Melting pot of tick-borne zoonoses : the European hedgehog contributes to the maintenance of various tick-borne diseases in natural cycles urban and suburban areas

Background: European hedgehogs (Erinaceus europaeus) are urban dwellers and host both Ixodes ricinus and Ixodes hexagonus. These ticks transmit several zoonotic pathogens like Borrelia burgdorferi (sensu lato), Anaplasma phagocytophilum, Rickettsia helvetica, Borrelia miyamotoi and " Candidatus Neoehrlichia mikurensis". It is unclear to what extent hedgehogs in (sub) urban areas contribute to the presence of infected ticks in these areas, which subsequently pose a risk for acquiring a tick-borne disease. Therefore, it is important to investigate to what extent hedgehogs contribute to the enzootic cycle of these tick-borne pathogens, and to shed more light at the mechanisms of the transmission cycles involving hedgehogs and both ixodid tick species. Methods: Engorged ticks from hedgehogs were collected from (sub) urban areas via rehabilitating centres in Belgium. Ticks were screened individually for presence of Borrelia burgdorferi (sensu lato), Borrelia miyamotoi, Anaplasma phagocytophilum, Rickettsia helvetica and " Candidatus Neoehrlichia mikurensis" using PCR-based methods. Infection rates of the different pathogens in ticks were calculated and compared to infection rates in questing ticks. Results: Both Ixodes hexagonus (n = 1132) and Ixodes ricinus (n = 73) of all life stages were found on the 54 investigated hedgehogs. Only a few hedgehogs carried most of the ticks, with 6 of the 54 hedgehogs carrying more than half of all ticks (624/ 1205). Borrelia miyamotoi, A. phagocytophilum, R. helvetica and B. burgdorferi genospecies (Borrelia afzelii, Borrelia bavariensis and Borrelia spielmanii) were detected in both I. hexagonus and I. ricinus. Anaplasma phagocytophilum, R. helvetica, B. afzelii, B. bavariensis and B. spielmanii were found significantly more in engorged ticks in comparison to questing I. ricinus. Conclusions: European hedgehogs seem to contribute to the spread and transmission of tick-borne pathogens in urban areas. The relatively high prevalence of B. bavariensis, B. spielmanii, B. afzelii, A. phagocytophilum and R. helvetica in engorged ticks suggests that hedgehogs contribute to their enzootic cycles in (sub) urban areas. The extent to which hedgehogs can independently maintain these agents in natural cycles, and the role of other hosts (rodents and birds) remain to be investigated

Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments

Background: The tick Ixodes ricinus has considerable impact on the health of humans and other terrestrial animals because it transmits several tick-borne pathogens (TBPs) such as B. burgdorferi (sensu lato), which causes Lyme borreliosis (LB). Small forest patches of agricultural landscapes provide many ecosystem services and also the disservice of LB risk. Biotic interactions and environmental filtering shape tick host communities distinctively between specific regions of Europe, which makes evaluating the dilution effect hypothesis and its influence across various scales challenging. Latitude, macroclimate, landscape and habitat properties drive both hosts and ticks and are comparable metrics across Europe. Therefore, we instead assess these environmental drivers as indicators and determine their respective roles for the prevalence of B. burgdorferi in I. ricinus. Methods: We sampled I. ricinus and measured environmental properties of macroclimate, landscape and habitat quality of forest patches in agricultural landscapes along a European macroclimatic gradient. We used linear mixed models to determine significant drivers and their relative importance for nymphal and adult B. burgdorferi prevalence. We suggest a new prevalence index, which is pool-size independent. Results: During summer months, our prevalence index varied between 0 and 0.4 per forest patch, indicating a low to moderate disservice. Habitat properties exerted a fourfold larger influence on B. burgdorferi prevalence than macroclimate and landscape properties combined. Increasingly available ecotone habitat of focal forest patches diluted and edge density at landscape scale amplified B. burgdorferi prevalence. Indicators of habitat attractiveness for tick hosts (food resources and shelter) were the most important predictors within habitat patches. More diverse and abundant macro- and microhabitat had a diluting effect, as it presumably diversifies the niches for tick-hosts and decreases the probability of contact between ticks and their hosts and hence the transmission likelihood.[br/] Conclusions: Diluting effects of more diverse habitat patches would pose another reason to maintain or restore high biodiversity in forest patches of rural landscapes. We suggest classifying habitat patches by their regulating services as dilution and amplification habitat, which predominantly either decrease or increase B. burgdorferi prevalence at local and landscape scale and hence LB risk. Particular emphasis on promoting LB-diluting properties should be put on the management of those habitats that are frequently used by humans. In the light of these findings, climate change may be of little concern for LB risk at local scales, but this should be evaluated further

Molecular detection of tick-borne pathogens Borrelia afzelii, Borrelia miyamotoi and Anaplasma phagocytophilum in Eurasian red squirrels (Sciurus vulgaris)

Eurasian red squirrels (Sciurus vulgaris) are common hosts of ixodid ticks and could thus carry tick-borne disease agents. The relative contribution of the red squirrel, a medium-sized rodent species, to the transmission dynamics of tick-borne pathogens in Europe yet remains unclear. We analysed spleen and liver samples from 45 dead squirrels collected in Flanders, Belgium, during tick activity season and detected the presence of Borrelia burgdorferi s.l. in the spleen of two squirrels (4.4%). One of the sequences could be identified as Borrelia afzelii. Borrelia miyamotoi was detected in the spleen of three squirrels (6.7%) and Anaplasma phagocytophilum in four spleen samples (8.9%). Both A. phagocytophilum ecotype I and II were found. We could not detect the presence of "Candidatus Neoehrlichia mikurensis" or tick-borne encephalitis virus in any of the squirrels. Our results suggest that Eurasian red squirrels can host B. afzelii, as already proposed by previous studies, but we could not confirm the previous established association between squirrels and B. burgdorferi sensu stricto. Our results demonstrate the epidemiological importance of the red squirrel, particularly in (sub) urban areas, since they can harbour a similar community of tick-borne pathogens as do mice and voles and can act as hosts for A. phagocytophilum ecotype I, which has important implications for human health risk

‘Animals under wheels’: Wildlife roadkill data collection by citizen scientists as a part of their nature recording activities

‘Animals under wheels’ is a citizen science driven project that has collected almost 90,000 roadkill records from Flanders, Belgium, mainly between 2008 and 2020. However, until now, the platform and results have never been presented comprehensively to the scientific community and we highlight strengths and challenges of this system. Data collection occurred using the subsite www.dierenonderdewielen.be (‘animals under wheels’) or the multi-purpose biodiversity platform observation.org and the apps, allowing the registration of roadkill and living organisms alike. We recorded 4,314 citizen scientists who contributed with at least a single roadkill record (207-1,314 active users per year). Non-roadkill records were registered by 85% of these users and the median time between registration of the first and last record was over 6 years, indicating a very high volunteer retention. Based on photographs presented with the roadkill records (n = 7,687), volunteer users correctly identified 98.2% of the species. Vertebrates represent 99% of all roadkill records. Over 145,000 km of transects were monitored, resulting in 1,726 mammal and 2,041 bird victims. Carcass encounter rates and composition of the top 10 detected species list was dependent on monitoring speed. Roadkill data collected during transects only represented 6% of all roadkill data available in the dataset. The remaining 60,478 bird and mammal roadkill records were opportunistically collected. The top species list, based on the opportunistically collected roadkill data, is clearly biased towards larger, enigmatic species. Although indirect evidence showed an increase in search effort for roadkill from 2010-2020, the number of roadkill records did not increase, indicating that roadkills are diminishing. Mitigation measures preventing roadkill could have had an effect on this, but decrease in population densities was likely to (partially) influence this result. As a case study, the mammal roadkill data were explored. We used linear regressions for the 17 most registered mammal species, determining per species if the relative proportion per year changed significantly between 2010 and 2020 (1 significant decrease, 7 significant increases). We investigated the seasonal patterns in roadkill for the 17 mammal species, and patterns per species were consistent over the years, although restrictions on human movement, due to COVID-19, influenced the seasonal pattern for some species in 2020. In conclusion, citizen scientists are a very valuable asset in investigating wildlife roadkill. While we present the results from Flanders, the platform and apps are freely available for projects anywhere in the world

Over teken, gastheren en het 'verdunningseffect': hoe bosomvorming het risico op de ziekte van Lyme kan veranderen

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Diversifying forest communities may change Lyme disease risk : extra dimension to the dilution effect in Europe

Lyme disease is caused by bacteria of the Borrelia burgdorferi genospecies complex and transmitted by Ixodid ticks. In North America only one pathogenic genospecies occurs, in Europe there are several. According to the dilution effect hypothesis (DEH), formulated in North America, nymphal infection prevalence (NIP) decreases with increasing host diversity since host species differ in transmission potential. We analysed Borrelia infection in nymphs from 94 forest stands in Belgium, which are part of a diversification gradient with a supposedly related increasing host diversity: from pine stands without to oak stands with a shrub layer. We expected changing tree species and forest structure to increase host diversity and decrease NIP. In contrast with the DEH, NIP did not differ between different forest types. Genospecies diversity however, and presumably also host diversity, was higher in oak than in pine stands. Infected nymphs tended to harbour Borrelia afzelii infection more often in pine stands while Borrelia garinii and Borrelia burgdorferi ss. infection appeared to be more prevalent in oak stands. This has important health consequences, since the latter two cause more severe disease manifestations. We show that the DEH must be nuanced for Europe and should consider the response of multiple pathogenic genospecies

Additional file 3: of Melting pot of tick-borne zoonoses: the European hedgehog contributes to the maintenance of various tick-borne diseases in natural cycles urban and suburban areas

The number of Ixodes ricinus and Ixodes hexagonus ticks infected with a certain pathogen, for all life stages together or for larvae (L), nymphs (N) or adults (A) separately. (CSV 719 bytes