Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis)

Given the intimate association in host–parasite systems, parasites are expected to initiate their own reproduction when vulnerable hosts become abundant and/or when adult hosts are less resistant. In this study, we examined the variation in the intensities of a blood-sucking mite ( Spinturnix myoti , Acarina) with respect to the reproductive cycle and immunocompetence of its host, the greater mouse-eared bat Myotis myotis . Reproductive, pregnant females were less immunocompetent and harboured more parasites than nonreproductive females, whilst, during lactation, immunocompetence was positively associated with female body mass. There was a dramatic increase in the T-cell response of gravid females with the advancement of gestation, which coincided with a diminution of individual parasite loads and a progressive switch of parasites from adults to juveniles. The latter not only harboured greater numbers of mites than adult female bats, but they also exhibited gravid parasites in higher proportions, indicating that juvenile hosts are more attractive for parasite reproduction than adult females.     

Roost selection and roost switching of female Bechstein’s bats (<Emphasis Type="Italic">Myotis bechsteinii</Emphasis>) as a strategy of parasite avoidance

Ectoparasites of vertebrates often spend part of their life cycle in their hosts’ home. Consequently, hosts should take into account the parasite infestation of a site when selecting where to live. In a field study, we investigated whether colonial female Bechstein’s bats (Myotis bechsteinii) adapt their roosting behaviour to the life cycle of the bat fly Basilia nana in order to decrease their contact with infective stages of this parasite. B. nana imagoes live permanently on the bat’s body but deposit puparia in the bat’s roosts. The flies metamorphose independently in the roosts, but after metamorphosis emerge only in the presence of a potential host. In a field experiment, the bats preferred non-contagious to contagious day-roosts and hence were able to detect either the parasite load of roosts or some correlate with infestation, such as bat droppings. In addition, 9 years of observational data on the natural roosting behaviour of female Bechstein’s bats indicate that the bats largely avoid re-occupying roosts when highly contagious puparia are likely to be present as a result of previous occupations of the roosts by the bat colony. Our results indicate that the females adapted their roosting behaviour to the age-dependent contagiousness (emergence probability) of the puparia. However, some infested roosts were re-occupied, which we assume was because these roosts provided advantages to the bats (e.g. a beneficial microclimate) that outweighed the negative effects associated with bat fly infestation. We suggest that roost selection in Bechstein’s bats is the outcome of a trade-off between the costs of parasite infestation and beneficial roost qualities.     

Anthropogenic impacts on Costa Rican bat parasitism are sex specific

While anthropogenic impacts on parasitism of wildlife are receiving growing attention, whether these impacts vary in a sex‐specific manner remains little explored. Differences between the sexes in the effect of parasites, linked to anthropogenic activity, could lead to uneven sex ratios and higher population endangerment. We sampled 1108 individual bats in 18 different sites across an agricultural mosaic landscape in southern Costa Rica to investigate the relationships between anthropogenic impacts (deforestation and reductions in host species richness) and bat fly ectoparasitism of 35 species of Neotropical bats. Although female and male bat assemblages were similar across the deforestation gradient, bat fly assemblages tracked their hosts closely only on female bats. We found that in female hosts, parasite abundance per bat decreased with increasing bat species richness, while in male hosts, parasite abundance increased. We hypothesize the differences in the parasite–disturbance relationship are due to differences in roosting behavior between the sexes. We report a sex‐specific parasite–disturbance relationship and argue that sex differences in anthropogenic impacts on wildlife parasitism could impact long‐term population health and survival.     

Are sexes equally parasitized in damselflies and dragonflies?

Parasitism plays an essential part in ecology and evolution of host species and understanding the reasons for differential parasitism within and among hosts species is therefore important. Among the very important factors potentially affecting parasitism is the gender of the host. Here, we studied whether either females or males are more likely to harbour parasites among Odonatan insects, by relying on an extensive literature review and new field data. We collected data on numerous dragonfly and damselfly species and their ectoparasites (water mites) and endoparasites (gregarines) to examine the generality of similarities and differences in prevalence, intensity and maximum number of parasites of male and female hosts. We found three main results. Firstly, most of the odonate host species showed no differences between sexes in either gregarine or water mite prevalence and intensity. The only exception was female damselflies’ higher gregarine prevalence and intensity compared to conspecific males. These inequalities in gregarine parasitism may be due to behavioral and physiological differences between conspecific males and females. In comparison, there were no differences in dragonflies between sexes in water mite or gregarine prevalence and intensity. Secondly, damselflies had higher prevalence and intensity levels of both gregarine and water mite parasites compared to dragonflies. Finally, we found a strong species level pattern between female and male parasitism: a certain level of gregarine or water mite parasitism in one sex was matched with a similar parasitism level for the other. This indicates similar exposure and susceptibility to parasites on both sexes. Even though significant differences of parasite levels between the sexes were observed within certain host species, our results strongly suggest that on a general level a more parasitized sex does not exist in the order, Odonata.     

Does the mode of transmission between hosts affect the host choice strategies of parasites? Implications from a field study on bat fly and wing mite infestation of Bechstein's bats

In a two-year field study, we analyzed the distribution of two hematophagous ectoparasites, the bat fly Basilia nana and the wing mite Spinturnix bechsteini , within and among 14 female colonies and among 26 solitary male Bechstein's bats Myotis bechsteinii . Our goal was to investigate whether differences in the transmission mode of the parasites, which result from differences in their life cycle, affect their distribution between host colonies and among host individuals within colonies. Bat flies deposit puparia in bat roosts, allowing for the transmission of hatched flies via successively shared roosts, independent of body contact between hosts or of hosts occupying a roost at the same time. In contrast, wing mites stay on the bat's body and are transmitted exclusively by contact of bats that roost together. As expected in cases of higher inter-colony transmissibility, bat flies were more prevalent among the demographically isolated Bechstein's bat colonies and among solitary male bats, as compared to wing mites. Moreover, the prevalence and density of wing mites, but not of bat flies, was positively correlated with colony size, as expected in cases of low inter-colony transmissibility. Within colonies, bat flies showed higher abundance on host individuals in good body condition, which are likely to have high nutritional status and strong immunity. Wing mites showed higher abundance on hosts in medium body condition and on reproductive females and juveniles, which are likely to have relatively weak immunity. We suggest that the observed infestation patterns within host colonies reflect different host choice strategies of bat flies and wing mites, which may result from differences in their inter-colony transmissibility. Our data also indicate that infestation with wing mites, but not with bat flies, might be a cost of sociality in Bechstein's bats.     

Sex-biased parasitism,seasonality and sexual size dimorphism in desert rodents

We investigated seasonality of gender differences in the patterns of flea infestation in nine rodent species to test if sex-biased parasitism in terms of mean abundance, species richness, prevalence and the level of aggregation (a) varies among hosts and between seasons, and (b) is linked to sexual size dimorphism. Sexual size differences were significant in both summer and winter in Acomys cahirinus, Gerbillus pyramidum and Meriones crassus, and in winter only in Acomys russatus, Gerbillus dasyurus, Gerbillus nanus and Sekeetamys calurus. Sexual size dimorphism was male biased except for A. russatus in which it was female biased. Manifestation of sexual differences in flea infestation was different among hosts between seasons. A significant effect of sex on mean flea abundance was found in six hosts, on mean flea species richness in five hosts and on prevalence in two hosts. Male-biased parasitism was found in summer in one host only and in winter in five hosts. Female-biased parasitism occurred in winter in A. russatus. Gender differences in the slopes of the regressions of log-transformed variances against log-transformed mean abundances occurred in three hosts. No relationship was found between sexual size dimorphism and any parasitological parameter in any season using both conventional regressions and the method of independent contrasts. Our results suggest that sex-biased parasitism is a complicated phenomenon that involves several different mechanisms.     

Ectoparasite Raymondia lobulata infestation in relation to the reproductive cycle of its host--the greater false vampire bat Megaderma lyra

To study variation of infestations by the bat fly Raymondia lobulata (Diptera: Streblidae) on the greater false vampire bat Megaderma lyra (Chiroptera: Megadermatidae), we captured individual bats at their day roost in the south of India and recorded their rate of infestation continuously for a year. All examined bats (n = 72 individuals, 202 captures) were infested with parasites (n = 3,008). However, the recorded intensity of infestation (range 1-33) was gender-related and statistically higher in females than in males (F(1, 200) = 304.45, P < 0.001). Furthermore, pregnant and lactating females had greater parasite loads than non-reproductive females and males (F(1, 63) = 23.34, P < 0.001 and F(1, 37) = 78.07, P < 0.001, respectively). No significant differences were observed between males either during mating and non-mating periods or breeding and non-breeding seasons. Analysis of the relationship between parasite infestation and the reproductive status of bats revealed that pregnant and lactating females with pups were more vulnerable hosts for parasites. Our results also suggest a well-developed coevolutionary strategy for synchronized reproduction within the host-parasite relationship and add to our understanding of how host sex and reproductive status shape the dynamics of parasitism.     

Alphacoronaviruses in New World bats: prevalence, persistence, phylogeny, and potential for interaction with humans

Bats are reservoirs for many different coronaviruses (CoVs) as well as many other important zoonotic viruses. We sampled feces and/or anal swabs of 1,044 insectivorous bats of 2 families and 17 species from 21 different locations within Colorado from 2007 to 2009. We detected alphacoronavirus RNA in bats of 4 species: big brown bats (Eptesicus fuscus), 10% prevalence; long-legged bats (Myotis volans), 8% prevalence; little brown bats (Myotis lucifugus), 3% prevalence; and western long-eared bats (Myotis evotis), 2% prevalence. Overall, juvenile bats were twice as likely to be positive for CoV RNA as adult bats. At two of the rural sampling sites, CoV RNAs were detected in big brown and long-legged bats during the three sequential summers of this study. CoV RNA was detected in big brown bats in all five of the urban maternity roosts sampled throughout each of the periods tested. Individually tagged big brown bats that were positive for CoV RNA and later sampled again all became CoV RNA negative. Nucleotide sequences in the RdRp gene fell into 3 main clusters, all distinct from those of Old World bats. Similar nucleotide sequences were found in amplicons from gene 1b and the spike gene in both a big-brown and a long-legged bat, indicating that a CoV may be capable of infecting bats of different genera. These data suggest that ongoing evolution of CoVs in bats creates the possibility of a continued threat for emergence into hosts of other species. Alphacoronavirus RNA was detected at a high prevalence in big brown bats in roosts in close proximity to human habitations (10%) and known to have direct contact with people (19%), suggesting that significant potential opportunities exist for cross-species transmission of these viruses. Further CoV surveillance studies in bats throughout the Americas are warranted.     

Information transfer about roosts in female Bechstein's bats: an experimental field study

Information transfer among group members is believed to play an important part in the evolution of coloniality in both birds and bats. Although information transfer has received much scientific interest, field studies using experiments to test the underlying hypotheses are rare. We used a field experiment to test if communally breeding female Bechstein's bats (Myotis bechsteinii) exchange information regarding novel roosts. We supplied a wild colony, comprising 17 adult females of known relatedness, with pairs of suitable and unsuitable roosts and monitored the arrival of individuals marked with transponders (PIT-tags) over 2 years. As expected with information transfer, significantly more naive females were recruited towards suitable than towards unsuitable roosts. We conclude that information transfer about roosts has two functions: (i) it generates communal knowledge of a large set of roosts; and (ii) it aids avoidance of colony fission during roost switching. Both functions seem important in Bechstein's bats, in which colonies depend on many day roosts and where colony members live together for many years.     

Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus)

Understanding the factors controlling the distribution of parasites within their host population is fundamental to the wider understanding of parasite epidemiology and ecology. To explore changes in parasite aggregation, Taylor's power law was used to examine the distributions of five gut helminths of the wild rabbit. Aggregation was found to be a dynamic process that varied with year, season, host sex, age class, and myxomatosis. Yearly and seasonal changes are thought, in the main, to be the result of variations in weather conditions acting upon infectious stages (or intermediate hosts). Evidence in support of this was the comparatively low degree of fluctuation in the aggregation of the pinworm, Passalurus ambiguus, as the infectious stage of this parasite is likely to be less susceptible to environmental variation. Host age had a marked effect on the level of aggregation of all parasites, but this effect varied between parasite species. P. ambiguus, Trichostrongylus retortaeformis and Cittotaenia denticulata aggregation were lower in adult than juvenile rabbits whilst Graphidium strigosum and Mosgovoyia pectinata aggregation tended to increase with age. Host immunity is thought to be responsible for these differences. Differences in aggregation for different parasites were also seen when the rabbit population was split into males and females. Myxomatosis had a marked effect on helminth distribution with substantially less aggregation in rabbits showing clinical signs of the disease.     

The Sicker Sex: Understanding Male Biases in Parasitic Infection,Resource Allocation and Fitness

The “sicker sex” idea summarizes our knowledge of sex biases in parasite burden and immune ability whereby males fare worse than females. The theoretical basis of this is that because males invest more on mating effort than females, the former pay the costs by having a weaker immune system and thus being more susceptible to parasites. Females, conversely, have a greater parental investment. Here we tested the following: a) whether both sexes differ in their ability to defend against parasites using a natural host-parasite system; b) the differences in resource allocation conflict between mating effort and parental investment traits between sexes; and, c) effect of parasitism on survival for both sexes. We used a number of insect damselfly species as study subjects. For (a), we quantified gregarine and mite parasites, and experimentally manipulated gregarine levels in both sexes during adult ontogeny. For (b), first, we manipulated food during adult ontogeny and recorded thoracic fat gain (a proxy of mating effort) and abdominal weight (a proxy of parental investment) in both sexes. Secondly for (b), we manipulated food and gregarine levels in both sexes when adults were about to become sexually mature, and recorded gregarine number. For (c), we infected male and female adults of different ages and measured their survival. Males consistently showed more parasites than females apparently due to an increased resource allocation to fat production in males. Conversely, females invested more on abdominal weight. These differences were independent of how much food/infecting parasites were provided. The cost of this was that males had more parasites and reduced survival than females. Our results provide a resource allocation mechanism for understanding sexual differences in parasite defense as well as survival consequences for each sex.     

A meta‐analysis of ant social parasitism: host characteristics of different parasitism types and a test of Emery’s rule

Abstract 1. In ant social parasitism, the process by which parasite–host systems evolved and the types of invasion mechanisms parasites use are being debated. Emery’s rule, for example, states that social parasites are the closest relatives to their hosts. The present study uses previously published data to test whether Emery’s rule applies equally to all parasitism types (i.e. xenobiosis, temporary, dulosis, and inquilinism). In addition, this study also investigates other links between parasite–host relatedness and host biology, which has implications for understanding the invasion mechanisms used by certain parasites. 2. We find that xenobiotic parasites typically use distantly‐related host species that are of at least medium colony size. Temporary parasites often have multiple host species that are very closely related to the parasite and hosts with medium‐size colonies. Dulotic parasites frequently have multiple host species that are slightly less related and of any size. Lastly, inquiline parasites tend to have a single, very closely related, host species with medium‐size colonies. 3. Parasites tend to be more closely related to host species if they have a single host species or when the host has a large colony size. In contrast, parasites with multiple host species or hosts of small colony size tend to be less related to their hosts. 4. This study is the first to examine trends in ant social parasitism across all known parasite species. Our meta‐analysis shows that Emery’s rule applies to inquilinism and temporary parasitism, but not to dulosis and xenobiosis. Our results also suggest that both parasitism type and parasite–host relatedness predict the number of hosts and host colony size. It may be that a chemical mimicry mechanism allows invasion of large host colonies, but requires close relatedness of parasite and host, and concentration on a single host species.     

Host sex and parasite genetic diversity

Is the genetic diversity of parasites infecting male and female hosts equal or different? This is the question we address in this paper by studying the neutral genetic variability of the plathyhelminth trematode Schistosoma mansoni within males and females of its natural murine host Rattus rattus in the marshy forest focus of Guadeloupe (French West Indies). Using seven microsatellite markers, we demonstrate that parasites from male hosts are genetically more diversified than parasites from female hosts. Three hypotheses are discussed that could explain this pattern: 1) a host sex-specific duration of cercariae recruitment; 2) a difference in the behaviour of male and female hosts that would lead to the exposure of males to a greater diversity of parasites; and 3) a host sex-biased immunocompetence that would lead to the selection of more genetically diversified individuals in male than in female rats. This finding is the first empirical evidence that each host sex may play different roles in the maintenance of parasite genetic diversity and so in their evolutionary dynamics and epidemiology.     

Male-biased parasitism by common helminths is not explained by sex differences in body size or spleen mass of breeding cormorants Phalacrocorax auritus

In vertebrates, males are often more parasitised than conspecific females. This bias in parasitism might result from sex differences in parasite exposure and/or susceptibility to infection. Such information is important for testing hypotheses about allocation of resources to life histories of males and females and for testing hypotheses about factors thought to influence parasite fitness and parasite dynamics. We tested whether double-crested cormorants Phalacrocorax auritus exhibit male-biased parasitism by gut helminths. The prevalence of nematode Contracaecum spp. and trematode Drepanocaphalus spathans infections was ∼90% and 39%, respectively. Cestode, primarily Paradilepis caballeroi and acanthocephalan Andracantha gravida infections were less common (<10%). Male and female cormorants did not differ in prevalence of infection by any helminth species. However, males had twice the abundance and intensity of Contracaecum spp. infections and twice the intensity of D. spathans infections than found in females. For common parasites showing male-biased parasitism, degree of parasitism was also unrelated to body size or mass in either sex. Males and females did not differ in spleen mass and spleen mass was unrelated to abundance of common parasites. Furthermore, abundance of trematodes and nematodes was not correlated. At present, male biases in parasitism by nematodes and trematodes in cormorants are independent patterns that remain unexplained, but are most likely attributable to sex differences in exposure and/or immunological differences not yet assessed.     

Roost and hunting site fidelity of female and juvenile Daubenton's bat Myotis daubentonii (Kuhl, 1817) (Chiroptera: Vespertilionidae)

We investigated roosting and hunting site fidelity of Daubenton's bats Myotis daubentonii (Kuhl, 1817) in the Forêt de Soignes, an old-stand forest dominated by 150–200-year-old beeches, during the summers of 2003 and 2004. Roosting behaviour and hunting activity over ponds of adult females and juveniles were monitored using radio-telemetry. Eighteen roosts were located, all in natural cavities. The bats occupied a limited number of trees located in a specific and small roosting area. This roost aggregation was not linked to the distribution of hollow trees. Furthermore, whereas all 11 ponds in the study area were exploited by Daubenton's bats, monitored individuals were limited to two ponds to which they showed high fidelity. These two ponds were not the closest to the roosting area. Overall, these results show that at least for the time we conducted our experiment, female and juvenile Daubenton's bats are highly faithful to specific roosting and hunting grounds.     

Nestling sex predicts susceptibility to parasitism and influences parasite population size within avian broods

Vertebrate hosts differ in their level of parasite susceptibility and infestation. In avian broods, variation in susceptibility of nestlings to ectoparasites may be associated with non‐uniform distributions of parasites among brood mates, with parasites concentrating feeding on the most vulnerable hosts. The presence of a highly susceptible nestling in a brood can benefit the remaining young by reducing the parasite pressure they experience; however, from a parasite’s perspective, broods with fewer susceptible hosts may provide effectively fewer resources than broods of the same size containing a greater abundance of susceptible hosts, and this could limit the number of parasites that a host brood can sustain. To test whether variation in number of susceptible hosts affects the number of parasites in bird nests, we first examined the role of host sex and induced immunity (via methionine supplementation) on susceptibility of mountain bluebirds Sialia currucoides to parasitism by blow flies Protocalliphora spp. We then assessed the effect of variation in number of susceptible hosts on the number of parasites inhabiting the nest. Only females showed a benefit of methionine supplementation, gaining mass more rapidly following supplementation compared to males. This suggests that females are more susceptible to parasites in this system; this was further supported by parasite feeding trials, in which parasites extracted larger blood meals from female than male hosts. Finally, the abundance of parasites in nests was predicted by brood sex ratio: broods containing more female young harboured more parasites. Hence, within‐brood variation in host susceptibility to parasites can not only influence the costs of parasitism for individual nestlings, but may also have consequences for the size of parasite populations within nests. If patterns of maternal investment affect the abundance of nest‐dwelling parasites, these interactions may be important for understanding fitness consequences of maternal resource allocation in many vertebrate hosts.     

Social Dispersion and Genetic Variation in Two Species of Emballonurid Bats

Saccopteryx leptura and S. bilineata are closely related, sympacric species of neotropical bats that exhibit marked differences in social organization and dispersion patterns. S. leptura is monogamous and roosts in small groups of 1 to 5 (Y = 2.6) individuals that are finely dispersed. S. bilineata is harem-polygamous and roosts in larger groups of 1 to 42 (Y = 8.1) individuals that are more coarsely dispersed. Allozyme genetic studies of individuals from Trinidad, W I. demonstrate that both species carry similar, high levels of polymorphism and heterozygosity. Although significant genetic heterogeneity was observed among geographical populations of S. leptura, there is no evidence for either species that social structuring leads to inbreeding and the loss of heterozygosity, or that it promotes the development of genetic heterogeneity among social units that could accelerate the evolutionary diversification of these taxa. These results do not support a recently proposed hypothesis that social structuring in mammals has these effects. Observed intercolony genetic heterogeneity among adult males resident in multimale groups of S. bilineata is greater than intercolony heterogeneity of adult females. This is an apparent result of female dispersal and the recruitment of males into their parental groups. These results suggest that the adult males within large colonies may be kin-related.     

Synergistic effects of seasonal rainfall, parasites and demography on fluctuations in springbok body condition

1. Seasonality of rainfall can exert a strong influence on animal condition and on host-parasite interactions. The body condition of ruminants fluctuates seasonally in response to changes in energy requirements, foraging patterns and resource availability, and seasonal variation in parasite infections may further alter ruminant body condition. 2. This study disentangles the effects of rainfall and gastrointestinal parasite infections on springbok (Antidorcas marsupialis) body condition and determines how these factors vary among demographic groups. 3. Using data from four years and three study areas, we investigated (i) the influence of rainfall variation, demographic factors and parasite interactions on parasite prevalence or infection intensity, (ii) whether parasitism or rainfall is a more important predictor of springbok body condition and (iii) how parasitism and condition vary among study areas along a rainfall gradient. 4. We found that increased parasite intensity is associated with reduced body condition only for adult females. For all other demographic groups, body condition was significantly related to prior rainfall and not to parasitism. Rainfall lagged by two months had a positive effect on body condition. 5. Adult females showed evidence of a 'periparturient rise' in parasite intensity and had higher parasite intensity and lower body condition than adult males after parturition and during early lactation. After juveniles were weaned, adult females had lower parasite intensity than adult males. Sex differences in parasitism and condition may be due to differences between adult females and males in the seasonal timing of reproductive effort and its effects on host immunity, as well as documented sex differences in vulnerability to predation. 6. Our results highlight that parasites and the environment can synergistically affect host populations, but that these interactions might be masked by their interwoven relationships, their differential impacts on demographic groups, and the different time-scales at which they operate.     

Day roost selection in female Bechstein's bats (Myotis bechsteinii): a field experiment to determine the influence of roost temperature

The decision where to live has far-reaching fitness consequences for animals. In contrast to most other mammals or birds that use sheltered nest sites, female Bechstein's bats frequently switch day roosts during one breeding season, and therefore must often decide where to spend the day. Selecting the right roost is important, because roost quality, e.g. microclimatic condition, influences survival and reproduction in bats. Although thermal factors are very important for the quality of roosts occupied by bats, whether bats base their day roost selection directly on roost temperature has not been tested in the field. Over one summer, we examined and tested the roost choice of 21 individually marked female Myotis bechsteinii living in one maternity colony. In a field experiment, we allowed the bats to choose between relatively warm versus cold bat boxes, while controlling for site preferences. We expected females to exhibit a preference for warm roosts during pregnancy and lactation to accelerate gestation and shorten the period of growth of their young. Roost occupancy over 160 census days reflected significant temperature differences among 89 surveyed roosts (14 tree holes and 75 bat boxes), and preferences changed with the season. Females significantly preferred cold roosts before parturition, whereas post-partum, they significantly favoured warm roosts. Temperature preferences were independent of the roost site, and thus roost selection was based directly on temperature. Boxes with significantly different daytime temperatures did not differ significantly at night. Consequently, bats would have to spend at least 1 day in a new roost to test it. Information transfer among colony members might facilitate knowledge of roost availability. Access to many roosts providing different microclimates is likely to be important for successful reproduction in the endangered Bechstein's bat.