Parasitol Res DOI 10.1007/s00436-014-3937-2

ORIGINAL PAPER

Variable effects of host characteristics on species richness of flea infracommunities in rodents from three continents Christian Kiffner & Michal Stanko & Serge Morand & Irina S. Khokhlova & Georgy I. Shenbrot & Anne Laudisoit & Herwig Leirs & Hadas Hawlena & Boris R. Krasnov

Received: 25 February 2014 / Accepted: 30 April 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract We studied the effect of host gender and body mass on species richness of flea infracommunities in nine rodent host species from three biomes (temperate zone of central Europe, desert of the Middle East and the tropics of East Africa). Using season- and speciesspecific generalized linear mixed models and controlling for year-to-year variation, spatial clustering of rodent sampling and over-dispersion of the data, we found inconsistent associations between host characteristics and flea species richness. We found strong support for male-biased flea parasitism, especially during the reproductive period (higher species richness in male hosts than in females) in all considered European rodents (Apodemus agrarius, Myodes glareolus and Microtus arvalis) and in one rodent species from the Middle East (Dipodillus dasyurus). In contrast, two of three African

rodent species (Lophuromys kilonzoi and Praomys delectorum) demonstrated a trend of female-biased flea species richness. Positive associations between body mass and the number of flea species were detected mainly in males (five of nine species: A. agrarius, M. glareolus, M. arvalis, D. dasyurus and Mastomys natalensis) and not in females (except for M. natalensis). The results of this study support earlier reports that gender-biased, in general, and male-biased, in particular, infestation by ectoparasites is not a universal rule. This suggests that mechanisms of parasite acquisition by an individual host are species-specific and have evolved independently in different rodent host-flea systems. Keywords Body mass . Fleas . Infestation bias . Rodents . Sex

Electronic supplementary material The online version of this article (doi:10.1007/s00436-014-3937-2) contains supplementary material, which is available to authorized users. C. Kiffner Department of Forest Zoology and Forest Conservation incl. Wildlife Biology and Game Management, Büsgen-Institute, Georg-August-University Göttingen, Göttingen, Germany C. Kiffner (*) Center for Wildlife Management Studies, The School for Field Studies, Karatu, Tanzania e-mail: [email protected] M. Stanko Institute of Parasitology, Slovak Academy of Sciences, Kosice, Slovakia

I. S. Khokhlova : G. I. Shenbrot : B. R. Krasnov Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel I. S. Khokhlova : G. I. Shenbrot : H. Hawlena : B. R. Krasnov Department of Life Sciences, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel A. Laudisoit : H. Leirs Evolutionary Ecology Group, University of Antwerp, Antwerp, Belgium

S. Morand CIRAD—AGIRs, Montpellier, France S. Morand CNRS—Institut des Sciences de l’Evolution, Montpellier, France

A. Laudisoit School of Biological Sciences, University of Liverpool, Liverpool, UK

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Introduction Gender-biased parasitism in higher vertebrates (birds and mammals) is a well-known phenomenon (see Krasnov et al. 2012 for review). In general, the common paradigm is that in the majority of birds and mammals, males are more parasitized than females due to either higher mobility (Jetz et al. 2004; Boyer et al. 2010; Calabrese et al. 2011) or lower immunocompetence (Sheldon and Verhulst 1996; NavarroGonzalez et al. 2011) or both (Zuk and McKean 1996; Harrison et al. 2010; Kiffner et al. 2011a; but see examples of female-biased parasitism in bats; Zahn and Rupp 2004). This suggests that pressure of parasitism and, consequently, negative impacts of parasitism are higher for males than those for females. Gender-biased impact may, in turn, have important consequences for host individuals (Folstad and Karter 1992; Råberg et al. 2009), populations (Anderson and Gordon 1982; Moore and Wilson 2002; Ferrari et al. 2004) and communities (Buckling and Rainey 2002). Male-biased parasitism has been reported for a variety of host and parasite taxa (Poulin 1996; Schalk and Forbes 1997; Perkins et al. 2003). However, many of these studies had at least two substantial flaws. First, they represented a snapshot of parasite distribution among host individuals and often did not control for temporal (annual and seasonal) and/or spatial variability of the observed patterns (cf. Vázquez et al. 2011 vs Vor et al. 2010). Second, they often ignored morphological differences between genders such as sexual size dimorphism so that it was unclear whether the reasons behind male-biased infestation were gender differences in mobility and/or immunocompetence (e.g. Krasnov et al. 2005) or differences in body size (Kiffner et al. 2011a). When spatial/temporal variability and body size differences were taken into account, gender-biased infestation appeared to not be a universal rule; its direction and manifestation depended on host-specific ecological and behavioural traits (Kiffner et al. 2013). Third, the degree of parasite pressure and infestation differences between males and females were often estimated via abundance and/or prevalence of parasites (Morand et al. 2004; Brunner and Ostfeld 2008; Kiffner et al. 2011b). These estimates of parasite pressure are undoubtedly important because they mirror the magnitude of the parasitological challenge. However, they do not take into account the diversity of challenges imposed by multiple parasite species (Bordes and Morand 2009). Parasite species richness as an indicator of parasite pressure started recently to attract attention (Bordes and Morand 2009). It was found that parasite species richness has substantial and diverse effects on a variety of host traits at a variety of levels. For example, at the genetic level, parasite species richness was correlated with genetic diversity at the major histocompatibility complex (MHC) (e.g. Goüy de Bellocq et al. 2008). At the physiological level, an association between parasite species richness and basal metabolic rate of host species was

demonstrated (Morand and Harvey 2000). At the immunological level, parasite species richness was found to be associated with investment in immunity (Moller and Rosza 2005; Šimková et al. 2008) and patterns of mounting an immune response (Khokhlova et al. 2004; Bordes et al. 2012). At the behavioural level, parasite species richness appeared to be linked to anti-predator behaviour of individual hosts (Alzaga et al. 2008). In addition, an interspecific correlation between parasite species richness and the degree of sociality was reported (Bordes et al. 2007; Hillegasss et al. 2008; Viljoen et al. 2011). Finally, evolutionary diversification of hosts could also be affected by parasite species richness (Nunn et al. 2004). All the studies mentioned above suggest that investigations of variation in parasite pressure among host individuals should take into account not only a magnitude of parasitological challenges but also their diversity. Recently, we studied flea infestation of nine rodent species from three different biomes (temperate zone of central Europe, desert of Middle East and tropics of East Africa) and tested for independent and interactive effects of host sex and body mass on the number of fleas harboured by an individual host while accounting for spatial clustering of host and parasite sampling and temporal variation (Kiffner et al. 2013). We estimated parasite infestation via the total number of all fleas collected from an individual host and found that (a) the effect of host individual characteristics on mechanisms responsible for flea acquisition differed among species and (b) among-host differences in the effect of sex on flea infestation were associated with among-host differences in ecology and behaviour. Ecological and/or behavioural features of a host species may affect the probability of encountering fleas and the probability of acquiring them once encountered. In this study, we used data from the same rodent surveys but focused on the number of flea species instead of the number of flea individuals on a rodent host. We asked whether hostrelated correlates for flea diversity mirror those for flea numbers. Similar patterns between gender or body mass/flea abundance and gender or body mass/flea species richness relationships would indicate amplified parasite pressure on individuals of a given gender or body mass cohort. Opposite patterns with respect to flea burdens and flea species richness would indicate a compensation of high magnitude of one of the components of parasite pressure (e.g. parasite abundance) by low magnitude of another component (e.g. the diversity of parasite challenges). In addition, the lack of conformity between gender or body mass/flea abundance and gender or body mass/flea species richness would suggest independence of the two components of parasite pressure.

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Materials and methods Sampling of rodents and fleas We analysed data on flea-rodent associations from various rodent communities in central Europe (Slovakia) (Apodemus agrarius Pallas, Myodes glareolus Schreber and Microtus arvalis Pallas), Middle East (Israel) (Gerbillus andersoni de Winton, Meriones crassus Sundevall and Dipodillus dasyurus Wagner) and East Africa (Tanzania) (Mastomys natalensis Smith, Lophuromys kilonzoi Verheyen et al. and Praomys delectorum Thomas). A detailed description of sampling procedures and parasitological examination of rodents in each of the geographic regions can be found elsewhere (Kiffner et al. 2013). In brief, rodents and fleas in Slovakia were collected in 18 localities between 1983 and 2001 (in various forests, agricultural areas and gardens; total area covered by sampling was about 600 km2). In Israel, sampling was carried out in hyperarid and arid stony desert and sand dunes of the Negev desert from 1992 to 2004 (area covered by sampling was about 800 km2). In Tanzania, rodents and fleas were sampled in four localities in the West Usambara Mountains (in submontane and montane forests, shrubbery in forests and grasslands, crop fields and commercial timber or fruit tree plantations) in 2005–2008 (total area covered by sampling was about 250 km2). Data were collected during both warm and cool seasons (May–September and October–April, respectively, in Slovakia and April–October and November– March, respectively, in Israel) or dry and wet seasons (June– September/January–February and October–December/ March–May, respectively, in Tanzania). Main breeding seasons for rodents from Slovakia, Israel and Tanzania are warm, cool and wet, respectively. Age of each rodent was estimated based on the visual investigation of their genitalia. Rodents were either sexually active (during the breeding season) or sexually inactive but nonetheless mature. Information on flea species recorded on these rodents can be found in the digital appendix. Some individual rodents with very low body mass could be subadult but erroneously identified as adults. However, the number of these individuals was small (their percentage ranged from 0.8 % in M. glareolus to 3.6 % in L. kilonzoi and only attained 7.2 and 12.5 % in P. delectorum and M. natalensis, respectively). In total, we used data on fleas collected from 8,539 individual rodents. Data analysis The response variable in our analyses was the number of flea species collected from each individual rodent. We analysed data using generalized mixed effects models. By definition, flea species richness on individual hosts is a count, and thus, analyses require count regression techniques (Hilbe 2011). Frequency

histograms of the number of flea species found on a rodent indicated that the data were over-dispersed (Fig. 1). Therefore, we followed Elston et al. (2001) and fitted a lognormal-Poisson model by including an individual-level random variable to account for overdispersion. Overall, our data analyses followed a multimodel approach outlined by Grueber et al. (2011). In order to test whether host body mass and sex were associated with the number of flea species, we fitted several a priori models to each rodent-flea species data set. Because many flea species occur during a certain season only (see Krasnov et al. 1997, 2002 for the Negev desert, Krasnov et al. 2006a for Slovakia and Laudisoit et al. 2009 for Tanzania), we fitted models for each rodent species separately for each season. Initially, we fitted a global generalized linear mixed model (GLMM) to the season-specific data using the package lme4 (Bates and Maechler 2009) implemented in R (R Development Core Team 2011). This global model included sampling grid (to account for nonindependence caused by the clustered sampling approach), year (to account for yearly variation) and observation effect (to account for over-dispersion) as random effects, and host sex, body mass and their interaction as fixed effects. We standardized the input variables of the global models using the arm package to simplify the interpretation of model coefficients (Gelman et al. 2013). To generate a full model set for each rodent-flea association (including an intercept-only model), we used the “dredge” function of the MuMIn package (Bartón 2013). For each of the generated models, the sample size-corrected Akaike information criterion (AICc) and corresponding Akaike weights were computed. Since several models received similar support, we used model averaging (Burnham and Anderson 2002) to estimate regression coefficients of the variables. We usually restricted model averaging of regression coefficients to models within two AICc scores of the top model. We extended model averaging to models within four AICc scores of the top model in G. andersoni, L. kilonzoi (wet season) and P. delectorum (wet season) and to models within three AICc scores of the top model in M. crassus and M. natalensis (wet season) to include at least three models for averaging regression coefficients. Model averaging was performed using the natural average method implemented in the MuMIn package (Bartón 2013). This method was chosen over the zero method because the natural average is more suitable when particular variables (body mass and sex) are of interest (Grueber et al. 2011). To illustrate our findings, we predicted flea species richness on an individual rodent for the range of body masses and rodent gender for an average year and each season. For easier interpretation,

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Flea species richness we transformed the model predictions into percentages of change in the number of flea species harboured by an individual rodent per unit (g) body mass change (further referred to as PCBM) and sex bias (further referred to as SB; percentage difference between the sexes for rodents with average body mass; male vs female) using the following equation:
Coefficient ð%Þ ¼ 1−einterceptþcoefficient = eintercept  100:

Results Model averaged effects of gender, body mass, locality and year on the number of flea species harboured by an individual rodent for European, Middle Eastern and East African rodents are presented in Tables 1, 2 and 3, respectively. Figures 2, 3 and 4 represent illustrative examples of gender, body mass and flea species richness relationships. In Europe, species richness of flea infracommunities in A. agrarius was significantly higher in males than that in females in both seasons (SB=48.83 in cool season and SB= 17.87 in warm season, p0.63 for all). In the warm season, males with average body mass tended to harbour more flea species than females of average body mass; this difference was marginally significant (SB=22.76, p=0.09). In addition, the number of flea species increased with an increase in body mass in males, but not in females (PCBM=108.09, p0.05, marginal statistical significance; **p≤0.05, statistical significance

Aa A. agrarius, Mg M. glareolus, Ma M. arvalis, SE standard error of Table 2 Averaged regression coefficients of host gender, and body mass on species richness of flea infracommunities in Middle Eastern rodents (desert biome) Species

Parameter

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Intercept

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Sex (male vs female) Body mass Sex (male) × body mass Intercept

Dd

Sex (male vs female) Body mass Sex (male) × body mass Intercept

Sex (male vs female) Body mass Sex (male)×body mass

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Warm season

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SE

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0.42** Grid 0.0001 Year 0.00 0.28 0.14 0.11 Grid 0.00 Year 0.0000 0.31** 0.260 0.60*

Empty cells indicate that the variable was not present in the best models. The standard deviation of the random intercepts for the sampling grid and year are reported in the intercept row Ga G. andersoni, Mc M. crassus, Dd D. dasyurus, SE standard error of estimate

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Table 3 Averaged regression coefficients of host gender, and body mass on species richness of flea infracommunities in East African rodents (tropical forest biome) Dry season

Wet season

Sex (male) × body mass 1.16* Intercept 0.21** Grid 0.00 Year 0.00 Sex (male vs female) Body mass −0.09 Sex (male) × body mass Intercept −0.77** Grid 0.38 Year 0.15 Sex (male vs female) −0.28* Body mass 0.05 Sex (male) × body mass

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−0.67** 0.27 −0.35 0.43 Grid 0.33 Grid 0.26 Year 0.00 Year 0.00 −0.60* 0.35 −0.03 0.21 0.70** 0.31 0.46** 0.19

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Fig. 3 Predicted species richness of flea infracommunities in relation to body mass of male and female D. dasyurus in the cool (a) and warm (b) season

Empty cells indicate that the variable was not present in the best models. The standard deviation of the random intercepts for the sampling grid and year are reported in the intercept row Mn M. natalensis, Lk L. kilonzoi, Pd P. delectorum, SE standard error of estimate

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Among Middle Eastern rodents, in both G. andersoni and M. crassus, neither sex nor body mass was associated with the number of flea species harboured by an individual rodent during either season (SB=4.16–31.82 and PCBM=5.13– 29.70, p>0.34 for all). Male D. dasyurus harboured more flea species than females in the cool season (SB=35.97, p=0.05), whereas the best models for the warm season did not include host gender at all (Fig. 3). The relationship between male body mass and the number of flea species was marginally significant in the cool season, but was non-significant in the warm season (PCBM=136.51, p=0.09 and PCBM=13.93, p=0.45, respectively). Host body mass and species richness of flea infracommunities were not significantly associated in female D. dasyurus during both the cool and warm seasons (PCBM= 30.29 and PCBM=13.94, respectively, p>0.13 for both). In East Africa, female M. natalensis and P. delectorum tended to harbour more flea species than males in the dry season (SB=−45.38, p=0.08 and SB=−24.60, p=0.07; see Fig. 4 for an illustrative example of M. natalensis) but not in the wet season (SB=−3.34 and SB=−24.13, respectively, p>0.56 for both). In M. natalensis, species richness of flea infracommunities was positively correlated with body mass in both genders and in both seasons; the relationship tended to be stronger in males than in females in the dry season (male PCBM =542.44, p=0.06 and female PCBM=102.10, p= 0.02). During the wet season, an increase in body mass was associated with higher flea species richness in both genders (male PCBM=57.97 and female PCBM=57.97, p=0.02 for both). However, the intercept in the models for M. natalensis did not reach statistical significance, suggesting that predictions from these models may be associated with a high margin of error. No relationship between the number of flea species and body mass was found in P. delectorum and L. kilonzoi (PCBM=−8.98–30.41, p>0.42 for all). Furthermore, no significant gender differences in the number of flea species were found in L. kilonzoi in the wet season (SB=16.46, p=0.640), whereas the best models for the dry season did not include host gender at all. Sampling locality (=grid) strongly affected species richness of flea assemblages on individual rodents in Europe as indicated by the standard deviation of the random intercepts being ≥0.1 in all six models (Table 1). However, this effect was much weaker in East Africa (three of six models; Table 3) and did not occur in the Middle East (none of the models; Table 2). Similarly, between-year variation mediated flea species richness in Europe and East Africa (four and three of six models, respectively), but not in the Middle East (one of six models).

Discussion The results of this study are compared with those of our earlier study (Kiffner et al. 2013) in Table 4. The pattern of gender

bias was similar for flea abundance and the number of species in the European rodents. This, however, was not the case for the Middle Eastern and African rodents. In the Middle East, gender (male)-biased flea abundance was not accompanied by male-biased flea species richness (G. andersoni) and vice versa (D. dasyurus). In East Africa, no gender-biased flea abundance was found, but trends of gender (female)-biased flea species richness were revealed in two species. Positive relationships between body mass and both flea abundance and flea species richness were found in females of only one species (M. natalensis). In females of four species (A. agrarius, M. glareolus, G. andersoni and M. crassus), body mass was correlated with flea abundance, but not with their species richness. In the remaining species, neither flea abundance nor species richness was affected by female rodent body mass. In males, the same direction of the body mass/flea abundance and body mass/flea species richness relationships was found in two species (M. glareolus and M. natalensis) and an opposite trend was found in one species (M. arvalis). In addition, body mass was correlated with either flea abundance or the number of their species (but never both) in four species and no relationships were found between body mass and either infestation variable in two species. Mechanisms of gender-biased parasitism The strongest support for gender-biased parasitism in terms of species richness of infracommunities was found in European rodents. This was manifested in (a) richer infracommunities in male than female rodents and (b) a positive relationship between the number of flea species and body mass in male hosts. The male-biased species richness of flea infracommunities together with malebiased flea abundance (Kiffner et al. 2013) suggests that pressures associated with fleas are substantially higher in males than those in females. The main mechanisms behind higher infestation by parasites of males in higher vertebrates (birds and mammals) are thought to be either their lower immunocompetence (Folstad and Karter 1992; Råberg et al. 2007; Navarro-Gonzalez et al. 2011) or higher mobility (Boyer et al. 2010; Calabrese et al. 2011) or both. Although these mechanisms have been repeatedly discussed, there is still no consensus which is the predominant driver of male-biased parasitism (see Krasnov et al. 2012). Nevertheless, the similar direction of host-related correlates for flea abundance and species richness of their infracommunities suggests that the same mechanisms cause male-biased parasitism in the European rodents. Moreover, male-biased parasitism was more pronounced in the warm season than in the cool season, and differences between males and females in pattern of flea infestation were stronger during the reproductive period. Indeed, sex differences in

Parasitol Res Table 4 Summary of the relationships between host sex and body mass and flea abundance and the number of flea species Characteristic of flea infracommunity

Abundance Species richness Abundance Species richness Abundance Species richness

Characteristic of host individual

Sex

Sex Body mass

Female

Body mass

Male

Europe

Middle East

East Africa

Aa

Mg

Ma

Ga

Mc

Dd

Mn

Lk

Pd

M MM + 00 0 0+

M MM + 00 + +* +

M* n M* 0 00 − 0+

M nn + 00 + 00

n nn + 00 + 00

n Mn 0 00 0 +* 0

n F* n + ++ + ++

n nn 0 00 0 00

n F* n 0 00 0 00

Source: Kiffner et al. (2013) and this study. For number of flea species, the first entry refers to cool season for Europe and Middle East and to dry season for East Africa. The second entry refers to the warm and wet season, respectively (see Tables 1, 2 and 3 for abbreviation of rodent species names)

M male bias, F higher parasite burden in females, + (−) positive (negative) relationships between body mass and abundance/number of species of fleas, n lack of gender bias, 0 non-significant (p>0.1) relationships between flea abundance/number of species and body mass

spatial behaviour of rodents are usually more distinct during the reproductive than non-reproductive period (Lott 1991). This may be because reproductive males increase their mobility and expand their home ranges for the sake of increasing mating chances (Schwarzenberger and Klingel 1994; Waterman 2007). In contrast, reproductive females may benefit from decreased mobility, so they may occupy a separate burrow for parturition (Wolff 1993). Moreover, territoriality during the reproductive period in, for example, bank voles and wood mice allows them to decrease food competition with other females (Bashenina 1962; Ostfeld 1985; Gliwicz 1988). As a result, highly mobile males have higher chances to encounter parasites (Clay et al. 2009), while these chances are obviously lower for territorial females. Androgens are associated with the functioning of the reproductive system (Bronson 1989) and play an important role in the development of aggressive behaviour related to mate competition (Bronson and Desjardins 1971; Razzoli et al. 2003). Concomitantly, these hormones are thought to suppress the immune function (Folstad and Karter 1992; Zuk 1996; Zuk and McKean 1996). Reproductive males are characterized by increased levels of androgens (Zuk 1996; Creel et al. 1992; Gleason et al. 2009) and thus not only represent a more suitable patch for parasites than females (Luong et al. 2010) but might also be more prone than females to host multiple parasite species. Although the immunosuppressive role of androgens is still debated (Casto et al. 2001; Rolff 2002; Schmid-Hempel 2003), there is experimental evidence for better parasite performance when exploiting male as compared to female rodents from laboratory colonies (Khokhlova et al. 2009, 2010). Because rodents in these experiments did not differ in their spatial behaviour, the most likely reason

for differential parasite performance was differences in host hormonal status.

*0.10≥p>0.05, marginally significant relationships

Consequences of gender-biased parasitism Even though we cannot elucidate the underlying mechanisms (higher immune investment in female vs male rodents and/or higher encounter rates with parasites in males) of male-biased parasitism, male-biased parasitism may have important consequences for parasite populations and community dynamics. Because parasites seem to have higher probability to encounter a male than a female host and feeding performance of parasites may be higher in a male than a female host, parasite populations may crucially depend on male vertebrate hosts. Indeed, Ferrari et al. (2004) demonstrated that the elimination of parasites (a nematode Heligmosomoides polygyrus) in female rodents (Apodemus flavicollis) did not influence the abundance and distribution of parasites in males, whereas removal of parasites from males caused a substantial decrease in parasite infestation in females. This suggests that male hosts—at least in this rodentnematode system—are responsible for driving parasite population dynamics. Furthermore, Krasnov et al. (2011) investigated patterns of co-occurrences of different flea species on individual males and females of 16 rodent species from Africa and Eurasia by comparing frequencies of co-occurrences with those expected by chance and found that the frequency of detecting non-randomness (aggregation) in flea cooccurrences was significantly higher in males than in females indicating that male hosts may drive not only populations but also community dynamics of parasites. Interestingly, host sex differences in flea infracommunity structure were found mainly in rodents from the temperate zone, while this difference was very weak, if at all present, in African rodents, supporting the results of the present study. In addition, a wider range of macroparasite species harboured by one but not by the other

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sex might also increase the likelihood for infections of individuals of this gender with microparasites (such as bacteria and viruses) which are often vector-specific. Geographic trends in gender-biased ectoparasitism In the present study, evidence for gender-biased parasitism in terms of the number of flea species in the Middle Eastern and East African rodents was much weaker than that for the European rodents. Nevertheless, some region-specific trends could be envisaged. Similarly to the European rodents, whenever gender bias in species richness of flea infracommunities was found in the Middle Eastern rodents, it was towards males and occurred mainly in the cool season (reproductive period of these hosts). In East Africa, gender-biased parasitism tended to be towards females and occurred mainly in the dry season. However, in the only species demonstrating a significant effect of body mass on the number of flea species, it tended to be steeper in males than in females. Comparison of these patterns with those of flea abundance (Kiffner et al. 2013, Table 4) suggests that the effects of gender or body mass on flea abundance and species richness are independent. In contrast to the European rodents, male-biased flea abundance in the Middle Eastern rodents was not accompanied by malebiased flea species richness and vice versa. One of the reasons for this pattern may be the substantially poorer pool of flea species occurring in the Negev desert as compared to Slovakia (see Krasnov et al. 1999 vs Stanko et al. 2002, respectively). For example, the total number of flea species recorded on G. andersoni, M. crassus or D. dasyurus was four, six and eight, respectively, while A. agrarius, M. glareolus or M. arvalis harboured 16, 18 and 13 flea species, respectively. Low number of flea species may mask an actual relationship between host gender and richness of flea infracommunities in the Middle East. In addition, earlier reports of gender-biased parasitism in terms of the number of flea species in G. andersoni and M. crassus (Krasnov et al. 2005) were not supported by the analyses applied in the present study. Similarly to gender effect on flea abundance (see Kiffner et al. 2013), the likely reason behind inconsistencies in Krasnov et al. (2005) and the present study is that temporal (yearly variation) and spatial (sampling locality) heterogeneity of parasite infestation had not been taken into account in the former study. However, spatial and/or temporal heterogeneity of infestation may not only affect individual flea infestation (Krasnov and Matthee 2010) but also may mask true effects of host gender on the number of flea species (Kiffner et al. 2013). Among African rodents, females of two species tended to harbour more flea species than males during the dry season. In one of these species, M. natalensis, this period is characterized by decreased reproduction and increased population density (on account of young animals) (Makundi et al. 2007; but see Leirs et al. 1989), although density decreases towards the end

of the dry season (Makundi et al. 2007). Increased population density often acts as a trigger of dispersal (Matthysen 2005). Interestingly, female-biased dispersal has been found for M. natalensis (van Hooft et al. 2008), although it is a rare phenomenon in small mammals (Stenseth and Lidicker 1992). Higher dispersal activity of females might increase encounter rates with multiple flea species. However, female-biased dispersal was reported for some but not all M. natalensis populations (van Hooft et al. 2008). This may be the reason for difference in species richness of flea infracommunities between male and female M. natalensis being only marginally significant. In addition, M. natalensis is characterized by unusually high male mortality during the breeding season when the adult female/male sex ratio may attain 2.5–9 (Leirs 1992). This may lead to accumulation of multiple flea species on female rodents and, consequently, to a female-biased infestation. Available information on P. delectorum is too scarce for providing reasonable explanations on the mechanism leading to female-biased flea species richness. Body mass and ectoparasitism One of the hypothetical mechanisms underlying the relationships between body mass and richness of directly transmitted parasites is that larger hosts constitute larger ‘islands’ for the parasites, so that interspecific competition between parasites is reduced in larger hosts and parasite co-existence is thus facilitated (Lindenfors et al. 2007; Poulin and George-Nascimento 2007). However, the absolute difference in body size among conspecific rodents is too small for this mechanism to be of substantial importance. It is more likely that the positive body mass-flea species richness relationship observed in some species (and see Klimpel et al. 2007) arises because body mass is correlated with some trait(s) that directly increase either the encounter rates with multiple flea species or the performance of any flea species (Rueesch et al. 2012) or both. For example, body mass in males of various rodent species has been shown to be positively correlated with the size of their home ranges (Borowski 2003; Koshev et al. 2005). Larger home range of an individual may lead to more frequent encounters with ectoparasites, higher probability of encounters with multiple parasite species and increased rates of intraspecific and interspecific direct and indirect contacts, such as visitation rates of other burrows (Jetz et al. 2004; Clay et al. 2009; Previtali et al. 2010). For instance, direct and indirect contacts between rodents belonging to different species may result in ectoparasite exchange (Krasnov and Khokhlova 2002). Furthermore, interindividual variability in home range size is mainly characteristic for the breeding period (Schwarzenberger and Klingel 1994) and was reported mainly for rodents from the temperate zone (Ims 1987; Erlinge et al. 1990; Attuquayefio et al. 2009). This explanation is strengthened by the fact that we found positive body mass-flea species richness

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relationships mainly in (a) the European host species, (b) males and (c) the reproductive period. An additional explanation for higher number of flea species in heavier individuals might be related to the fact that at least some of these individuals were senescent. The immune system in older individuals could be deteriorated (Ginaldi et al. 2001) and not be able to cope with multiple challenges from several flea species. Furthermore, the age-related decline of various immunological parameters tends to be less pronounced in females than in males (Caruso et al. 2013; Hirokawa et al. 2013). This may be the reason behind the lack of relationships between body mass and the number of flea species in females of most species.

Conclusion The results of this study supported our earlier results (Kiffner et al. 2013) that gender-biased, in general, and male-biased, in particular, ectoparasitism is not a universal rule. This suggests that mechanisms of parasite acquisition by an individual host are species-specific (Matthee et al. 2010) and have evolved independently in different host-flea systems (Korallo et al. 2007). While host characteristics were frequently related to flea abundance, they were less frequently associated with species richness in flea infracommunities (Table 4). Infracommunities of fleas are highly ephemeral (Krasnov et al. 2006a, b), and the majority of flea species occur at very low relative abundances (see Supplementary Material of Kiffner et al. 2013). Given this high variability, host-related factors are probably less important than environmental conditions in explaining species richness of ectoparasites (Krasnov et al. 2004). Acknowledgments Allan Degen read the earlier version of the manuscript and made helpful comments, and Kiri Brenner edited the English. Studies in Israel were partly supported by Israel Science Foundation (grant 26/12 to ISK and BRK). Studies in Slovakia were conducted under the licenses of the Ministry of Environment of the Slovak Republic No. 297/108/06-3.1 and No. 6743/2008-2.1 and partly supported by the Slovak Research and Development Agency (grant APVV 0267-10 to MS). Studies in Tanzania were supported by the Belgian Fund for the Research in Industry and Agro-alimentary, the Fund for Scientific Research—Flanders for scientific research, the University of Antwerp and the Sokoine University of Agriculture (Tanzania). This is publication no. 834 of the Mitrani Department of Desert Ecology.

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