequationsareasfollows:
ratory generationofwaspswasusedtoconduct
the experiments. The B. brassicae culture was N =(aTN)/(1+aT N) (1)
a t h t
originallystartedfromindividualscollectedfrom
the above cabbage field and kept in a growth N =N [1–exp(a(T N–T))] (2)
a t h t
chamberoncabbageplants.Bothparasitoidand
aphidindividualswerekeptinagrowthchamber whereN isthenumber ofparasitized hosts, N,
a t
at 25±1ºC, 60±5% r.h. and a photoperiod of the number of hosts offered, T, the total time
L16:D8h. available for the parasitoid, a, the attack rate
(searchingefficiency),andT thehandlingtime.
h
Statisticalanalyseswereperformedusingthe
2.2.Functionalresponse SASpackage(SASInstitute1989).Inordertoes-
timatethehandlingtimeandsearchingefficiency,
TheexperimentalarenaconsistedofaPlexiglas nonlinear regression, using the least square
cage (4×8×14 cm) with a micromesh screen on methodwithDUDinitialization,wasused.Fur-
thelidforventilation.Distilledwaterandhoney ther,thepredictednumberofparasitizedhostsfor
solution(10%)wereplacedincagesasthepara- agivenhostdensitywasalsodetermined.
sitoidfood.SecondinstarnymphsofB.brassicae
wererandomlyplacedonthecabbageleavesin-
sidethecagesatdensitiesof2,4,6,8,10,15,20, 2.3.Mutualinterference
30,40and50percage.Asinglefemaleparasitoid
(maximum 24 hours old) was introduced into The experimental arena and growth chamber
each cage. Each host density was replicated 10 conditions were the same as those used in the
times. After 24 hours, the parasitoids were re- functional response experiment. Host density
movedandthehostsweremaintainedinagrowth washeldconstantat120secondinstarnymphsof
chamberuntilallparasitized(mummified)aphids B.brassicae.Femaleparasitoidsatdensitiesof1,
wererecognized.Theexperimentwasconducted 2,4,6and8percagewereallowedtosearchthe
at 25±1ºC, 60±5% r.h. and a photoperiod of hosts for 24 h. Each combination of hosts and
L16:D8h. parasitoiddensitywasreplicated15times.Inthe
Two principal steps underlie the statistical endofeachexperiment,theparasitoidswerere-
analysisofthefunctionalresponse:1)modelse- movedandthecabbageleafwithaphidnymphs
lection,and2)hypothesistesting(Juliano1993, wasplacedingrowthchamberfordevelopment
DeClercqetal.2000).Inthefirststep,alogistic oftheparasitoids.
regressionanalysiswasmadeoftheproportionof Thepercapitasearchingefficiency(a)ofthe
ENTOMOL.FENNICAVol.17 (cid:127) DiaeretiellarapaeonBrevicorynebrassicae 93
parasitoids at different parasitoid densities was
calculatedbythefollowingequation(Nicholson
1933):
a=(1/PT)ln[N /(N–N)] (3)
t t a
where N is the total number of hosts available
t
(=120),N isthetotalnumberofhostsattacked,P
a
isthenumberofparasitoids,andTistheduration
oftheexperiment(setto1.0foroneday).
Searching efficiency was plotted against
parasitoid density, both on a logarithmic scale.
Thepointswerefittedtoalinearregressionbythe
leastsquaremethod, usingthefollowinginduc-
tive model given by Hassell and Varley (1969),
assumingtheparametermasaslopeandQasthe Fig.1.Functionalresponse(a)andpercentagepara-
interceptoftheregressionline: sitism(b)ofD.rapaeonB.brassicaesecondinstars.
Symbolsandlinesrepresenttheobservedandpre-
dictednumbers(Hollingdiscequation),respectively.
a=QP–morloga=logQ–mlogP (4)
where a is the searching efficiency of the
parasitoid, Q isthequestconstant, andmisthe Attack rate and handling time for the disc
mutualinterferenceconstant.Inthismodel,min- equationwere0.033±0.03h–1and0.892±0.102h,
cludesonlythecomponentofinterferencedueto respectively,andfortherandomparasitoidequa-
behaviouralinteractionsbetweenparasitoids,not tiontheywere0.049±0.007h–1and1.020±0.115
pseudointerferenceresultingfrompatchexploita- h,respectively(Table2).
tion(Freeetal.1977). The lower coefficient of determination [r2 =
1–(residualsumofsquares/correctedtotalsum
ofsquares)]forthediscequationandtherandom
parasitoidequationwerethus0.77and0.76,re-
3.Results
spectively.Theestimatedmaximumrateofpara-
sitism(T/T)forthediscequationandtherandom
3.1.Functionalresponse h
parasitoidequationweredeterminedas26.91and
23.53,respectively.
Functional response and percentage parasitism Theratesofr2andstandarderrorsoftheesti-
curvesaredepictedinFig.1.Thelogisticregres-
mated parameters indicated that both equations
sion analysis(Table1) indicated atypeII func-
(disc equation and random parasitoid equation)
tionalresponse.Theestimateofthelinearcoeffi-
adequately describe the functional response of
cientwassignificantlydifferentfrom0(p<0.01)
D.rapae.
anditsvaluewas–0.159.
Table1.ResultsoflogisticregressionanalysisoftheproportionofB.brassicaesecondinstarsparasitizedbyD.
rapaefemalestoinitialhostnumbers.
Parameters Estimate S.E. (cid:1)2 p
Constant 1.9825 0.3499 32.10 <0.0001
Linear –0.1595 0.0487 10.73 0.0011
Quadratic 0.00304 0.00189 2.58 0.1085
Cubic –0.00002 0.000022 0.66 0.4149
94 Fathipouretal. (cid:127) ENTOMOL.FENNICAVol.17
Table2.Parameters(mean±S.E.)estimatedbydiscandrandomparasitoidequations,evaluatingfunctionalre-
sponseofD.rapaefemalestodensitiesofB.brassicaenymphs.
Discequation Randomparasitoidequation
Type a(h–1) T(h) r2 a(h–1) T(h) r2
h h
II 0.033±0.003 0.892±0.102 0.77 0.049±0.007 1.020±0.115 0.76
Table3.Percapitaparasitismandpercapitasearch-
ingefficiency(mean±S.E.inboth)ofD.rapaeonB.
brassicae.
Parasitoid Percapita Percapita
densities parasitism searching
efficiency
1 80.800±4.210a 1.173±0.112a
2 48.150±1.370b 0.839±0.056b
Fig.2.RegressionlineinmutualinterferenceofD.
4 22.750±0.948c 0.373±0.031c
6 14.983±0.671d 0.244±0.022d rapae.
8 11.853±0.402e 0.205±0.016d
Valuesfollowedbydifferentletterswithincolumnsaresignificantlydiffer- sity.TheregressionlineisillustratedinFig.2us-
ent(p<0.01). inglogarithmicaxes.
3.2.Mutualinterference
4.Discussion
Thepercapitaparasitism(aphidnymphalmortal-
ity)decreasedsignificantlyfrom80.80(67.33%) D.rapaeisthemostabundantandimportantnat-
to11.85(9.88%)withincreasingparasitoidden- uralenemyofB.brassicaeinIranandplaysama-
sities from 1 to 8 per 120 host nymphs (F jorroleinreducingthepopulationdensityofits
4,
=198.51,p<0.001;Table3).Consequently,the host.InadditiontoD.rapae,therearesomeother
45
per capita searching efficiency also decreased parasitoidwaspsinIran,whicharelessabundant
significantlyfrom1.173to0.205withincreasing andlessimportantsuchasAphidiusspp.andLysi-
parasitoid densities from 1 to 8 (F =51.63, phlebusspp.fromthesamefamily(Aphidiidae)
4, 45
p<0.001;Table3). thatparasitizecabbageaphid(Staryetal.2000).
The linear regression between the logarithm Amongthenaturalenemiesofcabbageaphid,D.
of per capita searching efficiency and the loga- rapaeservesasagoodcandidatefornaturalsup-
rithmofparasitoiddensityinthemutualinterfer- port,massrearingandreleaseforcontrollingthis
enceanalysisresultedintheequation: aphid because of high population densities and
highratesofparasitism.Inthisregard,thestudy
loga=0.115–0.895logP(F =140.29, offoragingbehaviouranddemographicparame-
1,3
p<0.001,r2=0.97). tersofD.rapaeinahost-parasitoidsystemises-
sential.SomedemographicparametersofD.ra-
Theinterferencecoefficient(slopeoftheregres- pae and B. brassicae were calculated and com-
sionline)ism=–0.895.Thenegativevalueofthe paredbyHosseinietal.(2003).Theyinferredthat
regressionslopeindicatesaninverserelationship population growth rate of the parasitoid was
betweenparasitoiddensityandpercapitasearch- slightlylessthanthatoftheaphid.
ing efficiency. In other words, searching effi- In this study, different densities of host and
ciencydecreaseswithincreasingparasitoidden- parasitoid were selected according to the litera-
ENTOMOL.FENNICAVol.17 (cid:127) DiaeretiellarapaeonBrevicorynebrassicae 95
ture.Themainpurposeoftheselectionofthese would probably leave the patch because of the
densitieswastoidentifytheroleofdifferentden- verylowhostdensityorbecausemosthostsare
sities of the host and parasitoid on the foraging alreadyparasitized(Montoyaetal.2000).
behaviour of the parasitoid and on the host- Bernaletal.(1994)pointedoutthattherela-
parasitoid interactions. The selected densities tionbetweenfunctionalresponsesobservedinthe
maynotbecompletelycompatiblewiththoseof laboratoryandfieldperformanceofnaturalene-
thehostandparasitoidinnaturalpopulations. miesisnotclear,butsomestudiesshowedasig-
nificant difference between the responses ob-
servedinlaboratoryandfieldenvironments.Itis
4.1.Functionalresponse recognizedthatfunctionalresponsederivedfrom
laboratorystudiesmaybearlittleresemblanceto
ThetypeIIfunctionalresponsedisplayedbyD. thosethatcouldbemeasuredinthefield(Mon-
rapae to different densities of B. brassicae toyaetal.2000).
nymphs is characteristic of many aphid para- HouckandStrauss(1985)pointedout,how-
sitoids, though the type III responses have also ever,thatstudiesoffunctionalresponseinlabora-
beenreported(Bernaletal.1994).Inmostrelated torycouldbeusedtoinferbasicmechanismsun-
literature,thefunctionalresponseofD.rapaeto derlying natural enemy-host interactions. Such
differentdensitiesofDiuraphisnoxia(Bernalet studiesprovidevaluableinformationforbiologi-
al.1994,Lester&Holtzer2002),Lipaphisery- calcontrolprogrammes.Bernaletal.(1994)ex-
simi (Shukla et al. 1992, Yu et al. 1993) and pressedthatduringbiologicalcontrolevaluation
Myzuspersicae(Luetal.1992)hasbeendeter- processes, comparisons of parameter values of
minedtobeofthetypeII.However,inthestudies twoormoreparasitoidsmaybemoremeaningful
reportedbyPandeyetal.(1984)andAbidietal. andconvenientthansimilarcomparisonsinvolv-
(1987),D.rapaedisplayedatypeIIIfunctional ingfunctionalresponsecurves.
responsetomustardaphid(Lipaphiserysimi).
Theestimatedmaximumattackratehasbeen
determinedas28.8per0.5h(Abidietal.1987), 4.2.Mutualinterference
41.84(at15°C)and47.56(at18°C)per24h(Yu
etal.1993)and59.5per24h(Bernaletal.1994). Inthepresentstudy,thepercentageofparasitized
Inthisstudy,theestimatedmaximumnumberof aphidsincreasedwithincreasingparasitoidden-
parasitizedaphidsismuchsmallerthanthatob- sity;however,theincreasedparasitoiddensityre-
tainedbytheaboveresearchers. sulted in a constant decrease in the number of
Theratesofsearchingefficiency(a)andhan- aphids killed per parasitoid, as well as reduced
dlingtime(T)werereportedtobe1.341h–1and progenyperparasitoid.Thesearchingefficiency
h
0.408h,respectively(Bernaletal.1994)and1.74 of the parasitoid decreased with increasing
h–1 and 0.024 h, respectively (Lester & Holtzer parasitoid density, and the stability of co-exis-
2002).ThecitedratesofaaregreaterandT are tence between the host and the parasitoid in-
h
smaller than those obtained in our study. How- creased with an increase in mutual interference
ever, the differences among the experimental (Jonesetal.1999).
conditionssuchashostspeciesandphysicalcon- Shuklaetal.(1997)reportedthatwhen1,2,4
ditions between different studies were substan- or8parasitoids(D.rapae)werereleasedon200
tial. aphids (Lipaphis erysimi), the number of
ForthetypeIIresponse,parasitismisnotden- emerged parasitoids showed a significant posi-
sitydependent:thatis,theintensityofparasitism tive correlation with increasing parasitoid den-
does not increase with host density (Hassell sity. However, the rate of multiplication, ex-
1978).Severalauthors(sources)havetriedtoex- pressedasparasitoidegressed/femaleparasitoids
plain why the type III response is less common putin,wasthehighestwithoneparasitoidper200
than the type II. They agree that in laboratory hostsanddecreasedwithanincreasingparasitoid
tests,parasitoidsareforcedtoremaininthepatch, number. The fact that more parasitoids have a
whereas under natural field conditions they lowerrateofmultiplicationshowstheexistence
96 Fathipouretal. (cid:127) ENTOMOL.FENNICAVol.17
of mutual interference. The number of progeny MasoodAmir-Maafi&Dr.JafarMohaghegh(PlantPests
produced per female D. rapae parasitoid is in- andDiseasesResearchInstitute,Iran).Wealsothanktwo
reviewerswhogreatlyimprovedthemanuscript.
verselyproportionaltotheparasitoidnumber,in-
dicating intraspecific competition in the para-
sitoid (Abidi et al. 1989). Pandey et al. (1986)
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