Landscape aspects of host-parasite relationships between parasitic arthropods and the narrow-skulled vole Microtus gregalis (Rodentia) in Western Siberia

Comparative zoogeographic analysis of outcomes accumulated in the course of long-term investigation the parasitic and free-living arthropods (Acarina: Parasitiformes; Insecta: Siphonaptera) associated with three subspecies of the narrow-skulled vole (Microtus gregalis gregalis, M. g. major, M. g. eversmanni) in various landscape zones and subzones in a flat part of Western Siberia, foothills of the Altai-Sayan mountain system and mountains of Southwest Altai. The obtained data, on the one hand, recover specific features of certain parasite communities that reflect ecological peculiarity of a host species living in conditions of concrete landscapes, on the other hand, a high degree of similarity between species set of some ectoparasitic and nidicolous arthropod groups from different subspecies of M. gregalis. The systematic list of ectoparasitic and nidicolous arthropods associated with M. gregalis and representing Gamasoidea mites, ticks and fleas is provided.     

Zonal types of host-parasite complexes of arthropods and small mammals in the west Siberian Plain

Comparative analysis of the composition, population structure, and landscape distribution of small mammals and associated parasitic arthropods was performed for the plain part of West Siberia. Four main zonal complexes were distinguished, corresponding to different landscape zones or subzones: tundra, forest, forest-steppe (the northern forest-steppe subzone), and steppe (the southern forest-steppe subzone and steppes). The parasite specificity of each complex is defined by different systematic and ecological groups of arthropods: the tundra complex is defined by epizoic gamasid mites (Acari: Parasitiformes: Mesostigmata), the forest and forest-steppe complexes are defined by ticks (Acari: Parasitiformes: Ixodides) and fleas (Insecta: Siphonaptera), and the steppe complex is defined by fleas and nidicolous gamasid mites.     

Characteristics of zonal distribution of the gamasid mites connected with small mammals and their nests in Western Siberia

Analysis of long-term data on the fauna, landscape distribution, and structure of communities of the gamasid mites (Acari:Parasitiformes:Mesostigmata) connected with small mammals and their nests in the plain part of Western Siberia is carried out. By now, presence of 249 gamasid mite species is established in the territory under study, including 193 free-living and 56 parasitic species. Gamasid mites are represented by the maximal number of species on small mammals and in thers nests in northern forest-steppe (102 and 105 species respectively). Nine parasitic species from two ecological groups (epizoic and nidicolous) were found in all landscape zones of the West Siberian Plain, namely: 1) epizoic species Laelaps clethrionomydis Lange, 1955, Laelaps hilaris C. L. Koch, 1836, and Hyperlaelaps arvalis Zachvatkin, 1948 (obligatory non-exclusive hematophagous); 2) nidicolous species Androlaelaps casalis Berlese, 1887 (obligatory non-exclusive hematophagous), Eulaelaps stabularis C. L. Koch, 1836, Haemogamasus nidiformnes Bregetova, 1955 (facultative hematophagous), Haemnogamnasus ambulans Thorell, 1872 (obligatory non-exclusive hematophagous), Hirstionyssus isabellinus Oudemans, 1913, and Hirstionyssus eusoricis Bregetova, 1956 (obligatory exclusive hematophagous). Last three species demonstrate the mixed type of parasitism. The population of gamasid mites on small mammals is most specific in tundra, southern forest-steppe and steppe; the fauna of gamasid mites in nests is most specific in southern forest-steppe and steppe.     

Arthropods in the nests of lesser spotted eagle (Aquila pomarina)

In 2001–2007, altogether 57 nests of lesser spotted eagle were collected in the Orava region in northwestern Slovakia and four groups of arthropods were extracted from them. Richest in number of species and individuals were mites (23 species, 17,500 ind.), followed by beetles (12 species, 725 ind.), whereas pseudoscorpions were represented only by Pselaphochernes scorpioides (39 ind.) and fleas by Ceratophyllus garei (3 ind.). Unlike nests of other birds, free-living mites predominated in the nests fauna (83% of individuals), followed by nidicolous species with more or less free relationship to the nests, while parasitic species represented only a negligible part of the fauna. For the first time we observed phoresy of Nenteria pandioni, a specific and abundant mite in the eagles’ nests, on the nidicolous staphylinid Haploglossa puncticollis. The beetle fauna in the nests was much poorer than in nests of other birds. The predatory H. puncticollis was dominant in the nests (83%) and occurred continuously during the whole investigation period. Other beetles, even the widely distributed nidicols such as the histerid Gnathoncus buyssoni, were found rarely in nests. Predators were also the only abundant trophic group of beetles in the nests, while other trophic groups of beetles abundantly co-occur in nests of majority of other birds. The occurrence of all beetles was very unevenly distributed during the investigation period, but was positively correlated with occurrence of mites. The relatively low number of species and individuals of mites and beetles in the lesser spotted eagle nests resulted from their position on tree tops, at a height of 20–30 m and their quick drying out by sun and wind. It was also indicated by an enormously low number of species and individuals of mycetophagous beetles, which represent a significant component of the fauna in nests of other birds.     

Arthropods (Acarina, Coleoptera, Siphonaptera) in nests of hoopoe (Upupa epops) in Central Europe

In 1993–1995 and 2009–2011, during investigation of reproduction biology of hoopoe, 63 nests of this species were collected after fledging of the chicks in Slovakia and Austria and their arthropod fauna was analyzed. Altogether 5,481 individuals and 34 species of mesostigmatic mites were found in 82.5% of the nests examined. The nidicolous mite Androlaelaps casalis was most abundant and frequent, representing 91.7% of all individuals. The richest in species were saprophilous mites (64.7% of all recorded species), while ectoparasites of the genera Dermanyssus and Ornithonyssus represented only 0.4% of all mites. Only 8 beetle species represented by 65 individuals were found in 18 nests. The dominant trophical group were carnivores (mainly nidicolous Gnathoncus buyssoni) with almost identical representation in (86.2%), followed by a similar representation of necrophags (10.8%). Unlike nests of other birds, the typical nidicolous species Haploglossa puncticollis and the fungivors were absent due to the dry character of studied countryside and placement of the nests in boxes situated in vineyard cottages. Only one species of fleas, Ceratophyllus gallinae — parasitizing first of all in the passeriform birds and being particularly abundant in the cavity nesting birds was recorded in hoopoe nests.     

Structure and seasonal dynamics of the biotic community ectoparasites of the bank vole in the Il'men'-Volkhov lowland

A biodiversity, seasonal dynamics and parasite load of a single individual and local population of the bank vole (Clethrionomys glareolus) were studied in coniferous and mixed forests of the Ilmen-Volkhov lowland (neighborhood of Oskuy village, Chudovo region, Novgorod Province) in the period from June 1999 till May 2002. The Gero's traps were used for collecting the host. Lines of traps stood in each place during 3-5 days and were checked twice a day. Trapping of micromammalian hosts and collecting of parasites took place each month, except a few gaps. Total number of collected animals 2854 including 1405 bank voles. The 29 ectoparasite species were recorded on the bank vole in the area of study. Among some mites and fleas a few species are accidental parasites probably accepted by voles from other species of animals. In the Oskuy area, the bank voles are the main and additional hosts of 25 ectoparasite species: fleas--8, lice--1, ixodid ticks--2, gamasid mites--7, acariform mites 7. Species composition of ectoparasites, their occurrence and abundance change during the year. Seasonal changes of abundance and occurrence indices are most expressed in the temporary ectoparasites (ixodid ticks, chiggers, gamasid mites), while in the permanent parasites (lice, acariform mites: Myobiidae, Myocoptidae, Listrophoridae), the seasonal fluctuations of indices are displayed in a less scale. Most vole specimens were infected with this or that ectoparasite species. The parasitocenosis on an individual specimen usually included less than 10 species of the total number 29 species recorded on the bank vole in the area investigated. One ectoparasite species was recorded on 21% of host specimens, 2-5 ectoparasite species were found on 71% of host individuals. Maximal number of ectoparasite species (10 species) was registered on one specimen only. The parasite load was dispersed unevenly among the infected voles. Mean number of parasites of all species on a host individual varied from 124 to 295. The highest grade of parasites (237-297 parasite specimens) was found in the voles with 7-10 species of parasites.     

Co-occurrence of ectoparasites on rodent hosts: null model analyses of data from three continents

We studied patterns of species co-occurrence in communities of ectoparasitic arthropods (ixodid ticks, mesostigmate mites and fleas) harboured by rodent hosts from South Africa ( Rhabdomys pumilio ), South America ( Scapteromys aquaticus and Oxymycterus rufus ) and west Siberia ( Apodemus agrarius , Microtus gregalis , Microtus oeconomus and Myodes rutilus ) using null models. We compared frequencies of co-occurrences of parasite species or higher taxa across host individuals with those expected by chance. When non-randomness of parasite co-occurrences was detected, positive but not negative co-occurrences of parasite species or higher taxa prevailed (except for a single sample of mesostigmate mites from O. rufus ). Frequency of detection of non-randomness of parasite co-occurrences differed among parasite taxa, being higher in fleas and lower in mites and ticks. This frequency differed also among host species independent of parasite taxon, being highest in Microtus species and lowest in O. rufus and S. aquaticus . We concluded that the pattern of species co-occurrence in ectoparasite communities on rodent hosts is predominantly positive, depends on life history of parasites and may be affected to a great extent by life history of a host.     

Zonal types of host-parasite complexes of arthropods and small mammals in a flat part of Western Siberia

Within a flat part of Western Siberia distribution of the small mammals and parasitic arthropods connected with them is accompanied by formation zonal host-parasite complexes dated for corresponding landscape zones or subzones: tundra complex dated for a tundra zone; forest complex dated for a forest zone (including subzones northern taiga, middle taiga, southern taiga and subtaiga); forest-steppe complex dated for a northern forest-steppe subzone; steppe complex dated for a southern forest-steppe subzone and steppe. Parasitic specificity of each type of a complex is defined by arthropods of different systematical and ecological groups: a tundra complex is defined by epizoite gamasid mites (Mesostigmata), forest and forest-steppe complexes is defined by tick (Ixodides) and fleas (Siphonaptera), steppe complex is defined by fleas and nidicolous gamasid mites.     

Nidicolous arthropods associated with different chromosomal types of Spalax ehrenbergi Nehring*

The mole rat, Spalax ehrenbergi Nehring, is a complex group involving four chromosomal types of In = 52, 54, 58 and 60. These are clinally distributed from Mount Hermon in the north to the Negev in the south, covering humid, semihumid, semiarid and arid climates. Forty-seven breeding nests of Sehrenbergi were collected from 23 localities throughout the range and processed for nidicolous arthropods. A total of five species of fleas and 53 species of gamasid mites were collected. Their distribution in the investigated area has been analysed in relation to that of the chromosomal types of S.ehrenbergi. The following conclusions have been reached:(a) Only three of the species (two haematophagous gamasids and one fungivorous acarid) range across the whole investigated area, showing strong host specificity, (b) A correlation is apparent between the distribution of several nidicolous arthropods (fleas and gamasids) and the ‘54’ geographic region. This probably reflects geographical distribution rather than host specificity, (c) Palaearctic species reach their southern limit of distribution on Mount Hermon and the Golan Heights; possibly Ethiopian ones reach their northern limit in the Negev. (d) No direct correlation has been found between nidicolous arthropods and the chromosomal types of S. ehrenbergi. (e) Subjects for future investigation are outlined.     

The flea, Megabothris abantis: an invertebrate host of Hepatozoon sp. and a likely definitive host in hepatozoon infections of the montane vole, Microtus montanus

In searching for an invertebrate host for Hepatozoon sp. infecting the montane vole (Microtus montanus), we collected fleas, ticks, and mites from live-trapped voles and searched squash preparations for Hepatozoon oocysts. From 1989 through 1996, we identified six species of fleas in Grand Teton National Park: Megabothris abantis, Megabothris asio megacolpus, Aetheca wagneri, Peromyscopsylla selenis, Peromyscopsylla. hesperomys, and Hystrichopsylla dippiei dippiei. We found Hepatozoon oocysts only in M. abantis; we found no oocysts in mites or ticks. We conclude that M. abantis is an invertebrate host of Hepatozoon sp. and is likely to be the definitive host for theHepatozoon spp. of M. montanus.     

Species diversity and biocenotic relationships of gamasid mites (Parasitiformes,Gamasoidea) in the nests of the field vole <Emphasis Type="Italic">Microtus agrestis</Emphasis> L. of the Karelian middle taiga subzone

The species diversity and habitat relations of gamasid mites from nests of the field vole (Microtus agrestis L.) were studied in the middle taiga subzone of the Republic of Karelia. The fauna of gamasid mites on the field vole, in its nests, and in the forest litter is very diverse, comprising 49 species with a complex taxonomic structure (22 genera, 12 families) and a variety of life strategies (necrophages, zoophages, and hematophages). The fauna of gamasid mites is most diverse in the nests of M. agrestis and includes both primitive free-living forms and specialized obligatory (epizoic) parasites. The group with the highest diversity of mite species is that from the nest of M. agrestis, with the diversity index amounting to 2.65 (30 species, 18 genera, 11 families).     

Analysis of ectoparasites (chigger mites,gamasid mites,fleas and sucking lice) of the Yunnan red‐backed vole (Eothenomys miletus) sampled throughout its range in southwest China

The Yunnan red‐backed vole Eothenomys miletus (Rodentia: Cricetidae) is an endemic rodent species and reservoir host of zoonoses in southwest China. Based on a large host sample (2463 voles collected from 39 localities between 2001 and 2013), a general analysis of four categories of ectoparasite (fleas, sucking lice, chigger mites and gamasid mites) on E. miletus across its entire range of distribution was made. This analysis identified a total of 71 895 ectoparasites belonging to 320 species (30 species of flea, 9 of sucking louse, 106 of gamasid mite and 175 of chigger mite) with a high prevalence (87%), mean abundance (29.19) and mean intensity (33.69). Of the 18 vector species of zoonoses found on E. miletus, the flea Ctenophthalmus quadratus (Siphonaptera: Hystrichopsyllidae) and chigger mite Leptotrombidium scutellare (Trombidiformes: Trombiculidae) were the dominant species; these are the main vectors of zoonoses in China. All of the dominant parasite species showed an aggregated distribution pattern. Male voles harboured more species of parasite than females. Chigger mites represented the most abundant species group on voles and their prevalence was positively correlated with mean abundance (r = 0.73; P < 0.05). As a single rodent species, E. miletus has a high potential to harbour abundant ectoparasites with high species diversity and high rates of infestation. The sex of the vole affects ectoparasite infestation.     

Gamasid mites of common voles in the central Volga River region

The specific composition of gamasid mites from three species of voles (Microtus arvalis Pall., M. agrestis L., M. oeconomus Pall.) is given. Forest, field and flood-land groupings of the common vole having distinct phenotypical differences are characterized by differences in the structure of their parasite fauna. In the forest the number of meadow and meadow-field species decreases while that of forest species of mites regularly increases.     

Composition and seasonal changes of mesostigmatic mites (Acari) and fleas fauna (Siphonaptera) in the nests of Mus spicilegus (Mammalia: Rodentia)

Together 22,119 individuals and 47 species of mesostigmatic mites, and 485 individuals of fleas belonging to 6 species were obtained from 16 winter nests of mound-building mouse, Mus spicilegus. The most abundant mite species were Laelaps algericus (38.2%), Androlaelaps fahrenholzi (20.9%), Proctolaelaps pygmaeus (16.9%) and Alliphis halleri (8.3%). Ctenophthalmus assimilis (87%) was the highly predominant flea, present in all the positive nests. On the basis of trophic and topic relations, mites were assorted into four ecological groups; parasites had the highest abundance (67% of all individuals). The density peak values of individual ecological mite groups differed the during season. The population peak of the predominant mite species L. algericus was in December, predominance of females was registered throughout the study period. The maximum abundance of fleas was reported in January and May.     

Arthropods (Pseudoscorpionidea,Acarina, Coleoptera,Siphonaptera) in nests of the bearded tit (<Emphasis Type="Italic">Panurus biarmicus</Emphasis>)

In the period 1993–2006, during investigation of reproduction biology of the bearded tit, 106 deserted nests of the species were collected in Slovakia, Austria and Italy and their arthropod fauna was analyzed. Occasionally introduced individuals of the pseudoscorpion Lamprochernes nodosus, a frequent species in Central Europe, were recorded in the nests. Altogether 984 individuals and 33 species of mesostigmatic mites (Acari) were found in 46.2% of the nests examined. The ectoparasite Ornithonyssus sylviarum was most abundant and frequent; it represented almost 68.3% of all individuals. Due to it, the parasitic mites predominated (69.4% of individuals). Other ecological groups were less represented: edaphic detriticols − 11.6%, coprophils − 10.7%, species of vegetation stratum − 8.2%, and nidicols − 0.2%. Beetles (40 species, 246 individuals) were present in 57 nests. Most of the beetles were strongly hygrophilous species inhabiting soil surface in the reed stands or other types of wetlands and the shore vegetation. Predators represented 59% of all individuals. They might find food in the nests, but none of the species had a close relationship to bird nests and represented 35% of species. All beetle species penetrated the nests occasionally, when ascending on the vegetation or searching cover during periods of increased water level. Occasionally, larvae and nymphs of the Dermacentor marginatus tick were found. They were most probably introduced by insectivores of the genus Neomys. Only one species of fleas, Ceratophyllus garei — a parasite of birds nesting in humid environment, was recorded in the nests.     

Specificity of host-parasite relations between arthropods and terrestrial vertebrates

Specificity of partners in host-parasite system is one of its main characteristics. Unfortunately this term has different senses in scientific literature. In everyday practice one judges an extent of host specificity of a parasite mainly by indices of its occurrence and abundance on different host species. An occurrence of parasites in nature reflects general result of complex eco-physiological interrelationships between partners in hostparasite system. Specificity of parasites in a choice of hosts may depend on a belonging of the latter to certain taxa (phylogenetic specificity), or on biotic and abiotic factors (ecological specificity). In arthropods, the phylogentic specificity and coevolution are characteristic to a greater extent for permanent hosts (lice, Mallophaga, cheyletoid and feather mites). A coevolutionaryphylogenesis is disturbed by transfers of parasites onto new hosts, by different rates of speciation in filial lines or by an extinction of several parasite taxa. In temporary parasites different forms of ecological specificity are prevalent. A host specificity is expressed to the lesser extent in mosquitoes, horseflies and in other blood-sucking Diptera. In temporary parasites with a long-term feeding (ticks) coevolutionary sequences are relatively rare, because this parasites had to adapt not only to a life on host, but also to a lesser stable environment. In some nest-burrow bloodsuckers (fleas, gamasid mites and argasid ticks) the ecological specificity is shown no by their relations with certain host species, but by an associations with habitats occupied by hosts (burrow, nests, caves). In relation with a high dynamics of host-parasite system, a specificity of its partners is comparative and it is kept up only under specific ecological conditions.     

Weather dependent effects of nest ectoparasites on their bird hosts

This study reports the relationships between rainfall and ambient temperature with the abundances and prevalences of three species of ectoparasitic arthropods (viz, mites, blowfly larvae, fleas) in pied flycatcher Ficedula hypoleuca nests in three different breeding seasons In addition to its effects on the growth of nestling pied flycatchers, weather conditions were found to determine patterns of abundance and prevalence of ectoparasites Nest ectoparasites had detrimental effects on the fitness (nestling growth and survival until fledgling) of their hosts although the effects and the identity of harmful ectoparasites varied across the years Among the three species of nest ectoparasites, mites had the most consistent harmful effects on nestling growth Fleas were detrimental in the more cold and rainy year, while blowflies caused nestling mortality in the wanner year Different host-parasite interactions were present each year, most likely due to the effects of weather on the activity and timing of development of parasite populations     

Ectoparasites and phoresants of the root vole (Microtus oeconomus Pall.) in the Polesye

Drainage melioration in the Polesye resulted in a sharp increase in the number of tundra vole (Microtus oeconomus Pall.) which quickly included into the parasitocenosis of the drained land. There were found 26 parasitic and nonparasitic species of Gamasoidea, 3 species of Ixodidae and 2 species of Trombiculidae, 10 species of Aphaniptera, 3 species of Anoplura but there was found no species specific only for the tundra vole. All found parasites occur on many hosts. This explains wide parasitic links of the tundra vole with other homothermic animals which especially extensive with the bank vole and it may have important consequences for epizootiology of tularemia and tick-borne encephalitis.     

The seasonal dynamics of fleas (Siphonaptera) on bank voles (Clethrionomys glareolus) in the north part of Novgorod region

The twelve flea species were revealed on bank voles. Only four of them (Amalaraeus penicillige, Ctenophthalmus uncinatus, Megabothris turbidus, Peromescopsylla bidentata) were abundant in some seasons of the year. Four other species (Ct. agyrtes, Hystrichopsylla talpae, P. silvatica, Rhadinopsylla integella) are the parasites of bank vole too but their numbers were always low in the study area. The four last species (Amphypsylla rossica, M. walkeri, Doratopsylla dasycnema, Palaeopsylla soricis) are not peculiar to bank vole. They occurs on it occasionally from other animals--the voules of Mucrotus and shrews. The most species diversity of fleas on bank vole was observed at the period from August to October, the least one--in late winter, spring and early summer. The total abundance indices of fleas on the voles (mean number of the insects per host) ranged in different months from 0.17 to 5.65. The time of minimum flea numbers was August-September. The peak abundance was reached in springtime (March-April).     

Structure of populations and ecological nishes of ectoparasites in the parasite communities of small forest mammals

The paper reports the results of eight-year investigations on the ectoparasites of rodents and insectivores carried out in southern taiga of the Ilmen-Volkhov lowland (Novgorod Region) and Kurgolovsky reserve (Leningrad Region). Twelve species of small mammals were captured including three dominate species--bank vole Clethrionomys glareolus (2722 specimens), common shrew Sorex araneus (1658 specimens), and wood mouse Apodemus uralensis (367 specimens). Parasite community of the bank vole comprises 34 species of mites, ticks, and insects, the community of common shrew comprises 25 species, and the community of A. uralensis includes 28 species. Taxonomic diversity of the ectoparasite communities was shown to be based on the diversity of types of parasitism and ecological nishes of the host body. Permanent ectoparasites are found to be represented by 2 species of lie and 14 species of acariform mites. The group of temporary parasites includes 13 species of fleas, 10 species of gamasid mites. 3 ixodid species and 1 Trombiculidae. There is a common pool of temporary parasites of small mammals in the ecological system of taiga. Significance of different shrew and rodent species as hosts were found to be dependent on the population density in possible hosts and many other factors. Species diversity in the parasite communities of different small mammal species is dependent on the number of possible ecological nishes in the host body. Actual infill of these nishes by ectoparasites is usually lesser than potential one. Species composition of temporary parasites, their occurrence and abundance changes according to season. Interspecific competition in the temporary parasite species can decrease because of the seasonal disjunction of their population peaks. Diversification of the ecological niches of ectoparasites allow simultaneous feeding of more parasite individuals on one host, than in the case of parasitising of single species or several species with similar ecological nishes. The distribution of parasites on their hosts was also studied. The aggregative distribution has been found in ixodid larvae only, and the distribution of fleas was close to the Poisson distribution. Deviations from the aggregative distribution can be an effect of several independent factors, including limited ability of small mammals for providing numerous parasites with food. On the most part of hosts simultaneous parasitizing of no more than 1-3 individuals of each tick, mite, and flea species was registered. Excessive infestation by ectoparasites may probably be limited by effective reactions of self-purification in the mammal hosts.