ecological causes of sex-biased parasitism in threespine stickleback

Biological Journal of the Linnean Society (2001), 73: 51–63. With 8 figures

doi:10.1006/bijl.2001.0523, available online at http://www.idealibrary.com on

Ecological causes of sex-biased parasitism inthreespine stickleback

T. E. REIMCHEN∗

Department of Biology, University of Victoria, PO Box 3020, Victoria, B.C., Canada, V8W 3N5

P. NOSIL

Department of Biosciences, Simon Fraser University, Burnaby, B.C., Canada, V5A 1S6

Received 30 August 2000; accepted for publication 8 January 2001

Males and females can differ in levels of parasitism and such differences may be mediated by the costs of sexualselection or by ecological differences between the genders. In threespine stickleback, Gasterosteus aculeatus, malesexhibit paternal care and territorial nest defence and the costs of reproduction may be particularly high for malesrelative to females. We monitored levels of parasitism for 15 years in a population of stickleback infected by fourdifferent parasite species. Consistent with general predictions, overall parasite prevalence (total parasitism) wasgreater in males than in females. However, this excess did not occur for each species of parasite. Males had higherprevalence of a cestode Cyathocephalus truncatus and a trematode Bunodera sp. relative to females, while femaleshad higher prevalence of a cestode Schistocephalus solidus and nematodes. This suggested ecological sources todifferences in parasitism rather than reproductive costs and therefore we examined diet of unparasitized stickleback,predicting that differences in dietary niche would influence relative parasitism. This was partially confirmed andshowed that female stomach contents had increased frequency of pelagic items, the major habitat for the primaryhost of S. solidus whereas males exhibited increased frequency of benthic items, the dominant habitat of C. truncatusand Bunodera. Temporal shifts in the extent and direction of differential parasitism among years between the sexeswere associated with temporal shifts in dietary differences. Our results, combined with those in the literature,suggest that ecological differences between genders could be a more important component to patterns of parasiticinfection in natural populations than currently appreciated. 2001 The Linnean Society of London

ADDITIONAL KEYWORDS: parasitism – sexual dimorphism – ecological selection – sexual selection – diet –resource partitioning – Gasterosteus aculeatus – Queen Charlotte Islands.

field evidence to suggest that males should be moreINTRODUCTIONheavily infected than females, possibly due to the costs

Parasites are major ecological players in communities of sexual selection (Batra, 1984; Folstad et al., 1989;and differential parasitism can occur between males Folstad & Karter, 1992; Poulin, 1996a; Wedekind &and females (Bundy, 1988; Zuk, 1990; Poulin, 1996a Jacobson, 1998). For example, competition for matesfor review). Such sex-biased parasitism may result extracts costs on reproductive males and, consequently,from differences in immunocompetence resulting from males may be operating closer to their physiologicalunequal costs of reproduction or from natural selection limits than females (Trivers, 1972; Zuk, 1990; Clutton-favouring ecological divergence which results in dif- Brock & Parker, 1992). This can result in higher levelsferential exposure to infectious agents (Selander, 1966; of stress and reduced immunocompetence in malesTrivers, 1976; Reimchen, 1980; Hamilton & Zuk, 1982; relative to females (Herbert & Cohen, 1993 for review).Slatkin, 1984; Tinsley, 1989; Houston & Shine, 1993; Elevated testosterone levels can also lead to immuno-Perry, 1996). There is theoretical, experimental and suppression which further increases susceptibility of

infection or disease (Folstad et al., 1989; Folstad &Karter, 1992; but see Wedekind & Jacobson, 1998).

However, differences in parasitic infection between∗Corresponding author. E-mail: [email protected]

510024–4066/01/050051+13 $35.00/0 2001 The Linnean Society of London

52 T. E. REIMCHEN and P. NOSIL

genders might arise from ecological rather than sexual exposure to infected primary hosts. The largest para-site infecting Boulton Lake stickleback is the coelomicselection. For example, niche partitioning involvingtapeworm Schistocephalus solidus. This parasite util-habitat or diet (c.f. Selander, 1966; Grant, 1975;izes a pelagic copepod as a primary host, stickleback asReimchen, 1980; Grant, 1985; Shine, 1989; Raymonda secondary host and birds as definitive hosts (Clarke,et al., 1990; Houston & Shine, 1993) can result in1954). The second largest parasite is the intestinaldifferential exposure to parasites unrelated to the un-tapeworm C. truncatus, which utilizes benthic am-equal costs of reproduction (e.g. Tinsley, 1989). Suchphipods as primary hosts and fish as the definitivean ecological origin to parasitism would predict thathosts (Vik, 1958). Nematodes (Eustrongylides spp.),either males or females could exhibit excess parasitismwhich encyst in the muscle, utilize aquatic oligochaetesdependent on their probability of encountering theas primary hosts, while stickleback and avian pisci-parasite and that excess parasitism in males cannot bevores are intermediate and definitive hosts respectivelyimmediately ascribed to reduced immunocompetence.(Hoffman, 1967). Trematodes (Bunodera sp.) occur inHowever, the relative importance of niche partitioningthe lower intestine and use a variety of primary andas a general explanation for gender differences insecondary hosts, including molluscs and crustaceans,parasitism has not been established.while definitive hosts are fish (Cannon, 1971; Skorping,Costs of reproduction for males may be especially1981). Consequently, the composition of the diet ofhigh in fishes such as stickleback (Gasterostidae)each gender was also monitored over the sample periodwhere males provide all the parental care and exhibitto test for potential niche partitioning between gendersall the territorial defence (van den Assem, 1967; Fitz-that could result in differential exposure to infectedgerald, Guderley & Picard, 1989; De-Fraipont, Fitz-primary hosts. If niche variation, rather than re-gerald & Guderley, 1992; Bakker, 1994 for review). Asproductive costs, are involved in levels of parasitism,a result of these costs, stickleback provide a modelwe predict that differential parasitism between malesystem well suited to testing hypotheses concerningand female stickleback will be species-specific anddifferential parasitism between the sexes (Zuk, 1990).associated with differences in spatial and dietary com-Evolutionary studies of undisturbed stickleback popu-ponents of the ecological niche. Specifically, as femaleslations from the Haida Gwaii (formerly Queen Char-are more limnetic than males, we expect higher con-lotte Islands) off the west coast of Canada over the lastsumption of zooplankton in females and as a resultthree decades (Moodie & Reimchen, 1976; Reimchen,higher infections by S. solidus. Furthermore, our long-1994) have allowed sampling over extended time seriesterm data base provides an opportunity to test whetherand provide a unique opportunity to investigate tem-there are temporal shifts in differential parasitismporal associations between sex and parasitism in in-between the sexes and whether this is associated withdividuals from natural populations.temporal shifts in any dietary differences between theThreespine stickleback (Gasterosteus aculeatus)genders.from Boulton Lake in the Queen Charlotte Islands,

B.C. are infected by four species of parasites, includingtwo cestodes, a trematode and a nematode (Reimchen, STUDY AREA AND METHODS1982, 1997). Using stickleback from this population asa model, we monitored parasitism of males and females The investigation was carried out using samples fromfor 15 years and initially tested for differential para- Boulton Lake, Graham Island, off the coast of centralsitism between the sexes. Secondly, we examined onto- British Columbia, western Canada (habitat data andgenetic trends in relative infection between the genders sampling protocols in Reimchen, 1980, 1982). Thepredicting that the differential should be most ex- stickleback occupy all major habitats (littoral, limnetic,pressed during reproduction, and thirdly we examined benthic, pelagic) of the 15 ha lake and are preyed uponwhether there was heterogeneity in any trends over by macro-invertebrates and diving birds. Samples oftime. Based on the high costs of reproduction in male stickleback were obtained in 1970, 1971, and 1975–stickleback and on the literature concerning the costs of 1987. In addition to the measurements of body lengthsexual selection and male-biased parasitism in general, (SL), spine morphology, gender and stomach contents,we predict males will exhibit higher parasite pre- specimens were also scored for the number of S. solidusvalence than females for all four parasite species. (N=20 346), C. truncatus (N=19695) and nematodes

However, there are ecological factors that could (N=19 873). The contracted length of the largest plero-facilitate differences in parasitism between males and cercoid was also recorded for S. solidus. The trematodefemales in the Boulton Lake population. While males Bunodera sp. was only scored systematically duringand females are both found throughout the lake, males the latter part of the study (N=5272). Detailed de-tend to be more prevalent in littoral habitats whereas scriptions of scoring for morphology, parasite infection,females are more limnetic (Reimchen, 1980) and this sex and SL are described in Reimchen (1980, 1982,

1997). In some individuals (<100), the gonads werecould influence patterns of parasitism by mediating

SEX, PARASITISM AND DIET IN STICKLEBACK 53

extensively atrophied and sex could not be determined. seined fish collected from the same region of the lake(beach captures). We then examined associations be-We compared (pooled G-tests, GP) the prevalence

(presence/absence) and intensity (number) of parasites tween diet and gender using data from fish capturedby minnow traps from all seven localities in the lake.for male and female stickleback. We report results for

prevalence only as trends were congruent for the two These pooled results include only the localities a fooditem was detected in and were tested for heterogeneityindices of parasitism. For each of the large-bodied

parasites (S. solidus, C. truncatus and nematodes), we (heterogeneity G-tests) in trends among localities.We also specifically compared consumption of cope-examined single species infection rates between the

sexes and excluded fish that were infected with either pods and amphipods between the genders as theseprey items act as primary host for S. solidus andof the two alternate large parasites. For Bunodera, we

excluded all multiple species infections. We partitioned C. truncatus respectively. When testing for genderdifferences in these items we report results seasonallydata among size-classes of fish and tested (hetero-

geneity G-tests, GH) for continuity of trends across (Winter: Nov.–Apr.; Summer: May–Oct.) and includefish captured by seining and traps. As comparisonsize classes and among years over the study period

(1970–1987). Yearly comparisons for C. truncatus and between males and females for each parasite speciesand food item tests a different hypothesis, we did notnematodes were restricted to adult (≥45 mm) fish, as

juveniles and yearlings are not generally infected. adjust overall significance levels for the number ofparasite species and food items examined (Rice, 1989).We tested for differences in diet between the sexes

(G-tests). Only non-parasitized fish were compared as However, within each parasite species and food item wecorrected significance levels from G-tests for multipleparasites are known to modify stickleback behaviour

(Lobue & Bell, 1993; Reimchen, 1982; Ness & Foster, comparisons (sequential Bonferroni method).We examined whether temporal shifts in tem-1999). Unparasitized stickleback (N=9089) were ex-

amined and for each specimen the presence or absence perature were associated with temporal shifts inof various food items was recorded. The major taxo- stickleback diet and tested whether shifts in the dietnomic groups identified were (listed in decreasing fre- were associated with temporal shifts in overall parasitequency) cladocerans (Bosmina spp., Chydoridae, prevalence. To partially control for seasonal variabilityLeptodora kindtii, Polyphemus spp.), chironomids, in temperature, diet and levels of parasitism we ex-other dipteran larvae (Culicidae, Heleinae), amphipods amined such associations in two seasons; winter and(Gammarus spp.), surface insects, zygopterans, cope- summer. To examine associations between tem-pods (Diaptomus spp.) and trichopterans. Fish stom- perature and diet we calculated the consumption fre-achs in which food items were digested and quency of zooplankton (cladocerans + copepods) andunidentifiable were scored as (1) benthic, if they con- macrobenthos (macrobenthos+ chironomids) for eachtained more than 80% dark organic matter indicative gender for subadults and adults for each month ofof benthic prey items, (2) pelagic, if they contained sampling (1970–1987) and used Spearman rank cor-more than 80% zooplankton remnants and (3) mixed, relation (SR) to test whether these monthly dietaryfor combinations of benthic and pelagic. We excluded frequencies were correlated with monthly temperaturethese fish from taxon-specific comparisons and tested means. We used Spearman rank correlation to testseparately whether the proportion of fish scored as whether the diet (monthly frequency of a food item)‘benthic’ differed between the sexes. We grouped the of unparasitized fish within a monthly sample wascommon, distinguishable dietary items into four broad correlated with prevalence of infection by each parasitecategories; cladocerans (all spp.), chironomids (all species in a sample. Significance levels were adjustedspp.), Culicid larvae (90% Culicidae spp.+ 10% Hele- for multiple comparisons using the sequential Bon-inae spp.) and macrobenthos (amphipods, zygopterans, ferroni method. Lagging food consumption a fewtrichopterans) and compared overall consumption of months before or after infection prevalence did noteach between genders. We also partitioned the samples reveal any significant relationships. All statistical ana-into two major size classes (yearlings <45 mm, adults lyses were done using SPSS (v. 9.0).≥45 mm) and tested for heterogeneity between sizeclasses (heterogeneity G-tests). We examined yearlytrends in dietary differences between the genders and RESULTScompared these differences to differences in para-

RELATIVE PARASITISMsitism. Consumption of macrobenthos was too low insubadults to allow meaningful yearly comparisons. Among the 19 760 fish scored for sex and for the

prevalence of the three large-bodied parasite species,There was evidence for slight dietary shifts amongfish collected from different regions of the lake (un- the overall frequency of parasitic infection (all para-

sites grouped) was significantly higher in males thanpublished data) and to minimize any potential bias togender comparisons, we initially compared diet among in females (26.4%, 22.5% respectively, GP1=39.35,


Table 1. Log-likelihood G-tests comparing the relative number of individualsinfected by four parasite species (S. solidus, C. truncatus, Bunodera sp., Nematodes)between male and female G. aculeatus from Boulton Lake. Results exclude multiplespecies infections

Parasite % Males % Females N Ginfected infected

S. solidus 13.5 15.3 17314 11.49∗∗∗C. truncatus 21.2 10.1 9902 223.54∗∗∗Bunodera sp. 47.5 42.7 3761 8.64∗∗Nematodes 1.9 2.4 15147 3.55

∗∗P<0.01, ∗∗∗P<0.001.

Table 2. Log-likelihood G-tests comparing the relativeP<0.001, N=19 760). For infected fish, number of para-number of individuals with small (<15 mm) vs. largesite species was also associated with gender, with males(≥15 mm) S. solidus plerocercoids between male andexhibiting increased likelihood of having multiple vs.female G. aculeatus from Boulton Lake. Results are shownsingle species infections compared with females (21.1%for winter (Nov.–Apr.) and for summer (May–Oct.)and 17.9% multiple infections for males and females

respectively, G=8.71, P<0.01).Size class % of males % of females N GThis marginal excess parasitism of male stickleback(mm) with large with largedid not persist when samples were partitioned by

plerocercoids plerocercoidssingle species infections (multiple species infectionexcluded). Female stickleback had increased pre- Wintervalence of S. solidus relative to males (GP1, P<0.001) 11–29 41.2 50.0 19 0.57and a non-significant excess of nematodes (GP1, P= 30–39 61.1 72.7 62 0.790.06) whereas males had higher prevalence of C. trun- 40–49 62.5 69.6 146 0.17catus (GP1, P<0.001) and Bunodera (GP1, P<0.01, Table 50–56 38.5 50.0 85 0.591). Size of S. solidus differed between the genders as 57–70 0.00 42.1 22 2.98

Total (df 5) 4.59females were more likely to have mature plerocercoidsPooled 47.5 62.9 334 4.75∗and this effect was accentuated during winter monthsHeterogeneity 0.16(Table 2).(df 4)Ontogenetic comparisons were generally consistent

with pooled effects, although heterogeneity among size Summerclasses in relative infection rates was detected (Fig. 11–29 50.3 16.7 332 5.731). For S. solidus, female sticklebacks had greater 30–39 44.3 59.6 470 9.91∗∗infection than did males in yearlings (30–39 mm) and 40–49 49.1 45.2 608 0.29adults (>50 mm) size classes whereas infection rates 50–56 40.9 42.3 437 0.07were similar in the other size classes (GH4=28.94, 57–70 42.2 37.2 263 0.58

Total (df 5) 16.57∗∗P<0.001). For C. truncatus, which occurred only inPooled 0.01subadult and adult stickleback, males had higher pre-Heterogeneity 16.57∗∗valence of infection than females in each size class and(df 4)differences were accentuated in the largest fish (GH2=

110.34, P<0.001). For nematodes, female stickleback∗P<0.05, ∗∗P<0.01.had higher infection than did males in each size class

and this effect was most accentuated in the largest fish(GH4=14.72, P<0.01). For Bunodera, male sticklebacksexhibited increased prevalence of infection relative to P<0.01; Fig. 2). C. truncatus infections were male-

biased in 14 of 15 years (GH14=11.34, P>0.50; Fig. 3).females in the two smallest size classes and similarinfection rates in larger fish (GH4=4.37, P>0.25). Nematode infections were similar in most years but

included two years (1980, 1981) with a marked femaleThere was variability among years in the directionand extent of differential parasitism of the sexes. S. bias followed by a male bias in 1982 (GH13=28.19,

P<0.01; Fig. 4). Relative Bunodera infections of thesolidus infections were female-biased in 1970, 1975and 1976 (P<0.05, G-tests) whereas males had greater sexes did not vary significantly among years (GH6=

6.36, P>0.25).infection rates in 1981 (P<0.01, G-test; GH14=30.19,


–0.20

0.15D

N = 413 506 472 589 222

–0.10

0.00

0.05

G = 5.30 5.02 0.01 0.971.98

Fish length (mm)11–29 30–39 40–49 50–56 57–70

426 300 372 369 91–0.08

0.08C

Rel

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e in

fect

ion

of

the

sexe

s

N = 2043 1329 2286 1855 515

–0.04

0.00

0.04

G = 1.28 0.90 6.87* 2.20 7.01*

Fish length (mm)11–29 30–39 40–49 50–56 57–70

2137 1073 2316 1314 275

–0.20

0.10B

N = 2275 1596 2443 2442 839

–0.10

0.00

G = 27.89** 56.18**29.13**

11–29 30–39 40–49 50–56 57–702370 1408 2366 1497 315

–0.10

0.10A

Rel

ativ

e in

fect

ion

of

the

sexe

s

N = 2259 1567 2641 2047 591

–0.05

0.00

0.05

G = 0.03 26.61** 0.00 9.21* 4.59

11–29 30–39 40–49 50–56 57–702354 1384 2653 1496 318

–0.05

–0.15

0.10

Figure 1. Relative parasite prevalence for (Χ) male and (Β) female G. aculeatus for five size classes of stickleback.Each pair of error bars shows the mean (±95% CI) parasite prevalence for males and females within a size class,where the overall mean for each size class has been subtracted from each gender for graphical clarity. G-test statisticsand Bonferroni corrected probabilities (∗P<0.05, ∗∗P<0.01) are shown below each male/female pair. Probabilities areadjusted for multiple comparisons (sequential Bonferroni method; Rice, 1989). There was significant heterogeneityamong size classes in relative infection rates for all four species. (A) S. solidus. (B) C. truncatus. (C) Bunodera sp. (D)Nematode.

We then compared the consumption of each of theDIETfood categories between males and females in two sizeAmong the four food groups (cladocerans, chironomids,classes (<45 mm, ≥45 mm) and tested for hetero-culicids and macrobenthos), cladocerans were moregeneity between size classes (Fig. 5). Cladocerans wereprevalent in females than in males (GP1, P<0.001; Tablemore common in females than in males in adults but3) while macrobenthos were much more common innot in yearlings. However, no statistical heterogeneitymales than in females (GP1, P<0.001). The groupedbetween size classes was detected (GH1=1.51, P<0.25).data showed no significant differences in relative con-For chironomids, we detected elevated consumption ofsumption of chironomids or culicids. For fish withchironomids in male yearlings (P=0.06 after Bon-partially digested stomach contents, which were ex-ferroni correction), but slightly female-biased con-cluded from previous analyses, a significantly greatersumption in adults (GH1=3.86, P<0.05). Differencesproportion of males than females were scored as ben-between the genders in the consumption of culicidsthic (8.6%, 4.7% respectively, GP1=15.23, P<0.001, N=

2487). varied between size classes (GH1=5.11, P<0.05). In


–0.25

0.20

Year

Rel

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–0.20

–0.10

0.15

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0.00

8786858483828170 71 76 77 78 8079

MSLL**

LLLL**

LL*LL

LL**SLMS LL**

LLLL** LL*

LL**

75

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0.10

–0.15

–0.05

–0.15

0.10

Year

Rel

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8786858483828170 71 76 77 78 8079

MSLL

LLLL

LLLL

LLLL*MS LL**

LLLL LL

LL

75

LL**

–0.05

Figure 3. Yearly trends in relative prevalence (meanFigure 2. Yearly trends in relative prevalence (mean±95% CI) of C. truncatus infection for male and female±95% CI) of S. solidus infection for (Χ) male and (Β)stickleback. Includes all fish ≥45 mm SL. Bonferronifemale stickleback. Each pair of error bars shows meancorrected probabilities from G-tests (∗P<0.05, ∗∗P<0.01)parasite prevalence for males and females within a year,are shown below each male/female pair. Sample sizes arewhere the overall mean for each year has been subtractedshown above the horizontal axis (S – small, N<50; M –from each gender for graphical clarity. Bonferroni cor-medium, N=50–100; L – large, N>100). For details seerected probabilities from G-tests (∗P<0.05, ∗∗P<0.01) areFig. 1.shown below each male/female pair. Sample sizes are

shown above the horizontal axis (S – small, N<50; M –medium, N=50–100; L – large, N>100).

subadults, culicid consumption was slightly female-biased, but was male-biased in adults. Size-relatedanalyses revealed macrobenthos was more common inmales vs. females in both subadults and adults butalso showed differences were accentuated in adults(GH1=10.43, P<0.01). For fish with digested stomachcontents, a higher proportion of males than femaleswere scored as benthic in both subadults and adults(GH1=2.57, P>0.10).

We also compared the prevalence of the four mainfood types between adult males and females capturedusing minnow traps from all localities in Boulton Lake.These comparisons included fish from seven localitiesand yielded a non-significant female bias for cladoceranprevalence (34.9%, 33.8% females and males re-

–0.15

0.15

Year

Rel

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of

the

sexe

s

–0.10

–0.05

0.10

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8786858483828170 75 76 77 78 8079

SSLLLLLLLLLMLLSL LL LL LL LL LLLL

spectively, GP1=0.17, P=0.68, N=1275; GH6=10.65,P=0.10) and a significant, but heterogeneous, female Figure 4. Yearly trends in relative prevalence (meanbias in chironomid prevalence (46.4%, 38.6% females ±95% CI) of nematode infection for male and femaleand males respectively, GP1=7.942, P<0.01, N=1321; stickleback. Includes all fish ≥45 mm SL. BonferroniGH6=13.47, P<0.05). Culicid consumption occurred corrected probabilities from G-tests (∗P<0.05, ∗∗P<0.01)only in one of the other seven localities and was similar are shown below each male/female pair. Sample sizes arebetween the gender classes (0.6%, 1.0% females and shown above the horizontal axis (S – small, N<50; M –males respectively, G=0.36, P=0.55, N=862). The medium, N=50–100; L – large, N>100). For details seeprevalence of macrobenthos was significantly higher Fig. 1.in males than in females, but we detected heterogeneity


Table 3. Log-likelihood G-tests comparing the relative number of stickleback stom-achs with each of four main food types present between male and female G. aculeatusfrom Boulton Lake. Results are given for stickleback captured by seining between1970 and 1986

Prey item % prevalence % prevalence N Gin males in females

Cladocerans 75.4 80.7 3222 13.38∗∗∗Chironomids 39.6 37.2 3971 2.51Culicids 17.6 17.6 2826 0.00Macrobenthos 8.2 4.7 3964 19.71∗∗∗

∗∗∗P<0.001.

for S. solidus and C. truncatus respectively (Table 4). Insubadults, copepod consumption was significantlygreater in females than in males during winter (Nov.–Apr.) (P<0.01, G-test) and similar between genders insummer (May–Oct.) (P=0.31, G-test). In adults, copepodconsumption was significantly female-biased in bothsummer and in winter (P<0.05, G-tests). Amphipod con-sumptionwassignificantlygreater inadultmalesthaninadult females during winter (P<0.01, G-test) and similarbetween genders during summer (P=0.87, G-test).

Relative S. solidus infection between the genderstended to be female-biased but this pattern was re-versed in 1981 (Fig. 2). The most pronounced dif-ferences between the sexes in nematode infection alsooccurred in this year. We examined whether a switchin dietary differences between the sexes coincided withthese differences in relative parasite prevalence. Thiswas observed as cladoceran consumption was female-

–20

15

male excess

Per

cen

t di

ffer

ence

(%

mal

es –

% f

emal

es)

female excess

–15

–10

–5

10

5

0

cladocerans culicids 'benthics'

Food categorychironomids macrobenthos

0.26 1.37 8.83**

4.69 2.19

11.61** 3.74 3.83

1.68 7.09*

biased from years 1976–1980 but switched to male-bias in 1981 (Fig. 6). This trend occurred in bothFigure 5. Relative consumption (% male–% female) ofsubadults and adults. Relative chironomid con-food items between sexes of G. aculeatus for subadult (;;sumption also exhibited a reversal. Chironomids were15–45 mm) and adult (Ε; 45–75 mm) fish. Results aremore common in males than females from 1976 toshown for differences in consumption of cladocerans, chi-1980, but this pattern was reversed in 1981. For culicidronomids, culicids, macrobenthos. Also shown is the dif-and macrobenthos consumption and for fish scored asference in the proportion of males vs. females scored asbenthic (digested food items), we detected no marked‘benthic’ for fish with digested stomach contents (seereversals among years in relative frequency betweenmethods). G-test statistics and Bonferroni correctedthe genders.probabilities (∗P<0.05, ∗∗P<0.01) are shown above the

Such temporal variability in diet and relative para-horizontal axis.sitism could be tied to temporal variability in bio-physical parameters. Examination of weather data forHaida Gwaii revealed 1981 was an unusually warmand wet year. Mean yearly temperature graduallyincreased through the 1970s and reached a studyperiod high in 1981 (Fig. 7). The spring (Jan.–Apr.) ofin this trend among localities (29.3%, 16.9% re-1981 was the second warmest spring of the studyspectively, GP1=33.10, P<0.001, N=1598; GH6=30.87,period while the summer (May–Sept.) of 1981 was theP<0.001).second warmest summer. The spring of 1981 had theMales and females also differed in the consumption of

copepods and amphipods, which act as primary hosts highest rainfall of all the springs in the study period.


Table 4. Log-likelihood G-tests comparing the presence of amphipods and copepods between maleand female G. aculeatus stomach contents. Results are given for subadults (<45 mm) and adults(≥45 mm) in winter (Nov.–Apr.) and summer (May–Oct.) seasons

Prey item Winter Summer% in % in N G % in % in N Gmales females males females

SubadultsCopepods 2.3 7.2 483 6.89∗∗ 2.4 1.9 3884 1.03

AdultsAmphipods 19.6 10.7 638 9.94∗∗ 10.9 11.2 1706 0.03Copepods 2.8 6.0 638 3.95∗ 2.5 4.4 1706 4.63∗

∗P<0.05, ∗∗P<0.01, ∗∗∗P<0.001.

ASSOCIATIONS BETWEEN DIET, TEMPERATURE AND DISCUSSIONPARASITISM

We tested two hypotheses concerning differential para-We tested whether the temperature within a sample sitism between the sexes. Firstly, we tested whethermonth (each month of sampling 1970–1987) was as- male stickleback exhibit elevated levels of overall para-sociated with stickleback diet within that sample sitism relative to females, as predicted from the costsmonth. This was done for two separate seasons (Winter: of sexual selection. Secondly, we tested whether anyNov.–Apr.; Summer: May–Oct.). For winter, we de- potential dietary niche variation between the genderstected a positive correlation between mean monthly influenced gender differences in parasitic infection.temperature and the monthly consumption frequency Differential parasitism between the sexes has beenof macrobenthos (rho=0.47, P<0.001, N=82, SR), in- reported in a wide range of taxa, including amphibiansdicating stickleback consumed more macrobenthos (Hollis, 1972; Tinsley, 1989), mammals (Beital, Knappoverall during relatively warm sample months in win- & Vohs, 1974; Langley & Fairly, 1982; Folstad et al.,ter. Conversely, we detected a negative correlation 1989), fish (Batra, 1984; Tierney, Huntingford &between mean monthly temperature in summer and Crompton, 1996) and birds (Poulin, 1996a for reviewthe monthly consumption of macrobenthos (rho= in vertebrates). Such sex-biased parasitism can result−0.18, P<0.05, N=156, SR), indicating stickleback from differences in immunocompetence with malestended to consume less benthos during warm sample predicted to bear a greater cost of sexual selection andmonths in summer. All other correlations between the immunosuppressive effects of testosterone pro-diet and temperature were non-significant (rho<0.15, duction (Folstad et al., 1989; Zuk, 1990; Clutton-BrockP>0.10, SR). & Parker, 1992; Folstad & Karter, 1992), and thus to

We also tested whether the diet of unparasitized be more susceptible to parasitic infection than females.stickleback (frequency of a food item) within a monthly This may be especially true for stickleback, wheresample was associated with the prevalence of a parasite paternal care and territorial nest defence can renderspecies in a sample. This was confirmed in two cases. reproduction particularly costly for males (van denIn winter, the prevalence of cladocerans within a Assem, 1967; Wootton, 1976; Fitzgerald et al., 1989;sample was negatively correlated with the prevalence Bakker, 1994 for review). Despite these costs, we failedof C. truncatus infection within a sample (Fig. 8) and to find a consistent male bias in parasite prevalencethis correlation was significant after correction for when comparisons between male and female stickle-multiple comparisons (cladocerans, rho=−0.67, back were partitioned to single species infections. In-P<0.01, N=27, SR). The sample consumption fre- stead, our results suggest ecological differencesquency of chironomids was positively correlated with between genders or phenotypes may be important pre-the sample prevalence of Bunodera sp. infection in dictors of parasitism in individuals from natural popu-winter (rho=0.81, P<0.05, N=11, SR). All other cor- lations (see also Reimchen & Nosil, 2001). Presumably,relations between sample prevalence of a food item choice of hosts by parasites also represents an adaptiveand the sample prevalence of parasitism were non- strategy aimed at maximizing fitness (Holmes, 1976).significant after correction for multiple comparisons Male and female stickleback from Boulton Lake ex-

hibit differences in habitat use (Reimchen, 1980) and,(rho<0.36, P>0.10, SR).


86Year

Mea

n t

empe

ratu

re –

rai

nfa

ll70 72 74 76 78 80 82 84

45 mm

150 mm

6.3°C

9.0°C

Figure 7. Mean yearly temperatures (°C) for the HaidaGwaii (solid line) and mean spring (Jan.–Apr.) rainfall(dashed line). Yearly means are the average of monthlymeans.

–40

40

Year

B

Per

cen

t di

ffer

ence

(%

mal

es –

% f

emal

es)

70 76 77 78 79 80 81 82 83 84 85 86

30

20

10

0

–10

–20

–30

male excess

female excess

–50

30

Year

A

Per

cen

t di

ffer

ence

(%

mal

es –

% f

emal

es)

75 76 77 78 79 80 81 82 83 84 85 86

20

10

0

–10

–20

–30

75

–40

male excess

female excess

Figure 6. Yearly differences in relative consumption (%male–% female) of (A) cladocerans and (B) chironomidsbetween the sexes of G. aculeatus. Results are shown forsubadults (;; 15–45 mm) and adults (Ε; 45–75 mm) forall yearly samples including the diet of at least 20 in-dividuals.

–0.11.2

0.6

Cladoceran prevalence during winter

C. t

run

catu

s pr

eval

ence

du

rin

g w

inte

r

–0.2 0.0 0.2 0.4 0.6 0.8 1.0

0.5

0.4

0.3

0.2

0.1

0.0

79 78

80768584

8177

8380

79 78

80

77

7678

86

758675

79

77 79

7876

7882

Figure 8. Relationship between the mean prevalenceconsequently, we predicted that inter-gender dif- of cladocerans in a sample (each month of sampling,ferences in parasitic infection would be species-specific 1970–1987) and the mean prevalence of C. truncatusand associated with differences in spatial or dietary infection during winter (Nov.–Apr.). The inverse re-components of the ecological niche. Consistent with this lationship is significant (P<0.01, SR). Numbers aboveprediction, patterns of differential parasitism between each point on the scatter plot refer to the year of sample.the genders were species-specific and these patterns arepotentially interpretable in terms of dietary variationbetween the genders.

Males were more likely to be parasitized by C. trun- which results in differential exposure to infected prim-ary hosts. Males and females differed statistically incatus and Bunodera sp., whereas females were more

likely to be parasitized by S. solidus or nematodes. the relative consumption of two of the four main foodcategories, with males consuming more benthic itemsThese patterns could arise from dietary niche variation


and females consuming more cladocerans. Increased supported by associations between shifts in dietary dif-ferences between genders and shifts in sex-biased para-cladoceran consumption by females is indicative of a

more pelagic diet as few cladocerans are mud-dwelling sitism. From 1976 to 1980 S. solidus infections tendedtobe female-biasedwhilenematode infectionsweresim-(Ward & Whipple, 1959). Macrobenthos, such as tri-

chopterans and zygopterans, were more common in ilar between the sexes until 1980. Congruent with thedifferential forS.solidus, female dietduringtheseyearsmales than in females and this suggests males utilize

more littoral and benthic dietary niche than females. exhibited an excess of cladocerans while male diet ten-ded to show increased consumption of chironomids rel-Also, zooplankton-free, digested benthos was more pre-

valent in males than in females. Chironomids are ben- ative to females. In 1981, a marked shift to a male biasfor S. solidus infection occurred and this was ac-thic and were more prevalent in juvenile and

subadult males than in similar size females. companied by divergence in relative nematode in-fections (female-biased). Coinciding with these shifts inApelagic/benthicdietaryseparationbetweenthegen-

ders in Boulton Lake is consistent with spatial and mor- relative parasitism, we detected shifts in the dietarydifferences between the genders. In 1981, cladoceranphological gender differences in the population. For

example, males tend to be associated with littoral hab- consumption switched to a male bias while chironomidconsumption switched to a female bias (trends oppositeitat and exhibit reduction in the pelvic and dorsal spines

that are part of the stickleback defence apparatus, to preceding years). The excess cladoceran consumptionby males could have increased relative exposure to pe-whereas females exhibit the opposite trend. Potentially,

this results from spines being an advantage against pelagic copepods infected by S. solidus. Conversely, fe-male-biased chironomid consumption in 1981 couldlagic predators such as avian piscivores, but a dis-

advantage against benthic grappling predators such as have increased exposure to benthic oligochaetes in-fected by nematodes. This suggests the temporal shiftsdragonfly larvae (Reimchen, 1980). Similar spatial or

dietary differences among stickleback phenotypes dif- in relative parasitism were caused by shifts in the dietthat resulted in changes in exposure to infected preyfering inmorphological characterssuchas lateralplates

and pelvic spines and trophic structures such as gill items. Shifts in temperature or other biophysical para-meters provides one plausible mechanism that couldrakers have been documented both in other natural

populations (McPhail, 1983; Schluter & McPhail, 1992; account for the temporal shifts in gender biases in dietand parasitism.Larson & McIntire, 1993) and experimentally (Bentzen

& McPhail, 1984; Schluter, 1993, 1994, 1995). Such Our results are consistent with a number of studiesthat have examined associations among sex, ecology,niche variation may result in differential exposure to

infected prey between genders. The benthic habit of diet, and parasitism. In another study of stickleback,females also had heavier S. solidus infection than malesmales may result in increased exposure to amphipods,

the primary host of C. truncatus. Alternatively, the pe- but this study did not examine dietary differences (Ti-erney et al., 1996). In the central mudminnow (Umbralagic diet of females may result in increased exposure

to pelagic copepods, which act as primary hosts of S. limi), seasonal differences in Neoechinorhynchus limiinfection were correlated with dietary shifts (Muzzal,solidus.Forexample,wedetectedaninverseassociation

betweenmonthlycladoceranconsumptioninwinterand 1984). Batra (1984) suggests helminth infection in threespecies of cichlids is greater in males than in femalesmonthly prevalence of C. truncatus, suggesting that in-

creased cladoceran consumption reduces exposure to due greater food consumption, and thus increased prob-ability of consuming an infected prey item, in males.benthic food items such as amphipods. However, the

oligochaete primary host of nematodes, which are Similar associations have been reported in non-fish spe-cies. In wood mice (Apodemus sylvaticus), the ec-slightly more prevalent in females, tend to also be ben-

thic (Clifford, 1991). toparasitic tick Ixodes ricinus was more common inmales, who cover much more ground than females, andThese associations between sex, diet and parasitism

are supported by inter-gender differences in the con- flukes were most common during a period of intensivefeeding on invertebrate primary hosts (Langley &sumption of potentially infected prey items. Species

which act as primary hosts for the parasite species ob- Fairly, 1982). In spadefoot toads, male reproductive be-haviour requires spending long periods of time in theserved in this study were rarely observed in stickleback

stomachs. However, when they did occur, trends were waterwhich increasescontactwiththeparasitePseudo-diplorchis americanus (Tinsley, 1989). Consequently,highly consistent with the observed differences between

the genders. Males were more likely to consume am- males toads are more heavily infected by P. americanusthan females, who spend less time in the water. How-phipods, the primary host of C. truncatus. Females were

more likely to consume copepods, the primary host of S. ever, some studies on stickleback (Font, 1983; Bakker& Mundwiler, 1999) and other fish species (Lawrence,solidus. This provides strong evidence for differential

exposure to infected prey between the genders. 1970; Muzzal, 1980) have found no significant dif-ferences in parasitism between genders. Conceivably,A relationship between diet and parasitism is further


host-sex/parasite interactions are mediated by the eco- (Schluter & McPhail, 1992; Reimchen, 1995). Sexualdimorphism has been investigated in a wide rangelogy of the interaction. Also, our results indicate slightof species, but is often attributed to the action ofdifferences in parasitism between the genders may notsexual selection (e.g. Trivers, 1976; Perry, 1996)be detected unless populations are sampled over mul-rather than to ecological causes. However, researcherstiple years.have shown intra-specific resource partitioning inIn a recent comparative analysis (Poulin, 1996b) hel-response to competition or other ecological factorsminth growth was found to be greater in male than in(Selander, 1966; Grant, 1975; Raymond et al., 1990;female hosts. However, our result demonstrate femalesHouston & Shine, 1993; Schluter, 1994) and thehave an increased probability of harbouring large plero-opportunity for ecological release (Traniello &cercoids during winter and this suggests parasiteBeshers, 1991) can partially account for differencesgrowth may be increased in the more common host. Al-between genders or phenotypes. Morphological dif-ternatively, differences in S. solidus size simply reflectferences may arise as adaptations to divergent se-differences in the time since infection, with increasedlection regimes between ecological niches (Reimchen,time for growth resulting in increased size.1980, 1995) and to facilitate the utilization of differentIt is important to note that not all of the variability infood resources (Shine, 1991; Houston & Shine, 1993).parasitic infection between genders can be attributedStickleback are the only species of fish in Boultonto dietary differences. For example, there was hetero-Lake. Spatial and dietary niche differences betweengeneity in some parasitic or dietary trends among yearsthe genders may be driven by intraspecific com-and size classes and this heterogeneity was not alwayspetition for resources in the benthic habitat and maycongruent with differences between the genders in rel-be facilitated by the opportunity for females to exploitative parasitism or diet. Potentially, selective mortalitya pelagic niche in the absence of other competitivealso influences observed rates of infection. Fish infectedspecies of fish in open-water regions. However, dietarywith S. solidus exhibit a number of behavioural modi-differences between the genders were also detectedfications, including increased buoyancy, reduced swim-when males and females occupied similar habitat,ming speed and reduced responsiveness, which maysuggesting micro-spatial niche variation.make them more vulnerable to avian predators (Giles,

In summary, our results show infection rates in1983;Milinski,1985;Lobue&Bell,1993;Tierney,Hunt-Boulton Lake stickleback were species-specific andingford & Crompton, 1993; Ness & Foster, 1999). Fe-broadly associated with dietary differences, suggestingmales are more likely to be infected by S. solidus thanecological selection plays a major role in mouldingmales and thus may be more likely to suffer behaviouralparasite–host interactions. Examination of this long-modifications and thus predation. Also, five species ofterm data base also revealed that temporal shifts inavian piscivores forage on stickleback from Boultondifferential parasitism can be associated with temporalLake and these species exhibit differential foraging ef-shifts in the diet. Although numerous studies havefort between limnetic and littoral regions of the lakereported sex-biased parasitism (Poulin, 1996a for re-(Reimchen, 1980). Temporal changes in the relativeview), very few have looked for ecological differencesamount of littoral vs. limnetic foraging could influencebetween the genders that could provide a mechanismthe relative numbers of males (primarily littoral or ben-to account for such biases (but see Tinsley, 1989). Asthic) or females (primarily pelagic) predated, and thusthis is one of the first studies to examine sex differencesinfluenceobservedlevelsofmalevs. female infectedfish.in parasitism in relation to dietary niche variationIt is also possible that the female-biased S. solidusover multiple years, our results suggest associationsparasitism detected in this study results from higherbetween host-sex and parasitism are best interpretedmortality of parasitized males. This could occur ifin terms of both reproductive strategies and ecologicalmales are generally more stressed than females, duedifferences between the genders. Niche partitioningto the rigours of parental care during the reproductivebetween the sexes may be a cause of sexual dimorphismseason. However, this is inadequate to account for(Selander, 1966; Reimchen, 1980; Slatkin, 1984; Shine,our results. Firstly, pronounced female-biased S.1989, 1991; Anholt, 1992) and could contribute to sex-solidus parasitism occurred in pre-reproductive fishbiased parasitism.(30–39 mm), where males would not be subjected to

greater stress than females. Secondly, patterns ofdifferential parasitism for C. truncatus were opposite ACKNOWLEDGEMENTSto those for S. solidus (i.e. male-biased), suggestingsex-biased parasitism is unlikely to reflect increased T.E.R. thanks Natural Sciences and Engineering Re-mortality of infected adult males relative to females. search Council of Canada (A2354) for support, S.D.

The results of this study expand on previous work Douglas for field assistance and J. Westly for technicalon sexual dimorphism (Reimchen, 1980; Shine, 1989 assistance. P.N. thanks C. Shea and D. Wick for dis-

cussion.for review) and intra-population variability in general


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