Male-biased Parasitism Research Articles

Male-Biased Parasitism of Brandt's Voles (Lasiopodomys brandtii) in Inner Mongolia, China.

The abundance and prevalence of parasitic infection often vary in different host sexes, and this phenomenon has been named sex-biased parasitism. Brandt's voles are the dominant rodent species in typical steppe habitat and are widely distributed in Inner Mongolia, China, but the prevalence of parasites in Brandt's voles are poorly reported. In this study, we investigated the prevalence of six intestinal parasites in Brandt's voles in May, June, July, and August 2022 around the Xilingol Grassland in Inner Mongolia, China. The results showed that Syphacia obvelata, Aspiculuris tetraptera, and Trichostrongylidae family were the dominant intestinal parasites in Brandt's voles that we captured in this study, and the infection rates of the three parasites were significantly higher in males than females, which showed obvious male-biased parasitism. Season and human activities such as grazing had no significant effect on the infection rates for different parasites, while the parasite reproduction level was higher when the ambient temperature was around 18 °C. Sexual size dimorphism was ubiquitous in Brandt's voles, and it was mainly manifested by the differences in body weight and length between males and females. Simple linear regression analysis showed a significant positive correlation between bodyweight and parasite infection rates, so the sex-biased parasitism in Brandt's voles could be explained by the body size hypothesis, as a larger body could provide more ecological niches for parasitic infection.

Mortality cost of sex-specific parasitism in wild bird populations

Sex-specific mortality is frequent in animals although the causes of different male versus female mortalities remain poorly understood. Parasitism is ubiquitous in nature with widespread detrimental effects to hosts, making parasitism a likely cause of sex-specific mortalities. Using sex-specific blood and gastrointestinal parasite prevalence from 96 and 54 avian host species, respectively, we test the implications of parasites for annual mortality in wild bird populations using phylogenetic comparative methods. First, we show that parasite prevalence is not different between adult males and females, although Nematodes showed a statistically significant but small male-biased parasite prevalence. Second, we found no correlation between sex-biased host mortalities and sex-biased parasite prevalence. These results were consistent in both blood and gastrointestinal parasites. Taken together, our results show little evidence for sex-dependent parasite prevalence in adults in wild bird populations, and suggest that parasite prevalence is an unlikely predictor of sex difference in adult mortalities, not withstanding sampling limitations. We propose that to understand causes of sex-biased mortalities, more complex analyses are needed that incorporate various ecological and life history components of animals life that may include sex differences in exposure to predators, immune capacity and cost of reproduction.

Patterns of parasite eggs, oocysts and larvae shedding by moose in the Biebrza marshland (NE Poland).

The study analyses patterns of endoparasite eggs, oocysts and larvae shedding by moose from the relict population in the Biebrza marshland, NE Poland, which has grown to be one of the largest in Central Europe since the ban on hunting imposed in 2001. The analysis identified 10 species or groups of parasites among 230 faecal moose samples collected over 16 consequent months. The most prevalent were the eggs of Trichostrongylidae, Trichuris spp., Nematodirella alcidis, Parafasciolopsis fasciolaemorpha and the larvae of Elaphostrongylus sp. Four parasite species were more prevalent in males, indicating male-biased parasitism, and the studied moose population exhibited a female-skewed sex ratio. Nematodirella alcidis eggs and Protostrongylid larvae were more prevalent during winter, which indicated their resistance to harsh weather conditions. The prevalence of Eimeria alces and Aonchotheca sp. increased during the growing season, as did the number of eggs per gram of faeces (EPG) of P. fasciolaemorpha, possibly due to the availability of water sources. Higher mean monthly temperature was also found to have a positive effect on the excretion of Trichostrongylidae and Moniezia spp. eggs. In addition, the time of infection and the specificity of the parasite life cycle, being sensitive to certain climatic conditions, also appeared to have a strong influence on eggs, oocysts and larvae shedding in this non-harvested moose population.

Parasite-offspring competition for female resources can explain male-biased parasitism in plants.

Male-biased susceptibility to parasites is common in dioecious plants. However, why males have higher parasite loads than females is unclear. Unlike males, females must subsidize post-fertilization costs of reproduction (e.g. seed and fruit development). As a result, females may have smaller pools of resources potentially available to parasites, thus leading to lower parasite loads. We tested this prediction in New Zealand's largest native moth ( Aenetus virescens: Lepidoptera), whose larvae parasitize Aristotelia serrata (Elaeocarpaceae), an endemic species of dioecious tree. We measured parasite loads in male and female trees, as well as annual seed set in females. We then derived a technique to equate the energetic cost of seed set in females to an equivalent number of parasitic larvae. Our results showed evidence for male-biased parasitism: male trees harboured more larval parasites than female trees. However, when parasite loads in males were compared with parasite loads in females, plus the energetic cost of seed production calculated as an equivalent number of parasitic larvae, differences in parasitism between the sexes disappeared. We conclude that male-biased parasitism in plants could arise from parasite-offspring (i.e. herbivore-seed) competition for female resources.

The physiological cost of male-biased parasitism in a nearly monomorphic mammal.

BackgroundEven though male-biased parasitism is common in mammals, little effort has been made to evaluate whether higher parasitic burden in males results in an extra biological cost, and thus a decrease in fitness. Body condition impairment and the augmentation of oxidative stress can be used as indicators of the cost of parasite infections. Here, we examined relationships between gastrointestinal and respiratory helminths, body condition and oxidative stress markers (glutathione peroxidase, paraoxonase-1) in 28 Pyrenean chamois (Rupicapra p. pyrenaica) sampled in autumn.ResultsOnly male chamois showed a reduction in body condition and higher oxidative stress due to parasite infection, likely because of the extremely high parasite burdens observed in males.ConclusionsThis study made evident a disparity in the physiological cost of multiple parasitism between sexes in a wild mammal, mainly due to parasitic richness. Because of the similar life expectancy in male and female chamois, we suggest that males may have developed natural mechanisms to compensate for higher parasite loads during the rut.

Parasite diversity of disease-bearing rodents of Southeast Asia: habitat determinants and effects on sexual size dimorphism and life-traits

We investigated a causal chain of relationships between habitat specialization and parasite species richness in rodent communities in Southeast Asia, and the consequences for variation in immune investment (using spleen size), the degree of sexual competition (using testes) and sexual size dimorphism (SSD). We used data gathered on rodents, their habitat specialization and their parasites (macro- and micro-parasites) in Southeast Asian landscapes. The results supported the hypotheses that parasite diversity drives the evolution of host life-traits and sexual selection. Firstly host habitat specialization explained the variation in parasite species richness. Secondly high parasite species richness was linked to host immune investment, using the relative spleen size of rodents. Thirdly according to the potential costs associated with immune investment, the relative spleen size was found to be negatively correlated with the relative size of testes among rodents. Fourthly, a positive relationship between male-biased SSD and parasite species richness was observed supporting the role of parasitism in sexual selection. Finally, the variation in SSD was positively associated with the degree of habitat specialization. Highest values of female-biased SSD were associated with habitat specialization, whereas highest values of male-biased SSD concerned synanthropic or generalist rodent species. These results, also correlative, will help to facilitate selection of the species that should be thoroughly investigated at the population level to better understand the selective effects of parasites on rodent life-history and behavior.

Sex-biased parasitism in monogamous arctic foxes is driven by diet

Male-biased parasite loads are common in vertebrates, particularly in species with intense sexual selection, yet few studies have examined sex-biased parasite loads in monogamous species with low sexual selection and no differential investment in ornaments or other sexually selected traits. The circumpolar arctic fox (Vulpes lagopus) is a socially monogamous predator with low sexual selection; both parents invest heavily in their young. To determine if parasite loads (abundance and intensity) in arctic foxes vary with sex, age, or diet, we identified and enumerated parasites in arctic fox carcasses collected in winter from local trappers at Churchill, Manitoba, Canada. We measured stable isotope ratios in muscle samples as a proxy for diet. Males had more cestodes, which are only transmitted through prey, but numbers of nematodes, which are acquired by direct transmission, did not differ between sexes. δ15N values were lower in males, suggesting greater reliance on small mammals. Age did not affect diet or the number of cestodes, but the species of cestodes differed by age; for example, Echinococcus multilocularis was present only in subadults (< 1 year old). Nematodes were more abundant in subadults, likely because pups spend more time at dens in high densities, increasing exposure. Intraspecific differences in arctic fox parasites are best explained by variation in diet and foraging patterns, rather than hormone-mediated reduction in immunity. These results suggest that in monogamous species, males may not suffer compromised immunity as seen in species with strong sexual selection.

Reproductive effort and seasonality associated with male-biased parasitism in Gracilinanus agilis (Didelphimorphia: Didelphidae) infected by Eimeria spp. (Apicomplexa: Eimeriidae) in the Brazilian cerrado.

The aggregation of parasites among hosts is associated with differential host exposure and susceptibility to parasites, which varies according to host gender, body size, reproductive status and environmental factors. We evaluated the role of these factors on infestation by Eimeria spp. (Eimeriidae) in the agile gracile mouse opossum (Gracilinanus agilis), a semelparous didelphid inhabiting neotropical savannahs. Eimeria spp. abundance and prevalence among G. agilis were associated with the breeding status of individuals and to a lesser extent to climatic season, with both sexes presenting higher Eimeria spp. burdens during late breeding/wet season. On the other hand, male-biased parasitism was restricted to dry/mating season. We suggest that male spatial organization and diet may account for increased parasite burdens within this sex, although future studies should evaluate the role of physiological differences associated with androgen hormones. Finally, a rapid increase in Eimeria spp. loads among females during the late breeding/wet season seems associated with seasonal changes in susceptibility, due to breeding costs related to semelparity, and exposure to infective propagules, while male-die off seems to explain maintenance of higher Eimeria spp. burdens within this sex in the same period.

Male-biased gastrointestinal parasitism in a nearly monomorphic mountain ungulate.

BackgroundPyrenean chamois (Rupicapra pyrenaica pyrenaica) is a nearly monomorphic mountain ungulate with an unbiased sex-specific overwinter adult survival. Few differences in gastrointestinal parasitism have been reported by coprology as yet. This study aims to assess diversity, prevalence, intensity of infection and aggregation of gastrointestinal nematodes in male and female adult chamois. We expect no differences in the parasite infection rates between sexes.FindingsGastrointestinal tracts of 28 harvested Pyrenean chamois in the Catalan Pyrenees (autumn 2012 and 2013) were necropsied and sexual differences in the diversity and structure of parasite community, prevalence, intensity of infection, and richness were investigated. We found 25 helminth species belonging to 13 different genera.ConclusionsContrary to our expectations, male chamois showed different parasite communities, higher prevalence, intensity of infection and richness than females. Such sexual differences were clear irrespective of age of individuals. Hence, male chamois must cope with a more diverse and abundant parasite community than females, without apparent biological cost. Further research will be required to confirm this hypothesis.

Ectoparasite load in the crested porcupine Hystrix cristata Linnaeus, 1758 in Central Italy.

The crested porcupine Hystrix cristata is a large body-sized rodent, occurring in Europe only in the Italian Peninsula, where it may have been introduced in early Medieval times. Its parasite fauna is currently poorly known and limited to few anecdotal observations. We have analyzed the ectoparasite load of 165 crested porcupines from Tuscany and Latium (Central Italy). Both captured and road-killed individuals were checked for fleas and ticks. Overall, only 39 porcupines were infested by four species of ticks and five of fleas. Abundance of ectoparasites was higher in areas with higher habitat richness, with respect to densely wooded areas. The most frequent species was the flea Pulex irritans (25%), whose prevalence peaked in winter probably because of optimal abiotic conditions in the porcupine's den. The remaining species of both hard ticks (Rhipicephalus bursa, Pholeoixodes hexagonus, and Ixodes ventalloi) and fleas (Paraceras melis, Ctenocephalides canis, Dasypsyllus gallinulae, and Hystrichopsylla talpae), all with prevalence lower than 5%, could be due to den sharing with other vertebrates, mainly carnivores such as, e.g., red foxes and badgers. The second most prevalent species was the generalist tick Ixodes ricinus (21%). An adult male-biased parasitism for ticks has been detected, suggesting a possible role of testosterone related immune-depressive effect. The low richness in dominant ectoparasite species, built up by locally acquired generalist taxa, provides support to the allochthonous origin of this rodent in Italy.

Seasonal variation in infestations by ixodids on Siberian chipmunks: effects of host age, sex, and birth season.

In mammalian hosts, macroparasite aggregation is highly heterogeneous over space and time and among individuals. While the exact causes of this heterogeneity remain unclear, it has mainly been attributed to individual differences in exposure and susceptibility. Although some extrinsic (e.g., parasite availability) and intrinsic (e.g., sex or age) factors are well known to affect infestation patterns, the joint and possibly interacting effects of these factors are poorly understood. Here, we study the infestation of hard ticks (mainly Ixodes ricinus) in a small rodent, the Siberian chipmunk (Tamias sibiricus), introduced to an oak-hornbeam forest in France. We investigate the seasonal variation in infestation according to the sex, age, birth season (spring-born or summer-born), and body weight of individual hosts while controlling for interannual variability. During the 10-year study period, 3421 tick count events were recorded involving 1017 chipmunks monitored by the capture-mark-recapture procedure. Our results reveal a male-biased parasitism in the Siberian chipmunk, which is not consistent among individuals born in different seasons. This sex bias is observed among spring-born juveniles from July to the beginning of hibernation. For adults, this difference becomes apparent along the reproduction period (May-September) for summer-born adults only. These complex interactions between sex, age, and birth season suggest overall that the seasonal variation of tick load is critically linked to the reproductive behavior of this small ground sciurid.

The effects of mite parasitism on the reproduction and survival of the Taiwan field mice (Apodemus semotus)

Abstract Background The effects of parasitism on host survival and reproduction can be highly complex depending on the type of parasites, host sex and life-history characteristics, and ecological conditions. In this study, we tested sex-biased parasitism from Trombiculid mites (Acarina: Trombiculidae) and their sex-specific effects on host reproduction and survival, in a natural population of the Taiwan field mouse (Apodemus semotus). We performed surveys of A. semotus and their Trombiculid mites between April 2010 and August 2011 and again between June and September 2012 in a subtropical evergreen forest in Taiwan. Results Contrary to the commonly reported male-biased parasitism in mammals, we did not find sex-biased parasitism in A. semotus. We found that mite abundance was negatively associated with A. semotus reproduction and survival in both males and females. The mite abundance and rodent reproduction fluctuated seasonally, and the peak reproductive season coincided with the time period of relatively low mite abundance. Conclusions Trombiculid mites could potentially regulate A. semotus populations through reducing their reproduction and survival. The overlapping periods of peak reproduction and low parasitism implied that A. semotus may adjust their reproductive phenology to avoid periods of high parasitism or be constrained by parasites to reproduce only during periods of low parasitism. Although our results are correlational, host breeding season has been shown to increase in response to experimental reduction of parasitism. We suggest that parasites may shape host reproduction phenology through which they may influence host population dynamics.

Sex differences in flea infections among rodent hosts: is there a male bias?

Recognizing patterns of parasite distribution among wildlife hosts is of major importance due to growing risk of transmission of zoonotic diseases to humans. Thus, sex-dependent parasite distribution in higher vertebrates is extensively studied, and males are often found more parasitized than females. Male-biased parasitism may be the result of weaker immunocompetence of male hosts owing to the immunosuppressive effect of androgens. Moreover, larger hosts (males) may demonstrate higher parasite infestation levels than smaller individuals (females), as they constitute a better nutritional resource for parasites and provide them with a greater variety of niches. In the present work, we investigated sex-dependent patterns of flea distribution among three common rodent species (Apodemus agrarius, Apodemus flavicollis, and Myodes glareolus). We hypothesized that males have a higher flea infestation than females. We confirm male-biased parasitism in A. agrarius and M. glareolus, but not in A. flavicollis. Additionally, flea infestation increased with body mass in A. agrarius, but not in A. flavicollis and M. glareolus. The detected differences in parasite distribution among sexes are probably the result of immunosuppressive effects of androgens and spatial behavior of males.

Variable effects of host characteristics on species richness of flea infracommunities in rodents from three continents

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 species-specific 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.

Sex-biased transmission of a complex life-cycle parasite: why males matter

Male-bias in parasite infection exists in a variety of host – parasite systems, but the epidemiological importance of males and, specifi cally, whether males are responsible for producing a disproportionate amount of onward transmission events (malebiased transmission) has seldom been tested. Th e primary goal of our study was to experimentally test for male-biased transmission in a system with no sex-biased prevalence. We performed a longitudinal fi eld experiment and continuously removed intestinal nematode parasites from either male or female white-footed mice and recorded the subsequent transmission among the untreated sex. We predicted males are responsible for the majority of transmission and female mice would have lower infection prevalence under the male-anthelmintic treatment than controls and that male mice would experience little or no change in infection prevalence under female-anthelmintic treatment compared to controls. Our second goal was to evaluate physiological hypotheses relating to the mechanisms that could generate the observed transmission pattern. To that end, we examined a cross-sectional sample of hosts to explicitly test for diff erences in parasite intensity, parasite egg shedding rate and reproductive output per parasite between male and female hosts. Removing parasites from male mice resulted in lower infection rates among female mice but, in contrast, there was no eff ect of female-deworming on infection rates among male mice; providing evidence that males provide disproportionately greater numbers of transmission events than females. We found no diff erence in prevalence, intensity, or fecundity of parasites between sexes in the cross-sectional sample of mice and rejected the mechanistic hypotheses. Without male-biased prevalence, intensity, or parasite fecundity, we concluded that male-biased transmission is unlikely to be created via physiological diff erences and the parsimonious explanation is that male behavior spreads infective stages in a more successful manner. We demonstrate that transmission heterogeneities can exist in the absence of individual heterogeneities in infection.

Effects of life‐history traits on parasite load in grey squirrels

Life-history theory stipulates that resources are limited and consequently investment in one trait (e.g. reproduction) compromises resources allocated to another (e.g. immune defence). Differential investment of resources can occur at the level of the individual (i.e. between reproductive status and body condition) as well as at higher levels such as between individuals of different ages or sexes. Male mammals generally invest resources to secure the greatest number of matings while females maximize their own fitness by allocating more resources to body maintenance, including immune function. Accordingly, sex biases in parasite loads appear common among mammal species and have been linked to sex differences in morphology (e.g. body size), behaviour (e.g. mate searches) and physiology (e.g. testosterone). We examined sex biases in parasite load and potential trade-offs between body condition, reproductive investment and immune function in grey squirrels Sciuris carolinensis, a species with a highly promiscuous mating system but no sexual size dimorphism. We found male-biased parasite loads for two of four parasites. The intensity of infection with fleas but not nematodes was affected by testis size. This suggests that behavioural traits may contribute to nematode load. Neither reproductive effort nor nematode infection influenced body condition for either sex but lactating females were in better condition than non-lactating females. Immune function, as measured by spleen mass, was positively correlated with body size and negatively with body condition. Nematode infection was associated with a reduction in spleen mass only in males. Thus, the effects of behavioural and physiological differences as well as sex on parasite load depend on the parasite species involved. This provides support for the hypothesis that males favour investment in mating effort at the expense of immune function.

Life history and mating systems select for male biased parasitism mediated through natural selection and ecological feedbacks

tlsb-1%Males are often the ‘sicker’ sex with male biased parasitism found in a taxonomically diverse range of species. There is considerable interest in the processes that could underlie the evolution of sex-biased parasitism. Mating system differences along with differences in lifespan may play a key role. We examine whether these factors are likely to lead to male-biased parasitism through natural selection taking into account the critical role that ecological feedbacks play in the evolution of defence. We use a host–parasite model with two-sexes and the techniques of adaptive dynamics to investigate how mating system and sexual differences in competitive ability and longevity can select for a bias in the rates of parasitism. Male-biased parasitism is selected for when males have a shorter average lifespan or when males are subject to greater competition for resources. Male-biased parasitism evolves as a consequence of sexual differences in life-history that produce a greater proportion of susceptible females than males and therefore reduce the cost of avoiding parasitism in males. Different mating systems such as monogamy, polygyny or polyandry did not produce a bias in parasitism through these ecological feedbacks but may accentuate an existing bias.

Male Biased Parasitism in Cormorants and Relationships with Foraging Ecology on Lake Erie, Canada

Existing hypotheses only partially explain male biased parasitism in mammals and birds. The present study examined whether male biased parasitism by a common trematode and nematode exists in breeding Doublecrested Cormorants (Phalacrocorax auritus) from Lake Erie and if any sex bias in parasitism could be explained by sex differences in body size and foraging ecology, evaluated using stable isotope profiles (based on δ13C, δ15N). Male cormorants had three times the abundance of Drepanocephalus spathans (a trematode) than females; however, there were no significant sex differences in abundance or intensity of Contracaecum spp. Relationships between body size and parasitism were either non-existent or inconsistent. Stable carbon isotope profiles indicated that male and female cormorants that foraged in more pelagic habitats had more Contracaecum spp. In summary, male biased parasitism was present in a sample of Lake Erie cormorants and differences in foraging ecology might affect the levels of parasitism in cormorants.

Sex-Biased Phoretic Mite Load on Two Seaweed Flies:Coelopa frigidaandCoelopa pilipes

Two hypotheses explain male-biased parasitism. Physiological costs of male sexually selected characteristics can reduce immunocompetence. Alternatively, ecological differences could generate male-biased parasitism. One method of comparing the importance of the two theories is to investigate patterns of phoresy, which are only likely to be generated by ecological rather than immunological differences between the sexes. Here we studied the pattern of phoresy of the mite, Thinoseius fucicola, on two species of seaweed fly hosts, Coelopa frigida and Coelopa pilipes. We found a highly male-biased pattern of phoresy of T. fucicola on both species. These are the first reported instances of sex-biased phoresy in a solely phoretic parasite. We also show the first two cases of size-biased phoresy. We suggest that ecological factors, particularly, male mate searching, generated male biased patterns of phoresy. We highlight the potential importance of studies of phoresy in determining the relative roles of the immunocompetence and ecological theories in generating male-biased parasitism. We suggest that more studies of patterns of phoresy are carried out to allow detailed comparisons with patterns of parasitism.

Parasite-specific variation and the extent of male-biased parasitism; an example with a South African rodent and ectoparasitic arthropods

We asked whether the occurrence and the extent of host gender-biased parasitism vary among higher parasite taxa, among individual species within these taxa and within parasite species among localities. To answer this question, we studied prevalence, abundance, species richness and the level of aggregation of ectoparasites (ticks, mites, lice and fleas) collected from male and female striped mice (Rhabdomys pumilio) in 9 localities of the Western Cape Province of South Africa. We used meta-analyses to compare parasitological variables between male and female hosts across localities for individual parasite species and higher taxa as well as across parasite species within a higher taxon. Whenever gender-biased parasitism was found, it indicated higher infestation of male than female hosts (except 1 low abundant mite species). We found that the occurrence and extent of gender-biased infestation varied mainly within a parasite species among localities and among parasite species within a higher taxon but not among parasite taxa. Our results suggest that the extent of a gender-biased pattern of parasite infestation of the same host may not only involve host-related mechanisms but also depends on biological features of a particular parasite species.