DanielSol·RogerJovani ·Jordi Torres
Parasitemediatedmortalityandhostimmuneresponse explainage-relateddifferencesinbloodparasitisminbirds
AbstractAnimportantpatterninhost-parasite assem- blagesisahigherintensityofparasitesinjuvenilesthanin adults,butthereasonsforthesedifferences remain obscure.Threenon-mutuallyexclusivehypotheseshave been proposed: (1) heavily parasitized juveniles die beforebeingrecruitedintotheadultpopulation(‘selec- tion’hypothesis); (2)thedevelopment ofanacquired immunitybythehostinfrontoftheparasitereduces the intensity oftheparasiteinadulthosts(‘immunity’ hypothesis); and(3)differencesinbehaviormakesadults lessexposedtotheparasitethanjuveniles (‘vector exposure’hypothesis). Havingrejectedthe‘vectorexpo- sure’hypothesisinapreviousstudy,herewetestedthe
‘selection’and‘immunity’ hypotheses inferalpigeons (Columba livia)infectedbythebloodparasiteHaemo- proteuscolumbae. Inagreementwiththe‘selection’ hypothesis,young(butnotadult)pigeonsthatwerehighly parasitizedhadalowerprobability ofsurvivinguntil adulthood,independentoftheirbodycondition.However, selectionwasnotstrong enough toaccountforthe observeddifferences inparasiteintensitybetweenage- classes,andafterselectionparasiteintensity ofsurvivors stillremained85%higherinjuveniles thaninadults.In contrast,the‘immunity’ hypothesis offeredagreater explanatory power.Theintensityofbloodparasitesin youngpigeons,butnotinadults,decreasedovertimeso
dramaticallythatbythetimetheyhadbecome adultstheir intensitieswereindistinguishablefromthattypicallyseen inadults.Therefore, whileselectionagainsthighly parasitizedjuvenilescancontributetosomeextenttoa reductioninparasitismseenintheadultpopulation, age- specificbloodparasitisminferalpigeonsisbestexplained asatransitory phasejustbeforethehostdevelopsan effectiveimmuneresponse.
Keywords Columbalivia·Haematozoa·Haemoproteus columbae·Parasite-hostinteraction·Survivalselection
Introduction
Quantifying andinterpretingpatternsinhost-parasite interactionsisessentialforunderstandingtheecological andevolutionary implicationsofparasitesontheirhosts and,ultimately,onecosystems. Acommonpattern observedinhost-parasiteassemblagesisahigherintensity ofparasitesinjuvenilescomparedwithadults(reviewed inHudsonandDobson1997).Thispatternhasbeenfound inbothhuman(e.g.Gravesetal.1988)andnon-human mammals (e.g.Gregory etal.1992),andisalso widespread inbirds(e.g.AllanderandBennett1994; DawsonandBortolotti1999).Thereasonswhyjuveniles
tendto exhibit higherintensitiesofparasitesthanadultsis
D.Sol())
DepartmentofBiology,
McGillUniversity,
1205avenueDocteurPenfield,Montreal, Quebec,H3A1B1,Canada
e-mail:
Tel.:+1-514-3984116
Fax:+1-514-13985069
R.Jovani
DepartmentofAppliedBiology,EstaciónBiológicadeDoflana, C.S.I.C.,Avda.MªLuisas/n,41013Sevilla,Spain
J.Torres
DepartamentdeMicrobiologiaIParasitologiaSanitàries, UniversitatdeBarcelona,
Av.Diagonal643,08028Barcelona,Catalonia,Spain
anissueofconsiderable theoreticalinterest.Ahigher abundanceofparasites injuvenilesisprobablyoneofthe factorsresponsible forthehighmortalitythatyoung animalsexperience(e.g.Wunderle1991),anditiswell establishedthatsuchage-specificmortalitycanaffecta numberofimportantecologicalandevolutionary pro- cesses.Forexample,anincrease injuvenilemortality inducedbyparasiteshasrecentlybeenarguedtofavorthe evolutionofreducedclutchsizesinbirds(Martinetal.
2001).Thus,tofullyunderstandhost-parasite assem- blages, itisimportanttoinvestigatethecausesthatmake theparasitevaryinabundance andvirulenceamongthe differentdevelopmentstagesofthehost.
Threenon-mutually exclusivehypotheseshavebeen proposed toexplainwhyjuvenilestendtoexhibithigher intensitiesofparasitesthanadults(reviewedinGregoryet al.1992):(1) heavilyparasitizedjuvenilesdiebeforethey mayberecruitedintotheadultpopulation (‘selection’ hypothesis);(2)thedevelopmentofanacquiredimmunity by thehost infrontoftheparasitereducestheintensityof theparasiteinadulthosts(‘immunity’hypothesis);and (3)differences inbehaviormakesadultslessexposedto theparasitethan juveniles(‘vectorexposure’hypothesis). Evidenceinhumanandnon-human mammalstendto favorthe ‘immunity’hypothesis(Hudsonand Dobson
1997), butstudies todatehaveneitherexaminedthis questioninbirdsnorstudiedallthreehypothesestogether. Thus,thecausesunderlying theage-relatedpatternof parasitismremainobscure.
Here,weexploreforfirsttime the differenthypotheses thatmightexplainwhyjuveniles sufferhigher parasite levelsthanadults.Ourstudysubjects, Haemoproteus columbae (Kruse)infectingferalpigeons(Columba livia, Gmel),represent aparticularlysuitablemodelsystemfor exploringthesequestions. First,youngpigeonssuffer intensitiesofH.columbaebetweenthreeandfivetimes thatofadults(Soletal.2000).Second,pigeons are relativelyeasytomonitor inthefieldand,hence,itis possible toaccuratelyassesshowvariationinparasite intensity influences survivorship of individuals (Sol
2000).Finally,H.columbae isoneofthebest-known bloodparasitesofbirdsandessentialinformationaboutits cycleisalreadyavailable(AtkinsonandvanRiper1991). Thepossibilitythatage-specificparasitismwasassociated withdifferentialexposure totheparasitewaspreviously rejected,sincethevectorthattransmitstheparasitewas notfoundmorefrequentlyinjuvenilesthanadults(Solet al.2000).Thetworemaininghypothesesarenotmutually exclusive, but each makes different predictions. The
‘selection’hypothesis predictsthathighlyparasitized youngpigeons shouldbelesslikelytosurvive until adulthood thanlessparasitizedones.Wetestedthis hypothesis byexaminingtheoccurrenceofparasite- induced survivalselectionwithinjuvenileandadult pigeons.The‘immunity’hypothesis,ontheotherhand, predictsadecreaseininfectioninjuvenilesuntiladult- hood,whereasit remainsat lowlevelsin adults.We testedthissecondhypothesisbymonitoring theprogres- sionoftheinfectioninjuvenilesuntiladulthood andthat inadultsovera similarperiodtime. Theintegrationofthe resultsfromthesetwodistinctapproaches allowedusto assesstherelativecontribution ofeachhypothesistothe age-specificparasitisminpigeons.
Materialsandmethods
Wecapturedandsampledfree-livingferalpigeonsintheurbanarea of Barcelona,Catalonia(NESpain).Eachbirdwasbandedand two bloodsmearswereobtainedtomeasure theintensity ofblood parasites. Bloodsmearswereobtained fromadropofblood squeezed fromaclippedtoenailontoaglassslide(Davidar and Morton1993).Eachslidewasrapidlyairdried,fixedwithmethanol
for10minandstained withGiemsastain.Amagnificationof x1,000wasusedtoquantify bloodparasites. Allhaemoparasites observed weredeterminedasHaemoproteuscolumbae (Apicom- plexa:Haematozoa) accordingtothedescriptionofthemacroand microgametocytesinBennettandPeirce(1990).Theintensityof parasiteswascalculated asthesumofthenumberofparasitizedred bloodcellscounted in100microscopicfieldsbymoving randomly overtheslideinareas wheretheblood cellsformed amonolayer (Bennettetal.1995).Therepeatabilitiesofourmeasures of intensity werehigh,bothwithinthesamesmears (r=0.99, F1,38=4,852.3,P<0.0001)andbetween replicatedsmearsfroma sameindividual(r=0.99,F1,38=2,490.9,P<0.0001).
Protozoa belonging to the genus Haemoproteus are mostly
parasitesofbirdsandaretransmittedbyceratopogonid(Diptera,
Ceratopogonidae)andhippoboscidflies(Diptera,Hippoboscidae;
Atkinson and van Riper 1991). The species H. columbaeis a
cosmopolitan parasite of pigeons and is transmitted by the
hippoboscidflyPseudolynchiacanariensis (Soletal.2000).The
parasitehasanasexualphaseinthelungcellsofthepigeonanda
sexualstageintheredbloodcells(AtkinsonandvanRiper1991).
After21–32daysofprepatentperiod(Ahmed andMohamed1977,
citedinAtkinsonandvanRiper1991),gametocytes(thetransmis-
sible stage) appear in the circulating blood. In the blood, the
intensityofH.columbaefollowsthethreetypicalphasesofmost
microparasites(e.g.HudsonandDobson1997;Valkiünas1997):
first,the parasiteappearsin smallnumbersin the bloodstream
(acute phase);thenit experiencesa rapid increasein whichit
reachesamaximum (crisisphase);andfinally,theparasitereduces
dramaticallyitsnumbersremaininginlowerdensities(chronicor
latentphase).
Testofthe‘selection’hypothesis
Tostudytheoccurrenceofparasite-inducedsurvivalselectionin pigeons,fromJunetoJuly1996wecapturedatotalof18young and46adultpigeonswithintheinstallations oftheZoolôgicde Barcelona. Youngpigeons(i.e.individuals lessthan6monthsold) weredistinguishedfromadultsaccordingtothecolorofthecere andtheiris(KautzandSeamans 1986).Becauseaprevious study foundnoevidenceofsex-relateddifferences neitherinprevalence norinintensityofH.columbaeintwopigeonpopulations(Soletal.
2000),wedidnotconsidersexinthenextanalyses. Pigeons were marked with metallic and patagial tags, sampled for blood parasites,measuredandimmediatelyreleased.Allindividualswere foundtobeparasitizedbyH.columbae. Wemeasuredthewing lengthandmasstoassessbodyconditionofindividuals. The markedpopulationwasmonitoredby periodicalcensus(one ortwo non-consecutive daysperweek,n=107days)toidentifythose individuals thatwerealive6monthsafterbanding.A6-month period is more appropriate here than the usual 1-year period becausejuvenilemortalityisextremelyhighinthepopulation (Sol etal.1998).Wedefine“survivors”asindividualsthatwereseen afterthe6-monthperiod,whereas“nonsurvivors”wereindividuals notseenlater.Weareconfident thatthemaincauseofdisappear- anceismortalityratherthandispersalaspigeonsshowedahigh site-fidelityinthestudyarea(SolandSenar1995). Inaddition, censuseswere conductedoveramuch largerareathan thepigeons’ homeranges,and werecontinuedlong afterthenumberofdetected individualshadreachedits asymptote,tomaximizethedetectionof survivors(Sol2000).
Todemonstratesurvivalselectionagainstthemostparasitized birds,we estimateddirectionalselectiondifferentials(Endler1986)
and cubic splines (Schluter 1988). The directional selection
differential(Si) forthesurvivalanalysiswasestimatedasthe covariance between relative fitness and parasite intensity, and testedforsignificanceusingalogisticregression (Endler1986). Analyseswereperformedonsquare-roottransformeddatastan-
dardizedbydividingbythestandarddeviation(LandeandArnold
1983).Fitnesscurves estimatedusing cubicsplines(Schluter1988)
wereusedtofurtherconfirmtheselectionpattern.Thecubicsplines
were estimated with the program GlmWIN developed by D.
Schluter.Toassessifselectionalonewasstrongenoughtocause theobserved differences inparasitemiabetweenjuveniles and adults,wecompared theselectiondifferentialobtainedinthe survival analysiswiththatestimatedusingjuveniles andadultsas thebefore-selectiongroupandadultsastheafter-selectiongroup.
Becausewedetectedselectioninjuveniles,wealsoinvestigated whetherthiswasdirectlycausedbytheparasiteorwasanindirect
resultofahypotheticalcorrelationwithbodycondition.Thedirect
effectoftheparasitewasestimatedbymultipleregression(Lande
andArnold1983),usingtherelativefitnessofindividuals(w)asthe
dependentvariable andparasiteintensity,bodymassandwing
lengthasindependentvariables.Themethodusedheretocontrol
forbodyconditionisthatproposedbyGarcIa-Berthou(2001), who
suggestedthatincludingbodymassandameasureofbodysize
(winglength inourcase)inthesameregressionmodel isgenerally
moreappropriatethanusing theresidualsofalog-logregressionof
bodymassagainstbodysize.Thetwovariableswerepreviously
normalizedbylog-transformation.Partialregressioncoefficients
wereusedtoestimatethedirectionalselectioncomponents(the
selectiongradientb).
Testofthe‘immunity’hypothesis
Totestthe‘immunity’ hypothesis, wecapturedfree-livingferal pigeons(bothjuveniles andadults)fromFebruary toMay1998at theExperimentalCampusoftheUniversitat deBarcelona(seeSol etal.2000fordetails).Thebloodsampling determinedthatall individualswereparasitizedbyH.columbae.Afterbloodsampling, pigeonswerereleasedandfromJunetoAugustofthesameyearwe triedtorecaptureasmanyofthemaspossible toobtainasecond bloodsmearforassessingpossiblechangesinparasiteintensity.We recapturedatotalof 12juvenilesand8adultsof themarkedpigeon population.Timebetweenbothcaptureswasalwaysgreaterthan
30daysanddidnotdifferbetweenage-classes(Mann-Whitneytest, U=14,P=0.18).Alljuvenilesdisplayedadultmorphology when recaptured,makingthemindistinguishable fromtheadults.Before analyses,theintensityofbloodparasiteswassquare-root trans- formed to meet the assumptions for a t-test. In some cases, however,theassumption ofequalityofvarianceswasnotmet,and thenweevaluateddifferencesinmeansbetweengroupsusingeither Mann-WhitneytestsorWilcoxonMatchedPairs Tests.Throughout the paper,meansare reportedwith the correspondingstandard error.
Results
Testofthe‘selection’hypothesis
Themortalityratewashigherforjuvenilesthanfor adults (0.61vs.0.33,testofproportion,P<0.05).Similarage- related differences in mortality have also been found usinglargersamplesizes(D.Sol,inpreparation), which suggeststhatoursampleisrepresentative ofthepopula- tion.Beforeselection,parasiteintensityinjuvenileswas
93.8% higher thanthatofadults (t62=—6.91,P<0.0001; Fig.1),butafterselectionimportantchanges were observed. Thedirectionalselectiondifferentialrevealed thatinjuvenilesmortalitywasassociated withparasite intensity,nonsurvivors beingsignificantly morepara- sitizedthansurvivors(Si=—0.377,P=0.04).Fitnessanal- yseswithunivariatecubicsplinesindicatedamaximum intheprobabilityofsurvivorship associatedwithlow levelsofparasites,confirming theexistenceofselection against highlyparasitizedbirds(Fig.2).Inadults,no similar selection was detected (Si=—0.093,P=0.19).
Fig.1IntensityofHaemoproteuscolumbae(mean€SEnumberof parasitizedredbloodcellscountedin100microscopicfields)in juvenileandadultpigeons(Columbalivia)AbeforeandBafter selection
Fig.2Univariatecubicsplinefortherelationbetweensurvivaland Haemoproteuscolumbaeintensity(numberof parasitizedredblood cellscountedin100microscopicfields)inyoungpigeons
Therefore, selection associated with parasitism was mostly restrictedtothejuvenileperiod. Thepossibility that body condition,rather than the parasite, was the directcauseofjuvenilemortalityisnotsupported inour data,since juvenilemortalitystillremainedassociated withparasiteintensityaftercontrollingforbodycondition (b=—0.486€0.202, t14=—2.40,P=0.03).
Yetevenwithstrong selectionagainst themost parasitizedindividuals, selectionwasinsufficient to accountforthedifferences inparasiteintensityobserved betweenjuveniles andadults.Theselectiondifferential usingjuvenilesandadultsasthebefore-selectiongroup andadultsastheafter-selectiongroupwasestimatedas
—0.409, a value that is superior to the differential estimatedinthesurvivalselectionanalysis. Thus,not surprisingly,parasite intensity after selection was still
84.5%higherinjuveniles thaninadults(t52=—3.92, P<0.0002;Fig.1),withaclearsegregationbetweenthe valuesofthetwogroups. Forexample,adiscriminant analysisrevealedthatparasite intensity aloneallowed correctclassification of72%ofjuvenilesand95%of adults(Wilks’ Lambda:0.560, F1,61=47.754,P<0.0001; Fig. 3). Therefore, selection alone cannot explain the
Fig.3Frequencydistributionofintensity(numberofparasitized redbloodcellscountedin100microscopic fields,squareroot transformed) ofHaemoproteuscolumbaeinjuvenilesandadults beforetheepisodeofnaturalselection
Fig.4Changesintheintensity(mean€SEnumberofparasitized redbloodcellscountedin100microscopicfields)ofHaemoproteus columbaebetweenthefirstcaptureandtherecaptureinjuvenile andadultpigeons(**meansP<0.01;NSmeansnon-significant)
differencesinparasiteintensityobservedbetweenjuve- nilesandadults.
Testofthe‘immunity’hypothesis
Attheinitialcapture,parasiteintensityinjuvenileswas
76.3%higherthanthatofadults(Mann-Whitney test, U=17.5,P=0.009;Fig.4).However, whenjuvenileswere re-capturedshowingadultmorphology,theirintensities
hadundergone adramaticdecline(Wilcoxon Matched PairsTest,Z=2.59,P=0.009).Thisdecreasewasobserved inallbutoneindividual,whichhadinsteadexperienced anincreaseinparasiteintensity.Nosimilarreduction in parasite intensity was observed in adults (Z=1.40, P=0.16),exceptinoneindividual whichhadaninitial intensitythatwasabnormally highforadults.Asaresult ofthereduction inparasitesinjuvenilesandtherelative stabilityinadults,theparasiteintensityofjuvenilesinthe recapturewasindistinguishablefromthatfoundinadults (t19=—0.96,P=0.35; variables previously square-root transformedtomeettherequirements ofat-test;Fig.4). Thelackofdifference isnotjustaresultofinsufficient powerofthetest(power=0.2), butreflectstheconver- gence in parasiteintensityofjuvenilesto valuessimilar to thosefoundinadults.Thus,whileintheinitialcapture morethanhalfofindividuals hadparasiteintensities outsidetherangeseeninadults,inthere-captures only2 outof12juveniles remainedwithparasiteintensities outsidetheadultrange(Fig.5).
Discussion
ThepathogenesisofHaemoproteus ontheirbirdhostshas beenthesubjectofsomecontroversy inthepast,mostly amonglaboratoryandfield researchers(Atkinsonandvan Riper1991).Previous evidencefromexperimentalinfec- tionsincaptivity,coupled withadditionalanecdotaldata frommoribund birds,suggeststhatHaemoproteushas importantpathogeniceffectsontheirhosts(reviewedin Atkinson andvanRiper1991;Atkinson 1999).Yet, studiesinwildbirdpopulationshavebeenincapableto provide similar evidence in the field. Bennett et al. (1988),forexample, reportednodifferencesinbodymass betweeninfectedanduninfected birdsof15passerine species.Siikamäkietal.(1997)didnotdetectdifferences insurvivorship betweenuninfectedpiedflycatchers (Ficedulahypoleuca) andthoseinfectedbyHaemopro- teusspecies.Merinoetal.(2000)reportedthatbluetits (Paruscaeruleus)treatedwithamedicationagainstblood parasitestendedtoincreasetheirreproductive success compared tountreatedcontroltits.Yet,theyfailedto identifytheparasitethatwasresponsibleoftheeffect,
Fig.5Frequencydistribution ofintensity(numberofpara- sitizedredbloodcellscounted in100microscopicfields, squareroottransformed)of Haemoproteuscolumbaeinju- venilesandadultsonAinitial captureandBre-capture
since thetreatmentaffectednotonlyHaemoproteus parasitesbutalsoLeucocytozoonparasites,agenuswell knownforitsimportantpathogeniceffects(Atkinson and vanRiper1991).Finally,DawsonandBortolotti (2000) found that females (but not males) of the American kestrel(Falcosparverius)withhighestjointintensitiesof twoHaemoproteusspecieswere lesslikelytoreturnfrom theirwintering quartersthefollowingyear(Dawsonand Bortolotti 2000).But,thisstudycouldnotseparate survival fromdispersal, andtherefore alsofailedto demonstrate thattheparasitecausedthedeathofthe females.Thus,forsometime,researchers havefacedthe paradox ofusingHaemoproteusasamodeltoaddress importantecologicalandevolutionary questions(e.g. HamiltonandZuk1982;Poulinetal.2000),whilehaving no compelling evidence that it causes a detrimental impactonwildanimals.
Ourstudyprovides thefirstsolidevidencefora pathogenic effectofHaemoproteusonawildbird population, andthusreconcileslong-timediscrepancies between field and laboratory studies. We found that youngpigeonswithhighparasitemias werelesslikelyto surviveuntiladulthood thanlessparasitizedones,butno similareffectwasfoundinadults.Interestingly, the influenceoftheparasiteonjuvenilesurvival wasnot foundtobeaby-productofdifferencesinbodycondition betweenindividuals. Thislastresultisconsistentwitha recentexperimentinwhichwefoundnoevidencefora linkbetweenbodyconditionandintensityofH.columbae inferalpigeons(D.SolandR.Jovani,inpreparation). Thepossibilitythatmortalitywasacorrelatedeffectof otherbloodparasitesmayalsobediscarded, sinceH. columbae wastheonlybloodparasitedetectedinthe bloodsamples (seealsoSoletal.2000).Takentogether, theselinesofevidencestrongly suggestthattheparasite causesevereinjuriesontheirhosts.Inaddition,theresults emphasize thatthedamageproduced onthehostgreatly dependsontheabundance ofparasites, theeffectsbeing onlyimportantwhentheintensities areveryhigh(i.e.,in somejuveniles). Theideathatistheintensityofthe parasite,ratherthanitspresence perse,whathasfitness consequencesisgenerallyunder-appreciatedintheeco- logically-orientedparasite literature,butisclearlysug- gestedwhenoneexaminesthepossible mechanisms throughwhichtheparasitemayimpactonthehost.For example,ahighdensity oftheparasitecouldhave importanteffectson thegeneralfunctioningof theanimal by alteringtheefficiencyinthetransportofoxygentothe differentpartsofthe body.Thisis tobeexpectednotonly becauseH.columbae entersthebloodcells,butalso becauseithasanasexual stageinthecellsofthelung (Atkinson andvanRiper1991).Similarly, somelabora- toryevidencesuggeststhat,athighintensities, Haemo- proteuscancausesevereinjuries ontheiravianhostsby directtissuedamage(reviewedinAtkinsonandvanRiper
1991;Atkinson 1999).Theintensity oftheparasite appearsthusto bea morereliable predictorofthe parasite virulencethanitsprevalence,which could explainwhy Siikamäkietal.(1997)orBennettetal.(1988)didnot
detectanydifferenceinsurvivorship orbodymass betweeninfectedanduninfected birds.Overall,our findingsindicate that the impactofHaemoproteus species ontheirhost,andultimatelyonpopulation dynamics, shouldbereconsidered.
Thelinkbetweenparasiteintensityandsurvivalwould atfirstappeartobeconsistent withthe‘selection’ hypothesis: adultshavelowerparasiteintensitythan juveniles becauseheavilyparasitizedjuveniles diebefore theymaybe recruitedintotheadultpopulation.However, selectioninjuvenileswasnotstrongenoughtoaccount fortheobserveddifferencesinintensitybetweenjuveniles andadultsand,afterselection, parasiteintensity wasstill considerably higher in juveniles than in adults. In addition,therewasaclearsegregationbetweenthevalues ofparasiteintensity observed injuveniles andthoseseen inadults,which meansthatsomechanges inparasite intensitywerenecessary injuvenilestoachievevalues similar to those usually seen in adults. Thus, the
‘selection’hypothesisaccountsforonlyaminorpartof thedifference inparasiteintensityseenbetweenage classesinpigeons.Incontrast,the‘immunity’hypothesis offersagreaterexplanatory power.Wefoundthatthe intensityofbloodparasites inyoungpigeons,butnotin adults,dramaticallydecreasedovertime.Thisreduction wassosignificant that,bythetimejuveniles hadbecome adults,theirintensitywasindistinguishable fromthat typicallyobservedinadults.Thisisconsistentwiththe ideathatafteracertainlengthofexposure, individuals acquiresome degreeofimmunityagainsttheparasiteand arethusabletosuppress theintensity oftheinfection (Atkinson andvanRiper1991).Inourstudypopulation, thevectorisrelativelyabundant andtherateofparasite transmission ishigh(Soletal.2000).Thismeansthat almostallindividuals areinfectedasjuvenilesandare continuouslyre-infectedthroughouttheirlife(Soletal.
2000).Interestingly, whileadultsaresubjecttoacontin- uousentranceofnewparasites,onlyjuvenilessufferhigh parasiteintensities.Thissuggeststhatonlyinitialinfec- tionsarecharacterized byhighintensitiesofH.columbae. Thus,thecommonparasitecycleshownbyHaemopro- teusparasiteswithahighinitialintensity andarapid declineinagivenhostseemstobeconsequenceofthe actionoftheimmune systemofthehost,ratherthanan adaptiveresponseoftheparasitewithinthehost.Because thefirstinfectiontendstooccur earlyinthelifeof pigeons, mostadultsmusthavealreadyacquired some degreeofimmunityagainsttheparasite whenwere examinedforparasites.
Wethereforeconcludethatthereisselectionagainst highlyparasitizedjuveniles, butthiscanonlypartly explainthehigherparasite intensity ofjuveniles com- pared toadultpigeons.Thisdifferenceislikelytobebest explainedbythefactthatjuvenileshavenotyetacquired acompleteimmuneresponseagainsttheparasite.The highparasitemiainjuvenilepigeons maythusbemostly viewedasatransitory phasethatmaybecrucialforthe survivorshipofindividuals.
Acknowledgements WethankD.M.Santos,M.Bosch,J.Garcia andD.Venturafortheirassistance inthefield.Thepaperwas significantly improvedwiththevaluablecommentsofD.Ryan,D. Reale,J.L.Tella,S.M.Readerandananonymous referee.We speciallythankJ.D.RodrIguez-Teijeiroforhissupportandlogistic assistanceduringthestudy,J.Champeny, L.l.ColomandF.Costa forthefacilitiesgiventoworkwithintheinstallations ofthe “ZoolôgicdeBarcelona”andC.Pujol, J.D.RodrIguez-Teijeiroand L.Lefebvrefortheirconstantsupport. Thisworkwaspartially supported byaQuébecMinistry ofEducationPostdoctoral FellowshiptoD.S.
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