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Sex Differences in Parasitic Infections among 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 Published by: Wiley-Blackwell on behalf of Nordic Society Oikos Stable URL: http://www.jstor.org/stable/3547028 . Accessed: 21/08/2012 12:51

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http://www.jstor.org OIKOS 88: 327-334.Copenhagen 2000

Sex differencesin parasiticinfections among arthropod hosts: is therea male bias?

Letitia A. D. Sheridan,Robert Poulin, Darren F. Ward and MarleneZuk

Sheridan,L. A. D., Poulin, R., Ward, D. F. and Zuk, M. 2000. Sex differencesin 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 ultimateconsequence of the differentreproductive strategies favored by selectionin the two sexes. At the proximatelevel, the immunosuppressanteffects of testosterone in vertebratesprovide a mechanismthat can cause male biases in parasiteinfections. Invertebrates,however, lack testosteroneand other steroidhormones. We used a meta-analysisof published results to investigatewhether sex biases in parasite infectionswere generally observed among arthropodhosts despite the absence of the immune-endocrinecoupling provided by testosterone.Overall, male and female arthropodsdid not differin prevalenceor intensityof parasite infections.This is based on an analysisof sex differencescorrected for sample size and, whenpossible, variabilityin the originaldata. Sex biases in parasiteinfection were not more likely to be observedin certainhost or parasite taxa, and were not more pronouncedin experimentalstudies than in surveysof naturallyinfected hosts. Our resultssuggest that because of the absence of endocrine-immuneinteractions in ,males are not generallymore prone to parasiteinfections than femalesdespite the greater intensityof sexual selectionacting on males.

L. A. D. Sheridanand R. Poulin (correspondence),Dept of Zoology, Univ.of Otago, P.O. Box 56, Dunedin,New Zealand (robert.poulin(stonebow.otago.ac.nz).- D. F. Ward,School of Zoology,La Trobe Univ.,Bundoora, Victoria 3083, Australia.- M. Zuk, Dept of Biology,Univ. of California,Riverside, CA 92521, USA.

Ultimately,most if not all differencesbetween the sexes literaturesurveys have found small but consistent male are theproduct of sexualselection (Clutton-Brock and biasesin infectionsby helminthand arthropodpara- Parker1992, Owens and Thompson1994). In most sitesin birdsand mammals(Poulin 1996a, Schalk and species,males invest in costlysecondary sexual features Forbes 1997). The proximatemechanism most often or courtshipdisplays to attractfemales, while at the associatedwith male-biased parasitic infection is the same timecompeting intensely with other males for immunesuppression associated with androgens, pri- access to females.This resultsin greaterinter- and marilytestosterone, the hormonesnecessary for the intrasexualselection pressures on malesthan females, developmentof malesexual traits and behavior(Gross- withthe life of a malebeing more socially and energet- man 1985,Alexander and Stimson1988, Schuurs and icallystressful than that of a female.One consequence Verheul1990, Zuk 1990, 1996, Folstad and Karter of thismight be thehigher mortality incurred by males 1992). In contrast,female oestrogens may actually in manytaxa (e.g. Promislow1992, Promislow et al. boosthumoral immunity (Grossman 1985). These hor- 1992). mone-mediateddifferences between the sexes can pro- Anotherconsequence might be the higherparasite duce males that are relativelymore susceptibleto infectionlevels commonly observed in the males of parasiteinfections than females. In nature,sexual dif- many vertebratespecies relative to females.Recent ferencesin susceptibilityto parasites may be maskedto

Accepted 19 May 1999 CopyrightC) OIKOS 2000 ISSN 0030-1299 Printedin Ireland - all rightsreserved

OIKOS 88:2 (2000) 327 somedegree by differencesin exposureresulting from collectionand our own data sets. Most of the data sex-specificbehaviors (e.g. see McCurdyet al. 1998). (88% of themale-female comparisons used) came from Thusthe proximate effect of sex hormones on suscepti- studiesthat did not focuson sex biasesin bilityto parasitesis moreeasily detectable in experi- butreported these data nonethelessfor descriptive pur- mentalstudies, where exposure is controlled,than poses.It is thereforeunlikely that our data setsuffered amongnaturally infected males and females(see Schalk froma problemof under-representationof non-signifi- and Forbes1997). cantdifferences. The bulkof theresearch carried out thusfar on sex Two measuresof parasitismwere consideredand biasesin parasitismhas beenperformed on vertebrates,recorded separately for each sex: prevalence (percentage and almostnothing is knownof thegeneral patterns of hoststhat are infected)and intensity(mean number and processesin invertebrates(Zuk and McKean1996). ofparasites per infected hosts). To be included,a study On the one hand, the operationof sexual selection had to reportprevalence and/or intensity of infection shouldbe the same in invertebratesas in vertebratesby a parasitespecies and samplesizes for both sexes of (Clutton-Brockand Parker1992), ultimately producing a hostspecies. If available,we also recordedthe stan- differentreproductive strategies in malesand females darddeviation in intensityfor both males and females. and causingsex biasesin parasiteinfections. On the Finally,we only kept studiesin whichthe typeof otherhand, the proximatemechanism operating in infection(experimental or natural)was clearlystated. vertebrates,i.e. theimmunosuppressive effects of testos- Some studiesprovided more than one comparisonto terone,is absentin invertebrates.The relationshipbe- the data set. A totalof 33 studiescontributed to the tweensex and parasiteinfections may therefore be less data set(see Appendix1). likelyto developin invertebrates(Zuk and McKean 1996).However, other mechanisms could produce sex biasesin parasiteinfections among invertebrates. For instance,males may have less energyto investin im- Statisticalanalysis muneresponses than females because males engage in We treatedeach host-parasitespecies combination as intrasexualcompetition and courtshipof females.It an independentobservation. While phylogenetic effects wouldbe importantto quantifythe general pattern of mayinfluence sex biases in infection(Harvey and Pagel sex biasesin parasitismamong invertebrate species to 1991),it is difficultto controlsimultaneously for both determinewhether the expected ultimate effects of sex- thehost and parasite phylogenies. Previous meta-analy- ual selectionon parasiteinfections also occurin taxa ses of sex biasesin parasiteinfections have similarly thatlack testosterone and othersteroid hormones (Zuk treatedeach host-parasitecombination as statistically and McKean 1996). independent(Poulin 1996a,Schalk and Forbes 1997, The objectiveof this studywas to investigatethe McCurdyet al. 1998). occurrenceand generaldirection of sex biasesin para- Comparisonsof prevalence and intensityof infection siteinfections among arthropod species. We performedbetween the sexes were computed for each host-parasite a meta-analysisof publisheddata on maleand female systemto producestandard measures that are indepen- infectionlevels in whichwe controlledfor sample sizes dentof samplesize (Hedgesand Olkin 1985).Differ- as well as assessingthe influenceof othervariables. encesin prevalencewere calculated as Theseother variables were host and parasitetaxonomy andwhether the hosts had beennaturally or experimen- where J 1 - [3/(4(Nf+ Nm -2) - tallyinfected by theparasites. We examinedthe effect (pf-Pm)(J), 1)] ofthese variables because sex biases in parasitism might be morelikely to developin certainhost taxa infected The differencebetween the prevalencein females,pfp by certainparasite taxa, or moreeasily detected when and thatin males,PM, is weighedby J, whichis a exposureis experimentallycontrolled. correctionfor small sample sizes, Nf and Nm.As the totalsample size increases,J approachesone so that moreweight is givento comparisonsbased on many hostindividuals (Hedges and Olkin1985). This correc- Methods tionis importantbecause estimates of prevalenceare ofteninfluenced by host samplesize (Gregoryand Data collection Blackburn1991). Using the above formula,we get We searchedthe literature for data on fungal,proto- positivecomparisons when prevalence is greaterin fe- zoan or metazoaninfections in femalesand malesfrom males,and negativecomparisons when it is greaterin thesame natural population or fromthe same experi- males.Similarly, differences in intensity were computed mentalstudy. Specifically, we searchedall issues of as Parasitologyand theJournal of Parasitologyavailable at the Universityof Otago, as well as RP's reprint (If- Im)J/lI

328 OIKOS 88:2 (2000) Again,the difference between the intensity in females Amongcomparisons of prevalence,sex differences (If) and thatin males(IT) is correctedfor sample size. weresymmetrically distributed around zero, withal- Here,female and malesample sizes used in thecompu- most as manymale-biased differences as therewere tationof J arethe numbers of infected host individuals, female-biasedones (Fig. 1). The overallaverage differ- whereasin comparisonsof prevalencewe used the encein prevalence between the sexes was only about 1% numbersof individualsexamined. Also, differencesin and it did not differfrom zero (Table 1). In addition, intensityare expressedas a proportionof theintensity no sex bias was observedin anyof thesubsets of the in females.This procedurewas necessarybecause the largerdata setconsidered here, i.e. sexdifferences were actualintensities of infection recorded in thestudies we notinfluenced by eitherhost or parasitetaxonomy, or usedvary greatly among systems (see Poulin1996a). In by whetherthe hosts had beennaturally or experimen- a truemeta-analysis, differences between mean values tallyinfected (Table 1). formales and femalesshould be adjustedfor the vari- Sex differencesin intensityof infectionshowed a abilityamong individuals, i.e. eachdifference should be slightlyskewed frequency distribution; however, this dividedby the pooled standarddeviation of the two resultsfrom two stronglymale-biased comparisons, groups(Hedges and Olkin1985). This procedurewas withall othershaving values close to zero(Fig. 2). The used forthe smallsubset of comparisonsin intensityoverall average difference in intensity between the sexes betweenmales and femalesfor which standard devia- was relativelyvery small, less than 1% of theintensity tionswere available. in females(Table 2). We obtainedsimilar results in a The null hypothesis(i.e. no sex bias in levelsof separateanalysis using only the 12 comparisonsthat infection)is thatdifferences in prevalence and intensitycould be correctedfor the pooled standard deviation of are symmetricallydistributed around a meanof zero. the originaldata (mean difference= - 1.78, t = 1.061, We used one-group,two-tailed t-tests to comparethe P = 0.311). As withcomparisons of prevalence,there standardizedcomparisons to the expectedmean of was no effectof hostor parasitetaxonomy or modeof zero.The use of directionaltests instead of two-tailed infectionon sex differencesin intensityof infection testscould be justifiedgiven our specifichypothesis (Table 2). (Rice and Gaines 1994).Using one-tailed tests would not affectour conclusions,and thus we reportthe resultsof two-tailedtests. Analyses were performed followingthe log transformationof prevalenceand Discussion intensityvalues in thecomputations of differencesbe- In birdsand mammals, males are typically more suscep- tweensexes; however,untransformed values are re- tibleto parasiteinfections than females (Poulin 1996a, portedin all figuresand tables.We presentresults of Schalkand Forbes 1997),an observationusually at- analysesacross the entire data set,as wellas separate tributedto the immunosuppressionassociated with analysesfor subsets of the data in orderto highlightthe testosterone(Schuurs and Verheul1990, Zuk 1990, influence,if any,of thetype of infection,host taxon- omyand parasitetaxonomy. 20-

Ul) C 15 - 0 I=C) Results CO 0. E We obtained61 comparisonsof prevalenceand 31 0 of ofinfection between males and o10 comparisons intensity 0 females(see Appendix1). The majoritywere from naturalinfections. In general,sample sizes were large. E For instance,total sample size (males plus females) for z3 5 prevalencecomparisons averaged 1351 (range 44- 18540)for natural infections and 337 (range60-1160) forexperimental infections. Sample sizes were smaller 0 forintensity comparisons, because only infected hosts .. [i -65 EL2...22 -55 -45 -35 -25 -15 -5 5 15 25 35 45 wereused, but theywere still generally good (overall average= 203). No hosttaxon was involvedin a dis- Differencein prevalence proportionatenumber of comparisons.With respect to Fig. 1. Frequencydistribution of sex differencesin parasite parasite ,however, protozoans and ne- prevalence,corrected for sample size, in 61 host-parasitesys- temsinvolving arthropod hosts. Black columns indicate male- matodeswere better represented in the data set than biaseddifferences, and open columnsindicate female-biased othertaxa (Appendix1). differences.

OIKOS 88:2 (2000) 329 Table 1. Differencesin prevalenceof parasite infection between male and femalehosts. Results are presented for the entire data setas wellas forvarious subsets of thedata. Data set No. comparisons(no. hostspecies) Mean femaleminus male prevalence (SD) t* P All data 61 (46) -1.29 (15.58) 0.647 0.520 Typeof infection Experimental 11 (8) 0.19 (17.93) 0.035 0.973 Natural 50 (39) -1.62 (15.20) 0.752 0.456 Host taxon Decapods 9 (9) 2.28 (7.65) 0.892 0.398 Others 7 (7) - 5.74 (11.76) 1.291 0.244 Ticks 5 (2) 2.57 (8.99) 0.639 0.558 Insects Orthopterans 11 (8) -12.09 (24.67) 1.626 0.135 Blattarians 8 (4) -1.79 (13.51) 0.376 0.718 Coleopterans 6 (2) 1.87(4.56) 1.003 0.362 Dipterans 14 (13) 4.58 (15.97) 1.074 0.302 Odonates 1 (1) 0.10 (-) Parasitetaxon Protozoans 26 (19) -0.81 (12.23) 0.337 0.739 Fungi 2 (2) 19.12(29.85) 0.906 0.531 Helminths Nematodes 16 (11) -6.73 (20.06) 1.342 0.200 Others 7 (7) -7.81 (11.09) 1.863 0.112 Arthropods Isopods 7 (7) 4.56 (6.52) 1.850 0.114 Mites 3 (3) 11.46(16.86) 1.178 0.360 * Fromone-group, two-tailed tests.

1996, Folstad and Karter 1992, Zuk and McKean significantsexual bias had an effectsize similar to that 1996).To date,no one had investigatedthe possible in vertebratesbeen foundin arthropodhosts. The existenceof a similargeneral pattern among arthropods resultspresented here are thereforea good indication or otherinvertebrates, which lack testosteroneand thatthere is no consistentsex bias in parasiteinfections othersteroid hormones. The resultsof the present amongarthropod hosts comparable to whatis observed meta-analysisindicate that there is no generalsex bias in mammalsor birds. in parasiteinfection among arthropods. This absence of bias is independentof hostor parasitetaxonomy. In 20 addition,no consistentbias emergedfrom the data of experimentalinfections, in whichsexual differences in susceptibilityto parasites should be easierto detect. en 15 In meta-analysesof thisnature, it is oftentempting 0 to blame the lack of significanteffects on various 03 sourcesof error.For instance,the data on natural Cu infectionscame fromhosts that had been sampledat E differenttimes of theyear, and parasiteinfections can 0 show seasonal fluctuations.Also, most studiescon- .0 tributedcomparisons in bothprevalence and intensity E of infection,such that our two data setswere not truly :3 5- independent(Appendix 1). Theseand otherfactors can generatenoise in thedata set or bias theanalysis one wayor theother. However, the approach used hereis 0. thesame as thatused in surveysof sex-biased infections -13 -12 -11 -10 -9 -8 -7 -6 -5 -4 -3 -2 -1 0 1 in vertebrates,where clear patterns emerged from simi- lar typesof data (Poulin1996a, McCurdy et al. 1998). Differencein intensity The averagesex differencesin infection levels between Fig. 2. Frequencydistribution of sex differencesin parasite male and femalemammals or birdsreported in the intensity,corrected for sample size, in 31 host-parasitesystems literature(Poulin 1996a) can be 3-4 timesgreater than involvingarthropod hosts. The differencesare expressedas a proportionof the intensityin females.Black columnsindicate the ones presentedhere for male and female male-biaseddifferences, and open columnsindicate female-bi- arthropods.Our analysishad the powerto detecta ased differences.

330 OIKOS 88:2 (2000) Table2. Differencesin intensityof parasiteinfection between male and femalehosts, expressed as a proportionof the intensity in females.Results are presentedfor the entire data setas wellas forvarious subsets of thedata.

Data set No. comparisons(no. hostspecies) Mean femaleminus male intensity (SD) t P All data 31 (21) -0.50 (2.38) 1.176 0.249 Typeof infection Experimental 8 (5) -1.82 (4.59) 1.118 0.300 Natural 23 (17) -0.05 (0.48) 0.488 0.631 Host taxon Crustaceans 5 (5) -0.63 (1.54) 0.913 0.413 Ticks 5 (2) -2.34 (5.81) 0.900 0.419 Insects Orthopterans 7 (5) -0.33 (0.58) 1.483 0.189 Blattarians 4 (3) -0.04 (0.57) 0.138 0.899 Coleopterans 7 (3) 0.21 (0.39) 1.434 0.202 Others 3 (3) 0.05 (0.26) 0.335 0.770 Parasitetaxon Protozoans 10 (7) -1.27 (4.05) 0.988 0.349 Helminths Nematodes 13 (8) -0.04 (0.53) 0.257 0.801 Others 5 (5) -0.55 (1.59) 0.771 0.484 Arthropods 3 (3) 0.09 (0.04) 3.483 0.073 * Fromone-group, two-tailed -tests.

The absenceof a universaland consistentsex bias Experimentalstudies should be moresensitive than does not mean thatthere is no bias in any specific fieldsurveys to intrinsicdifferences in susceptibility to host-parasitesystem. Significant differences between parasitesbetween males and females,if theseexist, males and femalesin prevalenceand/or intensity of becausethey control for differences in exposure. Com- infectionwere reported for some (9 out of 24 compari- binedin themeta-analysis, the results of experimental sons forwhich a statisticaltest was reported)of the studiesdid not suggestany clear sex bias. Takenindi- comparisonsincluded in our data set. In some cases vidually,however, they can provideclear patterns (six), males were more parasitizedthan females, withinhost species. For example,Wedekind and Jakob- whereasthe oppositewas truein othercomparisons sen (1998) foundthat male had significantly (three).The authorsof only one (Wedekindand Jakob- higherprevalence and intensityof infectionthan fe- sen 1998)of these studies attributed the observed differ- malesin experimentalinfections with the larval cestode ence to sexualselection; other authors either did not Schistocephalussolidus. Their study suggeststhat the discussthe differenceor attributedit to ecological immuneresponse of males is somehowweaker than causes.It maybe thatthere exists no generalpattern thatof females. These results and interpretations mirror thefindings of otherstudies on bacterialinfections in among arthropods,but that the specificbiology of arthropods(e.g. Gray1998). Since the majority of the hostsand parasitesmay produce biases one wayor the studiesincluded in our data set involvednaturally otherin somehost-parasite species combinations. This infectedhosts, it will be importantto use an experimen- interpretationis not consistent with the generally more tal approachin moreinvertebrate-parasite systems to intensesexual selection pressure acting on malesthan elucidatethe influence of sex on infectionlevels. on femalesand producingmore stressful reproductive In addition,the relatively simple immune system of strategiesin males (Clutton-Brockand Parker1992, arthropodsand otherinvertebrates (Loker 1994) should Owens and Thompson1994). One factorthat may be amenableto studiesof sex differences in its function- obscuresex differencesin susceptibilityto parasites ing. All our conclusionsare strictlyabout sex differ- could be size dimorphism:in mostinvertebrates, fe- encesin actualparasitic infections, and not aboutsex malesare oftenlarger than males because of fecundity-differences in immuneresponse. It maybe thatmale drivenselection (see Poulin 1996b for review).The and femaleinvertebrates invest differentially in defense largersize of females could result in greaterexposure to againstpathogens because of differences in sexual selec- parasitesand provide more resources to incomingpara- tion,but that this differential investment is not reflected sites,thus negating a highersusceptibility of males to in termsof parasiteinfection to thesame degree as in infection.This maybe a commonphenomenon, since vertebratesbecause of the greatersimplicity of the positivecorrelations between host size and intensityof invertebrateimmune system. infection,regardless of host sex, were reported in many Takenas a whole,our results suggest that there may studiesthat we surveyed. be a differencebetween vertebrates and arthropods

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332 OIKOS 88:2 (2000) Tsai, Y.-H. and Cahill,K. M. 1970.Parasites of theGerman (Flagellata incertaesedis) and its incidencein a population cockroach(Blattella germanica L.) in New York City. - J. of Undinulavulgaris var. major (Crustacea Copepoda). - Parasitol.56: 375-377. Parasitology53: 293-296. vanWyk, P. M. 1982.Inhibition of the growth and reproduc- Young, A. S., Purnell,R. E., Kimber,C. D. and Payne,R. C. tionof the porcellanid crab Pachycheles rudis by the bopy- 1975. Correlationbetween the morphologyand infectivity rid isopod, Aporobopyrusmuguensis. - Parasitology 85: of Theilerialawrencei developing in the tick Rhipicephalus 459-473. appendiculatus.- Parasitology71: 27-34. Ward,D. F., Thomas,F. and Poulin,R. 1998.Fluctuating Young, A. S., Grootenhuis,J. G., Leitch,B. L. and Schein,E. asymmetryand parasitismin six New Zealandinsects. - 1980. The developmentof Theileria= Cytauxzoontauro - ActaOecol. 19: 409-412. tragi(Martin and Brocklesby,1960) fromeland in its tick Ward,P. I. 1986.A comparativestudy of thebreeding be- - haviourof a streamand a vector Rhipicephalusappendiculatus. Parasitology 81: pondpopulation of Gammarus 129-144. pulex (Amphipoda). - Oikos 46: 29-36. Wedekind,C. and Jakobsen,P. J. 1998.Male-biased suscepti- Zuk, M. 1987. Seasonal and individualvariation in gregarine bilityto helminthinfection: an experimentaltest with a parasite levels in the fieldcrickets Gryllus veletis and G. . - Oikos 81: 458-462. pennsylvanicus.- Ecol. Entomol. 12: 341-348. Welch,H. E. 1959.Taxonomy, life cycle, development, and Zuk, M. 1990. Reproductivestrategies and disease susceptibil- habitsof two new species of Allantonematidae (Nematoda) ity:an evolutionaryviewpoint. - Parasitol.Today 6: 231- parasiticin drosophilidflies. - Parasitology49: 83-103. 233. Wenner,E. L. 1978.Comparative biology of fourspecies of Zuk, M. 1996. Disease, endocrine-immuneinteractions and glyphocrangonidand crangonidshrimp from the continen- sexual selection.- Ecology 77: 1037-1042. tal slopeof the middle Atlantic Bight. - Can. J.Zool. 56: Zuk, M. and McKean, K. A. 1996. Sex differencesin parasitic 1052-1060. infections:patterns and processes. - Int. J. Parasitol. 26: Wickstead,J. H. 1963.A newrecord of Ellobiopsischattoni 1009-1024.

Appendix1. Data on femaleand male infectionlevels used in the analyses.

Host taxon Parasite taxon Type of study* Female infection Male infection Sample size Source**

Prevalenceof infection decapod nematomorph N 1.12 1.84 2500 1 decapod trematode N 57.14 67.85 647 2 decapod isopod N 62.85 46.15 471 3 decapod isopod N 35.20 33.90 4327 4 decapod isopod N 0.28 0.30 18540 5 decapod isopod N 69.90 61.15 2868 6 decapod isopod N 33.33 26.67 51 7 decapod isopod N 0.92 1.43 397 7 decapod isopod N 1.47 2.33 333 7 amphipod acanthocephalan N 2.70 4.16 4451 8 amphipod cestode N 3.50 3.90 870 9 amphipod trematode N 46.45 58.85 940 10 amphipod mite N 62.32 58.86 1183 11 copepod protozoan N 30.14 30.56 765 12 copepod cestode E 40.00 70.00 182 13 isopod acanthocephalan N 27.00 26.10 5340 14 tick protozoan E 38.00 26.80 500 15 tick protozoan E 11.63 1.51 944 16 tick protozoan E 88.20 91.40 138 17 tick protozoan E 10.00 20.00 60 18 tick protozoan E 31.29 26.70 1160 19 orthopteran protozoan N 56.25 66.67 58 20 orthopteran protozoan N 17.07 48.88 264 21 orthopteran protozoan N 46.62 51.39 349 21 orthopteran protozoan N 13.64 23.08 83 20 orthopteran protozoan N 38.71 44.00 87 22 orthopteran protozoan N 53.33 57.90 64 22 orthopteran protozoan N 36.28 30.00 132 22 orthopteran protozoan N 51.72 53.57 57 22 orthopteran nematode N 15.39 77.42 44 20 orthopteran nematode N 15.39 57.58 46 20 orthopteran mite N 83.33 52.00 49 22 blattarian protozoan N 27.27 21.88 76 23 blattarian protozoan N 90.91 96.88 76 23 blattarian protozoan N 45.46 46.88 76 23 blattarian protozoan N 31.82 25.00 76 23 blattarian nematode N 54.17 87.10 79 22 blattarian nematode N 68.97 61.11 65 22 blattarian nematode N 87.50 79.50 178 24 blattarian nematode N 97.73 100.00 76 23 coleopteran nematode N 19.20 16.60 156 25

OIKOS 88:2 (2000) 333 Appendix1. (Continued) Host taxon Parasitetaxon Typeof study* Femaleinfection Male infection Samplesizet Source** coleopteran nematode N 2.50 7.60 156 25 coleopteran nematode N 0.50 0.40 1214 25 coleopteran nematode N 3.80 2.20 1214 25 coleopteran nematode N 3.80 0.80 1214 25 coleopteran nematode N 39.20 30.20 1214 25 dipteran protozoan E 52.10 40.95 149 26 dipteran protozoan E 49.30 61.80 141 26 dipteran protozoan E 72.05 34.50 148 26 dipteran protozoan N 9.10 9.50 623 27 dipteran protozoan N 5.97 4.23 394 28 dipteran protozoan N 16.90 14.10 6344 27 dipteran protozoan E 47.85 65.05 142 26 dipteran protozoan E 4.20 4.00 146 26 dipteran fungus N 73.00 32.60 176 29 dipteran fungus N 80.00 82.00 100 29 dipteran nematode N 2.33 3.36 799 30 dipteran nematode N 21.68 19.86 1347 30 dipteran nematode N 1.85 2.08 570 30 dipteran nematode N 6.23 4.09 4569 30 odonate mite N 98.20 98.10 1847 31 Intensityof infection decapod trematode N 2.90 3.10 412 2 decapod isopod N 1.55 1.38 250 3 decapod isopod N 1.08 1.04 54 5 copepod cestode E 0.50 2.20 81 13 isopod acanthocephalan N 3.39 2.85 1417 14 tick protozoan E 1.12 15.51 63 16 tick protozoan E 21.45 9.20 338 19 tick protozoan E 3.98 2.08 162 15 tick protozoan E 17.10 14.43 124 17 tick protozoan E 1.67 2.00 9 18 orthopteran protozoan N 2.32 3.92 35 22 orthopteran protozoan N 10.68 3.07 46 22 orthopteran protozoan N 8.98 15.63 35 22 orthopteran protozoan N 2.48 3.43 30 22 orthopteran protozoan N 19.67 17.82 37 20 orthopteran nematode N 7.00 14.63 26 20 orthopteran nematode N 12.00 15.26 21 20 blattarian nematode N 1.71 2.32 53 22 blattarian nematode N 5.10 3.80 148 24 blattarian nematode N 1.97 1.94 42 22 blattarian acanthocephalan E 12.36 7.10 141 32 coleopteran nematode N 17.50 11.40 420 25 coleopteran nematode N 1.00 1.00 28 25 coleopteran nematode N 3.00 1.00 5 25 coleopteran nematode N 6.90 3.00 37 25 coleopteran nematode N 5.20 8.10 28 25 coleopteran nematode N 6.50 2.70 8 25 coleopteran cestode E 2.09 1.84 120 33 dipteran nematode N 1.91 2.38 22 30 dipteran nematode N 2.21 1.62 279 30 odonate mite N 35.60 31.40 1813 31 * E, experimentalinfection; N, naturalinfection. t For prevalence,total number of hostsexamined; for intensity, total number of infectedhosts in naturalinfections, or total numberof hostsexposed to infectionin experimentalstudies. ** Sources:1, Born1967; 2, Stromberget al. 1978;3, Kuriset al. 1980;4, van Wyk1982; 5, Field 1969;6, Beck 1979;7, Wenner1978; 8, Ward1986; 9, Stark1965; 10, Thomas et al. 1995;11, Kitron 1980; 12, Wickstead 1963; 13, Wedekind and Jakobsen1998; 14, Seidenberg 1973; 15, Purnell et al. 1973;16, Young et al. 1975;17, Young et al. 1980;18, Purnell et al. 1975; 19,Irvin et al. 1981;20, Luong and Zuk unpubl.;21, Zuk 1987;22, Ward et al. 1998;23, Tsai and Cahill1970; 24, Dobrovolny and Ackert1934; 25, Fincheret al. 1969;26, Moloo et al. 1993;27, Moloo et al. 1973;28, Rogerset al. 1972;29, Schlein et al. 1985;30, Welch1959; 31, Andresand Cordero1998; 32, Lackie1972; 33, Keymer1982.

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