Ticking off the ungulate box : the role of different ungulate species in the transmission of tick-borne pathogens

Ungulates play a central role in the life cycle of Ixodes ricinus, an important vector of tick-borne pathogens, and several ungulate species are increasingly common across Europe. I investigated the role of these different species in the spread of I. ricinus-borne pathogens. Through a meta-analysis, I quantified the relative importance of ungulate species in the transmission of Anaplasma phagocytophilum. Furthermore, through field studies, I compared the contribution of each species to the number of ticks and the transmission of A. phagocytophilum and Borrelia burgdorferi sensu lato (s.l.) by quantifying tick burdens, relative ungulate densities, vegetation structure and (infected) questing tick density. My studies indicated that Ticking off the ungulate box – the role of different ungulate species in the transmission of tick-borne pathogens deer contributed more to the spread of tick-borne pathogens than wild boar (Sus scrofa), and fallow deer (Dama dama) more than the other deer species. I then modelled how changing an ungulate community composition affects the establishment of pathogens, expressed by the reproduction number R0. High density of fallow deer along with low density of roe deer (Capreolus capreolus) resulted in a higher R0 of the zoonotic A. phagocytophilum ecotype 1, and a lower R0 of the nonzoonotic ecotype 2. The effects of ungulates on the R0 of B. afzelii and B. garinii were negligible. My thesis thus suggests that different deer species likely vary in their effect on the circulation of various tick-borne pathogens. Ungulate management, as a tool to mitigate public and veterinary health risk, should therefore not approach ungulates as one homogenous group, but depending on the pathogen, take note of potentially different roles that ungulate species may play

The circulation of Anaplasma phagocytophilum ecotypes is associated with community composition of vertebrate hosts

Anaplasma phagocytophilum is a tick-borne pathogen that has been detected in many tick and vertebrate species. It is among the most widespread tick-borne pathogens in animals in Europe. The bacterium can be genetically divided into four ecotypes, which are linked to distinct but overlapping host species. However, knowledge about the transmission dynamics of the enzootic cycles of the different ecotypes is limited. Here, we quantified the link between the ecotypes of A. phagocytophilum, the different life stages of the tick Ixodes ricinus, and vertebrate host groups through a meta-analysis. We extracted data on the mean I. ricinus burden and the A. phagocytophilum infection prevalence in both hosts and feeding I. ricinus from 197 papers on 77 wildlife species. With this information, we modeled the relative importance of different host taxonomic groups for the circulation of the different ecotypes of A. phagocytophilum in a theoretical assemblage of hosts with varying presence of red deer (Cervus elaphus) and densities of small mammals. We showed that the composition of the vertebrate community affects the relative abundance of different ecotypes of A. phagocytophilum in the different life stages of I. ricinus. The presence of red deer is likely to increase the infection prevalence of Ecotype 1 in ticks, while small mammal densities drive the prevalence in ticks of mainly Ecotype 3, and to a lesser extent Ecotype 1. In Europe, vertebrate communities are changing, with an increase in red deer abundance and changes in the population dynamics of small mammals. Our results suggest that these changes could imply an increase in the circulation of A. phagocytophilum and thus an increase in the risk for public and veterinary health

Exploring the influence of host community composition on the outbreak potential of Anaplasma phagocytophilum and Borrelia burgdorferi s.l.

In large parts of the northern hemisphere, multiple deer species coexist, and management actions can strongly influence wild deer communities. Such changes may also indirectly influence other species in the community, such as small mammals and birds, because deer can have strong effects on their habitats and resources. Deer, small mammals and birds play an important role in the dynamics of tick-borne zoonotic diseases. It is, however, relatively underexplored how the abundance and composition of vertebrate communities may affect the outbreak potential, maintenance and circulation of tick-borne pathogens. In this study we focus on the outbreak potential by exploring how the basic reproduction number R0 for different tick-borne pathogens depends on host community composition. We used published data on co-varying roe deer (Capreolus capreolus) and fallow deer (Dama dama) densities following a hunting ban, and different small mammal and bird densities, to investigate how the change in host community influences the R0 of four tick-borne pathogens: one non-zoonotic, namely Anaplasma phagocytophilum ecotype 2, and three zoonotic, namely A. phagocytophilum ecotype 1, Borrelia afzelii and Borrelia garinii. We calculated R0 using a next generation matrix approach, and used elasticities to quantify the contributions to R0 of the different groups of host species. The value of R0 for A. phagocytophilum ecotype 1 was higher with high fallow deer density and low roe deer density, while it was the other way round for A. phagocytophilum ecotype 2. For B. afzelii, R0 was mostly related to the density of small mammals and for B. garinii it was mostly determined by bird density. Our results show that the effect of species composition is substantial in the outbreak potential of tick-borne pathogens. This implies that also management actions that change this composition, can (indirectly and unintentionally) affect the outbreak potential of tick-borne diseases

The circulation of Anaplasma phagocytophilum ecotypes is associated with community composition of vertebrate hosts

Anaplasma phagocytophilum is a tick-borne pathogen that has been detected in many tick and vertebrate species. It is among the most widespread tick-borne pathogens in animals in Europe. The bacterium can be genetically divided into four ecotypes, which are linked to distinct but overlapping host species. However, knowledge about the transmission dynamics of the enzootic cycles of the different ecotypes is limited. Here, we quantified the link between the ecotypes of A. phagocytophilum, the different life stages of the tick Ixodes ricinus, and vertebrate host groups through a meta-analysis. We extracted data on the mean I. ricinus burden and the A. phagocytophilum infection prevalence in both hosts and feeding I. ricinus from 197 papers on 77 wildlife species. With this information, we modeled the relative importance of different host taxonomic groups for the circulation of the different ecotypes of A. phagocytophilum in a theoretical assemblage of hosts with varying presence of red deer (Cervus elaphus) and densities of small mammals. We showed that the composition of the vertebrate community affects the relative abundance of different ecotypes of A. phagocytophilum in the different life stages of I. ricinus. The presence of red deer is likely to increase the infection prevalence of Ecotype 1 in ticks, while small mammal densities drive the prevalence in ticks of mainly Ecotype 3, and to a lesser extent Ecotype 1. In Europe, vertebrate communities are changing, with an increase in red deer abundance and changes in the population dynamics of small mammals. Our results suggest that these changes could imply an increase in the circulation of A. phagocytophilum and thus an increase in the risk for public and veterinary health

The Genetic Diversity of Rickettsiella Symbionts in Ixodes ricinus Throughout Europe

Rickettsiella species are bacterial symbionts that are present in a great variety of arthropod species, including ixodid ticks. However, little is known about their genetic diversity and distribution in Ixodes ricinus, as well as their relationship with other tick-associated bacteria. In this study, we investigated the occurrence and the genetic diversity of Rickettsiella spp. in I. ricinus throughout Europe and evaluated any preferential and antagonistic associations with Candidatus Midichloria mitochondrii and the pathogens Borrelia burgdorferi sensu lato and Borrelia miyamotoi. Rickettsiella spp. were detected in most I. ricinus populations investigated, encompassing a wide array of climate types and environments. The infection prevalence significantly differed between geographic locations and was significantly higher in adults than in immature life stages. Phylogenetic investigations and protein characterization disclosed four Rickettsiella clades (I-IV). Close phylogenetic relations were observed between Rickettsiella strains of I. ricinus and other arthropod species. Isolation patterns were detected for Clades II and IV, which were restricted to specific geographic areas. Lastly, although coinfections occurred, we did not detect significant associations between Rickettsiella spp. and the other tick-associated bacteria investigated. Our results suggest that Rickettsiella spp. are a genetically and biologically diverse facultative symbiont of I. ricinus and that their distribution among tick populations could be influenced by environmental components

Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens

Background Several ungulate species are feeding and propagation hosts for the tick Ixodes ricinus as well as hosts to a wide range of zoonotic pathogens. Here, we focus on Anaplasma phagocytophilum and Borrelia burgdorferi (s.l.), two important pathogens for which ungulates are amplifying and dilution hosts, respectively. Ungulate management is one of the main tools to mitigate human health risks associated with these tick-borne pathogens. Across Europe, different species of ungulates are expanding their ranges and increasing in numbers. It is currently unclear if and how the relative contribution to the life-cycle of I. ricinus and the transmission cycles of tick-borne pathogens differ among these species. In this study, we aimed to identify these relative contributions for five European ungulate species. Methods We quantified the tick load and collected ticks and spleen samples from hunted fallow deer (Dama dama, n = 131), moose (Alces alces, n = 15), red deer (Cervus elaphus, n = 61), roe deer (Capreolus capreolus, n = 30) and wild boar (Sus scrofa, n = 87) in south-central Sweden. We investigated the presence of tick-borne pathogens in ticks and spleen samples using real-time PCR. We determined if ungulate species differed in tick load (prevalence and intensity) and in infection prevalence in their tissue as well as in the ticks feeding on them. Results Wild boar hosted fewer adult female ticks than any of the deer species, indicating that deer are more important as propagation hosts. Among the deer species, moose had the lowest number of female ticks, while there was no difference among the other deer species. Given the low number of infected nymphs, the relative contribution of all ungulate species to the transmission of B. burgdorferi (s.l.) was low. Fallow deer, red deer and roe deer contributed more to the transmission of A. phagocytophilum than wild boar. Conclusions The ungulate species clearly differed in their role as a propagation host and in the transmission of B. burgdorferi and A. phagocytophilum. This study provides crucial information for ungulate management as a tool to mitigate zoonotic disease risk and argues for adapting management approaches to the local ungulate species composition and the pathogen(s) of concern. Graphic abstrac

Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens

Background: Several ungulate species are feeding and propagation hosts for the tick Ixodes ricinus as well as hosts to a wide range of zoonotic pathogens. Here, we focus on Anaplasma phagocytophilum and Borrelia burgdorferi (s.l.), two important pathogens for which ungulates are amplifying and dilution hosts, respectively. Ungulate management is one of the main tools to mitigate human health risks associated with these tick-borne pathogens. Across Europe, different species of ungulates are expanding their ranges and increasing in numbers. It is currently unclear if and how the relative contribution to the life-cycle of I. ricinus and the transmission cycles of tick-borne pathogens differ among these species. In this study, we aimed to identify these relative contributions for five European ungulate species. Methods: We quantified the tick load and collected ticks and spleen samples from hunted fallow deer (Dama dama, n = 131), moose (Alces alces, n = 15), red deer (Cervus elaphus, n = 61), roe deer (Capreolus capreolus, n = 30) and wild boar (Sus scrofa, n = 87) in south-central Sweden. We investigated the presence of tick-borne pathogens in ticks and spleen samples using real-time PCR. We determined if ungulate species differed in tick load (prevalence and intensity) and in infection prevalence in their tissue as well as in the ticks feeding on them. Results: Wild boar hosted fewer adult female ticks than any of the deer species, indicating that deer are more important as propagation hosts. Among the deer species, moose had the lowest number of female ticks, while there was no difference among the other deer species. Given the low number of infected nymphs, the relative contribution of all ungulate species to the transmission of B. burgdorferi (s.l.) was low. Fallow deer, red deer and roe deer contributed more to the transmission of A. phagocytophilum than wild boar. Conclusions: The ungulate species clearly differed in their role as a propagation host and in the transmission of B. burgdorferi and A. phagocytophilum. This study provides crucial information for ungulate management as a tool to mitigate zoonotic disease risk and argues for adapting management approaches to the local ungulate species composition and the pathogen(s) of concern. Graphic abstract: [Figure not available: see fulltext.]

The circulation of Anaplasma phagocytophilum ecotypes is associated with community composition of vertebrate hosts

Anaplasma phagocytophilum is a tick-borne pathogen that has been detected in many tick and vertebrate species. It is among the most widespread tick-borne pathogens in animals in Europe. The bacterium can be genetically divided into four ecotypes, which are linked to distinct but overlapping host species. However, knowledge about the transmission dynamics of the enzootic cycles of the different ecotypes is limited. Here, we quantified the link between the ecotypes of A. phagocytophilum, the different life stages of the tick Ixodes ricinus, and vertebrate host groups through a meta-analysis. We extracted data on the mean I. ricinus burden and the A. phagocytophilum infection prevalence in both hosts and feeding I. ricinus from 197 papers on 77 wildlife species. With this information, we modeled the relative importance of different host taxonomic groups for the circulation of the different ecotypes of A. phagocytophilum in a theoretical assemblage of hosts with varying presence of red deer (Cervus elaphus) and densities of small mammals. We showed that the composition of the vertebrate community affects the relative abundance of different ecotypes of A. phagocytophilum in the different life stages of I. ricinus. The presence of red deer is likely to increase the infection prevalence of Ecotype 1 in ticks, while small mammal densities drive the prevalence in ticks of mainly Ecotype 3, and to a lesser extent Ecotype 1. In Europe, vertebrate communities are changing, with an increase in red deer abundance and changes in the population dynamics of small mammals. Our results suggest that these changes could imply an increase in the circulation of A. phagocytophilum and thus an increase in the risk for public and veterinary health

The Genetic Diversity of Rickettsiella Symbionts in Ixodes ricinus Throughout Europe

Rickettsiella species are bacterial symbionts that are present in a great variety of arthropod species, including ixodid ticks. However, little is known about their genetic diversity and distribution in Ixodes ricinus, as well as their relationship with other tick-associated bacteria. In this study, we investigated the occurrence and the genetic diversity of Rickettsiella spp. in I. ricinus throughout Europe and evaluated any preferential and antagonistic associations with Candidatus Midichloria mitochondrii and the pathogens Borrelia burgdorferi sensu lato and Borrelia miyamotoi. Rickettsiella spp. were detected in most I. ricinus populations investigated, encompassing a wide array of climate types and environments. The infection prevalence significantly differed between geographic locations and was significantly higher in adults than in immature life stages. Phylogenetic investigations and protein characterization disclosed four Rickettsiella clades (I–IV). Close phylogenetic relations were observed between Rickettsiella strains of I. ricinus and other arthropod species. Isolation patterns were detected for Clades II and IV, which were restricted to specific geographic areas. Lastly, although coinfections occurred, we did not detect significant associations between Rickettsiella spp. and the other tick-associated bacteria investigated. Our results suggest that Rickettsiella spp. are a genetically and biologically diverse facultative symbiont of I. ricinus and that their distribution among tick populations could be influenced by environmental components

Exploring the influence of host community composition on the outbreak potential of Anaplasma phagocytophilum and Borrelia burgdorferi s.l.

In large parts of the northern hemisphere, multiple deer species coexist, and management actions can strongly influence wild deer communities. Such changes may also indirectly influence other species in the community, such as small mammals and birds, because deer can have strong effects on their habitats and resources. Deer, small mammals and birds play an important role in the dynamics of tick-borne zoonotic diseases. It is, however, relatively underexplored how the abundance and composition of vertebrate communities may affect the outbreak potential, maintenance and circulation of tick-borne pathogens. In this study we focus on the outbreak potential by exploring how the basic reproduction number R0 for different tick-borne pathogens depends on host community composition. We used published data on co-varying roe deer (Capreolus capreolus) and fallow deer (Dama dama) densities following a hunting ban, and different small mammal and bird densities, to investigate how the change in host community influences the R0 of four tick-borne pathogens: one non-zoonotic, namely Anaplasma phagocytophilum ecotype 2, and three zoonotic, namely A. phagocytophilum ecotype 1, Borrelia afzelii and Borrelia garinii. We calculated R0 using a next generation matrix approach, and used elasticities to quantify the contributions to R0 of the different groups of host species. The value of R0 for A. phagocytophilum ecotype 1 was higher with high fallow deer density and low roe deer density, while it was the other way round for A. phagocytophilum ecotype 2. For B. afzelii, R0 was mostly related to the density of small mammals and for B. garinii it was mostly determined by bird density. Our results show that the effect of species composition is substantial in the outbreak potential of tick-borne pathogens. This implies that also management actions that change this composition, can (indirectly and unintentionally) affect the outbreak potential of tick-borne diseases