Structure of compound and component communities of fleas parasitic on small mammals in six different regions as revealed by environmental-based co-occurrence geometry analyses.

We inferred the patterns of co-occurrence of flea species in compound (across all host species) and component (across conspecific hosts) communities from six regions of the world (Mongolia, Northwest Argentina, Argentinian Patagonia, West Siberia, Slovakia, and South Africa) using the novel eigenvector ellipsoid method. This method allows us to infer structural community patterns by comparing species' environmental requirements with the pattern of their co-occurrences. We asked whether: (a) communities are characterized by species segregation, nestedness, or modularity; (b) patterns detected by the novel method conform to the patterns identified by traditional methods that search for non-randomness in community structure; and (c) the pattern of flea species co-occurrences in component communities is associated with host species traits. The results of the application of the eigenvector ellipsoid method suggested that the co-occurrence of flea species was random in all compound communities except in South Africa, where this community demonstrated a tendency to be nested. Flea species co-occurrences were random in many component communities. Species segregation was detected in the flea community of one host, whereas the flea communities of 14 hosts from different regions appeared to be nested. No indication of a modular structure in any community was found. The nestedness of flea component communities was mainly characteristic of hosts with a low relative brain mass. We concluded that the application of this novel method that combines data on species distribution and their environmental requirements allows better identification of the community structural patterns and produces more reliable results as compared with traditional methods.

Dark host specificity in two ectoparasite taxa: repeatability, parasite traits, and environmental effects.

We applied the concept of dark diversity (species that may potentially inhabit a locality but are absent) to the host spectrum of a parasite and defined it as dark host specificity (DHS). We studied the trait-associated and geographic patterns of dark host specificity in fleas and gamasid mites parasitic on small mammals, asking the following questions: (a) Is dark host specificity repeatable across populations of the same species? (b) Is it associated with morphological and/or ecological species traits? (c) What are the factors associated with geographical variation in the DHS among populations of the same species? The DHS was repeatable within species with a large proportion of variance among samples, accounted for by differences between species. The average DHS of fleas, but not mites, was affected by parasite traits, with the DHS being higher in fleas with larger geographic ranges, higher characteristic abundance levels, and summer reproduction peaks. In the majority of ectoparasites, the regional DHS decreased with an increase in either structural or phylogenetic host specificity. The associations between the DHS and the environmental or host-associated characteristics of a region were revealed in a few species (eight of 22 fleas and three of 12 mites). The DHS decreased with (a) an increase in air temperature in two fleas, (b) a decrease in precipitation in two fleas, and (c) an increase in regional host species richness (in three fleas and three mites). Overall, our results suggest that dark host specificity in arthropod ectoparasites is a species-specific character associated, to a large extent, with the breadth of their host-related niches, while the influences of parasite traits and local environmental conditions are minor.

Spatial and temporal variation of compositional, functional, and phylogenetic diversity in ectoparasite infracommunities harboured by small mammals.

We studied patterns of compositional, functional, and phylogenetic α- and ß-diversity in flea and gamasid mite infracommunities of small Siberian mammals, taking into account host-associated (species) and environmental (biome or sampling period) factors. We asked: (a) How do these factors and their interactions affect infracommunity diversity? (b) Does infracommunity composition, in terms of species, traits, and phylogenetic lineages, deviate from random? (c) Are species, traits, and phylogenetic lineages in infracommunities clustered or overdispersed?, and (d) Do patterns of diversity differ between the three diversity facets and/or the two ectoparasite taxa? We found that the α-diversity of infracommunities was strongly affected by host species, biome, and sampling period. The highest proportion of infracommunity diversity in both taxa was associated with the interaction between either host species and biome or host species and sampling period. Infracommunities of both taxa within, as well as between, host species, biomes, and sampling periods were characterized by the clustering of species, traits and lineages. The patterns of the effects of host species, biome, and sampling period on infracommunity diversity were congruent among the three diversity facets in both fleas and mites. We conclude that the assembly patterns in ectoparasite infracommunities mirror those characteristics of component and compound communities.

An annotated catalogue of the gamasid mites associated with small mammals in Asiatic Russia. The family Hirstionyssidae (Acari: Mesostigmata: Gamasina).

This article represents the third (and last) part of the catalogue of ectoparasitic gamasid mites associated with small mammals in Asiatic Russia (Siberia and the Russian Far East). A total of 19 species of the genus Hirstionyssus Fonseca, 1948 are indexed, with data on their taxonomic position, nomenclature, host range, and distribution within the region. As a conclusion, a brief overview of fauna of ectoparasitic gamasid mites parasitising Micromammalia (except bats) of Asiatic Russia is given. In total, 71 mite species belonging to nine genera of three families (Haemogamasidae, Hirstionyssidae, Laelapidae) are recorded and divided among taxonomic and ecological groupings.

Spatial and temporal turnover of parasite species and parasite-host interactions: a case study with fleas and gamasid mites parasitic on small mammals.

We studied patterns of ectoparasite species turnover and pairwise ectoparasite-host interactions across space and time in fleas and mites harboured by small mammals using a novel metric, zeta diversity (similarity between multiple communities). We asked whether the zeta diversity of parasites and their interactions with hosts follow a similar spatial or temporal trend. We found substantial differences in some (zeta decline and retention rate) but not in other (zeta decay) spatial patterns of zeta diversity between species and interactions, whereas the differences between the patterns of the temporal species versus interaction zeta diversity occurred to a much lesser extent. In particular, the parametric form of zeta decline suggested that the distribution of ectoparasite species across localities is driven mainly by niche-based processes, whereas the spatial distribution of flea-host and mite-host interactions is predominantly stochastic. We also found much stronger variation in the number of shared species and interactions over space than over time. Parasite community composition, in terms of species, appeared to be much more temporally stable than that in terms of parasite-host interactions. The parametric form of temporal zeta decline indicated that both parasite communities and parasite-host networks are assembled over time via niche-based processes.

Patterns of zeta diversity in ectoparasite communities harboured by small mammals at three hierarchical scales: taxon-invariance and scale-dependence.

We studied compositional turnover in communities of fleas and mites harboured by small mammals using zeta diversity metric (similarity between multiple communities) and asked whether the patterns of zeta diversity decline with an increase in the number of communities differ between taxa and hierarchical scales [infracommunities (parasite assemblages on individual hosts), component communities (parasite assemblages harboured by host populations), and compound communities (all parasite species in a locality)]. The average number of shared species declined with an increasing number of communities (zeta order). It attained zero at higher orders in infracommunities of both taxa with the shape of the zeta decline being best fitted by the negative exponential function, and the retention rate curves being modal. In contrast, zeta diversity values for compound communities of mites and fleas did not attain zero at higher zeta orders, and the form of the zeta decline was best fitted by the power-law function, whereas the retention rate curves were asymptotic. In component communities, the form of zeta decline was best fitted by either exponential or power-law function in dependence of whether communities were considered within a host across localities or across hosts within a locality and whether ubiquitous species were taken into account. Our main conclusions are that (a) the rules governing compositional turnover in parasite communities for the lowest and the highest hierarchical scales are taxon-invariant but scale-dependent and (b) species composition of infracommunities is mainly driven by stochastic assembly processed, whereas that of compound communities is mainly driven by niche-based processes.

The effects of environment, hosts and space on compositional, phylogenetic and functional beta-diversity in two taxa of arthropod ectoparasites.

We studied the effects of variation in environmental, host-associated and spatial factors on variation in compositional, phylogenetic/taxonomic and functional facets of beta-diversity in fleas and gamasid mites parasitic on small mammals and asked whether (a) the importance of these factors as drivers of beta-diversity differs among its multiple facets and (b) the effects of variation in environment, hosts and space on beta-diversity variation differ between the two ectoparasite taxa. To understand the relative effects of each group of predictors, we used a distance-based redundancy analysis and variation partitioning. The greatest portions of variation in the compositional beta-diversity of fleas were equally explained by host-associated and spatial predictors, whereas variation in host species composition contributed the most to variation in the compositional beta-diversity of mites. Variation in the phylogenetic (i.e. based on phylogenetic tree) beta-diversity of fleas was mainly due to variation in the phylogenetic composition of host communities, while the taxonomic (i.e. based on Linnean taxonomy) beta-diversity of mites was influenced by environmental variation. Unique contributions of spatial and environmental variation explained most of the variation in functional beta-diversity and its species replacement (= turnover) component (i.e. beta-diversity explained by replacement of species alone) in fleas and mites, respectively. Variation in the richness difference component (i.e. beta-diversity explained by species loss/gain alone) of functional beta-diversity was mainly affected by either variation in the functional composition of host assemblages (fleas) or its joint action with environmental variables (mites). We conclude that the pattern of the relative effects of environmental, host-associated and spatial factors on beta-diversity is context-dependent and may differ among different facets of beta-diversity, among different beta-diversity components and also among taxa dependent on biological affinities.

Do the pattern and strength of species associations in ectoparasite communities conform to biogeographic rules?

We tested whether biogeographic patterns characteristic of species diversity and composition may also apply to community assembly by investigating geographic variation in the pattern (PSA) (aggregation versus segregation) and strength of species associations (SSA) in flea and mite communities harbored by small mammalian hosts in Western Siberia. We asked whether (a) there is a relationship between latitude and PSA or SSA and (b) similarities in PSA or SSA follow a distance decay pattern or if they are better explained by variation in environmental factors (altitude, amount of vegetation, precipitation, and air temperature). We used a sign of a co-occurrence metric (the C-score) as an indicator of PSA and its absolute standardized value as a measure of SSA. We analyzed data using logistic and linear models, generalized dissimilarity modeling (GDM), and a logistic version of the multiple regression on distance matrices (MRM). The majority of the C-scores of the observed presence/absence matrices indicated a tendency to species aggregation rather than segregation. No effect of latitude on PSA or SSA was found. The dissimilarity in PSA was affected by environmental dissimilarity in mite compound communities only. A relatively large proportion of the deviance of spatial variation in SSA was explained by the GDMs in infracommunities, but not component communities, and in only three (of seven) and two (of eight) host species of fleas and mites, respectively. The best predictors of dissimilarity in SSA in fleas differed between host species, whereas the same factor (precipitation) was the best predictor of dissimilarity in SSA in mites. We conclude that PSA and SSA in parasite communities rarely conform to biogeographic rules. However, when a biogeographic pattern is detected, its manifestation differs among hosts and between ectoparasite taxa.

Biogeography of parasite abundance: latitudinal gradient and distance decay of similarity in the abundance of fleas and mites, parasitic on small mammals in the Palearctic, at three spatial scales.

We tested whether biogeographic patterns characteristic for biological communities can also apply to populations and investigated geographic patterns of variation in abundance of ectoparasites (fleas and mites) collected from bodies of their small mammalian hosts (rodents and shrews) in the Palearctic at continental, regional and local scales. We asked whether (i) there is a relationship between latitude and abundance and (ii) similarity in abundance follows a distance decay pattern or it is better explained by variation in extrinsic biotic and abiotic factors. We analysed the effect of latitude on mean intraspecific abundance using general linear models including proportional abundance of its principal host as an additional predictor variable. Then, we examined the relative effect of geographic distance, biotic and abiotic dissimilarities among regions, subregions or localities on the intraspecific dissimilarity in abundance among regions, subregions or localities using Generalized Dissimilarity Modelling. We found no relationship between latitude and intraspecific flea or mite abundance. In both taxa, environmental dissimilarity explained the largest part of the deviance of spatial variation in abundance, whereas the effect of the dissimilarity in the principal host abundance was of secondary importance and the effect of geographic distance was minor. These patterns were generally consistent across the three spatial scales, although environmental variation and dissimilarity in principal host abundance were equally important at the local scale in fleas but not in mites. We conclude that biogeographic patterns related to latitude and geographic distance do not apply to spatial variation of ectoparasite abundance. Instead, the geographic distribution of abundance in arthropod ectoparasites depends on their responses, mainly to the off-host environment and to a lesser extent the abundance of their principal hosts.

Sexual size dimorphism and sex ratio in arthropod ectoparasites: contrasting patterns at different hierarchical scales.

The aims of this study were to determine whether sexual size dimorphism in fleas and gamasid mites (i) conforms to Rensch's rule (allometry of sexual size dimorphism) and (ii) covaries with sex ratio in infrapopulations (conspecific parasites harboured by an individual host), xenopopulations (conspecific parasites harboured by a population of a given host species in a locality) and suprapopulations (conspecific parasites harboured by an entire host community in a locality). Rensch's rule in sexual size dimorphism was tested across 150 flea and 55 mite species, whereas covariation between sexual size dimorphism and sex ratio was studied using data on ectoparasites collected from small mammalian hosts in Slovakia and western Siberia. For fleas, we controlled for the confounding effect of phylogeny. The slope of the linear regression of female size on male size was significantly smaller than 1 in fleas, but did not differ from 1 in mites. The proportion of males in flea infrapopulations significantly increased with an increase in the female-to-male body size ratio. The same was true for obligatory haematophagous mites. No relationship between sex ratio and sexual size dimorphism was found for xenopopulations of either taxon or for mite suprapopulations. However, when controlling for the confounding effect of phylogeny, a significant negative correlation between sex ratio and sexual size dimorphism was revealed for flea suprapopulations. We conclude that (i) some macroecological patterns differ between ectoparasite taxa exploiting the same hosts (allometry in sexual size dimorphism), whereas other patterns are similar (sexual size dimorphism-sex ratio relationship in infrapopulations), and (ii) some patterns are scale-dependent and may demonstrate the opposite trends in parasite populations at different hierarchical levels.

Relationships among different facets of host specificity in three taxa of haematophagous ectoparasites.

Host specificity is a fundamental trait of a parasite species. Recently, multiple aspects of host specificity have been recognized, but the relationships between these facets are still poorly understood. Here, we studied pairwise relationships between basic, structural, phylogenetic and geographic host specificity in three taxa of haematophagous ectoparasitic arthropods that differ in tightness of their association with the host. We asked which metrics of host specificity are correlated within each parasite taxon and whether the patterns of the association between different facets of host specificity are similar among parasite taxa. Data on bat flies were taken from published surveys across the Neotropics while data on fleas and mites parasitic on small mammals were compiled from multiple published surveys across the Palaearctic. Basic, structural, phylogenetic and geographic specificity indices were calculated for 18 bat fly species recorded on 40 host species from 15 regions, 109 flea species recorded on 120 host species from 51 regions and 34 mite species recorded on 67 host species from 28 regions. Then, we tested for the correlation between any two measures of host specificity using model II regressions. We found that structural and basic specificity, as well as structural and geographic specificity, exhibited a positive association in all three taxa. However, basic and geographic specificity, as well as basic and phylogenetic specificity, were significantly positively associated in fleas but did not correlate in bat flies or mites. In addition, we found a significant negative association between structural and phylogenetic specificity in bat flies but no association in the remaining taxa. Moreover, geographic and phylogenetic specificity were not associated in any parasite taxon. Our results suggest that different facets of host specificity were shaped differently by natural selection in different taxa.

An annotated catalogue of the gamasid mites associated with small mammals in Asiatic Russia. The family Haemogamasidae (Acari: Mesostigmata: Gamasina).

We provide a list of the species of the family Haemogamasidae Oudemans, 1926 living in Asiatic Russia, with data on their synonymy, distribution, and relationships with mammal hosts. In total, 23 species of mites distributed between two genera (Eulaelaps Berlese, 1903, and Haemogamasus Berlese, 1889) are covered.

Beta-diversity of ectoparasites at two spatial scales: nested hierarchy, geography and habitat type.

Beta-diversity of biological communities can be decomposed into (a) dissimilarity of communities among units of finer scale within units of broader scale and (b) dissimilarity of communities among units of broader scale. We investigated compositional, phylogenetic/taxonomic and functional beta-diversity of compound communities of fleas and gamasid mites parasitic on small Palearctic mammals in a nested hierarchy at two spatial scales: (a) continental scale (across the Palearctic) and (b) regional scale (across sites within Slovakia). At each scale, we analyzed beta-diversity among smaller units within larger units and among larger units with partitioning based on either geography or ecology. We asked (a) whether compositional, phylogenetic/taxonomic and functional dissimilarities of flea and mite assemblages are scale dependent; (b) how geographical (partitioning of sites according to geographic position) or ecological (partitioning of sites according to habitat type) characteristics affect phylogenetic/taxonomic and functional components of dissimilarity of ectoparasite assemblages and (c) whether assemblages of fleas and gamasid mites differ in their degree of dissimilarity, all else being equal. We found that compositional, phylogenetic/taxonomic, or functional beta-diversity was greater on a continental rather than a regional scale. Compositional and phylogenetic/taxonomic components of beta-diversity were greater among larger units than among smaller units within larger units, whereas functional beta-diversity did not exhibit any consistent trend regarding site partitioning. Geographic partitioning resulted in higher values of beta-diversity of ectoparasites than ecological partitioning. Compositional and phylogenetic components of beta-diversity were higher in fleas than mites but the opposite was true for functional beta-diversity in some, but not all, traits.

An annotated catalogue of the gamasid mites associated with small mammals in Asiatic Russia. The family Laelapidae s. str. (Acari: Mesostigmata: Gamasina).

Twenty-nine species of mites of the family Laelapidae s. str. have been recorded as associated with small mammals (rodents, insectivores) in Asiatic Russia (Siberia and the Russian Far East). These species belong to two subfamilies (Laelapinae, Myonyssinae) and six genera: Androlaelaps Berlese, 1903, Dipolaelaps Zemskaya & Piontkovskaya, 1960, Laelaps C.L. Koch, 1836, Hyperlaelaps Zakhvatkin, 1948, Myonyssus Tiraboschi, 1904, Oryctolaelaps Lange, 1955. A list of the species, with data on synonymy, geographic ranges, and relationships with mammal hosts is provided. Some considerations concerning patterns of distribution of the parasitic Laelaptidae of Asiatic Russia are presented as well as their classifications from the point of view of known host association records.

Intraspecific variation of body size in a gamasid mite Laelaps clethrionomydis: environment, geography and host dependence.

We investigated intraspecific variation in body size of an ectoparasitic gamasid mite, Laelaps clethrionomydis, across 12 localities in the Palearctic. We asked whether mites collected from the same host species in different localities or from different host species in the same locality vary in body size. Within host species, mites collected in different localities differed significantly in body size, tending to be larger in northern than in southern localities. In addition, mite body size correlated negatively with mean annual temperature in a locality. Mites collected from different hosts in the same locality differed significantly in body size when hosts belonged to different genera but did not differ when collected from congeneric hosts. We conclude that intraspecific variation in mite body size is caused by interplay of environmental and host-related factors.

Temporal dynamics of direct reciprocal and indirect effects in a host-parasite network.

1. Temporal variation in the direct and indirect influence that hosts and parasites exert on each other is still poorly understood. However, variation in species' influence due to species and interactions turnover can have important consequences for host community dynamics and/or for parasite transmission dynamics, and eventually for the risk of zoonotic diseases. 2. We used data on a network of small mammals and their ectoparasites surveyed over 6 years to test hypotheses exploring (i) the temporal variability in direct and indirect influences species exert on each other in a community, and (ii) the differences in temporal variability of direct/indirect influences between temporally persistent (TP) and temporally intermittent species. 3. We modelled the temporal variation in (i) direct reciprocal influence between hosts and parasites (hosts providing resources to parasites and parasites exploiting the resources of hosts), using an asymmetry index, and (ii) indirect influence among species within a community (e.g. facilitation of parasite infestation by other parasites), using betweenness centrality. We also correlated asymmetry and centrality to examine the relationship between them. 4. Network dynamics was determined by TP species but even those species had strong among-species heterogeneity in the temporal variation of the direct/indirect effects they exerted. In addition, there was a significant positive linear correlation between asymmetry and centrality. 5. We conclude that the temporal dynamics of host-parasite interactions is driven by TP hosts. However, even within this group of persistent species, some exhibit large temporal variation, such that the functional roles they play (e.g. in promoting parasite transmission) change over time. In addition, parasites having a large negative impact on hosts are also those facilitating the spread of other parasites through the entire host community. Our results provide new insights into community dynamics and can be applied in the management of antagonistic networks aimed at preventing disease outbreaks.

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.

Similarity in ectoparasite faunas of Palaearctic rodents as a function of host phylogenetic, geographic or environmental distances: which matters the most?

Different host species harbour parasite faunas that are anywhere from very similar to very different in species composition. A priori, the similarity in the parasite faunas of any two host species should decrease with increases in either the phylogenetic distance, the distinctness of the environments occupied or the geographical distance between these hosts. We tested these predictions using extensive data on the faunas of fleas (Insecta: Siphonaptera) and gamasid mites (Acari: Parasitiformes) parasitic on rodents across the Palaearctic. For each pair of host species, we computed the similarity in parasite faunas based on both species composition as well as the phylogenetic and/or taxonomic distinctness of parasite species. Phylogenetic distances between hosts were based on patristic distances through a rodent phylogeny, geographic distances were computed from geographic range data, and environmental dissimilarity was measured from the average climatic and vegetation scores of each host range. Using multiple regressions on distance matrices to assess the separate explanatory power of each of the three dependent variables, environmental dissimilarity between the ranges of host species emerged as the best predictor of dissimilarity between parasite faunas, especially for fleas; in the case of mites, phylogenetic distance between host species was also important. A closer look at the data indicates that the flea and mite faunas of two hosts inhabiting different environments are always different, whilst hosts living in similar environments can have either very similar or dissimilar parasite faunas. Additional tests showed that dissimilarity in flea or mite faunas between host geographic ranges was best explained by dissimilarity in vegetation, followed by dissimilarity in climatic conditions. Thus, external environmental factors may play greater roles than commonly thought in the evolution of host-parasite associations.

Inferring associations among parasitic gamasid mites from census data.

Within a community, the abundance of any given species depends in large part on a network of direct and indirect, positive and negative interactions with other species, including shared enemies. In communities where experimental manipulations are often impossible (e.g., parasite communities), census data can be used to evaluate the strength or frequency of positive and negative associations among species. In ectoparasite communities, competitive associations can arise because of limited space or food, but facilitative associations can also exist if one species suppresses host immune defenses. In addition, positive associations among parasites could arise merely due to shared preferences for the same host, without any interaction going on. We used census data from 28 regional surveys of gamasid mites parasitic on small mammals throughout the Palaearctic, to assess how the abundance of individual mite species is influenced by the abundance and diversity of other mite species on the same host. After controlling for several confounding variables, the abundance of individual mite species was generally positively correlated with the combined abundances of all other mite species in the community. This trend was confirmed by meta-analysis of the results obtained for separate mite species. In contrast, there were generally no consistent relationships between the abundance of individual mite species and either the species richness or taxonomic diversity of the community in which they occur. These patterns were independent of mite feeding mode. Our results indicate either that synergistic facilitative interactions among mites increase the host's susceptibility to further attacks (e.g., via immunosuppression) and lead to different species all having increased abundance on the same host, or that certain characteristics make some host species preferred habitats for many parasite species.