Nordic Society Oikos
Sex Differences in Parasitic Infections among Arthropod Hosts: Is There a Male Bias?
Author(s): Letitia A. D. Sheridan, Robert Poulin, Darren F. Ward and Marlene Zuk
Reviewed work(s):
Source: Oikos, Vol. 88, No. 2 (Feb., 2000), pp. 327-334
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OIKOS 88: 327-334.Copenhagen
2000
in parasiticinfections
Sex differences
hosts:
amongarthropod
is therea male bias?
LetitiaA. D. Sheridan,RobertPoulin,DarrenF. Ward and MarleneZuk
in
Sheridan,L. A. D., Poulin, R., Ward, D. F. and Zuk, M. 2000. Sex differences
parasitic infectionsamong arthropod hosts: is there a male bias? - Oikos 88:
327-334.
A highersusceptibility
to diseases or parasites in males than femalesmay be an
ultimateconsequenceof the different
reproductivestrategiesfavoredby selectionin
the two sexes. At the proximatelevel,the immunosuppressant
effectsof testosterone
in vertebrates
providea mechanismthatcan cause male biases in parasiteinfections.
Invertebrates,
however,lack testosteroneand other steroidhormones.We used a
meta-analysisof published results to investigatewhethersex biases in parasite
infectionsweregenerallyobservedamong arthropodhostsdespitethe absence of the
immune-endocrine
coupling provided by testosterone.Overall, male and female
arthropodsdid not differin prevalenceor intensityof parasite infections.This is
based on an analysisof sex differences
correctedforsample size and, whenpossible,
variabilityin the originaldata. Sex biases in parasiteinfectionwere not more likely
to be observedin certainhost or parasitetaxa, and were not more pronouncedin
experimentalstudiesthan in surveysof naturallyinfectedhosts. Our resultssuggest
that because of the absence of endocrine-immune
interactionsin arthropods,males
are not generallymore prone to parasiteinfectionsthan femalesdespitethe greater
intensity
of sexual selectionactingon males.
L. A. D. Sheridanand R. Poulin (correspondence),
Dept of Zoology, Univ.of Otago,
- D. F.
P.O. Box 56, Dunedin,New Zealand (robert.poulin(stonebow.otago.ac.nz).
Ward,School of Zoology,La Trobe Univ.,Bundoora,Victoria3083, Australia.- M.
Zuk, Dept of Biology,Univ.of California,Riverside,CA 92521, USA.
surveys
havefoundsmallbutconsistent
mostifnotall differences
between
thesexes literature
Ultimately,
male
are theproductof sexualselection
(Clutton-Brock
and biasesin infections
by helminth
and arthropod
paraParker1992,Owensand Thompson1994). In most sitesin birdsand mammals(Poulin1996a,Schalkand
species,malesinvestincostlysecondary
sexualfeatures Forbes 1997).The proximate
mechanism
mostoften
or courtship
whileat the associatedwithmale-biased
displaysto attractfemales,
is the
parasiticinfection
same timecompeting
withothermalesfor immunesuppression
intensely
associatedwithandrogens,
priaccess to females.This resultsin greaterinter-and marilytestosterone,
the hormonesnecessaryfor the
on malesthanfemales, development
intrasexual
selection
pressures
ofmalesexualtraitsandbehavior
(Grosswiththelifeofa malebeingmoresociallyand energet- man 1985,Alexander
and Stimson1988,Schuursand
icallystressful
thanthatof a female.One consequence Verheul1990,Zuk 1990, 1996,Folstad and Karter
ofthismightbe thehigher
mortality
incurred
bymales 1992). In contrast,femaleoestrogensmay actually
in manytaxa (e.g. Promislow1992,Promislow
et al. boosthumoralimmunity
(Grossman1985).Thesehor1992).
mone-mediated
differences
betweenthesexescan proAnotherconsequencemightbe the higherparasite duce males that are relatively
more susceptibleto
infection
levelscommonly
observedin the males of parasiteinfections
thanfemales.In nature,sexualdifmanyvertebrate
speciesrelativeto females.Recent ferences
in susceptibility
to parasites
maybe maskedto
Accepted 19 May 1999
CopyrightC) OIKOS 2000
ISSN 0030-1299
Printedin Ireland - all rightsreserved
OIKOS 88:2 (2000)
327
somedegreeby differences
in exposureresulting
from collectionand our own data sets.Most of the data
sex-specific
behaviors(e.g. see McCurdyet al. 1998). (88% ofthemale-female
comparisons
used)camefrom
Thustheproximate
on suscepti- studiesthatdid not focuson sex biasesin parasitism
effect
ofsexhormones
bilityto parasitesis moreeasilydetectable
in experi- butreported
thesedatanonetheless
fordescriptive
purmentalstudies,whereexposureis controlled,than poses.It is therefore
thatourdata setsuffered
unlikely
amongnaturally
infected
malesand females
of non-signifi(seeSchalk froma problemofunder-representation
and Forbes1997).
cantdifferences.
The bulkof theresearch
Two measuresof parasitism
carriedout thusfaron sex
wereconsideredand
biasesin parasitism
has beenperformed
on vertebrates,recorded
separately
foreachsex:prevalence
(percentage
and almostnothingis knownof thegeneralpatterns of hoststhatare infected)
and intensity
(meannumber
andprocesses
ininvertebrates
(ZukandMcKean1996). ofparasites
perinfected
hosts).To be included,
a study
On the one hand,the operationof sexual selection had to reportprevalence
and/orintensity
of infection
shouldbe the samein invertebrates
as in vertebratesbya parasitespeciesand samplesizesforbothsexesof
and Parker1992),ultimately
(Clutton-Brock
producing a hostspecies.If available,we also recorded
thestandifferent
in malesand females darddeviation
reproductive
strategies
in intensity
forbothmalesand females.
and causingsex biasesin parasiteinfections.
On the Finally,we onlykept studiesin whichthe typeof
otherhand, the proximatemechanism
(experimental
operatingin infection
or natural)was clearlystated.
vertebrates,
i.e.theimmunosuppressive
effects
oftestos- Some studiesprovidedmorethanone comparison
to
terone,is absentin invertebrates.
The relationship
be- thedata set.A totalof 33 studiescontributed
to the
tweensexand parasiteinfections
be less data set(see Appendix1).
maytherefore
likelyto developin invertebrates
(Zuk and McKean
1996).However,othermechanisms
couldproducesex
biasesin parasiteinfections
amonginvertebrates.
For
analysis
instance,
malesmayhave less energyto investin im- Statistical
muneresponses
thanfemalesbecausemalesengagein We treatedeach host-parasite
speciescombination
as
intrasexual
competition
and courtshipof females.It an independent
observation.
Whilephylogenetic
effects
wouldbe important
to quantify
thegeneralpattern
of mayinfluence
sexbiasesin infection
(HarveyandPagel
sex biasesin parasitism
amonginvertebrate
speciesto 1991),it is difficult
to controlsimultaneously
forboth
determine
theexpected
whether
ultimate
effects
of sex- thehostandparasitephylogenies.
Previous
meta-analyual selectionon parasiteinfections
also occurin taxa ses of sex biasesin parasiteinfections
have similarly
thatlacktestosterone
and othersteroid
hormones
(Zuk treatedeach host-parasite
combination
as statistically
and McKean 1996).
independent
(Poulin1996a,Schalkand Forbes1997,
The objectiveof thisstudywas to investigate
the McCurdyet al. 1998).
occurrence
and generaldirection
of sexbiasesin paraofprevalence
Comparisons
and intensity
ofinfection
siteinfections
amongarthropod
species.We performedbetween
thesexeswerecomputed
foreachhost-parasite
a meta-analysis
of published
data on maleand female system
to producestandard
measures
thatareindepeninfection
levelsin whichwe controlled
forsamplesizes dentof samplesize (Hedgesand Olkin1985).Differas well as assessingthe influence
of othervariables. encesin prevalence
werecalculatedas
Theseothervariableswerehostand parasitetaxonomy
andwhether
thehostshadbeennaturally
orexperimenwhereJ 1- [3/(4(Nf+ Nm-2) - 1)]
tallyinfected
by theparasites.We examined
theeffect (pf-Pm)(J),
ofthesevariables
becausesexbiasesinparasitism
might
betweenthe prevalence
in females,
pfp
be morelikelyto developin certainhosttaxainfected The difference
bycertainparasitetaxa,or moreeasilydetected
when and thatin males,PM,is weighedby J, whichis a
correction
forsmallsamplesizes,Nf and Nm.As the
exposureis experimentally
controlled.
totalsamplesize increases,
J approachesone so that
moreweightis givento comparisons
based on many
hostindividuals
(Hedgesand Olkin1985).Thiscorrectionis important
Methods
becauseestimates
of prevalence
are
ofteninfluenced
by host samplesize (Gregoryand
Data collection
Blackburn1991). Using the above formula,we get
positive
comparisons
whenprevalence
is greater
in feWe searchedtheliterature
fordata on fungal,protocomparisons
whenit is greater
in
zoan or metazoaninfections
in females
andmalesfrom males,and negative
differences
in intensity
werecomputed
thesamenaturalpopulationor fromthesameexperi- males.Similarly,
mentalstudy.Specifically,
we searchedall issuesof as
Parasitologyand theJournalof Parasitologyavailable
at the University
of Otago, as well as RP's reprint (If- Im)J/lI
328
OIKOS 88:2 (2000)
in females Amongcomparisons
Again,thedifference
betweentheintensity
of prevalence,
sex differences
(If) and thatin males(IT) is corrected
forsamplesize. weresymmetrically
distributed
aroundzero,withalHere,femaleandmalesamplesizesusedin thecompu- mostas manymale-biaseddifferences
as therewere
tationofJ arethenumbers
ofinfected
hostindividuals,female-biased
ones(Fig. 1). The overallaveragedifferwhereasin comparisonsof prevalencewe used the enceinprevalence
between
thesexeswasonlyabout1%
numbers
of individuals
examined.Also, differences
in and it did notdiffer
fromzero(Table 1). In addition,
intensity
are expressed
as a proportion
of theintensityno sex bias was observedin anyof thesubsetsof the
in females.This procedure
was necessary
becausethe largerdatasetconsidered
here,i.e. sexdifferences
were
in thestudieswe notinfluenced
actualintensities
ofinfection
recorded
or
byeitherhostor parasitetaxonomy,
thehostshad beennaturally
or experimenusedvarygreatly
amongsystems
(seePoulin1996a).In bywhether
a truemeta-analysis,
betweenmeanvalues tallyinfected
differences
(Table 1).
formalesand femalesshouldbe adjustedforthevariin intensity
Sex differences
of infection
showeda
abilityamongindividuals,
i.e. eachdifference
shouldbe slightly
skewedfrequency
distribution;
however,this
dividedby thepooledstandarddeviationof the two resultsfromtwo strongly
male-biasedcomparisons,
groups(Hedgesand Olkin1985).This procedure
was withall othershavingvaluescloseto zero(Fig.2). The
in intensityoverallaveragedifference
inintensity
used forthesmallsubsetof comparisons
between
thesexes
betweenmalesand femalesforwhichstandarddevia- was relatively
verysmall,lessthan1% of theintensity
in females(Table 2). We obtainedsimilarresultsin a
tionswereavailable.
The null hypothesis
(i.e. no sex bias in levelsof separateanalysisusingonlythe 12 comparisons
that
is thatdifferences
in prevalence
infection)
and intensitycouldbe corrected
forthepooledstandard
deviation
of
= - 1.78, t = 1.061,
are symmetrically
arounda meanof zero. the originaldata (mean difference
distributed
two-tailed
t-teststo comparethe P = 0.311).As withcomparisons
We used one-group,
of prevalence,
there
standardized
ofhostor parasitetaxonomy
or modeof
comparisonsto the expectedmean of was no effect
zero.The use of directional
testsinsteadof two-tailed infection
on sex differences
in intensity
of infection
testscould be justifiedgivenour specifichypothesis(Table2).
(Rice and Gaines 1994).Usingone-tailed
testswould
and thuswe reportthe
not affectour conclusions,
resultsof two-tailed
tests.Analyseswereperformed
of prevalenceand Discussion
followingthe log transformation
valuesin thecomputations
of differences
intensity
beIn birdsandmammals,
malesaretypically
moresusceptweensexes;however,untransformed
values are retibleto parasiteinfections
thanfemales(Poulin1996a,
and tables.We presentresultsof
portedin all figures
Schalkand Forbes 1997),an observation
usuallyatanalysesacrosstheentiredata set,as wellas separate
tributedto the immunosuppression
associatedwith
the
analysesforsubsetsofthedatain orderto highlight
testosterone
(Schuursand Verheul1990,Zuk 1990,
if any,of thetypeof infection,
hosttaxoninfluence,
omyand parasitetaxonomy.
20-
Ul)
C
Results
We obtained61 comparisons
of prevalenceand 31
ofintensity
ofinfection
between
malesand
comparisons
females(see Appendix1). The majoritywere from
naturalinfections.
In general,samplesizeswerelarge.
For instance,
totalsamplesize(malesplusfemales)
for
prevalencecomparisonsaveraged1351 (range 44and 337 (range60-1160)
18540)fornaturalinfections
forexperimental
infections.
Samplesizesweresmaller
forintensity
becauseonlyinfected
hosts
comparisons,
wereused,but theywerestillgenerally
good (overall
average= 203). No hosttaxonwas involvedin a disnumber
ofcomparisons.
Withrespect
proportionate
to
parasite taxonomy,however,protozoansand nematodeswerebetterrepresented
in thedata set than
othertaxa (Appendix1).
OIKOS 88:2 (2000)
0
15 -
I=C)
CO
0.
E
0
0
10
o
E
z3 5
0
-65
-55
-45
[i
EL2...22
..
-35
-25
-15
-5
5
15
25
35
45
Difference
inprevalence
distribution
of sex differences
in parasite
Fig. 1. Frequency
corrected
forsamplesize,in 61 host-parasite
prevalence,
systemsinvolving
hosts.Blackcolumns
indicate
malearthropod
biaseddifferences,
and open columnsindicatefemale-biased
differences.
329
data
fortheentire
maleandfemale
hosts.Resultsarepresented
between
inprevalence
ofparasiteinfection
Table 1. Differences
setas wellas forvarioussubsetsof thedata.
Data set
No. comparisons
(no. hostspecies)
All data
61 (46)
Typeof infection
Experimental
11 (8)
Natural
Hosttaxon
Crustaceans
50 (39)
Others
7 (7)
Decapods
Ticks
Insects
9 (9)
5 (2)
Orthopterans
11 (8)
Dipterans
14 (13)
Blattarians
Coleopterans
Odonates
Parasitetaxon
Protozoans
Fungi
Helminths
Nematodes
Others
Arthropods
Isopods
Mites
8 (4)
6 (2)
1 (1)
(SD)
Mean femaleminusmaleprevalence
-1.29 (15.58)
t*
P
0.647 0.520
0.19 (17.93)
0.035
0.973
2.28 (7.65)
0.892
0.398
2.57 (8.99)
0.639
0.558
1.626
0.135
1.074
0.302
0.739
-1.62 (15.20)
- 5.74 (11.76)
-12.09 (24.67)
-1.79 (13.51)
1.87(4.56)
4.58 (15.97)
0.10 (-)
0.752 0.456
1.291 0.244
0.376 0.718
1.003 0.362
26 (19)
-0.81 (12.23)
0.337
16 (11)
-6.73 (20.06)
1.342 0.200
2 (2)
7 (7)
7 (7)
3 (3)
19.12(29.85)
-7.81 (11.09)
4.56 (6.52)
11.46(16.86)
0.906 0.531
1.863
0.112
1.850
0.114
1.178 0.360
* Fromone-group,
two-tailed
tests.
1996, Folstad and Karter1992,Zuk and McKean significant
sexualbias had an effect
sizesimilarto that
thepossible in vertebrates
1996).To date,no one had investigated
been foundin arthropodhosts.The
ofa similar
amongarthropods resultspresented
existence
generalpattern
hereare therefore
a good indication
whichlack testosterone
and thatthereis no consistent
or otherinvertebrates,
sexbiasin parasiteinfections
othersteroidhormones.The resultsof the present amongarthropod
hostscomparable
towhatis observed
meta-analysis
indicatethatthereis no generalsexbias in mammals
or birds.
inparasiteinfection
Thisabsenceof
amongarthropods.
In
of hostor parasitetaxonomy.
bias is independent
20
fromthedata of
bias emerged
addition,no consistent
in whichsexualdifferences
in
experimental
infections,
to parasitesshouldbe easierto detect.
susceptibility
15
In meta-analyses
of thisnature,it is oftentempting en
0
03
effectson various
to blame the lack of significant
sourcesof error.For instance,the data on natural Cu
infections
camefromhoststhathad beensampledat E
different
timesof theyear,and parasiteinfections
can 0
show seasonalfluctuations.
Also, most studiescon- .0
in bothprevalence
tributed
and intensity E
comparisons
ofinfection,
suchthatourtwodata setswerenottruly :3 5can
independent
(Appendix1). Theseand otherfactors
generate
noisein thedata setor bias theanalysisone
wayor theother.However,theapproachusedhereis
0.
ofsex-biased
thesameas thatusedin surveys
infections
-13 -12 -11 -10 -9 -8 -7 -6 -5 -4 -3 -2 -1 0 1
in vertebrates,
fromsimiwhereclearpatterns
emerged
Difference
inintensity
lar typesof data (Poulin1996a,McCurdyet al. 1998).
The averagesex differences
in infection
levelsbetween Fig. 2. Frequencydistributionof sex differencesin parasite
correctedforsamplesize,in 31 host-parasitesystems
male and femalemammalsor birdsreportedin the intensity,
are expressedas a
than involvingarthropodhosts.The differences
literature
(Poulin1996a)can be 3-4 timesgreater
in females.Black columnsindicate
proportionof the intensity
the ones presentedhere for male and female male-biaseddifferences,
and open columnsindicatefemale-biOur analysishad the powerto detecta ased differences.
arthropods.
330
OIKOS 88:2 (2000)
as a proportion
oftheintensity
Table2. Differences
in intensity
ofparasiteinfection
between
maleandfemalehosts,expressed
in females.
Resultsare presented
fortheentiredata setas wellas forvarioussubsetsof thedata.
Data set
No. comparisons
(no. hostspecies)
Mean femaleminusmaleintensity
(SD)
t
All data
31 (21)
-0.50 (2.38)
1.176 0.249
Typeof infection
Experimental 8 (5)
Natural
23 (17)
-1.82 (4.59)
-0.05 (0.48)
1.118 0.300
0.488 0.631
5 (5)
5 (2)
-0.63 (1.54)
-2.34 (5.81)
0.913 0.413
0.900 0.419
7 (5)
4 (3)
7 (3)
3 (3)
-0.33 (0.58)
-0.04 (0.57)
0.21 (0.39)
0.05(0.26)
1.483
0.138
1.434
0.335
10 (7)
-1.27 (4.05)
0.988 0.349
13 (8)
5 (5)
3 (3)
-0.04 (0.53)
-0.55 (1.59)
0.09 (0.04)
0.257 0.801
0.771 0.484
3.483 0.073
Host taxon
Crustaceans
Ticks
Insects
Orthopterans
Blattarians
Coleopterans
Others
Parasitetaxon
Protozoans
Helminths
Nematodes
Others
Arthropods
P
0.189
0.899
0.202
0.770
* Fromone-group,
-tests.
two-tailed
Experimental
studiesshouldbe moresensitive
than
The absenceof a universal
and consistent
sex bias
to intrinsic
in susceptibility
differences
to
does not mean thatthereis no bias in any specific fieldsurveys
host-parasite
system.Significant
differences
between parasitesbetweenmales and females,if theseexist,
in exposure.
Commales and femalesin prevalenceand/orintensity
of becausetheycontrolfordifferences
in
bined
the
the
of
meta-analysis,
results
experimental
werereported
infection
forsome(9 outof 24 comparitestwas reported)
of the studiesdid notsuggestanyclearsexbias. Takenindisons forwhicha statistical
includedin our data set. In somecases vidually,however,theycan provideclear patterns
comparisons
hostspecies.Forexample,
andJakobWedekind
(six), males were more parasitizedthan females, within
whereasthe oppositewas truein othercomparisons sen (1998)foundthatmalecopepodshad significantly
and intensity
of infection
thanfeandJakob- higherprevalence
(three).Theauthorsofonlyone(Wedekind
in
males
experimental
with
infections
the
larval
cestode
sen1998)ofthesestudiesattributed
differtheobserved
solidus.
Their
Schistocephalus
that
the
study
suggests
ence to sexualselection;otherauthorseitherdid not
immune
of
is
response
males
somehow
weaker
than
or attributed
it to ecological
discussthe difference
Theseresults
andinterpretations
mirror
causes.It maybe thatthereexistsno generalpattern thatoffemales.
thefindings
in
of otherstudieson bacterialinfections
but that the specificbiologyof
amongarthropods,
arthropods
(e.g. Gray1998).Sincethemajority
of the
hostsand parasites
mayproducebiasesonewayor the
studiesincludedin our data set involvednaturally
otherin somehost-parasite
This
speciescombinations.
infected
to usean experimenhosts,itwillbe important
withthegenerally
interpretation
is notconsistent
more
tal approachin moreinvertebrate-parasite
systems
to
intensesexualselectionpressure
actingon malesthan elucidatetheinfluence
of sex on infection
levels.
morestressful
on femalesand producing
reproductive In addition,therelatively
simpleimmunesystem
of
in males (Clutton-Brock
and Parker1992, arthropods
strategies
andotherinvertebrates
(Loker1994)should
Owens and Thompson1994). One factorthatmay be amenableto studiesofsexdifferences
initsfunctionobscuresex differences
in susceptibility
to parasites ing.All our conclusions
are strictly
about sex differin mostinvertebrates,
could be size dimorphism:
fe- encesin actualparasiticinfections,
and notaboutsex
malesareoftenlargerthanmalesbecauseoffecundity-differences
in immuneresponse.It maybe thatmale
drivenselection(see Poulin 1996b for review).The and femaleinvertebrates
investdifferentially
in defense
largersizeoffemales
couldresultingreater
exposure
to againstpathogens
becauseofdifferences
in sexualselecandprovidemoreresources
parasites
to incoming
para- tion,butthatthisdifferential
investment
is notreflected
a highersusceptibility
of malesto in termsof parasiteinfection
sites,thusnegating
to thesamedegreeas in
infection.
This maybe a commonphenomenon,
since vertebrates
becauseof the greatersimplicity
of the
positivecorrelations
between
hostsizeand intensity
of invertebrate
immunesystem.
ofhostsex,werereported
in many Takenas a whole,ourresults
infection,
regardless
suggest
thattheremay
studiesthatwe surveyed.
be a difference
betweenvertebrates
and arthropods
GIKOS 88:2 (2000)
331
withrespectto some of the consequences
of sexual Kuris,A. M., Poinar,G. 0. and Hess, R. T. 1980. Post-larval
mortalityof the endoparasiticisopod castratorPortunion
selection.
We shouldexpectbasic differences
between
conformis(Epicaridea: Entoniscidae) in the shore crab,
thesexesin terms
ofbasicparameters
suchas mortality Hemigrapsusoregonensis,with a descriptionof the host
rates,in bothvertebrates
and invertebrates.
However,
response.- Parasitology80: 211-232.
the potentialforendocrine-immune
interactions
pro- Lackie, J. M. 1972. The course of infectionand growthof
dubius(Acanthocephala)in the intermediate
Moniliformis
in a
videsa meansforselectionto act in vertebrates
host Periplanetaamericana.- Parasitology64: 95-106.
way thatit mightnot be able to achievein inverte- Loker,E. S. 1994. On beinga parasitein an invertebrate
host:
lackthenegative
feedback
brates.Invertebrates
system a shortsurvivalcourse. - J. Parasitol. 80: 728-747.
D. G., Shutler,D., Mullie, A. and Forbes, M. R.
betweenthe immunesystemand the expressionof McCurdy,
1998. Sex-biased parasitismof avian hosts: relationsto
sexualfeatures
and behaviorprovidedby testosterone blood parasite taxon and mating system.- Oikos 82:
invertebrates.
Thus,higher
levelsofparasitic
infections 303-312.
butnotso Moloo, S. K., Steiger,R. F. and Brun,R. 1973. Trypanosome
maybe a generalcostformalevertebrates
infectionratesin Glossinaswynnertoni
and G. pallidipesin
generalformaleinvertebrates.
Ikoma, Musoma District,Tanzania. - Parasitology66:
- We thankLien Luong forallowingus to
Acknowledgements
use some of her unpublisheddata.
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Appendix1. Data on femaleand male infectionlevelsused in the analyses.
Host taxon
Parasite taxon
Prevalenceof infection
decapod
nematomorph
decapod
trematode
decapod
isopod
decapod
isopod
decapod
isopod
decapod
isopod
decapod
isopod
decapod
isopod
decapod
isopod
amphipod
acanthocephalan
cestode
amphipod
amphipod
trematode
amphipod
mite
copepod
protozoan
copepod
cestode
isopod
acanthocephalan
tick
protozoan
tick
protozoan
tick
protozoan
tick
protozoan
tick
protozoan
orthopteran protozoan
orthopteran protozoan
orthopteran protozoan
orthopteran protozoan
orthopteran protozoan
orthopteran protozoan
orthopteran protozoan
orthopteran protozoan
orthopteran nematode
orthopteran nematode
orthopteran mite
blattarian
protozoan
blattarian
protozoan
blattarian
protozoan
blattarian
protozoan
blattarian
nematode
blattarian
nematode
blattarian
nematode
blattarian
nematode
coleopteran
nematode
OIKOS 88:2 (2000)
Type of study*
Female infection
Male infection
Sample size
Source**
N
N
N
N
N
N
N
N
N
N
N
N
N
N
E
N
E
E
E
E
E
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
1.12
57.14
62.85
35.20
0.28
69.90
33.33
0.92
1.47
2.70
3.50
46.45
62.32
30.14
40.00
27.00
38.00
11.63
88.20
10.00
31.29
56.25
17.07
46.62
13.64
38.71
53.33
36.28
51.72
15.39
15.39
83.33
27.27
90.91
45.46
31.82
54.17
68.97
87.50
97.73
19.20
1.84
67.85
46.15
33.90
0.30
61.15
26.67
1.43
2.33
4.16
3.90
58.85
58.86
30.56
70.00
26.10
26.80
1.51
91.40
20.00
26.70
66.67
48.88
51.39
23.08
44.00
57.90
30.00
53.57
77.42
57.58
52.00
21.88
96.88
46.88
25.00
87.10
61.11
79.50
100.00
16.60
2500
647
471
4327
18540
2868
51
397
333
4451
870
940
1183
765
182
5340
500
944
138
60
1160
58
264
349
83
87
64
132
57
44
46
49
76
76
76
76
79
65
178
76
156
1
2
3
4
5
6
7
7
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
21
20
22
22
22
22
20
20
22
23
23
23
23
22
22
24
23
25
333
Appendix1. (Continued)
Source**
Hosttaxon
Parasitetaxon
Typeof study* Femaleinfection Male infection Samplesizet
coleopteran
coleopteran
coleopteran
coleopteran
coleopteran
dipteran
dipteran
dipteran
dipteran
dipteran
dipteran
dipteran
dipteran
dipteran
dipteran
nematode
nematode
nematode
nematode
nematode
protozoan
protozoan
protozoan
protozoan
protozoan
protozoan
protozoan
protozoan
fungus
fungus
N
N
N
N
N
E
E
E
N
N
N
E
E
N
N
2.50
0.50
3.80
3.80
39.20
52.10
49.30
72.05
9.10
5.97
16.90
47.85
4.20
73.00
80.00
7.60
0.40
2.20
0.80
30.20
40.95
61.80
34.50
9.50
4.23
14.10
65.05
4.00
32.60
82.00
156
1214
1214
1214
1214
149
141
148
623
394
6344
142
146
176
100
25
25
25
25
25
26
26
26
27
28
27
26
26
29
29
dipteran
dipteran
dipteran
odonate
nematode
nematode
nematode
mite
N
N
N
N
21.68
1.85
6.23
98.20
19.86
2.08
4.09
98.10
1347
570
4569
1847
30
30
30
31
of infection
Intensity
N
trematode
decapod
N
decapod
isopod
N
decapod
isopod
E
copepod
cestode
acanthocephalan N
isopod
E
tick
protozoan
E
protozoan
tick
protozoan
E
tick
E
tick
protozoan
protozoan
E
tick
N
orthopteran protozoan
N
orthopteran protozoan
N
orthopteran protozoan
N
orthopteran protozoan
N
orthopteran protozoan
N
orthopteran nematode
N
orthopteran nematode
N
blattarian nematode
N
blattarian nematode
N
blattarian nematode
blattarian acanthocephalan E
N
coleopteran nematode
N
coleopteran nematode
N
coleopteran nematode
N
coleopteran nematode
N
coleopteran nematode
N
coleopteran nematode
E
coleopteran cestode
N
nematode
dipteran
N
nematode
dipteran
N
mite
odonate
2.90
1.55
1.08
0.50
3.39
1.12
21.45
3.98
17.10
1.67
2.32
10.68
8.98
2.48
19.67
7.00
12.00
1.71
5.10
1.97
12.36
17.50
1.00
3.00
6.90
5.20
6.50
2.09
1.91
2.21
35.60
3.10
1.38
1.04
2.20
2.85
15.51
9.20
2.08
14.43
2.00
3.92
3.07
15.63
3.43
17.82
14.63
15.26
2.32
3.80
1.94
7.10
11.40
1.00
1.00
3.00
8.10
2.70
1.84
2.38
1.62
31.40
412
250
54
81
1417
63
338
162
124
9
35
46
35
30
37
26
21
53
148
42
141
420
28
5
37
28
8
120
22
279
1813
dipteran
nematode
N
2.33
3.36
799
30
2
3
5
13
14
16
19
15
17
18
22
22
22
22
20
20
20
22
24
22
32
25
25
25
25
25
25
33
30
30
31
* E, experimental
N, naturalinfection.
infection;
forintensity,
totalnumber
ofinfected
hostsin naturalinfections,
or total
ofhostsexamined;
totalnumber
t For prevalence,
in experimental
number
of hostsexposedto infection
studies.
**Sources:1, Born1967;2, Stromberg
et al. 1978;3, Kuriset al. 1980;4, van Wyk1982;5, Field 1969;6, Beck 1979;7,
Wenner1978;8, Ward1986;9, Stark1965;10,Thomaset al. 1995;11,Kitron1980;12,Wickstead
and
1963;13,Wedekind
etal. 1973;16,Youngetal. 1975;17,Youngetal. 1980;18,Purnell
etal. 1975;
Jakobsen
1973;15,Purnell
1998;14,Seidenberg
19,Irvinetal. 1981;20,LuongandZuk unpubl.;21,Zuk 1987;22,Wardetal. 1998;23,Tsai andCahill1970;24,Dobrovolny
andAckert1934;25,Fincher
et al. 1969;26,Moloo et al. 1993;27,Moloo et al. 1973;28,Rogerset al. 1972;29,Schleinetal.
1985;30,Welch1959;31,Andresand Cordero1998;32,Lackie1972;33,Keymer1982.
334
OIKOS 88:2 (2000)