Behavioral Ecology Advance Access originally published online on June 23, 2008
Behavioral Ecology 2008 19(5):1006-1011; doi:10.1093/beheco/arn070
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The influence of sex and sociality on parasite loads in an African ground squirrel
Department of Biology, University of Central Florida, 4000 Central Florida Boulevard, Orlando, FL 32816, USA
Address correspondence to J.M. Waterman. E-mail: waterman{at}mail.ucf.edu.
Received 18 March 2008; revised 23 April 2008; accepted 26 April 2008.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Male-biased parasite loads, which are common in vertebrates, could be a consequence of sexual selection, and for species that group, the costs of parasites could vary with group size or social structure. We examined sex-biased parasitism and the influence of group size on parasite loads in Cape ground squirrels (Xerus inauris), a highly social species that occurs in the arid regions of southern Africa. Group size did not affect numbers of ectoparasites or endoparasites. Males carried 3 times as many ectoparasites as females, but females harbored nearly 3 times as many endoparasites as males. Age class did not affect parasite loads in females, but in males, adults carried more ectoparasites than juveniles. Allogrooming was performed primarily by females, but no sex difference was found in autogrooming. Males in the subadult age class are becoming scrotal (indicating an increase in sex hormones) but typically remain in the natal group until adulthood, maintaining home range sizes comparable to adult females. Our results suggest that sexual selection does influence parasite loads in this species; increased androgen levels may reduce ectoparasite resistance in males, and smaller home ranges may increase females’ exposure to endoparasites. Allogrooming could reduce ectoparasite loads of the group and mitigate the costs of grouping.
Key words: ectoparasite, endoparasite, fleas, group size, grooming, lice, sex-biased parasitism, sexual selection, ticks.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The distribution and abundance of parasites within a host species can be influenced by both the sex and social organization of the host (Altizer et al. 2003
). Different reproductive strategies of males and females have led to the evolution of many differences in physiology, morphology, and behavior (Mooring et al. 1996, 2006a; Rolff 2002; Tella 2002; Stoehr and Kokko 2006). In many species, sexual selection has produced males with larger body size (to compete for females), larger home ranges (to find females), or large ornaments (to attract females; Deviche and Cortez 2005; Perez-Orella and Schulte-Hostedde 2005; Deviche and Parris 2006; Hoby et al. 2006; Nunn and Dokey 2006; Poulin and Lefebvre 2006). However, this heavy investment by males to compete for females may carry a cost of increased vulnerability to predators or parasites (Folstad and Karter 1992; Moller et al. 1999; Moore and Wilson 2002; Rolff 2002; Ottova et al. 2005).
In vertebrates, males frequently carry higher parasite loads than females (Schalk and Forbes 1997; Freeman-Gallant et al. 2001; Moore and Wilson 2002; Ferrari et al. 2004; Skorping and Jensen 2004; Perez-Orella and Schulte-Hostedde 2005; Deviche and Parris 2006; Isomursu et al. 2006). Differences in movement patterns, habitat choice, diet, body size, and ornamentation may all contribute to this sex bias in parasite loads (Verhulst et al. 1999; Ferrari et al. 2004; Hoby et al. 2006; Stoehr and Kokko 2006). Males with larger home ranges may carry more parasites than female conspecifics because they encounter more parasite-dense areas (Greenwood 1980; Ims 1987; Brei and Fish 2003; Nunn and Dokey 2006). However, sex-biased parasite loads could be an artifact of sexual size dimorphism. Larger males may be able to tolerate higher parasites loads (Schalk and Forbes 1997; Moore and Wilson 2002) as the energetic pressure (measured by basal metabolic rate) exerted by parasites on smaller hosts appears greater per gram of body mass (George-Nascimento et al. 2004). Yet even when accounting for differences in body size and home range, sex-biased parasite loads are often higher in species with strong sexual selection (Moore and Wilson 2002).
Trade-offs between investment in sexually selected traits and immune function may also lead to sex-biased parasitism (Folstad and Karter 1992; Sheldon and Verhulst 1996; Hosken and O'Shea 2001). The immunocompetence handicap hypothesis suggests that male sexual traits may lower the ability to resist pathogens and parasites through steroid suppression of the immune system (Folstad and Karter 1992). Testosterone directly suppresses immune function and indirectly influences many physical and behavioral attributes, resulting in higher male parasite loads (Sheldon and Verhulst 1996; Schalk and Forbes 1997; Moore and Wilson 2002; Deviche and Parris 2006; Isomursu et al. 2006). However, testosterone and parasite loads are not correlated in all species (Bilbo and Nelson 2001; Hughes and Randolph 2001). An alternative explanation for this trade-off is that the energetic costs of maintaining many sexually selected traits conflict directly with the cost of fighting off infection (Sheldon and Verhulst 1996; Hosken and O'Shea 2001) or that males just invest less in immunity than females (Rolff 2002).
Parasites also could be a major cost of sociality (Hoogland and Sherman 1976; Tella 2002; Altizer et al. 2003; Brown CR and Brown MB 2004; Johnson et al. 2004; Nunn and Heymann 2005). As group size increases, more individuals may carry parasites into the group in close quarters, augmenting parasite transmission (Hoogland and Sherman 1976; Hoogland 1995). However, a weaker relationship between grouping and parasites is expected if social mammals mitigate the increased costs of parasitism with grouping through direct behavioral strategies such as autogrooming (self-grooming) and allogrooming (grooming another individual; Mooring and Hart 1992; Hart 1994; Kollars et al. 1997; Johnson et al. 2004; Hawlena et al. 2006).
Intense sexual selection in Cape ground squirrels (Xerus inauris), a highly social rodent, is evident from several aspects of their mating system and morphology, including 1) a short and intense period of female receptivity (Waterman 1996), 2) a high operational sex ratio on a day of mating (Waterman 1998), and 3) extremely large testes, suggesting that sperm competition is an important determinant of male reproductive success (Waterman 1998; Manjerovic et al. 2008). In this study, we examined the impact of sexual selection on parasitism and the relationship of parasitism with group size. We hypothesized that parasitism of Cape ground squirrels is influenced by group size, group composition (i.e., number of males, females, adults, subadults, and juveniles), rates of autogrooming or allogrooming, and male dispersal. We predicted that ecto- and endoparasite loads would increase with group size, adult males would carry more parasites (ecto and endo) than females or juveniles, dispersed males would have greater numbers of parasites (ecto and endo) than nondispersed males, and that autogrooming and allogrooming would increase with ectoparasite load and group size but not with endoparasite loads.
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MATERIALS AND METHODS |
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Biology of the study animal
Cape ground squirrels live in the arid regions of southern Africa (Waterman 1995
) and have high potential for parasite transmission due to their sociality and communal living. Females live in matrilineal groups with other related adult females and their subadult young. These groups usually contain 1–3 adult females and up to 9 subadults of either sex (Waterman 1995). Within a female group, animals share a communal sleeping burrow (part of one burrow system), which may allow external parasites to transfer to another individual through bedding and direct contact (Hoogland 1995; Altizer et al. 2003). Females allogroom more than males and therefore may influence group ectoparasite loads (Waterman 1995).
Adult males are slightly larger than females (1.08:1.0; Waterman 1996) and usually disperse by 16 months of age to join all-male bands, which travel and sleep together independent of female groups (Waterman 1997). Home ranges of these males are 3 times the size of females’ home ranges (Waterman 1995). However, some males delay dispersal and remain with their natal group for 2–4 years (resident males; Waterman 1995) even though they are reproductively active.
Documented parasites of Cape ground squirrels include Ctenocephallaes connatus, Echidniphaga bradyta, Echidniphaga gallinacea, Neohaematopinus faurei, Synosternus caffer (Straschil 1975), Rhipicephalus theileri (Waterman 2002), and Xeroxyuris parallela, which is exclusive to this host (Hugot 1995). Endoparasites found in adult females by Scantlebury et al. (2007) included roundworms (27.2%), hookworms (21.7%), coccidia (8.3%), and other types (42.5%). These data have not been reported for males.
Trapping and handling
The study was conducted at the S.A. Lombard Nature Reserve near Bloemhof, South Africa (27°35'S, 25°23'E), from May–September 2004. Social groups were located on a natural floodplain, where the habitat is uniform short grass (Van Zyl 1965). We trapped all squirrels in 18 social groups with Tomahawk live traps (15 x 15 x 50 cm) using trapping and handling techniques described in Waterman (1996, 2002). Captured squirrels were restrained using a cone-shaped handling bag that kept the squirrel immobile while allowing access to different areas of the body to perform different procedures (Koprowski 2002). We recorded body mass, reproductive condition, and sex. For identification from a distance, animals were dye marked (Rodol D, Lowenstein & Sons Inc., New York, NY) and freeze marked (Quik-freeze, Miller-Stephenson Chemical Co., Danbury, CT; Rood and Nellis 1980). Animals were also tagged with small transponders under the skin for permanent identification (AVID Inc., Norco, CA). Squirrels were classified as juveniles up to 6 months after first emergence from the natal burrow. If first emergence was not observed, age was estimated from a regression of age against body mass (Waterman 1996). Squirrels were classified as subadults from 6 months of age until reaching sexual maturity (around 8 months for males and 9 months for females; Waterman 1996; Pettitt 2006). At maturity (first estrus) female nipples swell and remain permanently elongated (Waterman 1996). Male maturity is evident from descent of the testes; adult males are scrotal year-round, whereas subadult males are partially or nonscrotal (Waterman 1996, 2002). Scrotal development most likely is facilitated by large increases in androgens (Deviche and Cortez 2005; Hoby et al. 2006).
We collected ectoparasites from each captured squirrel by combing all individuals with a metal flea comb using 3 strokes on each plane of the back (left, middle, and right), from the shoulders to the base of the tail. Ectoparasites (fleas, ticks, and lice) were combed directly into 95% ethanol in a petri dish, which immediately killed them, and counted immediately. We estimated endoparasite loads from fecal samples, which were collected using plastic tarp sections placed under livetraps (Pettitt et al. 2007). We collected feces using forceps dipped in 95% ethanol and sealed the samples in labeled plastic bags. Subsequently, 0.5 g of fecal matter was weighed out and frozen. We later thawed these samples and prepared fecal flotations using a magnesium sulfate solution (McCurin and Bassert 2002), which caused eggs released by adult endoparasites to float. We then observed these prepared samples under a compound microscope for endoparasite egg identification and count (Villanua et al. 2007). Some squirrels did not defecate in the traps, decreasing the sample size for endoparasite data relative to ectoparasite sample size.
Behavioral observations
Cape ground squirrels are diurnal and live in open habitats (Smithers 1971; Herzig-Straschil 1978). The low vegetative cover on the floodplain allowed for relatively easy observation from hides on the roof of vehicles or observation towers. Our observations focused on morning and evening hours (700–1000 h and 1500–1800 h) when the squirrels are nearest the burrows (Waterman 1995). We arrived before squirrels emerged from burrows for morning observations, and evening observations continued until all squirrels immerged for the night. We collected behavioral data using all-occurrences methods (Altmann 1974) to record autogrooming and allogrooming (Waterman 1995), including the occurrence and duration (s) of the behavior and the identity of any squirrel being allogroomed (Waterman 1995). The cumulative amount of time (s) spent allogrooming (or autogrooming) was divided by the total amount of time that animal was observed (h) to determine the proportion of time (s/h) that an individual spent allogrooming (or autogrooming). To determine whether any particular sex or age class in the group was preferentially allogroomed, we calculated rate at which each age/sex category (adult male, adult female, subadult male, or subadult female) was allogroomed by each female as the number of allogrooms received by squirrels in that category divided by the total time that female was observed (h). We then standardized this rate by dividing by the number of squirrels in that category in the group.
Analysis
We used trapping data from June to compare body mass, parasite loads, and age class. Behavioral data were collected from June to September. All data were checked for homogeneity and normality and transformed if necessary. Data that could not be normalized or homogenized were analyzed with nonparametric statistics (Fry 1993). We used social group identity as a main factor in our analyses to account for potential differences among groups on ectoparasite loads. The relationship of ectoparasitism and endoparasitism with sex and age was analyzed using body mass a covariate and social group as a main factor in an analysis of covariance (ANCOVA). We considered the number of adult females in a group as well as the total group size to account for the potential influence of higher female allogrooming rates. We compared proportion of time spent autogrooming and allogrooming for all individuals with a minimum total observation time of 60 min. One group that disbanded in June was excluded from behavioral analyses. To compare which squirrels were allogroomed, only adult females that allogroomed and had at least one member in each sex/age class (other than adult males) were included because Friedman's 
2 test requires balanced data. A 0.05 probability of a Type I error was considered significant (Moran 2003).
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RESULTS |
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Body mass of adult males (mean ± standard error [SE]; 703 ± 8 g) and females (638 ± 7 g) differed (analysis of variance [ANOVA] F1,96 = 35.79, P < 0.001), although the male–female body mass ratio was low (1.1:1). Groups consisted of 1–6 adult females and their subadult and juvenile offspring. Many groups (12 of 18) had 1–2 adult males (resident males) sleeping in the burrow cluster with the group, but these males rarely remained at the cluster during morning observations. Endoparasites carried by adult males, resident and dispersed, included roundworms (15.0%), hookworms (25.0%), coccidia (20.0%), and other types (40.0%).
Parasite loads
Group size did not affect average number of ectoparasites (Spearman rank correlation rS = –0.16, N = 18 groups, P = 0.52) or endoparasites (rS = 0.14, N = 18, P = 0.57; Figure 1), nor were endoparasites correlated with ectoparasites (males: rS = –0.06, N = 30, P = 0.77; females: rS = –0.26, N = 41, P = 0.87). Likewise, number of adult females or resident males in the group did not affect average numbers of ectoparasites (females: rS = –0.37, N = 18, P = 0.13, resident males: rS = 0.21, N = 18, P = 0.40) or endoparasites (females: rS = –0.14, N = 18, P = 0.58, resident males: rS = 0.075, N = 18, P = 0.77).
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Resident (N = 23) and dispersed (N = 20) adult males did not differ in total ectoparasite loads (t-test t = 1.38, degrees of freedom [df] = 32.48, P = 0.18) or specific ectoparasites (Mann–Whitney U test: fleas U = 191.0, P = 0.33; ticks U = 204.5, P = 0.46; lice U = 213.5, P = 0.68). Resident and dispersed males also had similar endoparasite loads (mean ± SE; resident 1.3 ± 0.5 eggs, dispersed 1.2 ± 0.4 eggs; Mann–Whitney U test: U = 72.00, resident N = 16, dispersed N = 12, P = 0.36). Thus, data from all adult males were pooled for subsequent analyses.
Ectoparasite numbers (square root transformed) were not influenced by body mass when controlling for social group and sex (ANCOVA F1,67 = 0.01, P = 0.96). Adult males were more parasitized by fleas, ticks, and lice than adult females (Mann–Whitney U test: fleas U = 600.0, males N1 = 44, female N2 = 52, P < 0.001; ticks U = 941.0, P = 0.039; lice U = 724.5, P = 0.001; Table 1). Overall, total numbers of ectoparasites (square root transformed) were also significantly higher on males than females (Figure 2A) in adults (2-way ANOVA F1,62 = 23.22, N1 = 44, N2 = 52, P < 0.001) and subadults (F1,8 = 5.79, N1 = 9, N2 = 17, P = 0.043) but not in juveniles (F1,1 = 2.05, N1 = 4, N2 = 7, P = 0.39). Age class did not affect number of specific ectoparasites (i.e., fleas, ticks, or lice) on males (Kruskal–Wallis test: fleas 
= 3.83, adults N = 44, subadults N = 9, juveniles N = 4, P = 0.15; lice = 4.59, P = 0.101; ticks = 1.62, P = 0.45) or females (fleas = 0.05, adults N = 52, subadults N = 17, juveniles N = 7, P = 0.98; lice = 5.42, P = 0.067; ticks = 0.06, P = 0.97; Table 1). Likewise, total ectoparasite loads did not differ among age classes for females (2-way ANOVA: F2,73 = 0.41, P = 0.66), but total male ectoparasite loads tended to differ among age classes (F2,54 = 2.90, P = 0.064), with adult males carrying more ectoparasites than juvenile males (Tukey's honestly significant difference = 1.37, P = 0.050).
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Adult females had greater total endoparasite loads than adult males (Mann–Whitney U test: U = 406.50, males N1 = 30, females N2 = 41, P = 0.012; Figure 2B), although numbers of specific endoparasites (roundworms, hookworms, coccidia, and other endoparasites) did not differ (roundworms U = 2.00, N1 = N2 = 9, P = 0.35; hookworms U = 2.00, P = 0.35; coccidia U = 2.50, P = 0.43; other U = 4.50, P = 1.00; Table 1). No sex difference was found in subadult or juvenile endoparasite loads (subadults U = 26.50, males N1 = 4, females N2 = 15, P = 0.74; juveniles U = 3.00, N1 = 2, N2 = 3, P = 1.00). Total endoparasite loads did not differ among age classes for either males (Kruskal–Wallis test:
= 0.97, adults N = 30, subadults N = 4, juveniles N = 2, P = 0.62) or females ( = 0.79, adults N = 41, subadults N = 15, juveniles N = 3, P = 0.67; Figure 2B).
Grooming
Autogrooming (s/h, square root transformed) did not differ among age classes (3-way ANOVA: F2,55 = 2.13, adults N = 40, subadults N = 8, juveniles N = 10, P = 0.14) between sexes (F1,55 = 0.39, males N = 24, females N = 34, P = 0.54, Figure 3) or between dispersed (4.41 ± 1.65 s/h) and resident males (2.05 ± 1.00 s/h; ANOVA: F1,20 = 0.946, dispersed N = 13, resident N = 9, P = 0.34).
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Dispersed (0.41 ± 0.35 s/h) and resident (0.87 ± 0.64 s/h) males did not differ in time spent allogrooming (Mann–Whitney U test: U = 33.0, dispersed N1 = 13, resident N2 = 9, P = 0.14). However, adult females allogroomed significantly more than adult males (Mann–Whitney U test: U = 163.0, N1 = 23, N2 = 24, P = 0.008; Figure 3). Adult female allogrooming was not correlated with number of adult females in the group (Spearman correlation: rS = 0.31, N = 30, P = 0.098) or overall group size (rS = 0.08, P = 0.68). There was no difference in the sex/age category (adult females, subadult males and females) groomed by adult females (Friedman's
2 = 4.23, df = 2,12, P = 0.12). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Ectoparasite loads were highest in males (adults and subadults), but endoparasite loads were greater in females (Figure 2). These differing patterns of sex-biased parasitism suggest that different mechanisms may be operating, depending on the life-history characteristics of the parasites. For ectoparasites, the extensive daily movements of males through grass and brush and interactions with multiple female groups may expose them to greater numbers of ectoparasites. However, home range differences cannot explain the high ectoparasite loads of subadult males, whose home range is the same size as their female group members (Waterman 1995
). The sex-biased ectoparasite load in the subadult age class persists even though subadult males are allogroomed as much as other members of the group by the adult females. Thus, there appears to be a physiological basis to sex-biased ectoparasitism in this species.
Male and female differences in androgens (typically testosterone) can affect behavior or inhibit immune function, thereby influencing parasite loads (Moller et al. 1999; Bilbo and Nelson 2001; Rolff 2002; Khokhlova et al. 2004; Hawlena et al. 2006; Hoby et al. 2006). Males generally have higher concentrations of testosterone and under the immunocompetence handicap hypothesis should then be more susceptible to parasitic infections than females (Folstad and Karter 1992; Bilbo and Nelson 2001; Hughes and Randolph 2001; Rolff 2002). Age-related and seasonal changes in testosterone have been related to parasitic infections in a variety of taxa (Schalk and Forbes 1997; Isomursu et al. 2006). In a free-ranging ungulate (Rupicapra rupicapra rupicapra), androgen and cortisol output levels were correlated to high lungworm larvae estimates (Hoby et al. 2006). Folstad and Karter (1992) empirically determined that testosterone can decrease immunocompetence, and an increase in immune function can inhibit expression of secondary sexual characteristics (male ornamentation). This androgen/immune function trade-off was also observed in a meta-analysis by Muehlenbein and Bribiescas (2005). In Cape ground squirrels, reproduction is not seasonal, and males’ continued investment in reproduction could come with a cost of higher parasite loads year-round. This reproductive investment begins when males mature during the subadult age class (the transition age from nonscrotal to fully scrotal) and testosterone increases (Bilbo and Nelson 2001; Hughes and Randolph 2001; Hoby et al. 2006; Isomursu et al. 2006).
We expected male dispersal to affect parasite load because dispersed males have larger home ranges (MB Manjerovic, unpublished data) and would be exposed more frequently to ectoparasites, as has been seen in other rodents (Krasnov et al. 2005). However, neither ecto- nor endoparasite loads were affected by male dispersal. Because dispersed and resident males have similar circulating testosterone concentration (Scantlebury et al. 2008), but different ranging patterns, these data also support a hormonal basis for sex biases in parasite loads in Cape ground squirrels. Similar conclusions were made in studies of male-biased parasite loads in northern flying squirrels (Glaucomys sabrinus; Perez-Orella and Schulte-Hostedde 2005) and red squirrels (Tamiasciurus hudsonicus; Gorrell and Schulte-Hostedde 2008).
Endoparasite loads were also sex biased, but in the opposite direction predicted by the immunocompetence handicap hypothesis. Although the numbers of specific endoparasites (roundworms, hookworms, coccidia, and other) did not appear to differ between males and females (possibly a result of diminished sample size for specific endoparasites), cumulative endoparasite numbers were higher in females. This difference was significant only in adults (Figure 2B). This sex bias may be due to the life cycles of intestinal parasites, where inoculation occurs generally through ingestion of contaminated food or debris (oral–fecal contracted; Gemmell 1990; Ferrari et al. 2004). The high levels of endoparasite infection could be a consequence of a high concentration of feces in small home ranges (Nunn and Dokey 2006). Cape ground squirrel females have smaller home ranges than adult males (Waterman 1995) and therefore are more frequently exposed to conspecific fecal pellets concentrated in foraging areas around their burrow clusters. Adult males, however, move over large areas and sleep in vacant burrow clusters (Waterman 1995), avoiding lengthy exposure to areas with high concentrations of endoparasites. In this species, male avoidance of endoparasites and their lower endoparasite loads may be a positive by-product of sexual selection.
In mammals, promiscuous mating systems, social contact, and coloniality increase exposure to parasites, with transmission of ectoparasites through social contact and endoparasites primarily through feces (Hoogland and Sherman 1976; Gemmell 1990; Arnold and Lichtenstein 1993; Loehle 1995; Tella 2002; Altizer et al. 2003; Ferrari et al. 2004; Johnson et al. 2004). However, group size and parasite loads (both ecto- and endoparasites) were unrelated in Cape ground squirrels (Figure 1). Although exposure to ectoparasites may increase in larger groups, auto- and allogrooming may mitigate higher transmission rates (Mooring and Hart 1997; Neuhaus 2003; Mooring et al. 2006a, 2006b). Ectoparasite removal is the major function of grooming in gerbils (Meriones crassus; Hawlena et al. 2007) and rats (Hart 1992), and both auto- and allogrooming appear to target ectoparasites in Cape ground squirrels (Hillegass 2007).
Our results indicate that the life history of parasites strongly affects the likelihood of infection. Investigating either ectoparasite or endoparasite infections alone would have led to very different conclusions about sex-biased parasitism in this species as only patterns of ectoparasite infection were consistent with the immunocompetence handicap hypothesis. In male Cape ground squirrels, parasite resistance may be suppressed directly by androgens affecting leukocyte production or merely may be a trade-off between investments in reproduction versus immune function. In females, parasitism may suppress metabolism (Scantlebury et al. 2007), possibly impacting reproductive success. To determine the evolutionary costs of parasitism in this species, we need to determine the physiological effects of parasitism and the potential impacts on reproductive success.
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FUNDING |
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National Science Foundation grant (IBN0130600) to J.M.W.
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ACKNOWLEDGEMENTS |
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We thank Northwest Parks and Tourism of South Africa and the staff of the S.A. Lombard Nature Reserve for their permission to conduct this research and their continued support. We also thank B. Pettitt, J. Calldo, M. Scantlebury, and T. Mulaudzi for their assistance in the field and C.J. Anderson, D. Jenkins, M.B. Manjerovic, and 2 anonymous reviewers for valuable suggestions and comments on the manuscript.
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