Contents xi 1IntroductiontotheEcologyEpidemiologyandEvolutionofParasitisminDaphnia 1 11Foreword 1 12SettingtheStage ID: 521160
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Contents Acknowledgments xi 1IntroductiontotheEcology,Epidemiology,andEvolutionofParasitisminDaphnia 1 1.1Foreword ............................................... 1 1.2SettingtheStage ........................................... 1 1.3DeningParasites .......................................... 2 1.4HostParasiteInteractions ..................................... 2 1.5OutlineofThisBook ........................................ 3 1.6UpdatesandCorrections ...................................... 4 2IntroductiontoDaphniaBiology 5 2.1Introduction ............................................. 5 2.2Physiology,Metabolism,andImmunity ............................. 7 2.3LifeCycleandDevelopment .................................... 10 2.4Habitat ................................................ 14 2.5BehavioralEcology ......................................... 15 2.6EvolutionaryGenetics ....................................... 17 2.7PopulationDynamics ........................................ 18 3SomeParasitesofDaphnia 19 3.1Introduction ............................................. 19 3.2Bacteria ................................................ 19 3.2.1PasteuriaramosaMetchniko1888 ............................ 21 3.2.2SpirobacilluscienkowskiiMetchniko1889 ........................ 22 3.2.3WhiteFatCellDisease ................................... 23 3.3Fungi ................................................. 24 3.3.1Metschnikowiabicuspidata(Metschnikov)Kamenski .................. 24 3.4Microsporidia ............................................ 25 3.4.1FlabelliformamagnivoraLarssonetal.1998 ........................ 26 3.4.2OctosporeabayeriJirovec1936 ............................... 26 3.4.3Glugoidesintestinalis( Chatton1907 )Larssonetal.1996 ................ 27 3.4.4OrdosporacolligataLarssonetal.1997 .......................... 29 3.5UnknownClassication ...................................... 30 3.5.1CaulleryamesniliChatton1907 ............................... 30 xiiAcknowledgments onit.Sincethen,mylabhasdevelopedculturingmethodsformorethan10speciesofparasites.ThisworkwiththeDaphniaparasiteshasab-sorbedmyattentionsincethen,andtogetherwithmyresearchgroup,IhavespentmanyexcitinghoursinthelaboratoryandintheeldndingoutmoreaboutDaphniaparasites,andaboutparasitesingeneral.TheDaphnia microparasite systemhasprovedtobeapowerfulmodelformanyquestionsinbasic epidemiology ,ecology,and evolution .Theupcominggenomedatawillextendthisintothe NarrowRoadsofGeneLand (thetitleofBillHamilton'ssecondbookwithmanypartsontheevolutionofhostparasiteinteractions,2001)andwillhopefullyopenupapluralisticapproachtounderstandinghostparasite coevolution .ThisbookwouldnothavebeenpossiblewithoutthecollaborationofthemarvelouspeopleworkingwithmeinOxford,Silwood,Basel,andFribourg,andalsocollaboratorsfromaroundtheworldwhosharedmyenthusiasmforhostparasitein-teractions.Iwanttothankthepeopleinandaroundmygroup(inroughlychronologicalor-der):ValentinoLee,KatrinaMangin,HeideStir-nadel,SvenKrackow,JudyWearing-Wilde(Ox-ford),DermotMcKee(SilwoodPark),ChristineZschokke-Rohringer,Hans-JochaimCarius,TomLittle,DanielFels,MarcCapaul,MyriamRiek,PatrickMucklow,PiaSalathé,KatjaPulkkinen(Basel),ChristophHaag,DominikRefardt,DitaVizoso,OlgaSakwinska(BaselandFribourg),Lu-siaSygnarski,SandraLass,MarcZbinden,KnutHelgeJensen,RaaelAye,FlorianAltermatt,HollyGanz(FribourgandBasel),andThomasZum-brunn(Basel).SpecialthankstoJürgenHottinger,whobecameovertheyearsnotonlyaclosefriendbutalsotheirreplaceablecenterofthegroup.Nu-merouscollaborators,manyofwhomaretheoreti-cians,helpedopenmyeyeswhenIwasblindedbythebeautyofDaphniasymbionts:SebastianBonhoeer,MarcLipsitch,MartinNowak,Wolf-gangWeisser,RichardLenski,BillHamilton,PaulRainey,MitjaScholz,MartinEmbley,JanneBengts-son,LizCanning,SteveStearns,IlmariPajunen,RolandRegoes,RonnyLarsson,KerstinBittner,EllenDecaestecker,andPaulSchmid-Hempel.Flo-rianAltermatt,HollyGanz,SandraLass,DominikRefardt,MarcZbindenandThomasZumbrunnreadmostofthebookinearlierdraftsandhelpedmetopolishstyleandcontent.DitaVizosopro-ducedseveralgurestoillustrateimportantas-pectsoflifecyclesandtransmission.DitaVizosoandFridaBen-Amiarethankedforcontributingphotographs.IthankmysonGlebforhelpwithproducingsomeofthegures.SuzanneZweizigimprovedthestyleandreadabilityofthelanguagethroughoutthebook.RitaGunasekerahelpedmewiththeformattingofthevariousles.JoMcEn-tyreandLauraDeanwereofgreathelpinallas-pectsofpublishingthisbook.Thankstotheirwork,thebookcanbemadeavailabletoawideaudienceviatheInternet.Finally,Iwanttothankmyfriendsandfamilyfortheirsupportandtheencourage-menttowritethisbook.November2005DieterEbert 2Ecology,Epidemiology,andEvolutionofParasitisminDaphnia researchhasaddressedanumberofevolutionaryquestions,resultinginawell-roundedpictureoftheevolutionaryecologyofthegenus.Foralongtime,researchfocusedon predators asthemainenemiesofDaphniaintheirnatu-ral habitat .Predatorysh,phantommidgelarvae,andwaterboatmenwereamongthekeyculpritsandreceivedalotofattention,inparticularafter predator-induceddefenses weredescribed.ThisinterestinpredatorsexistedinsharpcontrasttothelackofattentionpaidtoanotherclassofDaphnia'snaturalenemies, parasites and epibionts .DespitenumeroustaxonomicstudiesontheepibiontsandparasitesofDaphnia,therewaslessthanahand-fulofecologicalstudiesonthemupuntilabout15yearsago.Thegrowingawarenessthatparasitesareubiquitousandmayplayanimportantroleinmostnaturalecosystemshaschangedthis,astheincreasingnumberofpublicationsaboutDaphniaparasitesandepibiontsconrms( Figure1.1 ). 1.3 DeningParasitesAlthough parasites havetraditionallybeendenedbyacombinationofconceptualandtaxonomicfea-tures,Iuseanentirelyconceptualdenitionhere.Iconsideraparasitetobeanysmallorganism(in-cludingviruses)thatlivesincloseassociationwithahostorganismandforwhichitseemsreasonabletoassumethatthehostcarriessomecost.Thesecostsmaybeclearlyvisible,intheformofreducedfecundityorsurvival,butmayinsomecasesbesubtle.Forexample,reducedsexualattractiveness(leadingtoreducedmatingsuccess)orreducedcompetitiveabilitymaynotbeveryvisible.Ide-voteanentirechaptertodiscussingthe tness costscausedbyparasites.Thisconceptualdenitionofaparasiteincludesmembersofvarioustaxa,suchasviruses,bacteria,fungi,andprotozoa,butalsoincludesfunctionalcategories(nottaxonomicallydened),suchas pathogens and helminths .Incon-trasttotypical predators ,parasitesdonotalwayskilltheirhosts,andiftheydo,itmaytakeaconsid-erableamountoftime,duringwhichtheparasitemaybetransmittedtootherhosts,andthehostremainsinthecommunitycompetingwithotherorganismsforspace,food,andmatingpartners.Intheliteratureon Cladocera andmorespeci-callyonDaphnia,parasitesareoftendistinguishedfromepibionts.Whereastheformerareusually endoparasites ,i.e.,locatedwithinthebodyofthehost,thelatterarelocatedonthebodysurfaceandmaythereforebelabeledasectoparasites.Inthemainpartofthisbook,Iconcentrateonendopara-sitesandexcludeepibionts.However,thisisnottosaythat epibionts arenotparasitesorarenotim-portant.Infact,Ibelievethatmostepibiontsfulllthedenitionofparasitesusedhere,becausetheyareoftencloselyassociatedwiththeirhostsandcauseharmtotheirhosts.Thisharmmaynotbedi-rectlyvisible,buttherearecertainlyincreasedcostsforswimming,whichmayhaveconsequencesforother tness components,suchasfecundity,sur-vival,competition,andmatending( Threlkeldetal.1993 ).Ithasalsobeensuggestedthatepibion-ticlterfeederscompetewiththeirhostsforfood( KankaalaandEloranta1987 ).Ontheotherhand,ithasbeensuggestedthatundercertaincondi-tions,highloadsofalgalepibiontsmayprovideadditionalfoodforthehostandthusresultinanetbenet( Barea-Arcoetal.2001 ).However,thisformofafoodsupplementationiscertainlynotthetypicaleectofepibionts.Idonotincludeepibiontsinthisbook,becauseIfeelthatthereislessneedtodiscussthe epidemiol-ogy ofthisfunctionalgroupthanforendoparasites.However,IwillrefertothemwheneveritmightfurtherourunderstandingofDaphniaparasitein-teractions. 1.4 HostParasiteInteractions Parasites maybedirectlyorindirectlyinvolvedintheecologyand evolution ofabroadrangeofphenomena:host populationdynamics andextinc-tions,maintenanceofgeneticdiversity,sexual se-lection ,evolutionofgeneticsystems,andevolutionofsexualrecombination,tonamejustafew.Cer-tainly,parasitespossessfeaturesthatmakethemveryattractiveasexplanatoryfactorsintheevolu-tionandecologyoftheirhosts.Thesefeaturesin-cludetheirhigh abundance innearlyeveryecosys-tem,theirtypicallynarrowhostrange(comparedwithtypical predators ),theiradverseeectsontheirhosts(e.g.,reducedfecundityandsurvival),and densitydependence during horizontaltrans-mission ( Anderson1979, 1993 ; AndersonandMay1978 ; MayandAnderson1979 ; Price1980 ). 4Ecology,Epidemiology,andEvolutionofParasitisminDaphnia Chapters8 and 9 addressaspectsofparasitismatthe population level.Acentralchapterofthisbookis"Epidemiology."Itstwopartsdealwith transmis-sion processesandwiththeactualepidemiologyofDaphniaparasites.Chapter9introducestheimpor-tantquestionofwhetherparasitesregulatetheirhostpopulationsorevendrivethemtoextinction. Chapter10 introducesanumberofexperimentsthatonemaydowithDaphniaanditsparasiteswithintheframeworkofastudentcourseorforresearchpurposes.Thesesimpleexperimentsmaybeusedtoillustrateprinciplesofhostparasitein-teractions.Experimentsaresuggestedattheindi-viduallevelaswellasatthepopulationlevel.From Chapter4 onward,Iendeachchapterbyposingopenquestionsandhighlightingmajorgapsinourknowledge.A Glossary providesdenitionsoftermsfromDaphniabiologyandparasitologyusedthroughoutthebook. 1.6 UpdatesandCorrectionsIwillmaintainaWebsiteonmyhomeinstitu-tion'sservertoreportupdatesandcorrecterrors.Ifyounderrors,disagreewithcertainstatements,orndthatIneglectedimportantinformation,Iwouldbehappytoreadyourcomments.Pleasesendmeanemail: dieter.ebert@unibas.ch 6IntroductiontoDaphniaBiology Figure2.1ThefunctionalanatomyofDaphnia.Thisdrawingshowsanadultfemalewithparthenogeneticembryosinher broodchamber .Forbetterillustration,the carapace isshownastransparent.Theanimalmeasuresabout2mmfromthetopofitsheadtothebaseofitstailspine.ModiedafterMatthes( rstpublishedonpage154inKükenthalandMatthes1944 )(withpermissionfromKästner:LehrbuchderspeziellenZoologie,Band1,Teil4,1993c ElsevierGmbH,SpektrumAkademischerVerlag,Heidelberg).ComparethisgurewithFigure2.2. 2.2Physiology,Metabolism,andImmunity9 Figure2.5Daphnialongispina.Adultfemalewiththreeeggsinthebroodchamber.ThisfemalewasisolatedfromarockpoolinsouthernFinlandclosetoTvärminne. Daphniahavetheextracellularrespiratoryproteinhemoglobin(Hb),amulti-subunit,multi-domainmacromolecule.ThereareatleastfourHbgenes.DaphniatendtodevelopmoreHbtoincreaseoxy-genuptakefromthewater.Inresponsetoenvi-ronmentalchanges(oxygenconcentration,temper-ature),theHbconcentrationvariesuptoabout20-fold.Oxy-hemoglobin,theformthatisloadedwithoxygen,isredandgivesthetransparentan-imalsareddishappearance( Figure2.7 ).Becausecertainparasitesalsocausethehemolymphtobe-comered,onecannoteasilydeterminethecauseoftheredcolorfromsightalone.However,lowoxygenusuallyaectsanentire population ,color-ingallanimalsreddish,whereasparasitesusuallyinfectonlyaportionofthepopulation.Daphniahavetheusualosmoregulatoryprob-lemsoffreshwateranimals,i.e.,toomuchwaterandtoofewsolutes.Theyareabletoabsorbionswithchloride-absorbingglands.The shellgland ( maxillarygland ; Figure2.1 )mayhavearoleinexcretionand/orosmoregulation. Figure2.6GutofDaphniamagna.Gutdissectedfromafemale.Ontheleft,thepairedintestinalcecacanbeseen.Thegutendsattherightside.Theesophaguscannotbeseeninthispreparation.Thedarkmaterialispartiallydigestedgutcontent. Figure2.7TwoDaphniamagnawithcontrastinghemolymphcolorduetohaemoglobin(Hb).ThesetwoadultfemalesweretakenfromtwoadjacentrockpoolpopulationsinsouthernFinlandatatimewhenoneofthepoolswaslowinoxygen(becauseofoverfertilizationfrombirddroppings).Intheleftfemale,lowoxygentrig-geredtheproductionofHb,whichgivesthehemolymphareddishcolor.Thefemaleontherightwastakenfromapoolwithclearwaterandapparentlynormaloxygenlevels.Thesizedierenceoftheanimalsisattributabletothearbitrarychoiceofspecimens.Bothfemalesarecarryingembryosintheirbroodchambers. Thenervoussystemischaracterizedbythecere-bralganglion,whichislocatedclosetothegutandneartheeye.JuvenileandadultDaphniahaveonelargecompoundeye,whereasembryosshowtwobrownisheyespotsthatfuseduringthelastpartofthedevelopment.Thecompoundeyehelpstoori-enttheanimalwhileswimming.Asmallstructure 10IntroductiontoDaphniaBiology calledanaupliareyeislocatedbetweenthemouthandthecompoundeyeontopofthecerebralgan-glion.Manyinvertebrates,including crustaceans ,haveawell-developedinnateimmunesystemthatin-cludesmelanizationbyactivationoftheprophe-noloxidase(proPO)activatingsystem,aclottingprocess,phagocytosis,encapsulationofforeignmaterial,antimicrobialaction,andcellagglutina-tion( Söderhall1999 ).Ofthesemechanisms,onlythe proPOsystem ( MucklowandEbert2003 )andphagocytosis( Metchniko1884 )havebeeniden-tiedinDaphnia,althoughthereisnoreasontodoubtthattheothermechanismsworkaswell.TheproPOsystemisnotonlyadefensesystemagainstparasitesbutisalsoinvolvedinwoundhealingofthecuticle( Figure2.8 ).Theenzymeinvolvedin melanin formation,PO,hasbeendetectedinthebloodofmanyarthropods,includingD.magna.Melaninisabrownpigmentthatisalsousedfor carapace pigmentationinsomeDaphnia,particu-larlyDaphniainthehighArctic,wherethedarkpigmentprotectsthemfromuninterruptedsolarradiation(repairofUVdamageisonlypossibleinthedark).Acquiredimmunityisthoughttobeabsentininvertebrates;however, transmission ofstrain-specicimmunityfrommotherstoospringhasrecentlybeensuggestedforD.magna( Littleetal.2003 ). 2.3 LifeCycleandDevelopmentThelifecycleofDaphniaduringthegrowthseasonischaracterizedbyitsasexualmodeofreproduc-tion( apomixis )( Figure2.9 ).Afemaleproducesaclutchofparthenogenetic(amictic)eggsaftereveryadultmolt(iffeedingconditionspermit). Figures2.3 to 2.5 showfemaleswithparthenogeneticeggs.Theeggsareplacedinthe broodchamber ,whichislocateddorsallybeneaththe carapace andwhichisclosedbythe abdominalprocesses ( Figures2.1 and 2.10 ).Developmentofeggsisdirect(imme-diate).At20oC,theembryoshatchfromtheeggsafterabout1daybutremaininthebroodchamberforfurtherdevelopment( Figure2.11 ).Afterabout3daysinthebroodchamber,theyoungDaphniaarereleasedbythemotherthroughventralexionofthepost-abdomen.ThenewbornlookmoreorlessliketheadultDaphnia,exceptthatthebrood Figure2.8WoundhealinginDaphniamagna.Aninjuryinthecarapacehealswithinafewhourstodays.Woundhealinginvolvesamelanizationreactionthatstainsthewounddark.Hereaneedlewasusedtoinjurethecara-pace.Thesquaredpatterninthebackgroundshowstheepidermalcellstructure. chamberisnotyetdeveloped( Figure2.12 ).Inmostspecies,ajuvenileDaphniapassesthroughfourtosixjuvenile instars beforeitbecomes primipare ,i.e.,produceseggsforthersttime.Theageatwhichthersteggsaredepositedintothebroodchamberisaround5-10daysat20oC,butthismaytakelongerunderpoorfeedingconditions.Anadultfemalemayproduceaclutchofeggsev-ery3to4daysuntilherdeath.Inthelaboratory,femalesmayliveformorethan2months,withahigheragebeingreachedunderpoorerfeedingconditions.Clutchsizesvaryamongspecies,from1to2eggsinsmallspeciessuchasD.cucullata( Figure2.4 )tomorethan100inlargespeciessuchasD.magna( Figure2.3 ).AlthoughinatypicalgrowthseasonDaphniaproducediploid(2N)eggsthatdevelopdirectlyandwithoutarestingphase,adierenttypeofeggisproducedforresting( Figure2.9 ).These rest-ingeggs areencapsulatedinaprotective,saddle-likestructurecalledan ephippium ( Figures2.13 and 2.14 ),whichisusuallystronglymelanizedandcontains2largeeggs,1fromeachovary.Itisnotuncommon,however,tond ephippia withonly1egg,ornoneatall.Theephippiumiscastoatthenextmolt.Inmostcases,theseeggsareproducedsexually,butobligateparthenogeneticDaphnia,whicharetypicallyfoundinthenorth- 12IntroductiontoDaphniaBiology Figure2.10EgglayingbyDaphniamagna.Thisseriesofpictures,takenwithina15-minutetimespan,showstheprocessofplacingeggsintothebroodchamber.Theeggsareinitiallysausageshapedbutquicklyresumeanearlysphericalshape.Theovariesshrinkduringtheprocessofegglaying.Inthetoppictures,theyareclearlyvisibleasadark,thicklineparalleltotheintestine. Chapter3SomeParasitesofDaphnia Inthischapter,IgiveabriefintroductiontosomeendoparasitespeciesofDaphnia.Threebacteria,onefungus,fourmicrosporidia,andoneparasiteofunknowntaxonomicclassicationaredescribedwithaccompanyingphotographs.Ifocusonthoseparasitesthatarementionedfrequentlyinthisbook. 3.1 IntroductionThisbookismainlyconcernedwiththeecology, epidemiology ,and evolution of parasites .Itdoesnotgointodetailaboutthenaturalhistoryandtax-onomyofparasitespecies.Asecondbookwilldealwiththeseaspects.However,becauseitisusefultohavesomebasicknowledgeabouttheparasitesthatarefrequentlymentionedinthisbook,Igivehereabriefintroductiontothem.Moredetailswillbefoundintheupcomingbook,whichincludeschaptersonallknownDaphniaparasites. Table3.1 givesanoverviewaboutallparasitesofDaphniamentionedinthisbook.TheparasitesdescribedinthischapterarebynomeansmoreimportantthananyotherparasitesofDaphnia,buttheyarethosethathappentobethemoststudied,partlybecausetheyhavebeenfoundtobeatleastlocallyabundant.ParasitesofD.magnaarepredominantbecauseparasitesofthiswell-investigatedandlargestEuropeanDaph-niaspeciesarebestknown.MostofmyownworkonparasiteshasusedD.magnaasahost.Also,par-asitesforwhoseentirelifecyclecanbecompletedunderlaboratoryconditionsweremoreintensivelystudiedthanthenumerousspeciesthatwedonotcurrentlyknowhowtopropagate.Despitethisbiasinrepresentation,however,thespeciesintroducedinthischaptergiveagoodimpressionofthediver-sityofparasitesknowntoinfectthegenusDaphnia.Wehaveagoodknowledgeofthetaxonomicpo-sitionofonlyafewendoparasitesofDaphnia.Forsomespecies,wedonotevenknowtheapprox-imateposition,e.g.,Caulleryamesnili;therefore,Icannotuseastricttaxon-basedlistingofthepara-sitespecies.InsteadIprovideinformationonotheraspectsoftheirbiology,whichallowsustocatego-rizethemintogroupssothattheycanbeeasilyfound.WhenDNAsequencedataareavailableformorespecies,taxonomicpositionwillbeeasiertodene( Ebertetal.1996 ; Refardtetal.2002 ). 3.2 BacteriaSixspeciesofbacteriahavebeendescribedparasitizingDaphnia.Fouroftheminfectthehemolymph,whereastwoareintracellularinfec-tionsofthefatcellsandtheeggs,respectively.Bacterialinfectionsaregenerallyharmfultotheirhosts,drasticallyreducinghostreproductivesuc-cess.BacteriahavebeenobservedtoinfectDaphniaei-therasendoparasitesor epibionts .However,onlythetaxonomyforPasteuriaramosahasbeenworkedoutandpublishedthusfar( Ebertetal.1996 ).The 20SomeParasitesofDaphnia Parasite(Taxon)RecordedhostsInfectedtissueorsiteofinfectionTransmission Pasteuriaramosa(Bacteria)D.magna,D.pulex,D.longispina,otherCladoceraBlood,extracellularHorizontal,fromdeadhostWhiteFatCellDisease(Bacteria)D.magna,D.pulex,D.longispinaFatbody,intracellularHorizontal,fromdeadhostSpirobacilluscienkowskii(Bacteria)ManyDaphniaspeciesBlood,extracellularHorizontal,fromdeadhostAphanomycesdaphniae(Fungi)D.hyalina,D.pulexBodycavity,extracellularHorizontal,fromdeadhostMetschnikowiabicuspidata(Fungi)D.magna,D.pulex,D.longispinaBodycavity,extracellularHorizontal,fromdeadhostFlabelliformamagnivora(Microsporidia)D.magnaFatbody,ovaries,intracellularVerticalOctosporeabayeri(Microsporidia)D.magnaFatbody,ovaries,intracellularVerticalandhorizontal,fromdeadhostGurleyavavrai(Microsporidia)D.pulex,D.longispinaCarapace,intracellular?Glugoidesintestinalis(formerlyPleistophorai.)(Microsporidia)D.magna,D.pulexGutwall,intracellularHorizontal,fromlivinghostOrdosporacolligata(Microsporidia)D.magnaGutwall,intracellularHorizontal,fromlivinghostLarssoniaobtusa(=L.daphniae)(Microsporidia)D.magna,D.pulex,D.longispinaFatbody,intracellular?Pansporellaperplexa(Amoeba)D.magna,D.pulex,D.longispina,D.hyalina,D.obtusaGutwall,extracellularHorizontal,fromlivinghostCaulleryamesnili(unknown)D.pulex,D.longispina,D.magna,D.galeata,D.obtusa,DaphniahybridsGutwall,intracellularHorizontal,fromlivinghostEchinuriauncinata(Nematoda)D.pulex,D.magna,D.obtusa,otherCladoceraBodycavity,extracellularHorizontal,tosecondhostCysticercusmirabilis(Cestoda)D.magnaBodycavity,extracellularHorizontal,tosecondhost(?) Table3.1Listofparasitesmentionedinthisbook. 3.2Bacteria21 taxonomyofSpirobacilluscienkowskiiisinprepa-ration(M.Duy,personalcommunication).Theotherspeciesareeitherdescribedbytheirtypicalpathologyorarecollectivelyplacedintoagroupwithroughlysimilarcharacteristics.Mostspeciesdonotyethaveascienticname.Therecordedbacteriainfecteitherthehemolymphofthehostorareintracellular parasites .InfectionsofthehemolymphofDaph-niamaketheentirehostappearmilkish-white,brownish,pinkish,oryellowish.TheseinfectionscanbeseenthroughoutthebodyandhavebeenfoundinmanyDaphniaspecies.HereIintroducetwoofthesespecies:P.ramosaandS.cienkowskii.Incontrast,intracellularparasiticbacteriainfecteithercellsofspecichosttissuesoreggsofthehostwhiletheyareinthebroodpouch.HereIgiveashortdescriptionofalittle-knownbacteriumknownbythenameofWhiteFatCellDisease.Itscategorizationintotwogroupsofparasiticbacteriaisnotataxonomicclassicationbutafunctionalgrouping. 3.2.1 PasteuriaramosaMetchniko1888P.ramosaisaGram-positivebacteriumbelongingtoadistinctcladewithinthefamilyoftheAlicy-clobacillaceae( Ebertetal.1996 ; Andersonetal.1999 ; Prestonetal.2003 ).Otherendospore-formingbac-teria,suchasBacillusandClostridium,arecloselyrelatedtoit.P.ramosaismostfrequentlyfoundtoinfectD.magna,butitalsoinfectsD.pulexandD.longispina.Itshowsahighdegreeofclone specicity withinspecies( Cariusetal.2001 ).Afewother Cladocera havebeendescribedashosts,butitisnotclearwhetherthe parasite wasindeedP.ramosa.P.ramosawasrecordedinEuropeandNorthAmerica.P.ramosainfectsthehemolymphandisex-tracellular( Figure3.1 )( Metchniko1888 ).In-fectedhostsstopreproduction,growlarge,andthebodybecomesdarkishandnontransparentinlight.Squashpreparationsreveallargenumbersoflarge,nearlysphericalspores(about5-mdi-ameter)orgrapeseed-shapedpre-sporesinthehemolymph( Figure3.2 ).Thisbacteriumcauseschronicinfections.In-fectedhostsaretotallycastrated,i.e.,theystopre-producingabout5to15daysafterinfectiontakes Figure3.1D.magnawith(right)andwithout(left)P.ramosainfection.Theparasitecanbeseenasadarkcloudymassllingtheentirebody.Thebroodpouchoftheinfectedfemaleisempty,whereasthehealthyfemalecarriesaclutchofeggs.Thisphotographwastakenwiththelightshiningfrombelow.Theinfectedhostislargerthanthehealthyfemale,whichistypicalforP.ramosainfections. Figure3.2DevelopmentalstagesofP.ramosa.Inthenalstageofsporedevelopment,thehostislledwiththeroundsporesthatserveastransmissionstages.Thesesporesarelong-lasting.Inhostsintheterminalstageofaninfection,oneoftenobservesafewcauliowerstages,suggestingthatsomesporesgerminatetostartanothergrowthcycle.ThecauliowerstageistherststageofP.ramosathatisclearlyvisibleafteraninfection. 3.2Bacteria23 Figure3.4D.magnawithWFCD.Thesameanimalisshownunderthreedierentlightconditions,withlightcomingfromthetop(left),fromthebottom(right),andfromthetopandbottom(center).Notethattheinfectedfatcellsbecomelessvisiblewithlightshiningthroughtheanimal. Figure3.5WFCDinD.longispina.D.longispinafromanaturalrockpoolpopulationinsouthernFinland. Metchniko(1889) describedthelengthofthelifecycleofthebacteriumasabout5days.Thelifecycleincludesseveralmorphologicalforms,in-cludingovals,rods,spirillae,laments,androundspores.Hostscollectedfromnatural populations intheterminalstage(redcolorstage)surviveonly1-3daysunderlaboratoryconditionsandusuallycarrynoeggs( Duyetal.2005 ). Transmission isstrictlyhorizontal. Prevalence canreach10to15%forshorttimeperiods( Duyetal.2005 ). 3.2.3 WhiteFatCellDiseaseWFCDiscausedbyasmallcoccoid pathogen ,mostlikelyabacterium.Infectionswiththisbac-teriumhavebeenrecordedinD.magna,D.pulex,andD.longispina.ClonesofD.magnahavebeenfoundtodierintheirsusceptibilitytoWFCD( De-caesteckeretal.2003 ).ThediseasehasbeenfoundonlyinWesternandNorthernEuropethusfar.ThecausativeagentofWFCDishardlyvisiblewithlightmicroscopy.Infectedhostshavebrightwhitefatcellswithaslightgreenishshinethat 24SomeParasitesofDaphnia isvisibleonlyinreectedlight( Figures3.4 and 3.5 ).Theinfectiondoesnotshowthefuzzyspreadthroughthebodycavitythatisseenwithother parasites infectingthefatcellsandovaries(e.g.,Octosporeabayeri).Usually,theinfectedtissueisclearlydistinguishablefromothertissues.WFCDisratherharmful.Itusuallykillsthehostwithin2weeks,oftenmuchmorequickly.Lessvir-ulentinfectionshavebeenobservedaswell.Fe-cunditydropsstronglywithdiseaseprogression,andinfectedhostshavestuntedgrowth. Transmission isstrictlyhorizontal.Transmissionstagesarereleasedfromdeadhosts.Thereseemstobenotransmissionfromlivinginfectedhostsandno verticaltransmission . 3.3 FungiSeveralspeciesoffungihavebeenobservedpara-sitizingDaphniaandother Cladocera .Taxonom-ically,theyarepoorlyunderstood.Theyvarystronglyintheirappearanceandtheireectsontheirhosts.Fungalinfectionsaregenerallyharm-fultotheirhosts,drasticallyreducinghostrepro-ductivesuccessandsurvival.Somespeciesmaynotbeobligate parasites ,openingthepossibilitytoculturethemonanarti-cialmedium( Couch1935 ; Prowse1954 ; Whisler1960 ).Indeed,ithasbeenreportedthatthe en-doparasites Aphanomycesdaphniae,Metschnikowiabicuspidata,andthe epibiontic Amoebidiumpara-siticumcanbeculturedinvitro,whichopensuptremendouspossibilitiesforexperiments.Tomyknowledge,nootherparasitegroupcancurrentlybeculturedoutsideDaphnia.Host specicity seemstoberatherlowinfungiinfecting crustaceans .Frommyexperience,theparasiticfungiofDaphniaarethemostdiculttoworkwithandtoidentify.Ontheotherhand,par-asiticfungiseemtobethemostdevastatingdis-easesofDaphnia,oftenkillingthehostsquicklyordestroyingthebroods. 3.3.1 Metschnikowiabicuspidata(Metschnikov)KamenskiThisyeastisbetterknownbythenamesMonosporabicuspidataandMetschnikowiellabicuspidata.IthasbeenrecordedfromD.magna,D.pulex,andD. Figure3.6D.magnawithaninfectionofM.bicus-pidata.Thisfemalewasinfectedwithasuspensionofspores.Thehostisintheterminalstageofinfection.Theneedle-likeascosporesofM.bicuspidatalltheentirebodycavityofthehost. longispinaaswellasfromanumberofother crus-taceans .Itappears,however,thatunderthisnameacomplexofsimilarspecieshasbeendescribed.M.bicuspidataisanendoparasiticAscomycete(Endomycetales).Itproducesneedle-likeas-cospores,whichpenetratethegutwallsofitshostsandgerminateinthehemolymph( Green1974 ).Needle-like spores areusuallyupto45mlong,althoughtheycanbeupto90mlong( Green1974 ; CodreanuandCodreanu-Balcescu1981 ),andarevisiblethroughthetransparentbodyofthehosts( Figure3.6 ).Thefungusgrowsinsidethehostun-tiltheentirecavityislledwiththeneedle-likespores( Figure3.7 ).Sporesarefoundineverypartofthebodycavity,evenintheantennae.Hostsin 4.2OverviewofEpidemiologicalFieldStudies33 icallyfoundonlybetweenAprilandDecember.Theabundancepatternsofotherparasitespecieswerenottiedtoseasons,however,leadingGreentoconcludethatthedistributionofcertainpara-sitesisinuencedbytheseverityofwinterandspringtemperatures.Hedidnotdiscusstheroleofhostdensityasanexplanatoryfactor.Hedidob-serve,however,thatseveralparasitespecieshavenegativeeectsonhostsurvivalandfecundity. Brambilla(1983) studiedthemicrosporidiumThelohaniasp.inaD.pulex population overa3-yearperiodinasmall,apparentlyshlessvernalpoolinMichigan,USA.Henotedthatparasiteprevalencevariedstrongly,from20%topeaksofnearly100%ofadultfemales.ParasiteswerepresentinMayandJuneinall3yearsandwererstseenwhen-everthehostdensityroseabove2-3animals/liter.Oneyear,however,theparasitesdisappearedinmid-summerdespitehighhostdensities,suggest-ingthathighdensityalonecannotexplainpara-sitespread.Infectionoffemaleswith ephippia wasneverobserved.Parasitizedanimalswereusuallylargerthanuninfectedhostsbuthadlowerfecun-dityandsurvival. YanandLarsson(1988) followedthedynamicsoftwoundescribedandverysimilarmicrosporid-ianparasitesofHolopediumgibberumina32-haCanadianshieldlake(maximumdepth,16m)fromApriltoOctober1985.Thelakehasseveralplank-tivorousshspecies.ParasitesappearedonlyinJulyandreachedaprevalenceof4%,whichtheymaintainedfortherestofthesummer.Thepara-sitesappearedwhenhostdensitywashighbutdidnotdeclinewhenhostdensitydecreased.Theau-thorsarguedthatelevatedsummertemperatureswerenotthecauseoftheseasonaloccurrenceoftheparasites.Theyfurtherrejectedtheideathatchangesinhost resistance inuencedtheabun-dancepatternoftheparasites.Theysuggest,in-stead,thattheinterplaybetweenhostandpar-asite populationdynamics mayhavecausedtheseasonalchangesinprevalenceandthatpredationbyplanktivorousshmayhavefurtherinuencedthesechanges,becauseinfectedhostsmaybe,theyspeculate,thepreferredtargetofvisuallyhuntingsh.Infectedhostshadalowerfecunditythanhealthyhostsandmayhavehadlowersurvival.Inclosing,theauthorsnotedthatinasurveyof15otherH.gibberumpopulationsinshieldlakes,3ad-ditionalpopulationswerefoundtobeparasitizedbymicrosporidians. Vidtmann(1993) studiedparasitismbythemicrosporidiumLarssoniadaphniae(latercalledLarssoniaobtusa( VidtmannandSokolova1994) )inaD.pulexpopulationinashallow,shless,eutrophicpondattheKaunasZoologicalGar-deninLithuania.Heobservedthatalthoughmi-crosporidianswerepresentonlyduringtimesofhighhostdensity,theywerenonethelessoftenab-sentduringperiodsofhighhostdensityaswell.Prevalenceamongadultfemalespeakedinsum-meratamaximumof52%,buttheaveragepreva-lence(allageclasses)withinseasonsandacrossyearswasmuchlower:0.63%inspring,3.2%insummer,and2.4%infall.Prevalencewasgenerallylowerinjuvenilesandinmales.Over3years,themicrosporidianswereseenonlyfromlateMaytoearlyOctober.Becausethisperiodcloselyoverlapswiththepresenceofthehost,thisapparentsea-sonalitymayberelatedtotheseasonaloccurrenceofthehost.Nevertheless, Vidtmann(1993) spec-ulatedthatthedelayedonsetofL.daphniae epi-demics inMaywasaconsequenceoflowspringtemperatures. SchwartzandCameron(1993) studiedanunde-scribedtrematodeparasiteofD.obtusafromsevenseasonal,shlesspondsinsoutheasternTexas,USAover4years.Theyrecordedstrongwithin-season,between-year,andbetween-ponddynam-icsinthepresenceoftheparasite.Despiterecord-ingmaximum prevalences upto79%,theymoretypicallyfoundprevalencestobearoundafewpercents.Largeanimalsweremoreofteninfectedthansmallfemales.Hostfecunditywasonlyre-ducedininfectionswiththreeormoreparasitesperhost. Stirnadel(1994) and StirnadelandEbert(1997) studiedparasitesofD.magna,D.pulex,andD.longispinainthreeshlesspondsnearOxford,UKoveraperiodof1year(about10-12Daph-niagenerations,65samplesintotal).Sheassessedhostdensityandfecunditytogetherwithparasiteprevalence, richness ,diversity,andhost specicity .Overallparasiteprevalence(allspeciescombined)washighthroughouttheyear,averaging84.7%inadultD.magna,53.6%inD.pulex,and38.6%inD.longispina.Overall,31%ofD.magna,17%ofD.pulex,and11%ofD.longispnawereinfectedwithmorethanoneparasitespecies.Inallthree 4.3GeneralizationsaboutParasitisminNaturalPopulations35 4.2.2 ComparativeAnalyses Table4.2 givesonoverviewoverallcomparativeeldstudiesonCladoceranparasites. Green(1957) studied parasites and epibionts of Cladocera in67rockpoolpopulationsintheSkerryislandsofsouthernFinland.Thesepoolsweresmall(3-4minlengthandupto0.4mdeep)andshless. Parasiterichness declinedfromD.magnatoD.pulextoD.longispina,suggestingthatlargerDaphniaspeciesharbormoreparasites.Greenfoundthatsomeparasitespeciesloweredhostfecunditymorethanothers,andinonecase,heobservedthat ephippial femaleswereoverpar-asitized.Theauthorsuggestedthatcertainspeciesofepibiontscompetewitheachotherforspaceonthehostandthusexcludeeachotheratthepopu-lationlevel. Brunner(1996) (D.BrunerandD.Ebert,unpub-lishedobservations)investigatedsinglesamplesfrom43DaphniapopulationsinsouthernEngland,mainlywestofLondon.Waterbodiesrangedfromsmallpondsinparkstolargenaturalpondsandmedium-sizeddrinking-waterreservoirs.Mostofthesepondswereshless.Ninety-onepercentofthesepopulationsharboredatleastone endopara-sitic infection(mainlymicrosporidians).Theav-erageprevalencewasratherhigh.InthemorecommonDaphniaspecies,parasiteshadanav-erageprevalenceof43%(n=17)inD.magna,69.7%(n=17)inD.pulex,and43%(n=9)inD.longispina(allparasitespeciescombined).AmongtheD.magnapopulations,averageprevalencewas58.4%(standarderrorofthemean(SE),8.4)inpermanentponds,andonly23%(SE,6.4)ininter-mittentponds.Thisdierencewas,however,mostlikelyattributabletothesmallersizeoftheinter-mittentponds.Asseeninotherstudies( StirnadelandEbert1997 ; Decaestecker2002 ),themostcom-monparasitesofD.magnaweremicrosporidiangutparasites. BengtssonandEbert(1998) conductedasimilarsurveywithonlyonesampleperpondinarockpool metapopulation alongtheSwedisheastcoastnearUppsala.Inthesepools,24of50(48%)D.pulexpopulationsand9of25(36%)D.longispinapopu-lationsinvestigatedharboredatleastoneparasitespecies.Acrossallponds,theaverage micropara-site prevalencewas15.5%forD.pulexand9.1%forD.longispina(about30%and25%whenonlypop-ulationswithatleastoneparasitespeciesarecon-sidered).Theinfectionsinthepoolswereprimar-ilyattributabletoasingle,virulentmicrosporid-iumspecies(possiblyLarssoniaobtusa( VidtmannandSokolova1994 )),whichreducedclutchsizeby98%. Ebertetal.(2001) studiedD.magnainthesamerockpool metapopulation insouthernFinlandasdid Green(1957) (seeaboveand Figure2.18 ).Be-causetheecologyofthismetapopulationiswellknown,itwaspossibletoaddressseveralaspectsofparasitedistributionacrosspopulationsinrela-tiontovariouspoolcharacteristics.Eightendopar-asitesandeightepibiontspecieswerefoundin137rockpoolpopulations.Thenumberofendopara-sitespeciesperpopulationincreasedwiththeageoftheDaphniapopulation.Typically,newerpop-ulationsfoundedintheyearthesurveywascon-ductedhadnoorfewparasitespecies,whereasolderpopulationshadincreasinglymore.Further-more,largerockpoolswithpresumablylargerandmorepermanentDaphniapopulationsweremorelikelytoharborparasitesthansmallerpools.ThemostprevalentparasiteintheFinnishrockpoolswasthemicrosporidiumOctosporeabayeri,whichoftenoccurredinaprevalenceof100%.ThisparasiteexclusivelyinfectsD.magnaandwasfoundinnearly50%ofallpopulations,withmuchhigherpercentagesinolderpopulations.Surpris-ingly, Green(1957) foundthisparasiteinonly8.3%ofD.magnapopulations. 4.3 GeneralizationsaboutParasitisminNaturalPopulations 4.3.1 WhatCanWeLearnfromPrevalenceEstimates?Prevalenceestimatesareacommonandconve-nientmeasureof parasiteabundance .Theyallowtheinvestigatortofollowchangesinparasiteabun-danceovertimeandprovideareasonablepictureofthedegreetowhichthehost population isin-fested.Prevalenceestimateshavesomelimitationsthathavetobetakenintoaccountwhendoingpar-asitologicalresearch.First,theyareusuallyunder-estimates,becauseparasitesareonlydetectableaf-tersignsofinfectionhavedeveloped.Infections 4.3GeneralizationsaboutParasitisminNaturalPopulations37 wererelativelymoreofteninfectedthanpartheno-geneticfemales.Theassociationbetweengenderandparasitismcertainlyneedsfurtherinvestiga-tion.Theeectofparasitesonhostsurvivalhasbeentestedineldstudiesbybringingplanktonsam-plestothelaboratory,dividingtheindividualsintoinfectedanduninfectedgroups,andthenmoni-toringtheirsurvivalundercontrolledconditions.Foranumberofreasons,Iconsiderthisapproachtobeunsatisfactory.First,infectedandapparentlyuninfectedhostsmaydierinsize,age,andexpe-rience.Becauseparasitesofteninuencegrowth,itisnotpossibletocorrectforthesedierenceseasily.Second,theassessmentofinfectionstatusisoftendicult,withstrongvariationacrossinvestigatorsandamongdiseases.Forexample,certaininfec-tionsmayonlyberecognizableshortlybeforethedeathofthehost,whereasotherscanbedetectedafewdaysafterinfection.Thus,comparinginfectedanduninfectedanimalsfromeldsamplesdoesnotallowonetojudgetheeectofparasitismonhostsurvivalinameaningfulway. 4.3.4 InfectionDynamicsAllofthelongitudinalstudiesfoundthatpreva-lencevarieddynamicallyovertime,withcertain parasite speciesbeingseenonlyovershorttimein-tervals.Insomecases,thedynamicsappearcyclic,withseasonalreoccurrenceofparasites(mostlyinsummer),butforthemajorityofparasitespecies,itisunclearwhatdetermines abundance patterns.Extremecasesofparasitedynamicshavebeenob-servedinsomeofthelongerstudies,wherecer-tainparasitesdisappearedforextendedperiodsoftimeandthenreemergedwithoutanynoticeablereason( Green1974 ; Bittner2001 ).Itistotallyun-clearwhetherenvironmentalorevolutionaryfac-torsplayaroleintheseextremedynamics.Afewofthelongitudinalstudiesanalyzedthedynamicswithrespecttohostdensity.Thusfar,nostudyhasshownacleardensityeect,al-thoughdensity-dependent transmission hasbeenshowninthelaboratory( Ebert1995 ; Bittneretal.2002 ).Somestudiesobservedthatparasitesrstappearedwhenhostdensitywashigh,butincontrasttowhatwouldbeexpectedifdynamicsweredrivenby densitydependence ,parasitesdidnotdeclinewhenhostdensitydeclined( Brambilla1983 ; YanandLarsson1988 ).Thistrendhasalsobeenobservedforparasitesofplanktonicrotifers( Miracle1977 ; Ruttner-Kolisko1977 ).Severalstud-iessuggestedthathostdensityandwatertemper-aturearetosomedegreeconfounded,becausethedensityofmostplanktonorganismsishighdur-ingthewarmerperiods.Therefore,itisnotcleartowhatdegreeelevatedtemperaturesplayaroleinsummer epidemics ( Green1974 ; Brambilla1983 ).Atleastforonemicrosporidium,ithasbeensug-gestedthatlowtemperaturecanhindertransmis-sion( Ebert1995 ).Thereare,however,severalre-portsofparasiteoccurrenceatlow(winter)watertemperatures,indicatingthattemperaturealonecannotexplaintheoccurrenceofepidemics( Stir-nadel1994 ; Bittner2001 ; Decaesteckeretal.2005 ).Apossibleexplanationcouldbethatparasitesdonotgrowatlowtemperaturesbutmaybeabletopersistforsometime.Therelationshipbetweenthespreadofparasitesinrelationtohostdensityandwatertemperaturecertainlyneedsfurtherinvesti-gation.Thecommunity-levelperspectiveof De-caesteckeretal.(2005) revealedremarkablepat-terns.Daphniadensitywasobservedtobeneg-ativelyrelatedwithoverall endoparasite preva-lence,whereas epibiont abundancecorrelatedpos-itivelywithDaphniadensity.Furthermore,parasitespeciesthatseverelyreducedhostfecundityper-sistedforshorteramountsoftimeinthepopula-tionandhad,onaverage,lower prevalences thanbenignspecies.Thedatadidnotallowaneres-olutionofthesepatterns,butthefollowinginter-pretationmayexplainthesendings.Higherhostdensityallowsparasitestospreadandthusin-creasesprevalence.Thus,harmlessparasites(suchasepibionts)aremoreabundantwhenhostden-sityishigh.Hereitisthehostthatgovernspara-sitedynamics.However,harmfulparasitesmayatthesametimereducethehostpopulationgrowthratesomuchthattheirneteectonthehostpop-ulationisareductionindensity.Thisreductioninhostdensitydestabilizestheparasitepopulation,whichleadstoshortparasitepersistencetimes.Thus,forharmfulparasites,theepidemiologicalfeedbackbetweenhostandparasitegovernstheparasitedynamics.Thestrongdynamicsofmanyparasitespeciesalsoindicatethatstudiesthatuseonlyoneorfewsamplesperpopulationtoestimatethe richness of 38ParasitisminNaturalPopulations thelocalparasitecommunityarelikelytovastlyunderestimate parasiterichness . 4.3.5 AreThereFewerParasitesinLakeswithFish?Thereseemstobeadierenceinthedegreeofpar-asitisminwaterbodieswithandwithoutplanktiv-oroussh.Thelower parasiterichness andpreva-lenceestimatesinlakeswithshpredationareun-derscoredbythefactthattherearefewerliteraturereportsofDaphnia parasites fromlakeswithsh.Severalfactorsmayworktogethertoexplainthisfact.First,thelikelihoodofinfectionincreaseswithbodysize( Vidtmann1993 ; StirnadelandEbert1997 ),whichisprobablyaresultofbothhigherltrationrates(andthushigheruptakeratesofpar-asitespores)andanaccumulationeectwithage.Inpondswithhighadultmortality,asistypicalforpopulationswithplanktivoroussh,theaveragelifeexpectancyofaDaphniaislow,andthus,para-sitesmayhavealowerchanceofcompletingtheirdevelopment.Thisreducesnotonlyparasitesur-vivalbutalsoparasitetransmission,becauseolderinfectedhostsarethosethatreleasemost(orevenall)ofthetransmissionstages.Apredictionofthishypothesisisthatparasitesfoundinlakeswithhighpredationpressureshouldcompletetheirde-velopmentquickly(short prepatentphase )andthuskilltheirhostearly.ThemostvirulentDaphniaparasiteshavebeenindeeddescribedfrom habitats withplanktivoroussh( Bittner2001 ; Wolinskaetal.2004 ; Duyetal.2005 ).Anotherpredictionisthatparasitismratesinlakesshouldbehigherattimeswhenshpredationislow.Indeed,para-sitisminLakeConstanceismainlyfoundinfallandwinter( Bittner2001 )whenpredationisstronglyre-duced,whereasinshlesspondsandlakes,preva-lencepeaksinsummer( Brambilla1983 ; Vidtmann1993 ; Stirnadel1994 ). Duyetal.(2005) linkedtheseasonaloccurrenceofSpirobacillus epidemics inseveralNorthAmericanlakestoadropinpreda-tionratebybluegillsunsh.Second,somediseasesmaketheirhostsmoreconspicuousthroughareductionintransparency,thusincreasingthelikelihoodofpredationbyvisu-allyhunting predators ( Lee1994 ; YanandLarsson1988 )(P.T.J.Johnson,personalcommunication).Similarly,increasedsusceptibilitytopredationwasreportedforhostscarryinglargeloadsofepibionts( Willeyetal.1990 ; Allenetal.1993 ; Chiavellietal.1993 ; Threlkeldetal.1993 ).Consistentwiththis, WilleyandThrelkeld(1993) reportedareductionintheprevalenceofclearlyvisible epibionts afterstockingwithsh.Apredictionofthishypothesisisthatparasitesfoundinlakeswithvisuallyhunt-ingshshouldnotmaketheirhoststoovisibleor,ifso,onlyintheterminalphaseofinfection.Con-sistentwiththis,themainparasitesofD.galeataandD.hyalinainLakeConstancearehardlyvisiblewiththenakedeye( Bittneretal.1998 , 2002 ; Bittner2001 ).However,thishypothesisneedsfurthercare-fulexamination.Atwisttothishypothesisisthatinturbidwaterswithlowvisibility,infectedhostsmaynothaveareducedlifeexpectancyrelativetouninfectedhosts( Decaesteckeretal.2005 ).Third,sh predators aretypicallymorecommoninlargerpondsandlakes.Anumberoffactorsthatgohand-in-handwiththesizeoflakesmaylimitthespreadofparasites.Summertemperaturesinlargerwaterbodiesmaynotriseashighasinsmallerlakesinthesameregion,thusinuenc-ingparasitedevelopmentorshorteningtheseasonduringwhichparasitescanoccur( Ebert1995 ).Fur-thermore,thesedimentoflarger,andinparticulardeeper,lakesmaybeasinkforparasitetransmis-sionstages.Parasite spores areknowntorestinsediment,wheretheycanbepickedupbyDaphnia( Ebert1995 ; Decaesteckeretal.2002 ).Indeeplakes,Daphniaarelesslikelytocomeincontactwithlakesediment,thusreducingtransmissionrates.Apre-dictionofthishypothesisisthatparasitesthatrelyexclusivelyontransmissionfromdeadhostsarelesslikelytobefoundindeeplakes(see Chapter8 , Epidemiology ,sectiononTransmission),asforex-ampleP.ramosa.Indeeplakes,transmissionfromlivinghosts(e.g.,gutparasites)maybemuchmoreimportantforthepersistenceofparasites.Fourth,becauseDaphniapopulationsinlakesmaynotreachthedensitylevelsofpondpopula-tions,parasitetransmissionmaybereduced.Twofactorsmayaccountforthissituation:a)lakesareoftenlessnutrientrich(eutrophic)thanponds,sothatlowerratesofprimaryproductionmaylimitthemaximumdensityof zooplankton populations;andb)predationbyplanktivorousshmayinu-enceDaphniadensity,andthusparasitetransmis-sion,negatively. 5.2EectsonHostFecundityandSurvival43 Figure5.1TheeectoffourparasitespeciesonrelativefecundityandsurvivalofDaphniamagna.Relativefecundityiscalculatedasthetotalnumberofospringofaninfectedfemale(untilherdeath)relativetothetotalnumberofospringofanuninfectedfemale,assumingthatthehealthyfemalewouldhavediedthesamedayastheinfectedfemale.Thus,theserelativefecunditymeasuresarenotconfoundedwithdierentlifeexpectanciesofinfectedanduninfectedfemales.WFCD,WhiteFatCellDisease;P.ram.,P.ramosa;M.bic.,Metschnikowiabicuspidata;G.int.,Glugoidesintestinalis.Redrawnandadaptedfrom Ebertetal.(2000a) . galeataproducedmoreeggsunderlowfoodcondi-tionsthanunderhighfoodconditions.IncontrasttothefoodstudyinD.galeata,astudyonD.magnainfectedwithP.ramosafoundthatwell-fedinfectedhostsproducedmoreeggsthanpoorlyfedinfectedhosts( Ebertetal.2004 ).Interestingly,thewell-fedinfectedhostsalsoproducedmoreP.ramosa trans-mission stages,indicatingthatgoodfeedingcon-ditionsbenetboththehostandthe parasite .Bothantagonistsarepossiblyresourcelimited.TemperatureEectsHealthyDaphniamatureearlierandatasmallersizeandhaveashorterlifespanwhengrowingun-derconditionsofhighertemperature.SurprisinglylittleisknownabouttheinuenceoftemperaturefortheexpressionofdiseaseinDaphnia. Duyetal.(2005) reportedanecdotallythatD.dentiferain-fectedwithSpirobacilluscienkowskiisurvivelongeratlowertemperatures.Becauseusuallyeverythingwithinvertebratestakeslongeratlowertempera-ture,thisobservationmaysimplybetheresultofthehosts'and parasites 'lowermetabolicrates.Amorecomplexrelationshipbetweentemperatureanddiseaseexpressionwasreportedby Mitchelletal.(2005) .TheyfoundthatthenegativeeectofP.ramosaonD.magnafecunditywasmorebe-nignwhenthetemperaturewaslower.Atalowertemperature,theparasitegainedlatercontroloverhostfecundity.Theauthorsemphasizethatthisef-fectweakensparasite-mediated selection duringpartoftheseason.Furthermore,thisparasiteeectinteractedbothwithhost genotype andtempera-turesuchthatclonalranksinhosttnessdieredunderdierenttemperatureconditions.Thiseectcannotbeexplainedbythetemperaturedepen-denceofmetabolicrates.Alteredrankordersof 44TheEectsofDaphniaParasitesonHostFitness hostgenotypesmayhaveprofoundconsequencesforthe evolution ofhost resistance .However,itisnecessarytoseetheseinteractionsinrelationtothemaineectsandtheseasonaldynamicsofthediseasetojudgehowevolutionwillbeinuenced.ChemicalCuesfromPredatorsDaphniahavebeenaworkhorseforthestudyof phenotypicplasticity .Inparticular,theirreac-tiontochemicalcuesreleasedby predators (i.e., kairomones )hasreceivedalotofattention. LassandBittner(2002) testedforinteractionsbetweentheeectsoftwoantagonistsonD.galeata,thepro-tozoangut parasite C.mesniliandkairomonesfromplanktivoroussh.Theyfoundnoevidenceforin-teractionsbetweenshandparasitewithregardtohostfecundityandsurvival.DoseEectsAnotherenvironmentaleectthatinuencestheharmcausedby parasites isthedoseoftransmis-sionstagestowhichahostisexposed.Typically,higherdosesgohand-in-handwithahigherlike-lihoodofinfectionandwithmoreseveredamagetothehost( Ebert1995 ; Ebertetal.2000b ; Regoesetal.2003 ; Ebertetal.2004 ).Veryhighdosesmayevenharmthehostsomuchthattheparasiteisnotabletocompleteitsdevelopmentbeforethehostdies( Ebertetal.2000b ). 5.2.2 GeneticEectsGeneticVariationamongHostsandParasites Parasitevirulence variesacrossparasiteisolates(strains,genotypes)andhostclones.Tomyknowl-edge,everyattempttotestfor geneticvariation withinparasite-inducedhostdamageintheDaph-niasystemhasshownsignicanteects.Hostclonesoriginatingfromwithinorbetween pop-ulations dierinthedegreewithwhichtheyex-pressdiseasesymptoms,andparasiteisolatesvarygreatlyintheextenttowhichtheycausedamagetothesamehostclones( Ebert1994a ; Ebert1998a ; LittleandEbert2000 ; Bittner2001 ; Decaesteckeretal.2003 ).Furthermore,therearestronghostclonexparasiteisolateinteractions:Withinpopulations,theinfectivityofP.ramosadependsstronglyontheinteractionbetweenthePasteuriaandtheD.magnagenotypes( Cariusetal.2001 )( Figure5.2 ).Thesameistrueiffecundityreductionisconsid-eredamonginfectedfemalesonly( Cariusetal.2001 ).Whatmaintainsthesehighratesofwithin-populationvariationisnotfullyunderstood,butithasbeensuggestedthatantagonistic armsraces playakeyroleinmaintaining geneticvariation forvirulenceand resistance ( Hamilton1980 ; EbertandHamilton1996 ; Cariusetal.2001 ).GeneticVariationacrossPopulationsandLocalAdaptation Geneticvariation for parasite virulenceismostpro-nouncedacrosspopulations.Thisvariationoftenfollowsacertainpattern,whichisfrequentlydis-cussedinthecontextof localadaptation ( KaweckiandEbert2004 ).ForfourD.magnaparasites,ithasbeenshownthatlocalparasiteisolatescausemoreharmtotheirhoststhanparasiteisolatesfromotherpopulations( Ebert1994b ; Ebert1998a )(D.RefardtandD.Ebert,manuscriptinpreparation).Thesendingsareconsistentwiththeideathatpara-sitesevolvelocaladaptationtothehoststheyhaveencounteredrecently( Figures5.3 and 5.4 ).Often(butnotalways)parasitesthatperformbetterintheirlocalhostthanotherforeign(ornovel)para-sitesalsoperformbetterintheirlocalhoststhaninotherhosts( Figures5.3 and 5.5 ).Locallyadaptedparasitesshownotonlyhigherlevelsofdamagetotheirlocalhostsbutalsohavehigherlevelsoftransmission-stageproduction( Ebert1994b ).Thendingofparasite localadaptation seemsrathergeneralinDaphniasystemsbutisnotal-waysfoundinotherhostparasitesystems.Someauthorsreportedthathosts,ratherthanparasites,canbelocallyadapted( Morandetal.1996 ; KaltzandShyko1998 ; Kaltzetal.1999 ).Ithasbeensuggestedthatthekeyvariablefortheevolutionofhostorparasitelocaladaptationistherelativespeedofevolutionofthetwoantagonists( Gandonetal.1996 , 1997 ; Gandon2002 ).Higherratesofmu-tation,recombination,anddispersalmayfacilitatelocaladaptation.Giventhesetheoreticalconsider-ationsandthendingthatDaphniaparasitesseemtobelocallyadapted,onemayspeculatethatpara-sitesofDaphniausuallyhaveahigherevolutionarypotentialthantheirhosts.Adierentapproachtohostparasiteinterac-tionsacrosspopulationsisthequestionofhow 46TheEectsofDaphniaParasitesonHostFitness Figure5.3LocaladaptationofG.intestinalisinD.magna.StrainsofthemicrosporidiumG.intestinalisfromthreedierentD.magnapopulationsshowthehighestratesofsporeproductionwheninfectinghostsfromthetheirownnativepopulation(bluecolumns).Thesamestrainsincombinationwithhostsfromfourotherpopu-lations(graycolumns)producemuchfewertransmissionstages.Notethelog10scaleforsporecounts.PopulationsHost1,Host2,andHost3arefromsouthernEngland,populationHost4fromsouthernGermany.Formorein-formation,see Ebert(1994b) . muchadispersinghostsuerswhenitencountersalocallyadaptedparasiteinanovelpopulation.Notethatthisquestionisdierentfromtheques-tionaboutparasite localadaptation . KaweckiandEbert(2004) explainthesedierencesinfulldetail.Ifparasitesarelocallyadaptedandthuscausemoreharmtotheirlocalhosts,ahostthatmigratesintosuchapopulationshould,oneexpects,suerlessonaveragefromthelocalparasitesthanthelocalhosts.Thisobservationhasbeenreportedinsev-eralexperiments( Ebert1994b ; Ebertetal.1998 ; Al-termatt2004 ).Itisimportanttonotethatalthoughthispatternisfoundwhenaveragingacrossseveralhostparasitecombinations,occasionallyahostinanovelcombinationismuchmoreaectedbythe Figure5.4LocaladaptationofP.ramosainD.magna.Threedierentstrainsofthebacteriumshowthehighestwithin-hostgrowthrateswheninfectinghostsfromtheirownnativepopulation(bluecolumn)(meanandstandarderror).OtherPasteuriaisolates(Novel)testedinthesamehostclones(graycolumn)havelowergrowthrates.Formoreinformation,see Ebert(1998a) . newparasitesthanexpected( Ebert1994b ).Theseinstancesarelikelytobeexceptions,buttheymayhaveprofoundconsequences,becausetheymaybethebeginningofadevastating epidemic .Furtherinformationaboutthe evolution ofvirulencecanbefoundinanumberofreviews( Bull1994 ; Ebert1998a , 1999 ; EbertandBull2003 ). 5.3 ParasiteEectsonOtherHostTraitsBesidesfecundityandsurvival, parasites mayinuenceotheraspectsofhost tness ,fewofwhichhavebeenstudied.G.intestinalis(formerlyPleistophoraintestinalis)reducesadultgrowthinitshostD.magna( Ebert1994b ).Thestrengthofthisef-fectwasshowntodependbothonhostcloneandparasiteisolate,withlocalparasiteisolateshaving 5.3ParasiteEectsonOtherHostTraits47 Figure5.5O.bayerisporeproductioninclonesofitsnativeD.magnapopulationandinclonesfromthreeotherD.magnapopulations.TwostrainsofO.bayerioriginatingfromtwoislandsofarockpoolmetapopulationofD.magnainsouthernFinlandweretestedincombinationwiththeirownandthreecentralEuropeanpopulationsofD.magna.Means(acrossclones)andstandarderrorsaregiven(between4and11cloneswereusedperhostpopulation).FormoreinformationonMaterialandMethods,see Mucklowetal.(2004) . 48TheEectsofDaphniaParasitesonHostFitness thestrongesteect. LassandBittner(2002) showedthatC.mesnilireducedtheadultgrowthofitshostD.galeata.Incontrast,P.ramosacausesitshostD.magnatogrowtoanunusuallylargesize( Ebertetal.1996 , 2004 ).Thisformofparasite-inducedhost gigantism maybeadaptivefortheparasite,aslargerhostsresultinmoreparasite spores beingproduced( Ebertetal.2004 ).Parasitesmayalsoinuenceaspectsoftheirhosts'sexuallifecycle.Forexample,theymayre-ducethehosts'likelihoodofndingmatesormayincreaseordecreasethefrequencywithwhichafemaleproducesephippiaandmaleospring.Fur-thermore,verticallytransmittedparasitesmayin-uencethesurvivaloftheirhostduringresting( LassandEbert2005 ). 5.4 ParasitesMayInuencePredationonTheirHostsThepotentialeectthat parasites haveonhostpredatorinteractionsisalsoimportant.Para-sitesmaylowertheabilityoftheirhoststoescape predators ;infectedhostsmayswimandreactmoreslowlythanhealthyhosts,forexample.Thesome-timesdramaticvisualeectthatparasiteshaveonDaphniamayevendirectlyincreasethehosts'at-tractivenesstovisuallyhuntingpredators( YanandLarsson1988 ; Lee1994 ; Duyetal.2005 ). LassandBittner(2002) testedformoreindirecteectsofparasitesonhostpredatorinteractions.TheytestedwhetherhostsarelessabletoshowadaptivephenotypicchangesagainstpredatorswhenexposedtoC.mesnili.Theirexperimentsre-vealednosignicantinteractionsbetweenparasiteandkairomon-inducedlifehistorychanges.Theyconcludedthatthisisbecausethehost'sadaptiveresponseagainstshpredatorschangeslifehis-torytraitsexpressedearlyduringthehost'slife,whereastheparasiteaectsitshostduringlaterstages.Ontheotherhand,onecanimaginethatpara-sitesaltertheirhost'sbehaviorsothathostsmoreeectivelyprotectthemselvesfrompredators,e.g.,byaltering verticalmigration .Thismaystillbedisadvantageousforthehostbecausethepara-site'sinterestisinhostsurvival,whilethehosthasto trade-o protectionfrompredatorsagainstother tness components,suchasreproduction. Lee(1994) and Felsetal.(2004) showedthatvar-iousparasitespeciesinuencethe depthselectionbehavior ofD.magna.Infectedhostsstaydeeperinthewaterthanuninfectedcontrols.Itisnotclear,however,whetherthisisadaptiveforthehost,theparasite,both,ornone.Anextremeexampleofalteredpredatorexpo-surewouldbeacaseinwhichtheparasitema-nipulatesitshost'sbehaviortofacilitateitown transmission tothenexthost.Tomyknowledge,noneofthedescribedunicellularparasitesofDaph-niahasaknownsecondhost,althoughthisoptionhasbeenspeculated( Manginetal.1995 ).However,the macroparasites ( helminth )parasitesofDaphnia,whichhavenotyetbeenextensivelystudied,havesecondhostsandmaywellmanipulatetheirhoststotheirownadvantage( Stammer1934 ; Green1974 ; SchwartzandCameron1993 ). 5.5 ConclusionsandOpenQuestionsThereislittledoubtthat parasites ofDaphniaandother Cladocerans aregenerallyharmful.Occa-sionalreportsof"nonsignicant"eectsofpara-siteshavetobeconsideredinthelightoflowsta-tisticalpowerorlargeenvironmentalnoise.Thusfar,everyspeciestestedundercontrolledcondi-tionsprovedharmful.WhatIndmoreinterest-ingthanthefactthattheparasiteharmsitshostarequestionsregardingthecovariablesofthede-greeofharm.Thereareanumberofinterestingquestionsaboutthis: 1. Whyaresomeparasitesmoreharmfulthanothers?Whatroledoestheparasite'staxo-nomicpositionplayforits virulence ?Whatroledoesthemodeof transmission play?Whatroledoesthespecictissueinfectedplay? 2. AretherefurtherhiddencostsofparasitisminDaphnia?Forexample,doparasitesinu-encematechoiceduringsexualreproduction?Doparasitesinuencethesurvivalof restingeggs ? 3. Doesinter-andintra-speciccompetitionofparasitesinuencevirulence? Chapter6HostAdaptationsagainsttheCostsofParasitism Asparasitesharmtheirhosts,thehostmaycounteradapt,reducingthetnesscostsofpara-sitism.HereIsummarizethelittleweknowaboutthewaysDaphniaadaptstolowerthecostsofparasitism.OneknownexampleisthatD.magnamaturesearlierinthepresenceofinfec-tions.IfurtherdiscusswhatisknownaboutinduceddefenseandtheevolutionofresistanceinDaphnia.Thechaptercloseswithadiscussionofthelimitsofhostresistance.Thusfar,noevidenceforacostofdefensehasbeenfoundinDaphnia. 6.1 Introduction Parasites harmtheirhoststofostertheirownneeds.Asstudiesthusfarhaveshown,thisdamagevariesacrosshostclones,suggestingthepresenceof geneticvariation amonghostsfor resistance ortheexpressionofdisease.Thisgeneticvariationfortness-relatedtraitsmaybringaboutdierentreproductionandsurvivalratesamonghost geno-types ,sothathostclonesthatsuerlessfrompar-asitismincreasetheirnumericalrepresentationinthehost population .Ifatleastpartofthegeneticvariancefortnessisbasedon additivegeneticvariance ,thehostpopulationmayadapttocoun-teractparasitesevenacrossthesexuallifecycle,i.e.,evenafterthegenecombinationsintheclonesarerecombinedintonewgenotypes.Thusfar,wehaveonlyafewclearexamplesofDaphniahostsadaptingtoparasitism.Therearetwomainproblemswithdetectinghostadapta-tions.First,ifhost adaptations lowerparasite t-ness (whichisoftenbutnotnecessarilyalwaysthecase),parasitesmayrapidlyevolvecounteradapta-tionsthatreducetheeectivenessofthehostadap-tationsandmaymaketheminvisible.Apredictionofthistheoryisthathostadaptationsaremorelikelytobefoundinthepresenceofcoevolvingparasitesiftheadaptationbenetsthehostgreatlybutposeslittleornodisadvantagetotheparasite.Forexample,thereductionof"unnecessary viru-lence ",i.e.,parasite-induceddamagetothehostthathasnobenetfortheparasite,couldbeaneasilydetectedhostadaptation(innovel,notyetcoevolved,hostparasiteassociations,suchunnec-essaryvirulenceissometimesobserved).Second,theadaptivevalueofhosttraitsexpressedinthepresenceofparasitesmaybediculttojudgebe-causetheystemfromtheinteractionbetweentwoorganismsandmayormaynotbebenecialtoboth( Moore2002 ).Forexample,istheDaphnia'sparasite-inducedchangein dielverticalmigration ( Felsetal.2004 )benecialforthehost,theparasite,both,ornone?Hostadaptationstoparasitesmaybeobservedatseverallevels.Themostimpressiveexamplesarethosewhereatraitisexpressedonlyinex-posedorinfectedindividualsandconfersabene-tcomparedwithindividualsthatdonotexpress 66Epidemiology Figure8.4ProportionofinfectedD.magnarelativetothenumberofP.ramosasporesinthemedium.Thesig-moidalincreaseinproportionofinfectedhostsfollowstheexpectationofthemassactionmodelclosely.Eachsporedosewasreplicatedabout100times.Redrawnaf-ter Regoesetal.(2003) . tosusceptibility( LittleandEbert2000 ; Cariusetal.2001 ).ParasiteTransmissionCanBeLimitedbyLowTemperaturesPlanktonepidemicsarepredominantlyfounddur-ingthewarmsummermonths( Green1974 ; Brambilla1983 ; YanandLarsson1988 ; Vidtmann1993 ). Ruttner-Kolisko(1977) ,workingwithami-crosporidian parasite inarotifer population ,pro-posedthat transmission isimpairedatlowtem-peratures.ItestedthishypothesiswithG.intesti-nalisinD.magnaandfoundthattransmissionwasindeedimpairedbelow12C( Ebert1995 ).ThisisconsistentwiththeobservationthatG.intestinalisdecreasedinlateautumninD.magnapopulationsinsouthernEngland( Stirnadel1994 ).Poortrans-missabilityattemperaturesbelow25Cwasre-portedforP.ramosa,whichparasitizestheClado-ceranMoinarectirostris( Sayreetal.1979 ).(Note:ItisquestionablewhetherthisMoinaparasitewasindeedP.ramosa.)Incontrast,P.ramosainD.magnacanbetransmittedbetween10and25Cinthelaboratory( Ebertetal.1996 ; Mitchelletal.2005 ).Thus,temperaturecriterionappearstobespeciesandstraindependent.ReportsofnaturalDaphniapopulationsfurtherindicatethatcertainparasitescanbefoundunderwinterconditions( Stirnadel1994 ; Bittner2001 ).InLakeConstance,Daphniaparasitesoftenoccurpre-dominatelyinfallandwinterconditions( Bittner2001 ),suggestingthattemperatureiscertainlynotuniversalinlimitingparasitespread.Theabsenceofparasitesduringsummerinlargelakeshasbeensuggestedtoberelatedtointensepredationduringsummermonths( Duyetal.2005 )andisunlikelytobeaconsequenceoftemperatureeectsontrans-mission.HostStressMightFacilitateParasiteSpreadIthasbeenclaimedthatstressedhost populations aremore susceptible to parasites andthusfacilitateepidemics.ThistheoryhasbeenusedtoexplaindiseaseoutbreaksinCladoceranskeptunderpoorlaboratoryconditions( Seymouretal.1984 ; Stazietal.1994 ).Likewise, FranceandGraham(1985) observedhigherratesofmicrosporidiosisamongstressedcrayshinacidiedlakes.ForDaphnia,thereisnosupportforthestresshypothesisbutrathertheopposite.Experimental transmission ofG.intestinalistoindividualD.magnaappearedtobelargelyindependentofthehost'sfeedingcon-ditions(anddidnotdieramongagegroupsorsex)( Ebert1995 ).SimilarresultswereobtainedforC.mesniliinD.galeata( Bittneretal.2002 ).Adirecttestofthestresshypothesiswascarriedoutinex-perimentalpopulationsofD.magnainfectedwithG.intestinalis.Whenhalfoftheexperimentalpopu-lationswerestressed(reducedfoodlevel),parasitepopulationssueredmorethanthehostpopula-tions( PulkkinenandEbert2004 )becausemortal-itywasdisproportionatelyhigheramongthemostheavilyinfectedhosts(thosethatcarriedthemostparasites).Thisresultcountersconventionalwis-domaboutvertebratepopulations,inwhichstressisthoughttogohand-in-handwithdiseaseout-break.Experimentsthattestedtherelationshipbe-tweentransmissionstageproductionandhostnu-tritionalstatusfurthersupporttheobservationthatDaphniaparasitesdonotfarewellwhentheirhostsarestressed.Asinotherinvertebratesystems,par-asitesinpoorlyfedhostsproducefewertransmis-sionstagesthanparasitesinwell-fedhosts( Ebertetal.1998 ).Thus,althoughsomeobservationshavebeeninterpretedtosuggestthatstressmayleadtodiseaseoutbreaks,experimentalresultsshow 68Epidemiology Figure8.5Variationinresistanceamong19D.magnaclonesinresponsetoveparasitespecies.Micro1and2aretwoundescribedmicrosporidianparasitesofD.magna.Allhostclonesandparasiteisolatesoriginatedfromthesamepopulation.Redrawnandmodiedafter Decaesteckeretal.(2003) . diapause,Daphniahatchfromtheir ephippia andrecolonizeapond.Undergoodfeedingconditions,thepopulationincreasesrapidlyduringspringun-tilfoodshortagesleadtoaswitchfromlterfeed-inginthefreewatertobrowsingonthebottomsed-iments.Browsingsupplementsthefoodbecauseitstirsupfoodparticles( Hortonetal.1979 ; Freyer1991 ),whicharetheningestedbylterfeeding.However,browsingalsostirsupparasite transmis-sion stages,whichmayinfectthedaphniid.Oncethersthostsareinfected,thediseasemayspreadfurther.Theepidemicendseitherwhenenviron-mentalconditionsdeteriorate(e.g.,lowtempera-ture)orwhenthehostpopulationbecomessparseordisappearsaltogether.Akeyfeatureofthismodelistheuptakeof spores fromthepondsediments,whichhasveryimportantconsequencesforthe epidemiology ofthesystem,aswasshowninamathematicalver-sionofthismodel( Ebertetal.1997 ).First,uptakeofsporesfromthesedimentsisindependentfromhostdensity.ThebasicreproductiverateR0be-comesredundantasameansofpredictingpara-sitepersistencewhenthereisalarge,nondeplet-ingsporebankinthesediment.Instead,thefeed-ingbehaviorofDaphniaandthepropertiesoftheresourcedetermineparasiteinvasions.ThismayexplainwhylongitudinalstudiesofDaphniapond populations havefailedtondarelationshipbe-tweenparasitismandhostdensity.Second,the sporebanks allowtheparasitestosurvivelongperiodsoflowhostdensity.Althoughthisepidemiologicalmodelwasdevel-opedforponddwelling zooplankton ,itsndingsaboutdensity-independentinfectioncouldalsoberelevanttoanumberofsoil-bornediseases. Flem-ingandcolleagues(1986) investigatedthedensity-dependenttransmissionofavirusindierentpopulationsofthesoil-dwellingpasturepestWis-canasp.(Lepidoptera:Hepialidae).Evidencefordensity-dependenttransmissionwasfoundonlyinyoungpasturesbutnotinoldpastures,per-hapsbecauseinolderpasturestransmissionoc-curredmainlyfromasporepoolthathadaccumu-latedoverseveralgenerations.Inlaboratorypopu-lationsofavirusinsectsystem,Saitandcolleagues( Saitetal.1994 )failedtodetect densitydepen-dence andattributedthisresulttotherapidaccu-mulationandlongpersistenceofvirustransmis-sionstageswithinthecages.Contaminationofthesoilhasbeenrepeatedlycitedasthesourceofvar-iousinfections( KellenandHomann1987 ; Young1990 ; Woodsetal.1991 ; Daietal.1996 ).Thus,itappearsthatdurabletransmissionstagesandtheiraccumulationinpondsedimentsorsoilmightbeawidespreadphenomenoninnaturalhostparasitesystemsandmayobscureanypatternofdensity-dependenthost-to-hosttransmission.TheDaphniaparasitemodelforshlesspondsoersonlythemostbasicpatternofparasitedy- 8.2EpidemiologyofDaphniaMicroparasites69 Figure8.6DierenceinsusceptibilityofeitherinfectedorhealthyD.magnacollectedfromanaturalpopulation.Allfemaleswerecuredandreinfectedunderstandardizedconditionswithdierentdoses(sporesofP.ramosaperhost).Inthreeoffourpopulations,thedescendantsofpreviouslyinfectedfemalesweremoresusceptibletoinfectionunderstandardizedlaboratoryconditions.Modiedafter Little&Ebert(2000) . 70Epidemiology namics,leavingmanydetailsunexplained.Itcan-not,forexample,explainthedynamicsofpreva-lenceinlakeswheretherearelikelytobenosporebanksandmayalsofailtopredictepidemicsinpondswithpermanent(withoutdiapause)Daphniapopulations.Itisfurtherunabletoexplainwhycer-tainparasitespeciesshowshort-lastingepidemicsofafewweeks.Clearly,ourunderstandingofpar-asitedynamicsinnaturalDaphniapopulationsisstillverylimited. 8.2.2 SuggestionforaLakeModelAsdiscussedabove,lakeswithshpredationseemtohavelowerratesofparasitismthanshlessponds(see Chapter4 onDaphnia Microparasites inNatural Populations ).Thefollowingmodelmaybeastartingpointforunderstanding zooplankton epidemicsinlakeswithsh.MyideasarepartiallybasedontheworkofKerstinBittneratLakeCon-stance( Bittneretal.1998 , 2002 ; Bittner2001 ).FishpredationcanbeaseveremortalityfactorforDaphniaandwillcertainlyinuencethe abun-dance ofparasites.Ifshpredationishigh,para-sitesmaynotbeabletospreadinDaphniapop-ulations,becausetheaveragelifeexpectancyofaDaphnia(andthusofaninfection)istooshort(see Chapter4 ,AreThereFewerParasitesinLakeswithFish?).K.PulkkinenandD.Ebert(manuscriptinpreparation)haveshownhighparasiteextinc-tionratesinarticiallypredated,experimentalD.galeatapopulations.Thus,duringperiodsofhighpredation,parasitesareexpectedtobeabsentorfoundinlowprevalence.Becausepredationpres-sureoftenvariesovertime,parasitesmayspreadduringperiodswhenadulthostmortalityisrela-tivelylow.ThistheorycoincideswithndingsthattheprevalenceofDaphniaparasitesinlakepopu-lationsishighinfallwhenshpredationislow,whereasparasitesareabsentoronlyfoundinlowprevalenceduringsummertime,whenpredationishigh( Bittneretal.2002 ; Duyetal.2005 ).Inshlessponds,parasitessurvivetheabsenceoftheirhostsinthesediments.Becauselakeswithsharelesslikelytohaveecologicallyimportant sporebanks inthesediments(Daphniaaremuchlesslikelytocomeintocontactwiththesedimentinlakes),adierenthypothesisisneededtoexplainhowtheseparasitescansurviveunfavorablecon-ditions.Apossibleexplanationmightbethelargesizeofplanktonpopulations,whichmayenableparasitestosurvivelongperiodsofnegativepopu-lationgrowth(R01).Withahugehostpopulationsize,forexample,aparasitepopulationmightde-clineconsiderablyforseveralgenerations,reach-ingverylowprevalence.Butlowprevalenceinlargelakesishardlyanindicationofextinction.Forexample,inalakethesizeofLakeConstance(volume,50x109m3),ifthehostdensityfallsto0.1Daphniaperm3and1in100,000hostsisin-fected,therewouldbestillabout50,000infectedhosts,certainlyenoughtomaintaintheparasitepopulation,althoughatlevelsfartoolowtobede-tectedwithconventionalsamplingmethods.Thisargumentneedscarefulevaluation,takingabso-lutehostandparasitepopulationsizesintoaccountaswellasyear-roundgrowthconditions.Analternativehypothesisisthatparasitesgoex-tinctlocallybutoccasionallyrecolonizethelake.However,ifonlyoneorafewimmigrantparasitesareintroducedintoalargehostpopulation,theirspreadtodetectablelevelstakesconsiderabletimeunlessR0ishigh(»1).Nevertheless,thismecha-nismmaystillexplainsomeoftheobservedcasesofparasitedisappearanceandreappearance.Asmentionedabove,parasitesinlargelakeswithshpredationmayevolvecertainstrategiestoreducetheirmortality.Themostobviousofthesearefastdevelopment(evenifithascostsintermsofhigh virulence )andlowvisibilitytovisuallyhunt-ingsh.Acomparativestudybetweenlakeswithandwithoutshpredationwouldallowthesetwopredictionstobetested.Insummary,parasitesmaybeabletosurviveinlargelakeswithshpredationbyexploitinghostsattimesoflowpredationpressureandoutlastingunfavorabletimesinastateofextendednegativepopulationgrowth. 8.3 ConclusionsandOpenQuestionsAtpresent,wehavenosatisfactorymodelforthe epidemiology ofDaphnia parasites ,norofanyother zooplankton parasite.Thetwomodelspre-sentedabovearegeneralframeworksthattreatallparasitespeciesofacommunityalikeandthuslackmanyimportantfeatures.Amoreprotableap-proachmaybetofocusoncertainparasitespecies 74PopulationDynamicsandCommunityEcology Mathematicalmodelspredictdierentpopula-tiondynamicsforhostsinfectedwithmicropar-asitesthatreducehostfecundityversusthosein-fectedwithparasitesthatreducehostsurvival( An-derson1979 , 1982 ).Hostdensityispredictedtodecreasemonotonically,withthenegativeeectthataparasitehasonhostfecundity(allotherthingsbeingequal).Incontrast,meanhostpopula-tiondensityispredictedtorstdecreaseandthenincreaseasparasite-inducedhostmortalityrises.Thisisbecause(foragiven transmission ratepa-rameter)parasitesthatkilltheirhostsveryrapidlyarelesslikelytobetransmittedtootherhostsandwill,therefore,remainatlowprevalence,whereasparasiteswithlittleeectonhostmortalitywillhavelittleeectonhostdemographics.Theseepi-demiologicalmodelsalsopredictpopulationuc-tuations,positingthathostdensityuctuationsin-creaseasamicroparasiteshowsanincreasinglynegativeeectonhostsurvivalandfecundity.Ac-cordingtothesemodels,densityuctuationsin-creasethechanceofextinctionofsmallhostpop-ulationsbecausehostdensityismorelikelytodroptozeroduringpopulationbottlenecks( May1974 ; McCallumandDobson1995 ).Epidemiolog-icalmodels,suchasthosecitedabove,haveoftenbeenusedtoexplainempiricalresultsinsituationswhereparasitesreducedthedensityoftheirhostsorcontributedtotheextinctionofthehostpopu-lation.Thesamemodelspredictthatbenignpara-siteshavelittleeectonhostpopulationdensitiesandthereforecanbeappliedequallywelltocaseswhereparasiteshavelittleornoapparenteectonhostpopulationdynamics.Therefore,alongwithcontrastingparasitizedwithnonparasitizedpopu-lations,itisimportanttocomparehostpopulationsinfectedbyparasiteswithdierenteectsonhostfecundityandsurvival. 9.2 DoParasitesRegulateHostPopulations?AreviewofeldstudiesonparasitisminDaph-nia populations (see Chapter4 ,GeneralizationsaboutParasitisminNaturalPopulations)revealsverylittleaboutthepopulation-leveleectsof par-asites ontheirhosts.Becausetherearenoreplicatesorcontrolpopulationswithoutparasitesineldstudies,itisdiculttodrawconclusionsaboutpopulation-leveleects.Tomyknowledge,only Brambilla(1983) hasattemptedtoanalyzehisdataforpossiblepopulation-leveleectsofparasitism.HetestedfortheeectofthemicrosporidiumThe-lohaniaontheinstantaneousbirthanddeathratesinalongitudinalstudyofaD.pulexpopulationandcomparedtheserateswithratescalculatedundertheassumptionthattheparasitewasabsentfromthepopulation.Theimpactoftheparasiteonbirthratevariedwidelyoverthesummerandacrosstheyearbutwasgenerallystrongerthanitwasforthedeathrate.Fornearlyallsamplingdates,hecalcu-latedthattheparasitesdecreasedthe populationgrowthrate ,r,byabout20%onaverage.Hestates,however,thattheparasitealoneprobablydoesnotregulatethepopulationgrowthofitshost,becauservariedsubstantially,independentofparasitism( Brambilla1983 ).Hewasnotabletocarryoutlab-oratoryexperiments.Population-levelexperimentswithDaphniapar-asiteswererstproposedby EbertandMangin(1995) ,whoshowedthatD.magnapopulationsin-fectedwiththemicrosporidiumFlabelliformamag-nivora(intheirpapercalledTuzetiasp.)hadalowerdensitythanuninfectedcontrolpopulations.Thisparasiteisexclusivelyverticallytransmittedunderlaboratoryconditions( horizontaltransmission hasnotbeenfoundforthisparasite)andwaspresentataprevalenceof100%.Therefore,onecanexcludedensity-dependenttransmissionastheregulatoryfactor.Becauseexclusivelyverticallytransmittedparasitesinasexualpopulationsbehavelikeadele-teriousgene( Manginetal.1995 ),thereducedden-sityisadirectconsequenceofthereducedfecun-dityandsurvivalofthehosts. Ebertetal.(2000a) comparedtheeectsofsixparasitesonthefecundityandsurvivalofindi-vidualhoststotheireectsonhostpopulationdensityandthehost'sriskofextinction.Fivehori-zontallytransmitted microparasites (twobacteria:WhiteFatCellbacterium,Pasteuriaramosa;twomi-crosporidia:Glugoidesintestinalis,Ordosporacolli-gata;onefungus:Metschnikowiabicuspidata)andsixstrainsofaverticallytransmittedmicrosporidium(F.magnivora)ofD.magnawereused.Lifetableexperimentsquantiedfecundityandsurvivalinindividualparasitizedandhealthyhostsandcom-paredthesewiththeeectoftheparasitesonhostpopulationdensityandonthelikelihoodofhostpopulationextinctioninmicrocosmpopulations. 78PopulationDynamicsandCommunityEcology Figure9.2RelationbetweenthedensitiesofColaciumvesiculosumandperitrichsonD.magna.Thesedataarecollectedfromanaturalpopulation.InexperimentsitwasshownthatlightfavorsC.vesiculosumoverper-itrichs,whereasdarknessfavorsperitrichsoverC.vesicu-losum.Thisindicatesthatthenegativecorrelationintheabundanceofthesetwoepibiontsisdrivenbyinterspe-ciccompetition.Redrawnfrom Green(1955) . peritrichciliates(favoredunderpoorlightcondi-tions).Acrossseveralindividualswithinapopu-lation,thiscompetitionleadstoanegativecorre-lationbetweenthenumberofperitrichsandthenumberofC.vesiculosum( Figure9.2 ).Thestrongvariationinepibiontcompositionacrossindivid-ualsmayreectindividualdierencesinbehav-ior.Forexample,cloneswithaphototactic-positivebehaviormayhavemorealgaethanphototactic-negativeclones.Thesendingsclearlydemonstratethestrengthofwithin-hostcompetitionforshapingentire metapopulation communities.Theclearnessofthepatternsissurprising,however,giventhatsimi-larstrongpatternsarerarelyseenfromotherpar-asites.Ispeculatethatacombinationofspecichostepibiontinteractionfactorsplayarolehere.First,Daphniamolteveryfewdays(1-2daysasjuvenilesand3-4daysasadultsat20C).Aftermolting,the carapace isclean,andepibiontsstrug-gletorecolonizeit( Threlkeldetal.1993 ).Thus,competitionforspaceisresetaftereverymolt,stronglydiminishingtheroleofhistory(whocolo-nizesrst)andleadingtostrongerhomogenizationamonghostsintheentirepopulation.Second,thelow virulence (harmdonetothehost)causedbyepibiontsdecoupleshostmortalityfromtheactionofepibionts.Third,thereislikelytobelittleornoimmunedefenseofthehostagainstepibionts.Allofthesefactorsaredierentforendoparasites,whichareunaectedbyhostmoltingbutareaf-fectedbytheimmuneresponseofthehostandmaybevirulentforthehost.Tomyknowledge,nostudyhasyetdemonstratedparasitecompetitioninplanktonhosts. 9.5 ConclusionsandOpenQuestionsItseemsratherclearthatparasiteshavethepo-tentialtoinuencehost populationdynamics andcommunitiesandthatinterspeciccompetitionandecologicalfactorsaectingthehostinuenceparasitecommunities.Whatwearelackingaregeneralpatternsthatwouldallowustomakepre-dictionsforsystemswehavenotyetstudied.Forthis,weneedtostudynotonespeciesoronecom-munityatatimebutseveralinparallel.Anumberofissueshavenotyetbeenaddressedregardingplanktonparasites.HereIsuggestafewquestionsforfurtherresearch: 1. Someparasitesmayaltertheoutcomeofhostcompetition.Whichpropertiesofaparasiteaecthostcompetition,andwhichdonot? 2. Isthereinterspeciccompetitionamongen-doparasitesinplanktonhosts? 3. Arethere trade-os betweencompetitionatdierentlevels?Forexample,aparasitemightbeagoodcompetitoronahostbutispoorindispersalamonghostsoramong populations . 4. Doevolutionaryprocesses(e.g.,clonal selec-tion )inuencecommunityaspects? Chapter10ExperimentswithDaphniaandParasites ThischapterdescribeshowtousetheDaphniaparasitesystemforexperiments.Irstdiscusstheadvantagesofthesystemforresearchandeducation.ThenIdescribeanumberofexperiments,someofwhichareverysimpleandaresuitableforcoursesinexperimentalparasitologyandecology.Theexperimentsectionhastwoparts.Therstdiscussesexperimentsinwhichtheindividualhostistheunitofreplication.Suchexperimentscanbeusedtoaskquestionssuchas:Howdoesaparasiteaectitshost?Howisaparasitetransmitted?Thenextpartexpandstodiscussexperimentsthatuseentirepopulationsastheunitofreplication.HereIsuggestexperimentsthatposequestionssuchas:Doesaparasiteinuencehostdensity?Canaparasitedriveitshostpopulationtoextinction?Howquicklycanhostsevolveresistance? 10.1 AdvantagesofUsingtheDaphniaParasiteSystemforExperimentsTheDaphnia parasite systemisparticularlysuit-ablefortestinghypothesesbecauseitallowsforthecreationofrathersimpleexperiments.Amongtheadvantagesofthissystemare: Underlaboratoryconditions(20C),Daphniaproducetheirrsteggsafter7-15days(de-pendingonthefoodlevel).Thisequalstheshortestpossiblegenerationtimeinexperi-ments.Thereafter,theyproduceaclutchofparthenogeneticeggsevery3-4daysuntildeath,whichresultsinanapproximatelycon-stantfecundityacrosstheadultlifespan.Therstclutchisusuallysmallerthanthefollow-ingclutches.Onlyverylowfoodlevelsmayresultinskippedclutches. Controlledconditionsallowotherextrinsicsourcesofmortality,e.g.,predationbysh,infectionbyotherparasites,tobeexcluded. Parthenogeneticreproductionallowsthefe-malestoremainisolated(1femalein30-200mlofculturemedium)sothatfecundityanddeathschedulescanberecordedaccurately.Fromthese,birthanddeathratescanbecal-culatedintheabsenceofdensitydependence.Individualfemalescanbekeptwithorwith-outparasites. Parthenogeneticreproductionfurtherallowsfortheseparationofgenetic(among-clonevariancecomponents)andnongeneticeects(within-clonevariancecomponents). ManyDaphniaparasitestthedenitionthatepidemiologicalmodelsusefor micropara-sites verywell:small,unicellularparasitesthatreproducedirectlywithintheirhostsandare 10.3ExperimentswithIndividuals81 oftransmissionstagesfromthetreatmentsuspen-sion.ItmayalsolacknutritionalmaterialfortheDaphniathatthetreatmentsuspensionmaycon-tain.Second,theplacebomayhavesomeeectonthecontrols.Thiseect,oftencalledaplaceboeect,describesadierencebetweentheplacebotreat-mentandatotallyuntreatedcontrol.Iftheeectoftheactualtreatmentandtheeectoftheplacebotreatmentdonotinuenceeachother,thisisnotaproblem,butiftheeectoftheplacebointer-actswiththeeectoftheactualtreatment,there-sultsmaybediculttointerpret.Forexample,supposeyoutestfortheimmuneresponseofahostafteritisexposedto parasite spores .Ifboththeplaceboandsporesuspensionscontaincom-poundsthatinuencetheimmuneresponseofthehost(e.g.,certainbacteria),oneobtainsestimatesofhostresponse,whichhavetobeseenwithinthelightofthissuspension.Awatercontrolmaynothavethesameeect.Theresponsetotheex-posuretosporesmayhavebeendierentifthesporeshadbeeninawatersuspensionwithoutanyothercompounds.Irecommend,therefore,us-ingtwocontrolsinindividual-levelexperiments:aplacebocontrolandacontrolwithoutanything.Youmaynotbeabletoavoidaplaceboeect,butitisimportanttoknowaboutit. 10.2.1 UninfectedControlsinParasiteStudiesControlshavemorefunctionsthanjustbeingthesampleagainstwhichthetreatmentistested.Whentestingfortheeectofcertaintreatmentsona par-asite's performance,infectedhostsshouldbekeptunderdierenttreatmentconditions(e.g.,parasitegrowthunderdierentenvironmentalconditions; transmission ratesunderdierentdensities).Be-causealltreatmentgroupsareinfected,anunin-fectedcontroldoesnotseemnecessary.Therearereasonswhyuninfectedcontrols(actuallyplacebo-exposedcontrols)shouldbeincluded.First,theuninfectedcontrolsallowyoutoverifythatallma-terialwasuninfectedbeforethestartoftheexperi-ment.Second,someexperimentsfailforunknownreasons,e.g.,theremaybehighunexplainedmor-tality.Thecontrolsallowyoutojudgewhethertheparasitesplayedaroleintheseresults. 10.2.2 UsingAdditionalTreatmentsasaQualityControlIncertainexperiments,itisnotclearwhetherthetreatmentappliedwillshowanyeect.Anegativeresultisdiculttopresentinaconvincingway,becausethenonsignicanceofthetreatmentsmayhavebeencausedbyotherreasonsthantheab-senceofaneecttheabsenceofevidenceisnotevidenceforabsence.Forexample,statisticalnoisemaydisguiseatreatmenteectinapoorlyexe-cutedexperiment.Toascertainthequalityoftheexperiment,Irecommendusinganadditionalfac-torthatisknowntoproduceavisibleeect,evenifthiseectisnotthefocusofyourresearchques-tion.Forexample,onemayusetwofoodlevels,alongwiththeothertreatment.Thenifafoodef-fectisapparent,youmayconvincetheobserverthatothertreatmenteectscouldalsobefound,providedtheyarethere.Ifyoufailtondafoodeect,yourexperimentmayhavebeenpoorlyper-formed. 10.3 ExperimentswithIndividualsAnumberofDaphnia parasites caneasilybebredunderlaboratoryconditionsandarethereforesuit-ableforexperimentalwork.Theseexperimentscanbeconductedincoursesonthe evolution andecol-ogyofhostparasiteinteractionsbutalsoforre-searchpurposes.Whatfollowsaresomesugges-tionsforsimpleexperimentsthatwillworkevenifonehaslittleexperiencewithDaphniaparasites. 10.3.1 EectsofExposureDoseonParasiteandHostSuccessThe transmission stagesofhorizontallytransmit-ted parasites maybeadministeredtothehostindierentconcentrations.Typically,higherdosesaremorelikelytoproduceinfections( Ebertetal.2000b ; Regoesetal.2003 ).Toquantifytheinfectionsuccessofparasiteisolates,astandardizedmea-sureisused:the ID50 (or infectivedose50% ),whichisthedoseatwhich50%oftheexposedhostsbe-comeinfected.TheID50mayvarystronglyamongparasiteisolatesandhostclones( Ebert1998b ).Itisusuallyestimatedwithastatisticalprocedure 86Glossary thespecies'interactionwithoneanother.Co-evolutioncanoccuramongmutualistsandhostparasitepairs,aswellasamongen-tiregroupsofinteractingorganisms(e.g.,pollinatorplantsystems). CrustaceaAquaticarthropodscharacterizedbythepresenceofbiramousappendagesandtwosetsofantennae.Examplesincludecrabs,lob-sters,copepods,barnacles,shrimps,andwa-tereas. CyclicalparthenogenesisModeofreproductioninwhichphasesofparthenogenetic(asex-ual)andsexualreproductionalternate.Sev-eralasexualgenerationsmayfollowasexualgeneration.FoundinCladocera,Rotifera,andaphids. CyclomorphosisSeasonalchangeinphenotypeofmanyplanktonspecies.Forexample,someDaphniaspeciesproducespinestoprotectthemselvesagainstpredatorsduringthesum-merseason. DemePopulationthatissucientlyisolatedsothatitcanbeconsideredanevolvingunit.Demeismoretypicallyusedbyevolutionarybiologists. DensitydependenceIndicatesthattheintensityofaprocessdependsonthedensityofapopu-lation.Whenfecundityorindividualsurvivalinapopulationarenegativelydependentondensity(e.g.,parasite-inducedhostmortality),theprocesscouldpotentiallyregulatepop-ulationdensity.Transmissionofhorizontallytransmittedparasitesisusuallyhostdensitydependent. DepthselectionbehaviorBehaviorbywhichthezooplanktonmaintainsaparticularverticaldistributioninrelationtothestraticationofthewater(light,temperature,food,predationpressure).SeealsoDVM. DiapauseRestingperiodduringunfavorablecon-ditions,e.g.,duringwinterfreezingorduringdraughts. Dielverticalmigration(DVM)Specialcaseofdepthselectionbehaviorinwhichthepre-ferreddepthchangesinadiel(daily)pattern. DoseeectAchangeinresponsetoexposuretosomeagentattributabletoachangeinthatagent'sconcentration.Forexample,thein-creaseinvirulenceorinfectionriskforhostsduringexposuretoincreasingparasitesporedoses. ElectrophoresisMethodtostudythemovementofchargedmoleculesinsolutioninanelec-tricaleld.Thesolutionisgenerallyheldinaporoussupportmediumsuchascelluloseacetateoragelmadeofstarch,agar,orpoly-acrylamide.Electrophoresisisgenerallyusedtoseparatemoleculesfromamixturebasedupondierencesinnetelectricalchargeandalsobysizeorgeometryofthemolecules,de-pendentuponthecharacteristicsofthegelma-trix. EndemicPermanentpresenceofaparasitepop-ulationinahostpopulation.CompareEpi-demic. EndoparasiteSymbiontslocatedwithinthebodyofthehost.Theymaybeintra-orextracellular. Ephippium(pluralephippia)1.Membranousex-ternalwallssurroundingtherestingeggs(usuallysexualeggs)ofCladocera.2.RestingstageofCladoceraconsistingofoneortworestingeggs,surroundedbyamembranousexternalwall. EpibiontOrganismthatlivesattachedtothebodysurfaceofanotherorganism.Sometimesregardedasecto-parasites.Inzooplankton,epibiontsareoftenciliates,algae,bacteria,andfungi. EpidemicSudden,rapidspreadorincreaseintheprevalenceorintensityofaninfection.Com-pareEndemic. EpidemiologyStudyofinfectiousdiseasesanddisease-causingagentsonthepopulationlevelinaparasitologicalcontext.Itseekstochar-acterizethedisease'spatternsofdistributionandprevalenceandthefactorsresponsibleforthesepatterns.Inamoreappliedcontext,italsostrivestoidentifyandtestpreventionandtreatmentmeasures. EvolutionChangesinallelefrequenciesovertime. 88Glossary andshortgenerationtimes.Thekeyepidemi-ologicalvariable,bycontrastwithmacropara-sites,iswhethertheindividualhostisinfected. MicrosatellitelocusPlaceinthegenomewhereashortstringofnucleotides,usuallytwotovebaseslong,isrepeatedintandem.Thenumberofrepeatsatanygivenlocusisusuallyhighlyvariable(manyalleles)inapopulationandcanbeusedforDNAngerprinting. MorbidityStateofill-healthproducedbyadis-ease.Includesaspectsofreducedfecundity,lethargy,andothersignsofdisease. MultipleinfectionsInfectioninwhichanindivid-ualisinfectedbyparasitesofmorethanonespeciesormorethanonegenotypeofthesamespecies. ParasiterichnessSeeRichness. Parasite1.Disease-causingorganism.2.Organ-ismexhibitinganobligatory,detrimentalde-pendenceonanotherorganism(itshost).Con-ceptually,parasiteandpathogenarethesame.Endoparasitesliveinthehost'sinterior(Theymaybeintra-orextracellular).Ectoparasitesliveonthesurfaceofthehost. ParthenogenesisDevelopmentofanorganismfromanunfertilizedegg.Seealsocyclicparthenogenesis. PathogenDisease-causingmicroorganism,suchasviruses,bacteria,andprotozoa.Inthecon-textofthisbook,equivalenttoparasite. PhenotypicplasticityPhenotypicvariationex-pressedbyasinglegenotypeindierentenvi-ronments. PhototacticbehaviorBehaviorthatisexpressedinthepresenceoflightstimuli. PhyllopodaOrderofEntomostracaincludingalargenumberofspecies,mostofwhichliveinfreshwater.Theyhaveattenedorleaf-likelegs,oftenverynumerous,whichtheyuseforswimming.AlsocalledBranchiopoda. PopulationdynamicsChangesinthepopula-tionsizethroughtime.Alsousedtodescribechangeinthedemographicstructureofthepopulation(sexratio,ageandsizestructure,etc.). PopulationGroupofinterbreedingindividualsandtheirospring.Inasexualspecies,thisdef-initioncannotbeapplied;inthiscase,apop-ulationisagroupofphenotypicallymatchingindividualslivinginthesamearea. Populationgrowthrate(Malthusiangrowthrate,r)Measureofpopulationgrowth.Theinstan-taneousrateofincreaseofapopulationorgenotype.Itisusedasameasureoftness. Predator-induceddefenseDefensereactionofpreytriggeredbythepresenceoractionofapredatorsoastoreducetheexpecteddamageofthepredator. PredatorAnanimalthatkillsitsvictim,thepreyitem,andthenfeedsonittosubsistuntilthenextkill. PrepatentphaseInhelminthinfections,timepe-riodfrominfectionuntilafemalestartstopro-duceeggs.Itisequivalenttothelatentperiodinmicroparasiticinfections. PrevalenceProportionofhostindividualsin-fectedwithaparticularparasite.Oftenex-pressedasapercentage.Ameasureofhowwidespreadaninfectionordiseaseinahostpopulationis.Sometimesusedtoindicatetheproportionofinfectedhostsinasamplewithanyparasitespecies.Inmanystudies,preva-lenceismeasuredonlyinacertainfractionofhosts.Inzooplanktonstudies,oftenonlyadulthostsoradultfemalesareconsidered.Prevalenceisusuallyunderestimatedineldsamplesbecausenewinfectionsmayescapedetectionbytheinvestigator. 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