Ixodoidea of the Western Palaearctic: A review of available literature for identification of species.

We aim to produce a review of the most important literature references necessary for the identification of ticks of the families Ixodidae and Argasidae in Europe and northern Africa (i.e. the Western Palaearctic region). The purpose of this paper is to pinpoint a set of critically selected papers that contain reliable information on morphology, taxonomic keys, and comparative discussions which are critical for the identification of the ticks reported in the target region. When necessary, comments are provided on the systematic position of a species, or on suitable papers already addressing the issue. This review includes a list of 216 references which cover all Ixodoidea species reported as permanent residents of the Western Palaearctic, namely 28 species of the genus Ixodes, two Dermacentor, seven Haemaphysalis, nine Hyalomma, eight Rhipicephalus, five Argas and about seven species of Ornithodoros.

Estimating Ixodes ricinus densities on the landscape scale.

BACKGROUND: The study describes the estimation of the spatial distribution of questing nymphal tick densities by investigating Ixodes ricinus in Southwest Germany as an example. The production of high-resolution maps of questing tick densities is an important key to quantify the risk of tick-borne diseases. Previous I. ricinus maps were based on quantitative as well as semi-quantitative categorisations of the tick density observed at study sites with different vegetation types or indices, all compiled on local scales. Here, a quantitative approach on the landscape scale is introduced. METHODS: During 2 years, 2013 and 2014, host-seeking ticks were collected each month at 25 sampling sites by flagging an area of 100 square meters. All tick stages were identified to species level to select nymphal ticks of I. ricinus, which were used to develop and calibrate Poisson regression models. The environmental variables height above sea level, temperature, relative humidity, saturation deficit and land cover classification were used as explanatory variables. RESULTS: The number of flagged nymphal tick densities range from zero (mountain site) to more than 1,000 nymphs/100 m(2). Calibrating the Poisson regression models with these nymphal densities results in an explained variance of 72 % and a prediction error of 110 nymphs/100 m(2) in 2013. Generally, nymphal densities (maximum 374 nymphs/100 m(2)), explained variance (46 %) and prediction error (61 nymphs/100 m(2)) were lower in 2014. The models were used to compile high-resolution maps with 0.5 km(2) grid size for the study region of the German federal state Baden-Württemberg. The accuracy of the mapped tick densities was investigated by leave-one-out cross-validation resulting in root-mean-square-errors of 227 nymphs/100 m(2) for 2013 and 104 nymphs/100 m(2) for 2014. CONCLUSIONS: The methodology introduced here may be applied to further tick species or extended to other study regions. Finally, the study is a first step towards the spatial estimation of tick-borne diseases in Central Europe.

Host preferences of immature Dermacentor reticulatus (Acari: Ixodidae) in a forest habitat in Germany.

Dermacentor reticulatus is widespread throughout Europe and is expanding its range in several European countries. It is associated with a number of different pathogens. Its role in the transmission of disease to humans is currently small; however, it might play an important role in the maintenance of pathogens in enzootic cycles. The ecology of D. reticulatus, especially of the immatures, is not well known. In this study, ticks from small mammals, caught in a capture-mark-release study between May 2012 and October 2014 in a unique woodland area close to Karlsruhe, Germany, were collected. The main host species trapped were the yellow-necked mouse (Apodemus flavicollis) and the bank vole (Myodes glareolus). Small mammal populations showed high variability in their density between the study years, which is probably due to harsh winter conditions in 2012/2013 and missing mast leading to high winter mortality. Larvae and nymphs of D. reticulatus were predominantly found in July and August, respectively, and the infestation rates among the different small mammal species suggest a host preference of D. reticulatus for M. glareolus.

Different parasite faunas in sympatric populations of sister hedgehog species in a secondary contact zone.

Providing descriptive data on parasite diversity and load in sister species is a first step in addressing the role of host-parasite coevolution in the speciation process. In this study we compare the parasite faunas of the closely related hedgehog species Erinaceus europaeus and E. roumanicus from the Czech Republic where both occur in limited sympatry. We examined 109 hedgehogs from 21 localities within this secondary contact zone. Three species of ectoparasites and nine species of endoparasites were recorded. Significantly higher abundances and prevalences were found for Capillaria spp. and Brachylaemus erinacei in E. europaeus compared to E. roumanicus and higher mean infection rates and prevalences for Hymenolepis erinacei, Physaloptera clausa and Nephridiorhynchus major in E. roumanicus compared to E. europaeus. Divergence in the composition of the parasite fauna, except for Capillaria spp., which seem to be very unspecific, may be related to the complicated demography of their hosts connected with Pleistocene climate oscillations and consequent range dynamics. The fact that all parasite species with different abundances in E. europaeus and E. roumanicus belong to intestinal forms indicates a possible diversification of trophic niches between both sister hedgehog species.

Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing.

Anaplasma phagocytophilum is a Gram-negative obligate intracellular bacterium that replicates in neutrophils. It is transmitted via tick-bite and causes febrile disease in humans and animals. Human granulocytic anaplasmosis is regarded as an emerging infectious disease in North America, Europe and Asia. However, although increasingly detected, it is still rare in Europe. Clinically apparent A. phagocytophilum infections in animals are mainly found in horses, dogs, cats, sheep and cattle. Evidence from cross-infection experiments that A. phagocytophilum isolates of distinct host origin are not uniformly infectious for heterologous hosts has led to several approaches of molecular strain characterization. Unfortunately, the results of these studies are not always easily comparable, because different gene regions and fragment lengths were investigated. Multilocus sequence typing is a widely accepted method for molecular characterization of bacteria. We here provide for the first time a universal typing method that is easily transferable between different laboratories. We validated our approach on an unprecedented large data set of almost 400 A. phagocytophilum strains from humans and animals mostly from Europe. The typability was 74% (284/383). One major clonal complex containing 177 strains was detected. However, 54% (49/90) of the sequence types were not part of a clonal complex indicating that the population structure of A. phagocytophilum is probably semiclonal. All strains from humans, dogs and horses from Europe belonged to the same clonal complex. As canine and equine granulocytic anaplasmosis occurs frequently in Europe, human granulocytic anaplasmosis is likely to be underdiagnosed in Europe. Further, wild boars and hedgehogs may serve as reservoir hosts of the disease in humans and domestic animals in Europe, because their strains belonged to the same clonal complex. In contrast, as they were only distantly related, roe deer, voles and shrews are unlikely to harbor A. phagocytophilum strains infectious for humans, domestic or farm animals.

The ecology of tick-borne diseases.

Zoonotic diseases are major causes of infection related morbidity and mortality worldwide. Of the various arthropods capable of transmitting pathogens that cause such diseases to humans, ticks, which are vectors of more kinds of pathogens than any other group of invertebrate, have become an increasing focus of attention. This is particularly the case in the temperate northern hemisphere where they are a significant vector of human disease. Here, we provide an overview of the complex ecological systems defining the various epidemiological cycles of tick-borne diseases. We highlight the abiotic and biotic factors influencing the establishment and persistence of tick populations and their associated pathogens. Furthermore, we emphasize the dynamic nature of such systems, especially when they are under the influence of both small and large-scale anthropogenic changes to the environment. Although a great deal of work has been done on ticks and the diseases which they transmit, the very dynamism of the system means that new factors are continually arising which shift the epidemiological pattern within specific areas. We therefore consider that more detailed, long-term (i.e. at least 10 years), multidisciplinary studies need to be carried out to define why and how these pattern shifts take place and to determine their public health significance.

Population biology of establishment in New Zealand hedgehogs inferred from genetic and historical data: conflict or compromise?

The crucial steps in biological invasions, related to the shaping of genetic architecture and the current evolution of adaptations to a novel environment, usually occur in small populations during the phases of introduction and establishment. However, these processes are difficult to track in nature due to invasion lag, large geographic and temporal scales compared with human observation capabilities, the frequent depletion of genetic variance, admixture and other phenomena. In this study, we compared genetic and historical evidence related to the invasion of the West European hedgehog to New Zealand to infer details about the introduction and establishment. Historical information indicates that the species was initially established on the South Island. A molecular assay of populations from Great Britain and New Zealand using mitochondrial sequences and nuclear microsatellite loci was performed based on a set of analyses including approximate Bayesian computation, a powerful approach for disentangling complex population demographies. According to these analyses, the population of the North Island was most similar to that of the native area and showed greatest reduction in genetic variation caused by founder demography and/or drift. This evidence indicated the location of the establishment phase. The hypothesis was corroborated by data on climate and urbanization. We discuss the contrasting results obtained by the molecular and historical approaches in the light of their different explanatory power and the possible biases influencing the description of particular aspects of invasions, and we advocate the integration of the two types of approaches in invasion biology.

Detection of Rickettsia helvetica in ticks collected from European hedgehogs (Erinaceus europaeus, Linnaeus, 1758).

The role of wild mammals in the dissemination and maintenance of Rickettsia in nature is still under investigation. European hedgehogs (Erinaceus europaeus) are often heavily infested by tick and flea species that are known to harbor and transmit different Rickettsia spp. We investigated ixodid ticks sampled from European hedgehogs for the presence of Rickettsia. A total of 471 Ixodes ricinus and 755 I. hexagonus were collected from 26 German and 7 British European hedgehogs. These were tested by a genus-specific real-time PCR assay targeting the citrate synthase gene (gltA). The rickettsia minimum infection rate was 11.7% with an increase detected with each parasitic tick stage. No significant difference in Rickettsia prevalence in the 2 Ixodes species was detected. Using sequencing of partial ompB, Rickettsia helvetica was the only species identified. More than half of the hedgehogs carried Rickettsia-positive ticks. In addition, tissue samples from 2/5 hedgehogs (where tissue DNA was available) were PCR-positive. These results show that European hedgehogs are exposed to R. helvetica via infected ticks and might be involved in the natural transmission cycle of this Rickettsia species.

Occurrence of different Borrelia burgdorferi sensu lato genospecies including B. afzelii, B. bavariensis, and B. spielmanii in hedgehogs (Erinaceus spp.) in Europe.

In order to determine whether European hedgehogs (Erinaceus europaeus and E. roumanicus) play a role in the epidemiological cycle of Borrelia burgdorferi sensu lato in Central Europe and Great Britain, tissue samples of hedgehogs from Germany (n=211), Austria (n=4), the Czech Republic (n=22), and the U.K. (n=32) were tested for the presence of these tick-borne pathogens. PCR for amplification of the B. burgdorferi s.l.-specific 5S-23S intergenic spacer region as well as the outer surface protein A (ospA) gene were used. B. burgdorferi s.l. DNA was detected in 35 of the 259 E. europaeus and in 2 of 10 E. roumanicus. B. burgdorferi prevalences in E. europaeus ranged from 0% (U.K.) to 37.5% (Czech Republic), for E. roumanicus from 0% (Czech Republic) to 50.0% (Austria). Sequencing revealed the occurrence of 3 different B. burgdorferi genospecies in E. europaeus: B. afzelii was the dominant genospecies, followed by B. bavariensis (previously B. garinii OspA serotype 4) and B. spielmanii, the latter was detected for the first time in Hamburg (Germany). B. afzelii and B. bavariensis were also found in E. roumanicus. Our results suggest that hedgehogs modulate the epidemiology of certain species of the B. burgdorferi s.l. complex, potentially affecting the distribution and abundance of individual B. burgdorferi s.l. genospecies in various habitats. We hypothesise that juvenile or individuals with low immune competence in particular, have a high reservoir potential for the 3 genospecies identified here.

The European hedgehog (Erinaceus europaeus)--a suitable reservoir for variants of Anaplasma phagocytophilum?

The European hedgehog (Erinaceus europaeus) is a common insectivore in most parts of Europe and is frequently infested by the ticks Ixodes ricinus and I. hexagonus. I. ricinus ticks have been found infected with Anaplasma phagocytophilum, an obligate intracellular bacterium, but little is known about the potential of the hedgehog as a reservoir host. In this study, the infection with A. phagocytophilum and the genetic variants involved were investigated in a captive hedgehog population which was kept in a fenced, natural grass and bush garden habitat, and also in its ticks. Additionally hedgehogs from hedgehog caretaking stations were investigated. EDTA blood and ticks were collected from the captive hedgehog population once a month from March to October 2007 and in March and April 2008. All 3 developmental stages of I. ricinus and I. hexagonus occurred on the hedgehogs. After DNA extraction, the samples were screened for A. phagocytophilum with a real-time PCR, and selected samples were further investigated with a nested PCR targeting the partial 16S rRNA gene, followed by sequencing. One hundred thirty-six out of 220 hedgehog blood samples (61.8%) from altogether 48 individuals, 413 out of 563 I. ricinus samples and 90 out of 338 I. hexagonus samples were PCR-positive. Thirty-two hedgehogs were positive more than once, most frequently twice or 3 times, but also up to 9 times. Sequencing of the partial 16S rRNA gene resulted in 6 variants, but one variant ('A') was the most frequent which appeared in 93.8% of the positive hedgehogs. This variant (equaling Frankonia II, GenBank AF136712) has recently been reported from human, equine, and canine granulocytic anaplasmosis cases and thus, its specific association with hedgehogs is an important finding in the epidemiology of A. phagocytophilum in Europe. The high infection rate of both hedgehogs and ticks with A. phagocytophilum and the simultaneous infestation with 2 tick species of all developmental stages suggest that the hedgehog may be a suitable reservoir for at least some variants of A. phagocytophilum.

Necker cube: stimulus-related (low-level) and percept-related (high-level) EEG signatures early in occipital cortex.

During observation of an ambiguous Necker cube, our percept changes spontaneously although the external stimulus does not. An EEG paradigm allowing time-resolved EEG measurement during endogenous perceptual reversals recently revealed a chain of ERP correlates beginning with an early occipital positivity at around 130 ms (Reversal Positivity, "RP"). In order to better understand the functional role of this RP, we investigated its relation to the P100, which is spatiotemporally close, typically occurring 100 ms after onset of a visual stimulus at occipital electrodes. We compared the relation of the ERP amplitudes to varying sizes of ambiguous Necker cubes. The main results are: (1) The P100 amplitude increases monotonically with stimulus size but is independent of the participants' percept. (2) The RP, in contrast, is percept-related and largely unaffected by stimulus size. (3) A similar pattern to RP was found for reaction times: They depend on the percept but not on stimulus size. We speculate that the P100 reflects processing of elementary visual features, while the RP is related to a processing conflict during 3D interpretation that precedes a reversal. The present results indicate that low-level visual processing (related to stimulus size) and (relative) high-level processing (related to perceptual reversal) occur in close spatial and temporal vicinity.

Molecular detection of Anaplasma phagocytophilum in the European hedgehog (Erinaceus europaeus) and its ticks.

The European hedgehog (Erinaceus europaeus) is a common wild mammal in Central Europe that shares habitats with humans in urban, peri-urban, and rural areas. Thus, this species may play a role in human contact with zoonotic diseases. Here we report the presence of the pathogen Anaplasma phagocytophilum in hedgehogs and their ticks in Germany.

The avian acanthocephalan Plagiorhynchus cylindraceus (Palaeacanthocephala) parasitizing the European hedgehog (Erinaceus europaeus) in Europe and New Zealand.

The palaeacanthocephalan Plagiorhynchus cylindraceus is a common intestinal parasite of passerine birds, which can also occur parenterally or in the intestinal tract of mammals, often as an invading species in many countries worldwide. In this survey, introduced hedgehogs (Erinaceus europaeus, n = 183) killed in New Zealand during a biocontrol campaign and conspecifics (n = 174) that had died in hedgehog rehabilitation centers in Germany and Britain were examined for this parasite. In New Zealand, P. cylindraceus is recorded for the first time here, in the vicinity of Auckland. In Europe, prevalences ranged from 4.2% up to 47.6%, while in New Zealand, only 1.6% (Auckland 7.9%). Most of the worms occurred inside the peritoneal cavity where they had partly degenerated. Since hedgehogs are seldom preyed upon in continental Europe but often become traffic victims, we hypothesize that the worms inside them, whether extra- or intraperitoneally, contribute to the abundance and persistence of the parasite by being ingested by scavenging birds. Accordingly, we consider P. cylindraceus as a "modern parasite" taking advantage of two aspects of global change: anthropogenic promoted transmission (road kills) and the transcontinental spread of infected intermediate and/or final hosts caused by humans.