Flea Communities Research Articles

Community structure of fleas within and among populations of three closely related rodent hosts: nestedness and beta-diversity.

We studied nestedness and its relationships with beta-diversity in flea communities harboured by three closely related rodent species (Rhabdomys pumilio, Rhabdomys intermedius, Rhabdomys dilectus) at two spatial scales (within and among host populations) in South Africa and asked (a) whether variation in species composition of flea communities within and among host populations follows a non-random pattern; if yes, (b) what are the contributions of nestedness and species turnover to dissimilarity (= beta-diversity) among flea communities at the two scales; and (c) do the degree of nestedness and its contribution to beta-diversity differ among host species (social vs solitary) and between scales. We found that nestedness in flea assemblages was more pronounced (a) in social than solitary host species and (b) at lower (among host individuals within populations) than at higher scale (among host populations). We also found that higher degree of nestedness was associated with its higher contribution to beta-diversity. Our findings support earlier ideas that parasite community structure results from the processes of parasite accumulation by hosts rather than from the processes acting within parasite communities.

Host-Parasite Associations in Small Mammal Communities in Semiarid Savanna Ecosystems of East Africa.

Despite the established importance of rodents as reservoirs of vector-borne zoonoses in East Africa, there is relatively limited information regarding the infestation parameters and host associations of ectoparasites that vector many such pathogens among small mammals in this region. Between 2009 and 2013, small mammals were live-trapped in the semiarid savanna of Kenya. A subset of these individual hosts, including 20 distinct host taxa, was examined for ectoparasites, which were identified to species. Species of fleas, ticks, mites, and sucking lice were recorded. Based on these data, we calculated host-specific infestation parameters, documented host preferences among ectoparasites, conducted a rarefaction analysis and extrapolation to determine if ectoparasites were adequately sampled, and assessed nestedness for fleas to understand how pathogens might spread in this system. We found that the flea community structure was significantly nested. Understanding the ectoparasite network structure may have significant human relevance, as at least seven of the ectoparasite species collected are known vectors of pathogens of medical importance in the region, including Yersinia pestis, Rickettsia spp., and Theileria parva, the causative agents of plague, spotted fevers and other rickettsial illnesses in humans, and theileriosis, respectively.

Effect of temperature and relative humidity on the development times and survival of Synopsyllus fonquerniei and Xenopsylla cheopis, the flea vectors of plague in Madagascar.

BackgroundPlague, a zoonosis caused by Yersinia pestis, is found in Asia, the Americas but mainly in Africa, with the island of Madagascar reporting almost one third of human cases worldwide. In the highlands of Madagascar, plague is transmitted predominantly by two flea species which coexist on the island, but differ in their distribution. The endemic flea, Synopsyllus fonquerniei, dominates flea communities on rats caught outdoors, while the cosmopolitan flea, Xenopsylla cheopis, is found mostly on rats caught in houses. Additionally S. fonquerniei seems restricted to areas above 800 m. Climatic constraints on the development of the two main vectors of plague could explain the differences in their distribution and the seasonal changes in their abundance. Here we present the first study on effects of temperature and relative humidity on the immature stages of both vector species.MethodsWe examined the two species’ temperature and humidity requirements under experimental conditions at five different temperatures and two relative humidities. By employing multivariate and survival analysis we established the impact of temperature and relative humidity on development times and survival for both species. Using degree-day analysis we then predicted the average developmental threshold for larvae to reach pupation and for pupae to complete development under each treatment. This analysis was undertaken separately for the two relative humidities and for the two species.ResultsDevelopment times and time to death differed significantly, with the endemic S. fonquerniei taking on average 1.79 times longer to complete development and having a shorter time to death than X. cheopis under adverse conditions with high temperature and low humidity. Temperature had a significant effect on the development times of flea larvae and pupae. While humidity did not affect the development times of either species, it did influence the time of death of S. fonquerniei. Using degree-day analysis we estimated an average developmental threshold of 9 °C for S. fonquerniei, and 12.5 °C for X. cheopis.ConclusionsWhile many vector-borne diseases are limited to warm, low-lying regions, plague in Madagascar is unusual in being most prevalent in the cool, highland regions of the country. Our results point towards the possibility that this is because the endemic flea vector, S. fonquerniei, is better adapted to cool temperatures than the exotic flea vector, X. cheopis. Future warming caused by climate change might reduce the area suitable for S. fonquerniei and may thus reduce the incidence of plague in Madagascar.

Molecular Survey of Bartonella Species and Yersinia pestis in Rodent Fleas (Siphonaptera) From Chihuahua, Mexico.

Rodent fleas from northwestern Chihuahua, Mexico, were analyzed for the presence of Bartonella and Yersinia pestis. In total, 760 fleas belonging to 10 species were tested with multiplex polymerase chain reaction analysis targeting the gltA (338-bp) and pla genes (478-bp) of Bartonella and Y. pestis, respectively. Although none was positive for Y. pestis, 307 fleas were infected with Bartonella spp., resulting in an overall prevalence of 40.4%. A logistic regression analysis indicated that the presence of Bartonella is more likely to occur in some flea species. From a subset of Bartonella-positive fleas, phylogenetic analyses of gltA gene sequences revealed 13 genetic variants clustering in five phylogroups (I–V), two of which were matched with known pathogenic Bartonella species (Bartonella vinsonii subsp. arupensis and Bartonella washoensis) and two that were not related with any previously described species or subspecies of Bartonella. Variants in phylogroup V, which were mainly obtained from Meringis spp. fleas, were identical to those reported recently in their specific rodent hosts (Dipodomys spp.) in the same region, suggesting that kangaroo rats and their fleas harbor other Bartonella species not reported previously. Considering the Bartonella prevalence and the flea genotypes associated with known pathogenic Bartonella species, we suggest that analysis of rodent and flea communities in the region should continue for their potential implications for human health. Given that nearby locations in the United States have reported Y. pestis in wild animals and their fleas, we suggest conducting larger-scale studies to increase our knowledge of this bacterium.

Flea-Associated Bacterial Communities across an Environmental Transect in a Plague-Endemic Region of Uganda.

The vast majority of human plague cases currently occur in sub-Saharan Africa. The primary route of transmission of Yersinia pestis, the causative agent of plague, is via flea bites. Non-pathogenic flea-associated bacteria may interact with Y. pestis within fleas and it is important to understand what factors govern flea-associated bacterial assemblages. Six species of fleas were collected from nine rodent species from ten Ugandan villages between October 2010 and March 2011. A total of 660,345 16S rRNA gene DNA sequences were used to characterize bacterial communities of 332 individual fleas. The DNA sequences were binned into 421 Operational Taxonomic Units (OTUs) based on 97% sequence similarity. We used beta diversity metrics to assess the effects of flea species, flea sex, rodent host species, site (i.e. village), collection date, elevation, mean annual precipitation, average monthly precipitation, and average monthly temperature on bacterial community structure. Flea species had the greatest effect on bacterial community structure with each flea species harboring unique bacterial lineages. The site (i.e. village), rodent host, flea sex, elevation, precipitation, and temperature also significantly affected bacterial community composition. Some bacterial lineages were widespread among flea species (e.g. Bartonella spp. and Wolbachia spp.), but each flea species also harbored unique bacterial lineages. Some of these lineages are not closely related to known bacterial diversity and likely represent newly discovered lineages of insect symbionts. Our finding that flea species has the greatest effect on bacterial community composition may help future investigations between Yersinia pestis and non-pathogenic flea-associated bacteria. Characterizing bacterial communities of fleas during a plague epizootic event in the future would be helpful.

Seasonal fluctuations of small mammal and flea communities in a Ugandan plague focus: evidence to implicate Arvicanthis niloticus and Crocidura spp. as key hosts in Yersinia pestis transmission.

BackgroundThe distribution of human plague risk is strongly associated with rainfall in the tropical plague foci of East Africa, but little is known about how the plague bacterium is maintained during periods between outbreaks or whether environmental drivers trigger these outbreaks. We collected small mammals and fleas over a two year period in the West Nile region of Uganda to examine how the ecological community varies seasonally in a region with areas of both high and low risk of human plague cases.MethodsSeasonal changes in the small mammal and flea communities were examined along an elevation gradient to determine whether small mammal and flea populations exhibit differences in their response to seasonal fluctuations in precipitation, temperature, and crop harvests in areas within (above 1300 m) and outside (below 1300 m) of a model-defined plague focus.ResultsThe abundance of two potential enzootic host species (Arvicanthis niloticus and Crocidura spp.) increased during the plague season within the plague focus, but did not show the same increase at lower elevations outside this focus. In contrast, the abundance of the domestic rat population (Rattus rattus) did not show significant seasonal fluctuations regardless of locality. Arvicanthis niloticus abundance was negatively associated with monthly precipitation at a six month lag and positively associated with current monthly temperatures, and Crocidura spp. abundance was positively associated with precipitation at a three month lag and negatively associated with current monthly temperatures. The abundance of A. niloticus and Crocidura spp. were both positively correlated with the harvest of millet and maize.ConclusionsThe association between the abundance of several small mammal species and rainfall is consistent with previous models of the timing of human plague cases in relation to precipitation in the West Nile region. The seasonal increase in the abundance of key potential host species within the plague focus, but not outside of this area, suggests that changes in small mammal abundance may create favorable conditions for epizootic transmission of Y. pestis which ultimately may increase risk of human cases in this region.

Bartonella infection in rodents and their flea ectoparasites: an overview.

Epidemiological studies worldwide have reported a high prevalence and a great diversity of Bartonella species, both in rodents and their flea parasites. The interaction among Bartonella, wild rodents, and fleas reflects a high degree of adaptation among these organisms. Vertical and horizontal efficient Bartonella transmission pathways within flea communities and from fleas to rodents have been documented in competence studies, suggesting that fleas are key players in the transmission of Bartonella to rodents. Exploration of the ecological traits of rodents and their fleas may shed light on the mechanisms used by bartonellae to become established in these organisms. The present review explores the interrelations within the Bartonella-rodent-flea system. The role of the latter two components is emphasized.

Fleas (Siphonaptera) associated with mammals in the mountain area between the Kuban and Bolshaya Laba Rivers

The flea fauna of mammals in the area between the Kuban and Bolshaya Laba Rivers counts 47 species. Most of them parasitize several hosts. The species composition and the structure of flea communities in different altitudinal belts are characterized. The flea Ctenophthalmus wagneri and some other flea species with Ancient Mediterranean ranges show the highest dominance indices in the foothills. Ctenophthalmus proximus and Leptopsylla taschenbergi, possessing ranges of the Caucasian type, prevail in the middle mountain belt. Megabothris turbidus and some other boreal species dominate among the species collected in the high mountain belt.

Fleas of small mammals in St. Petersburg

In the territory of St. Petersburg, 26 sites situated in areas with 4 types of forest vegetation, were examined. Fleas of 16 species were collected from small mammals belonging to 13 species. The flea Ctenophthalnius agyrtes was the most abundant species. Two types of flea communities can be distinguished, including communities of fleas of forests and forest parks and communities of fleas of urban parks and cemeteries.

Assembly rules of ectoparasite communities across scales: combining patterns of abiotic factors, host composition, geographic space, phylogeny and traits

We investigated the role of environmental filtering as an underlying mechanism of assembly of compound communities of fleas parasitic on Palearctic small mammals at two spatial scales; a continental scale (encompassing regions across the entire Palearctic) and a regional scale (across sampling localities within Slovakia). We used the three‐table ordination (the RLQ analysis) and its extended version that links species occurrences with geographic space, environmental variables, and species traits and phylogeny (the ESLTP analysis). We asked whether environmental filtering acts as an assembly rule of compound communities of fleas and, if yes, a) whether the effect of environment on species composition of compound communities of fleas differs between spatial scales and b) what are the relative importance of the abiotic and host environments. We found that compound communities of fleas are, to a great extent, assembled via environmental filters that represent interplay between filtering via abiotic environment and filtering via host composition. The relative importance of these two components of environmental filtering differed between spatial scales. Host composition had a stronger effect on flea assembly than abiotic environment on the continental scale, while the opposite was true for the regional scale. The likely reason behind this scale‐dependence is that communities on the regional scale are mainly governed by ecological and epidemiological processes, while communities on the continental scale are mainly affected by evolutionary, biogeographic and historical forces.

Patterns of host and flea communities along an elevational gradient in Colorado

Patterns in community composition across a landscape are the result of mechanistic responses and species interactions. Interactions between hosts and parasites have additional complexity because of the contingency of host presence and interactions among parasites. To assess the role of environmental changes within host and parasite communities, we surveyed small mammals and their fleas over a dynamic elevational gradient in the Front Range in Colorado, USA. Communities were characterized using several richness and diversity metrics and these were compared using a suite of frequentist and randomization approaches. We found that flea species richness was related to the number of host species based upon rarefaction, but no patterns in richness with elevation were evident. Values of diversity measures increased with elevation, representing that small-mammal and flea communities were more even upslope, yet turnover in composition was not related to examined variables. The results suggest there are strong local effects that drive these small-mammal and flea communities, although the breadth of flea species is tied to host availability.

Differentiation of flea communities infesting small mammals across selected habitats of the Baltic coast, central lowlands, and southern mountains of Poland

Only a few studies comparing flea composition on the coast and in the mountains have been conducted. We investigated differences in flea communities infesting small mammals in selected habitats in northern, central, and southern Poland. We predicted (1) a greater number of flea species in the southeastern Poland and a lower number in the north, (2) a greater number of flea species in fertile and wet habitats than in poor and arid habitats, and (3) a low similarity of flea species between flea communities in western and eastern Poland. We found a negative effect of increasing latitude on flea species richness. We suppose that the mountains providing a variety of environments and the limits of the geographic ranges of several flea subspecies in southeastern Poland result in a higher number of flea species. There was a positive effect of increasing wetness of habitat on flea species richness. We found a high diversity in flea species composition between western and eastern Poland (beta diversity = 11) and between central and eastern Poland (beta diversity = 12). Re-colonization of Poland by small mammals and their ectoparasites from different (western and eastern) refugees can affect on this high diversity of flea species.

Community structure of Great Gerbils (Rhombomys opimus) parasitic fleas in Junggar Basin focus and related epizootiological characteristics on plague

To understand the community structure of Rhombomys opimus parasitic fleas in the natural plague focus in Junggar Basin, so as to explain the relationship between the community structure and the prevalence of animal plague in this area. The body fleas of R.opimus which were collected in 2005-2010 from the Junggar Basin was analysed by community ecology method, an each clustered flea community was compared with information of pathogenic and serological indicators of animal plague epidemic by statistic method. The community structure of R. opimus parasitic fleas included 19 species and was very complicated, with only 3 were identified as 'common' species but the others belonged to 'rare' species. Both the average richness and diversity of flea community were higher, as 1.66 and 1.5556, with dominance not obvious (0.332) and the homogeneity as moderate (0.5283). The community structure of R. opimus parasitic fleas could be changed by the following factors as: the rates of flea parasitic/flea index and the proportions of main fleas etc. The flea community could be divided into 5 clusters according to the above said elements. All these data showed that the fleas of R. opimus parasitic fleas possess the nature of multi-parasitism. The community of R. opimus parasitic fleas existed heterogeneous of geographic region, and this phenomenon associated with the animal plague epidemic strength.

Co‐occurrence and phylogenetic distance in communities of mammalian ectoparasites: limiting similarity versus environmental filtering

Similarity between species plays a key role in the processes governing community assembly. The co‐occurrence of highly similar species may be unlikely if their similar needs lead to intense competition (limiting similarity). On the other hand, persistence in a particular habitat may require certain traits, such that communities end up consisting of species sharing the same traits (environmental filtering). Relatively little information exists on the relative importance of these processes in structuring parasite communities. Assuming that phylogenetic relatedness reflects ecological similarity, we tested whether the co‐occurrence of pairs of flea species (Siphonaptera) on the same host individuals was explained by the phylogenetic distance between them, among 40 different samples of mammalian hosts (rodents and shrews) from different species, areas or seasons. Our results indicate that frequency of co‐occurrence between flea species increased with decreasing phylogenetic distance between them in 37 out of 40 community samples, with 14 of these correlations being statistically significant. A meta‐analysis across all samples confirmed the overall trend for closely related species to co‐occur more frequently on the same individual hosts than expected by chance, independently of the identity of the host species or of environmental conditions. These findings suggest that competition between closely related, and therefore presumably ecologically similar, species is not important in shaping flea communities. Instead, if only fleas with certain behavioural, ecological and physiological properties can encounter and exploit a given host, and if phylogenetic relationships determine trait similarity among flea species, then a process akin to environmental filtering, or host filtering, could favour the co‐occurrence of related species on the same host.

Yersinia pestis infection and laboratory conditions alter flea-associated bacterial communities

We collected Oropsylla montana from rock squirrels, Spermophilus varigatus, and infected a subset of collected fleas with Yersinia pestis, the etiological agent of plague. We used bar-tagged DNA pyrosequencing to characterize bacterial communities of wild, uninfected controls and infected fleas. Bacterial communities within Y. pestis-infected fleas were substantially more similar to one another than communities within wild or control fleas, suggesting that infection alters the bacterial community in a directed manner such that specific bacterial lineages are severely reduced in abundance or entirely eliminated from the community. Laboratory conditions also significantly altered flea-associated bacterial communities relative to wild communities, but much less so than Y. pestis infection. The abundance of Firmicutes decreased considerably in infected fleas, and Bacteroidetes were almost completely eliminated from both the control and infected fleas. Bartonella and Wolbachia were unaffected or responded positively to Y. pestis infection.

The arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks

Bacterial community composition in blood-sucking arthropods can shift dramatically across time and space. We used 16S rRNA gene amplification and pyrosequencing to investigate the relative impact of vertebrate host-related, arthropod-related and environmental factors on bacterial community composition in fleas and ticks collected from rodents in southern Indiana (USA). Bacterial community composition was largely affected by arthropod identity, but not by the rodent host or environmental conditions. Specifically, the arthropod group (fleas vs ticks) determined the community composition of bacteria, where bacterial communities of ticks were less diverse and more dependent on arthropod traits--especially tick species and life stage--than bacterial communities of fleas. Our data suggest that both arthropod life histories and the presence of arthropod-specific endosymbionts may mask the effects of the vertebrate host and its environment.

Compositional and phylogenetic dissimilarity of host communities drives dissimilarity of ectoparasite assemblages: geographical variation and scale-dependence

We tested the hypothesis that compositional and/or phylogenetic dissimilarity of host assemblages affect compositional and/or phylogenetic dissimilarity of parasite assemblages, to different extents depending on scale, using regional surveys of fleas parasitic on small mammals from 4 biogeographical realms. Using phylogenetic community dissimilarity metric, we calculated the compositional and phylogenetic dissimilarity components between all pairs of host and parasite communities within realms and hemispheres. We then quantified the effect of compositional or phylogenetic dissimilarity in host regional assemblages, and geographical distance between assemblages, on the compositional or phylogenetic dissimilarity of flea regional assemblages within a realm, respectively. The compositional dissimilarity in host assemblages strongly affected compositional dissimilarity in flea assemblages within all realms and within both hemispheres. However, the effect of phylogenetic dissimilarity of host assemblages on that of flea assemblages was mostly confined to the Neotropics and Nearctic, but was detected in both the Old and New World at the higher scale, possibly because of phylogenetic heterogeneity in flea and host faunas between realms. The clearer effect of the compositional rather than the phylogenetic component of host community dissimilarity on flea community dissimilarity suggests important roles for host switching and ecological fitting during the assembly history of flea communities.

Flea diversity on small carnivores in the Northern Cape Province, South Africa

Small carnivores are parasitized by various ectoparasites that include fleas (Siphonaptera). To date few parasite studies in South Africa, and especially the Northern Cape, have focused on fleas, while those that have are biased by small sample sizes. In an attempt to address the paucity of information fleas were collected from five small carnivore species trapped at Loxton and Kimberley in the Northern Cape Province, South Africa. The aim of the study was to contribute to current data on the flea diversity found on various small carnivore species. Small carnivores were trapped and while anesthetized the fleas were manually removed from the fur of the animals. In total 48 small carnivores were trapped of which 30 harboured fleas. Of the five flea species that were recorded the most numerous and prevalent was Echidnophaga gallinacea followed by Ctenocephalides connatus and Ctenocephalides damarensis. Fleas were more numerous and prevalent on the small-spotted cat, Felis nigripes, followed by the yellow mongoose, Cynictispenicillata. The flea community on the small carnivores consisted of fleas that prefer carnivores as principal hosts and also fleas that prefer rodents. The latter maybe acquired through predation on rodents.

Male hosts drive infracommunity structure of ectoparasites

We studied the co-occurrence of flea species in infracommunities of 16 rodents from four regions (South Africa, Tanzania, central Europe and western Siberia) using null models, and predicted that flea co-occurrences will be expressed more strongly in male than in female hosts. We examined patterns of co-occurrence (measured as the C score) in infracommunities of fleas that are parasitic on male and female hosts by comparing co-occurrence frequencies with those expected by chance. When a significant degree of nonrandomness in flea co-occurrences was detected, it indicated aggregative infracommunity structure. In Tanzanian rodents, no significant flea co-occurrences were detected in either male or female hosts. In a South African rodent, significant flea co-occurrences were not detected in males, but were found in females in some localities. In Palaearctic rodents, significant nonrandomness was detected either equally for males and females or more frequently in males than in females. Meta-analyses demonstrated that the frequency of the detection of nonrandomness in flea co-occurrences was significantly higher in male than in female hosts. The values of the standardized effect size (SES) for the C score differed significantly among host species, but not between host genders. When the Palaearctic hosts were analyzed separately, the effects of both host gender and species appeared to be significant, with the SES values for the C score in males being smaller than those in females. The strength of the gender difference in the manifestation of flea community structure increased with increasing gender difference in flea species richness, and with decreasing gender difference in flea prevalence for the Palaearctic hosts. We conclude that male hosts are the main drivers of flea infracommunity structure. However, the manifestation of gender bias in flea community structure varies among host species, and is likely determined by the pattern of species-specific spatial behavior.

Aggregative structure is the rule in communities of fleas: null model analysis

We used null models to examine patterns of species co-occurrences in 59 communities of fleas parasitic on small mammals from 4 biogeographic realms (Afrotropics, Nearctic, Neotropics, and Palaearctic). We compared frequencies of co-occurrences of flea species across host species with those expected by chance, using a null model approach. We used 4 tests for non-randomness to identify pairs of species (within a community) that demonstrate significant positive or negative co-occurrence. The majority of flea communities were non-randomly assembled. Patterns of flea co-occurrences on the same host species indicated aggregation but not segregation of flea species (except for the flea community of Madagascar). Although only a small fraction of species pairs were associated significantly (264 of 10, 943 species pairs according to the most liberal criterion), most of these associations were positive (except for 2 negatively associated species pairs). Significantly associated pairs were represented mainly by non-congeneric species. The degree of non-randomness of the entire flea community was similar among biogeographic regions, but the strength of pair-wise association varied geographically, being the highest in the Afrotropics and the lowest in the European region of the Palaearctic.