Eugregarine parasitism of Erythemis simplicicollis (Say) at a constructed wetland: a fitness cost to females? (Anisoptera: Libellulidae)

2010·1.8 MB·English

by  Locklin, J L

Odonatologica39(4):319-331 December 1,2010
Eugregarineparasitism
ofErythemissimplicicollis (Say)
ata constructed wetland:
a fitness cost to females?
(Anisoptera: Libellulidae)
J.L.Locklin**and D.S.Vodopich
DepartmentofBiology,BaylorUniversity,One BearPlace 97388,Waco,TX 76798,United States
Received May28, 2010/Revised andAcceptedSeptember13,2010
Eugregarineparasitesinfectawide varietyofinvertebrates. Someauthorssuggest
thateugregarinesareratherharmless,butrecentstudies suggest otherwise. Among
odonate-eugregarineinvestigations,Zygopterahave been more frequentlystudied
than Anisoptera. Adultdragonfly populationsweresurveyed foreugregarinesata
constructed,flow-throughwetland systemand thefitness cost ofinfection wasas-
sessedinacommonandwidespreaddragonflyhostsp.,E. simplicicollis. Populations
weresampledweeklythroughouttheflightseason.Hostfitnessparametersmeasured
included wingload,eggsize,clutchsize,and totaleggcount.Ofthe22hostspp.sur-
veyed,8hosted eugregarinesand2oftheseodon.spp.werepreviously undocumented
ashosts.Whileeugregarineparasitism hasbeenshowntoexhibitseasonality,parasite
prevalenceand intensityin E. simplicicollisin thisstudy showed noseasonal trend.
Thefitness parametersmeasured werenotcorrelated with the presence orintensity
ofeugregarines.These findingssuggest thateither eugregarinesdo not affectwing
loadingandeggproductionin E.simplicicollis,orthat virulence dependsonparasite
intensityand/orthespecificeugregarinespp.infectingthehosts.
INTRODUCTION
Dragonflies host a variety of ecto- and endoparasites, most ofwhich influ-
ence theirhosts’ fitness(BONN etal., 1996; REINHARDT, 1996;ROLFF et
al.,2000;CORDOBA-AGUILAR,2002; CORDOBA-AGUILAR etal.,2003;
MARDEN&COBB,2004;CANALES-FAZCANOetal., 2005). Eugregarine-
-odonateinvestigations havefocusedprimarily ondamselfly hosts(ABRO, 1971,
‘Currentaddress; DepartmentofBiology,TempleCollege,MBS.Temple,TX76504,United States;
— [email protected]
320 J.L. Locklin&D.S.Vodopich
1976;SIVA-JOTHY & PLAISTOW, 1999; SIVA-JOTHY, 2000; CORDOBA-
-AGUILAR,2002;HECKER etal.. 2002;CORDOBA-AGUILAR etal.. 2003;
CLOPTON,2004; TSUBAKI & HOOPER, 2004; CANALES-LAZCANO et
al.. 2005)with relatively fewstudies on dragonfly hosts (MARDEN &COBB,
2004; SCHILDER& MARDEN,2006;CLOPTON etah, 2007;LOCKLIN&
VODOPICH,2009;2010).
Ninegeneraof eugregarines (Apicomplexa; Eugregarinorida: Actinocephali-
dae) havebeenidentifiedas odonateparasites: Actinocephalus, Calyxocephalus,
Domadracunculus, Geneiorhynchus, Hoplorhynchus, Mukundaella, Nubenocepha-
lus, Prismatospora, andSteganorhynchus (RICHARDSON & JANOVY, 1990;
CLOPTON etah, 1993;CLOPTON, 1995;PERCIVAL etah, 1995;SARKAR,
1997;CLOPTON,2004; HAYS etah, 2007). All are monoxenous eugregarines
thatinfect theirhosts when odonatesingest oocyst-contaminated water and/or
insect prey phoretically carrying oocysts on/in theirbodies(ABRO, 1976). Ex-
cysted sporozoites attach to theodonate’sintestinalepithelium as trophozoites,
absorbnutrients, mature, and detach as gamonts. Two gamonts fuse to form a
gametocyst thatpasses outof the hostwithfeces. Withinthegametocyst, hun-
dreds of gametesformand fuseto produce the infective oocysts. To complete
the lifecycle, oocysts are thenreleasedinto theenvironmentas thegametocyst
ruptures(BUSH etah,2001;ROBERTS& JANOVY, 2005).
Eugregarine parasites have been historically viewed as relatively harmless
(BUSH etah, 2001),butsomestudieshaveshownthatthecostofeugregarine in-
fections involveseffectson fecundityandmortalityofinvertebrates(see SMITH
&CLOPTON,2003). Among odonatestudies,eugregarines havebeenshownto
reducelongevity (HECKER et ah,2002;CORDOBA-AGUILAR et ah, 2003;
CANALES-LAZCANOetah,2005;TSUBAKI& HOOPER,2004),reducefe-
cundity (CORDOBA-AGUILAR etah, 2003; CANALES-LAZCANO et ah,
2005), influencemating success (CORDOBA-AGUILAR etah, 2003), impair
flight-muscle performance (SCHILDER& MARDEN,2006), hindertheability
to maintain territories (MARDEN & COBB, 2004; CORDOBA-AGUILAR,
2002), reduce fat content (SIVA-JOTHY& PLAISTOW, 1999),and impairfat
oxidationin flightmuscles(MARDEN &COBB, 2004).
Thepresent studywas designed to(1) survey dragonfly populations foreugre-
garineparasitism,(2) determinetheprevalenceandintensitypatterns throughout
aflight season at a constructed wetlandsystem, and (3) investigate impacts of
eugregarine parasitism on fitnessparametersincluding wingload,eggsize, total
eggcount,andclutchsize inacommonandwidespread host,Erythemissimplici-
collis(Libellulidae).
EugregarineparasitismofErylhemissimplicicollis 321
METHODS
Thisstudy wasconductedattheLakeWacoWetland (LWW),TX,USA(31°60’88N,97°30’69W).
Thewetlandwasconstructedin 2001 ashabitatmitigationfora2-mpoolriseofnearbyWaco Lake.
The80-hawetlandreceivespumpedwaterfromtheNorthBosqueRiverandroutestheflow through
five sequentialwetland cellsbefore returningit 5-10days later to theriver that feeds Waco Lake
(SCOTTetal„2005).
Adult dragonflypopulationswere sampledweeklyfromMay-October 2009(= flightseason).All
collected individuals werenettedwithin 15m ofthe shorelines,takentothe laboratory,killed with
ethyl acetate,identified (ABBOTT,2005),and stored in70% ethanol. Priortopreservation,speci-
mensofE.simplicicollis weredorsallyscanned at600 dpi(MITCHELL& LASWELL,2000)and
weighedtothenearest0.1 mg.Weightlossduetodessicationinthelaboratorywascorrectedfollow-
ingLOCKLIN &VODOPICH(2010). Tosurveyforparasitesanddeterminetheirprevalence(per-
centageofindividuals infected)andintensity(numberofparasitesperinfected individual),preserved
abdomens wereplacedventral-side uponaStyrofoamtrayand dissected.Theabdomens weresplit
longitudinallyand pinnedtoexpose thecropsand intestines. Parasites (trophozoites andgamonts)
that werevisible throughtheintestinalepitheliumwerecounted.
Wecalculated monthlyeugregarineprevalences andintensities inE. simplicicollis throughoutthe
flightseasonandinvestigatedpotentialimpactsonparametersrelatingtospeciesfitness,i.e.differ-
encesinwingload,eggsize,total eggcount,andclutchsize. We defineclutchsizeasthenumber of
eggs laid(WATANABE& MATSU’URA,2006)duringinducedoviposition(see methodsbelow).
Totalegg countisthe sumofeggsreleased duringinducedovipositionandtheeggs retained inthe
abdomen.Egg viabilitywasnottested.In adult dragonflies,eugregarinesarenotvisuallydetectable
inrecentlyemergedtenerals (LOCKLIN&VODOPICH, 2010).Onlymaturehost individuals are
candidates foransweringquestionsaboutparasiteprevalenceandintensity.Because wingloads(mg
bodywtxwingsurfacearea1)werenotaffectedbyeugregarines(seebelow),weusedwingloadsasa
surrogateformaturityof£ simplicicollis.Minimum wingloadvalues forparasitizedE. simplicicol-
lis(<J = 18.0mg cm2; 9=21.8 mgcm2) wereused tosignify matureadults(LOCKLIN&VODO-
PICH,2010).
Tocalculate wingloads, totalwingsurface areaofeachE.simplicicolliswasestimated bymeas-
uringtherighthindwinglength(mm)fromthe second axillarysclerite tothewingtipusingAdobe
Photoshopandregressingtotalwingsurfacearea,y,usingthefollowingequations:
6 y =0.470a:- 5.94(r2=0.92, 18d.f„p<0.001)
9 y =0.450a- 4.66(r2=0.83,23d.f,p <0.001),
wherexishindwinglength(mm).
Tocollecteggs,femaleswerecapturedand inducedtoovipositinthefield(SUSA&WATANABE,
2007).Thetipofeachfemale’sabdomenwasrepeatedlydippedvertically intoa7-ml vialofwetland
wateronceper second untilshe stoppedreleasingeggs. Ifnoeggs werereleased initially,thendip-
pingcontinued forthree minutestoensurethatshe hadnoeggs torelease orthatshewasunwilling.
Thefemales werepreserved.Thewidthsand lengthsoftenrandomlyselectedeggsfrom24females
weremeasured (mm)usinganocularmicrometermountedinacompoundmicroscope.Eggcircum-
ference,C,wascalculated usingaformulaforellipseperimeter:
C=ii[l,5(a+b)- ((axft)'2’)]
wherea=0.5 xlengthandh=0.5xwidth (SCHENK&SONDGERATH,2005).Theeggsfromthe
other femaleswerepreserved in50%ethanol and later countedat60X. Eggsretained inabdomens
werealsocountedafterdissection. Thefemalescaughtforanalysisofclutch sizeandtotaleggcount
werecapturedmid-momingpresumablybefore dailyovipositingbegan.
322 J.L.Locklin& D.S.Vodopich
RESULTS
Specimensof twenty-twoanisopteran species (n= 1,378)were collectedatthe
wetland, eightofwhichwereparasitized by eugregarines (TabI).Fouroftheun-
parasitized species collected(Tab II),Anaxjunius (Aeshnidae), Epithecaprinceps
(Corduliidae), Tramealacerata(Libellulidae), and T. onusta (Libellulidae) have
beenpreviously reported to hosteugregarines (CLOPTON etal.,2007; LOCK-
LIN&VODOPICH, 2010). Eugregarines weretentativelyidentifiedas members
of the genera Actinocephalus and Geneiorhynchus (Eugregarinorida: Actinoce-
phalidae).
Monthly eugregarine prevalences inmatureE. simplicicollisshowedno season-
altrend through theflight season(Freedman’s test, V = 0.07,p =NS) (Fig. 1).
N
Table I
Dragonfly species (allmembersofLibellulidae)infectedwitheugregarineparasitesatthe Lake
Waco Wetland;- IQR =interquartilerange- [* indicates newlyreportedhost]
SSppeecciieess NN PPrreevvaalleennccee MMeeddiiaann IIQQRR MMaaxxiimmuumm
((%%)) iinntteennssiittyy iinntteennssiittyy
BBrraacchhyymmeessiiaaggrraavviiddaa 11
MMaalleess 11 110000 1111 -- 1111
FFeemmaalleess 00 -- -- -- --
CCeelliitthheemmiisseeppoonniinnaa 6677
MMaalleess 3344 99 22 11--99 99
FFeemmaalleess 3333 33 33 -- 33
EErryytthheemmiissssiimmpplliicciiccoolllliiss 888811
MMaalleess 335500 2277 22 11--55 6600
FFeemmaalleess 553311 3322 22 11--44 5555
LLiibheelllluullaa iinncceesstlaa** 33
MMaalleess 11 00 -- -- --
FFeemmaalleess 22 5500 11 -- 11
LLiibheelllluullaa lluuccttuuoossaa I1I1
MMaalleess 77 1144 11 -- 11
FFeemmaalleess 44 00 -- -- --
PPaannttaallaaffllaavveesscceennss** 5522
MMaalleess 2200 00 - - -
FFeemmaalleess 3322 33 11 -- 11
PPaacchhyyddiippllaaxx lloonnggiippeennnniiss 113344
MMaalleess 110088 1122 22 11--22 44
FFeemmaalleess 2266 1122 11 11--22 22
PPeerriitthheemmiiss tteenneerraa 6644
MMaalleess 4411 1100 22 11--66 77
FFeemmaalleess 2233 2222 33 11--44 44
Eugregarineparasitism ofErylhemissimplicicollis 323
Eugregarine intensitieswerenotnormallydistributedamonghosts(Shapiro-Wilk
test, p< 0.001), thereforenonparametric analyses were usedto assess intensity
data.Monthly medianintensitiesranged from 1.0 - 3.5 eugregarines in E. sim-
plicicollis (Fig. 1)and the maximumintensity of 60eugregannesoccurred in a
maleE. simplicicollis.
Wing loads amongmature E. simplicicollis individualswerenot relatedto the
presence/absence orintensityofeugregarines. Medianwing loads(mgcm2with
IQR)ofinfectedversusuninfectedindividuals,respectively, were25.6(24.6- 27.3)
and25.3 (23.8- 27.0) in malesand 30.9(28.6 - 33.6) and29.9 (27.1 - 32.4)in
females.No differencewas detectedbetweenmedianwingloads ofinfectedver-
sus uninfectedin eithermales(Wilcoxon RankSumTest, Z =-1.36, p=0.173)
or females(Z = -2.36, p=0.18). Likewise, wing loaddidnot correlatewitheu-
gregarine intensityin eithermales(N = 189,Spearman’s correlation, r =0.37, p
= 0.79) orfemales(N =288, r = 0.01,p=0.99)(Fig. 2).
Eggsize, totaleggcount,andclutchsizeofE.simplicicolliswerenot correlated
withthepresence/absence or intensity ofeugregarines. Of the femalescaptured
foregganalyses, 88%weregravidand57%ofthesegravidfemalesreleasedoneor
moreeggsintotheglassvials.Eggsizes(circumference) forfemaleE. simplicicol-
lisranged from 1.2 - 1.4mm,but thepresenceofeugregarines hadnoeffecton
meaneggsize. Meaneggsizes from infectedversus uninfectedfemalesdidnot
differ(t= 1.41,p =0.17, N = 24),and eggsize didnot correlatewith theinten-
sity ofinfection(N =24, r=-0.19,p = 0.37)(Fig. 3). Totaleggcounts ranged
from0 - 1,611 eggs female'. Mean numbersoftotaleggs from infectedversus
Fig. 1.Median gregarineintensity(dashedline)andgregarineprevalence(solidline)in£simplici-
collisthroughoutthe odonateflight seasonatthe LakeWaco Wetland,Texas,USA,2009.Intensity
datainclude interquartilerange(boxes) and range(extended bars).
324 J.L. Locklin& D.S.Vodopich
uninfectedfemaleswere not significantly different(t= -1.63, p= 0.11), andeu-
gregarine intensity didnotcorrelatewiththe totalnumberofeggs (N =84, r=
0.143, p = 0.193) (Fig. 3). Clutch size data(Fig. 3) includedonly females hav-
ing eggsavailabletorelease.Meanclutch size was 199eggs female’1(range =0-
967). Thepresence/absence ofeugregarines hadnosignificant effectonwhether
or not afemalereleasedeggs (Xt= 0.168, p=0.682). No differencewas found
between themeanclutchsizesof infectedversus uninfectedfemales(t=-0.741,
p=0.461). Clutchsizes didnotcorrelatewitheugregarine intensity (N = 74,r =
0.09, p=0.44) (Fig. 3).
DISCUSSION
Of theeight parasitized dragonflyspecies collectedatthewetland(Tab. I),two
(Libellula incesta andPantalaflavescens, Libellulidae) are reported as hosts for
thefirsttimeinthispaper,andsix werereported previously to hosteugregarines
(LOCKL1N & VODOPICH, 2009; 2010). Those odonatespecies surveyed in
LOCK LIN & VODOPICH (2010) and those in this paperthat lacked eugre-
garines should be consideredas non-hostsonly tentatively becausethe number
ofindividualsexaminedwas relativelysmall (Tab. II).
The lack of seasonal variationin parasite prevalence and intensity at LWW
maybeassociatedwithwater residence time.This wetland’scontinualflowand
shortresidencetime(5-10 days)islikely to dampenseasonalvariationinoocyst
density through time.LOCKL1N& VODOPICH (2010) foundthateugregarine
prevalence andintensity increasedduring the dragonfly flight seasonofeach of
Fig.2.Wingloadsofmales(opensymbols)andfemales(closedsymbols)E. simplicicollisversusgre-
garineintensity.Nocorrelation wasdetectedinmales(N=189,r =0.37,p=0.79)orfemales(N =
288,r=0.01,p=0.99).
EugregarineparasitismofErythemissimplicicollis 325
two subsequent years in dragonfly populations at BattleLake, a small nearby
reservoir withalongerwater residencetime. Inthatstudy, we speculated thatvi-
ableeugregarineoocystconcentrationsand/oravailabilityto hostsincreaseddur-
ingtheflight seasonand resultedinhigherlevelsofinfectiontowardstheendof
theseason. In thecurrent study, however, wedetectednosignificant seasonality
ineugregarine prevalence or intensity(Fig. 1).Weproposethatoocysts shedby
infectedhosts are constantly being washed through thewetlandintothenearby
NorthBosque Riverbecause ofthewetland’sbrief waterresidencetime.Conse-
quently, areduced butstableconcentrationofeugregarine oocysts is likely and
wouldresult intherelativelyunchanged levelsofeugregarine infectionsfoundin
thisstudy.
Localphysical, chemical,andbiological processesmayalsoinfluencethedistri-
butionandlongevity ofviableeugregarineoocysts andfosterthesteadyprevalence
andintensity foundatLWWcompared to BattleLake.Becausethemorphometry
andflowregimes differbetweenthetwo aquaticsystems, abiotic conditions(e.g.
water temperature, dissolvedoxygen levels, etc.) in each arealso likely to differ
(KVARNAS, 2001). Theinfluenceofthese conditionson oocyst viability war-
rants furtherresearch. Inananalogous system, muchresearch hassought to de-
tectandevaluateoocystviabilityoftheclosely-related Crypotosporidium parvum
(e.g., CALLetal„2001;K.ATO etal„ 2002;POKORNY etal„ 2002). Unfortu-
nately, the degree to whicheugregarine oocysts areencounteredby dragonflies
inaquatic and/orterrestrialenvironmentsremainsuncertain,andthefactorsin-
fluencing oocyst viabilityandlongevity are stillunknown.
Commonly, digestive-tractparasitesreducethehost’sabilitytoabsorbnutrients
andtoaccumulateandappropriately distributefat(SIVA-JOTHY&PLAISTOW,
1999). During maturationfromteneraltoreproducing adult, odonatesacquire
color andmass critical formate selection, and build fat reserves for sustained
flight andeggproduction (CORDOBA-AGUILAR&CORDERO-RIVERA,
2005). Malesdistributemost oftheirfatinthethorax(ANHOLT etal„ 1991) to
support sustainedflightandmaintainterritories(MARDEN& WAAGE, 1990;
PLAISTOW & SIVA-JOTHY, 1996). Theinitialmoments offlight depend on
carbohydrate oxidationandthentransitiontolipidoxidationifflightissustained
(SCHILDER& MARDEN,2006). SIVA-JOTHY & PLAISTOW(1999)found
thateugregarines reduced fatcontent inpre-reproductive Calopteryxsplendens
xanthostomamales (Zygoptera: Calopterygidae). SCHILDER & MARDEN
(2006) reportedthateugregarines impaired fattyacid oxidationby flightmuscles
in infectedLibellulapulchella males (Anisoptera: Libellulidae). Decreased fat
contentand/or impaired fatoxidationin infectedodonatesare likely toreduce
malefitnessbecausethey hindersustainedflight.
Femaleodonatesdistributemorefatintheabdomenpresumably foreggpro-
duction(ANHOLT etal., 1991). Ifparasitized femaleshavelessfat contentand/
oran impaired fatmetabolism,thenwehypothesized thateggsizes, clutchsizes,
326 J.L.Locklin&D.S. Vodopich
Fig. 3.Eggcircumference (A), total eggcount(B),andclutch size(C)ofE.simplicicollisversusgre-
garineintensity.A;Eachdatapointrepresentsthemeancircumference(mm)ofteneggsfromafemale;
errorbars represent95%Cl. Nocorrelation wasdetected(N=24,r =-0.19,p=0.37).B:Totalegg
countincludes alleggsreleased duringinducedovipositionplusretained eggs foundduringabdomi-
naldissections.No correlation wasdetected(N= 84,r =0.14,p=0.19).C:Clutchsizedatainclude
only femaleswith eggstooviposit. Nocorrelation was detected(N=74,r =0.09,p=0.44).
EugregarineparasitismofErythemissimplicicollis 327
and/orthenumberofeggsproduced wouldbelessamonginfectedfemalesthan
uninfectedfemales.CORDOBA-AGUILAR etah, (2003)founda negative cor-
relationbetweeneugregarine intensity andeggproduction in Calopteryxhaem-
orrhoidalis. CANALES-LAZCANO et al. (2005) also found that eugregarine
infectionreducedeggnumbersinfemaleEnallagmapraevarum. However, wede-
tectedno correlationbetweenparasiteintensityandthe dragonflyeggparameters
measured.
Parasitesoftenhavelifehistory strategies thatdamage orimpairthemorphol-
ogy and/orphysiology oftheirhost.Butquantifyingthefitnesscostsofsuchdam-
age isdifficult because the magnitude of hostcost is determinedby the damage
aparasite causes (S1VA-JOTHY& PLAISTOW, 1999). Thelack of detectable
virulencedescribed inthisstudy maybe due to 1)relatively loweugregarine in-
tensitiesinthepopulation, and/or2) variationofvirulenceassociatedwithindi-
vidualgregarine species.
Thelevelof virulenceahostexperiences may depend onparasite intensity. Eu-
gregarine (order Eugregarinorida) and neogregarine (order Neogregarinorida)
infections, for example, manifestdramatically differentimpacts ontheirhosts-
eugregarines generally do littleharm(RODRIGUEZ et al., 2007) whereasne-
ogregarine infectionsoftensignificantly impact theirhosts negatively (ALTIZ-
ER & OBERHAUSER, 1999; LORD, 2006; BRADLEY& ALTIZER,2005;
LINDSEY etal.,2009). Thedifferencein impact maystemfrom neogregarines
proliferating vegetatively inthe hostwhile eugregarines donot. Specifically, ne-
ogregarines undergo multipleasexual divisions(merogony) afterentering host’s
cellsandtheresulting merozoitesspreadandinfectothertissuesinthathost. Eu-
gregarine intensity, however, depends entirely on thenumberofoocysts ingest-
edbecausethey lack a vegetative reproductive stage.Consequently, eugregarine
intensities tendto be lowerthan neogregarine intensities.RODRIGUEZ et al.
(2007) suggested thatunless parasite intensitiesexceed somethreshold number,
fitnessimpacts inthe hostmaybe negligible. ABRO(1974) reported thateugre-
garine intensities greaterthan 100causedlesionsin thealimentary canalsofin-
fectedZygoptera whichmayhavepermittedentryofpathogens intothehaemo-
coel. Unfortunately foroureffortsto detect fitness costs, intensitieswere lowin
E.simplicicollisfemales(median =2,max =55). Analyzingindividualswithmore
intenseinfectionsmayshowthateugregarines canaffectfitnessofE.simplicicol-
lisfemaleswithrespecttoeggproduction. However,CANALES-LAZCANO et
al.(2005) andSIVA-JOTHY& PLAISTOW(1999)foundthateugregarines were
associatedwithreducedeggnumbersandfatcontent,respectively, indamselflies
withrelatively low intensities.This suggests thatsignificant fitness costs donot
depend exclusively oneugregarine numbers, atleastfor someodonatehostspe-
cies. Moreover, ifintensityrelates directlytofitness costsof E.simplicicollis,then
mostindividualswillnotshowsignsofparasitism duetothenatureofeugregarine
reproduction (no merogony)andtheiraggregated distribution(i.e. a negative bi-
328 J.L. Locklin & D.S. Vodopich
TableII nomialdistribution)across dragon-
Dragonfly species collected atthe Lake Waco Wet- flypopulations. Mostinfectedodo-
land that did not host eugregarineparasites -
nates have low parasite intensities
[* indicatesapreviouslyreportedhost species]
(LOCKLIN&VODOPICH.2010).
FFaammiillyy SSppeecciieess nn Asaconsequence,detectingeffects
ofintenseeugregarine infectionsin
AAeesshhnniiddaaee AAnnaaxxjJuunniiuuss** 2217 naturaldragonfly populations may
MMaalleess 2244
provedifficultbecauserelativelyfew
FFeemmaalleess 33
hosts havehigh intensities.
CCoorrdduulliiiiddaaee EEppiitthheeccaapprriinncceeppss** 11 Parasitevirulence may also de-
MMaalleess 11
FFeemmaalleess 00 pendonthe parasitespecies infect-
ingahost.Forexample. Entamoeba
GGoommpphhiiddaaee AArriiggoommpphhuussssuubbmmeeddiiaannuuss 99
histolytica andE. disparare proto-
MMaalleess 55
FFeemmaalleess 44 zoan parasites that infecthumans.
DDrroommooggoommpphhuussssppoolliiaattuuss 1100 Theseclosely-related congenersare
MMaalleess 55 difficulttodifferentiatemorpholog-
FFeemmaalleess 55
ically (CLARK et al.. 2006), but
GGoommpphhuussmmiilliittaarriiss 1188
MMaalleess 1133 theirvirulencelevelsare significant-
FFeemmaalleess 55 ly different.Theformerkills up to
SSttyylluurruussppllaaggiiaattuuss 22 100,000 people annually whereas
MMaalleess 22 the latter is a commensal (DIA-
FFeemmaalleess 00
MOND & CLARK, 1993; ROB-
LLiibbeelllluulliiddaaee DDyytthheemmiissnniiggrreesscceennss 44 ERTS& JANOVY,2005). Our un-
MMaalleess 44
derstanding of species-level diver-
FFeemmaalleess 00
LLiibbeelllluullaa ccoommaanncchhee 11 sity among the eugregarine fauna
MMaalleess I1 infecting Odonatais progressing.
FFeemmaalleess 00 Severalspecies havebeendescribed
LLiibbeelllluullaa vviibbrraannss 11 fromnineeugregarine generaiden-
MMaalleess 11
FFeemmaalleess 00 tifiedinodonates, although noneof
OOrrtthheemmiissffeerrrruuggiinneeaa 22 the adultdragonfly species thatwe
MMaalleess I1 surveyed inthe current study orin
FFeemmaalleess 11 LOCKLIN& VODOPICH(2010)
PPaannttaallaa hhyymmeennaaeeaa 2266
were hosts identifiedin those de-
MMaalleess 1133
FFeemmaalleess 1133 scriptions. However, ifodonate-in-
PPllaatthheemmiissllyyddiiaa 4455 fecting eugregarines exhibitstrong
MMaalleess 2211 host species- and/or stage-specif-
FFeemmaalleess 2244
TTrraammeeaa llaacceerraattaa** 1177 icity, then many new eugregarine
species await description. Further-
MMaalleess 1122
FFeemmaalleess 55 more, ifvirulencevariesamongeu-
TTrraammeeaa oonnuussttaa** 22 gregarine species andtheirhostspe-
MMaalleess 22 cies, thenconclusionsonthefitness
FFeemmaalleess 00
costs (or lack thereof) in this host