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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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Record number 510087
Title The wild life of tick-borne pathogens
Author(s) Hofmeester, Tim R.
Source University. Promotor(en): Herbert Prins, co-promotor(en): Sip van Wieren. - Wageningen : Wageningen University - ISBN 9789462579699 - 224
Department(s) Laboratory of Entomology
PE&RC
Publication type Dissertation, internally prepared
Publication year 2016
Keyword(s) ixodes ricinus - metastigmata - life cycle - tickborne diseases - disease vectors - mammals - birds - hosts - population ecology - tick infestations - host parasite relationships - levenscyclus - ziekten overgebracht door teken - vectoren, ziekten - zoogdieren - vogels - gastheren (dieren, mensen, planten) - populatie-ecologie - tekenbesmettingen - gastheer parasiet relaties
Categories Population Ecology / Arachnida / Medical Entomology
Abstract

Diseases that are transmitted by arthropod vectors from animal hosts to humans – so called zoonotic vector-borne diseases – have increased in incidence in the last decades. In North America and Europe, tick-borne pathogens cause the majority of vector-borne diseases, including Lyme borreliosis and tick-borne encephalitis. The pathogens causing these diseases are transmitted by tick species within the Ixodes ricinus complex. These are generalist ticks that have a multi-year lifecycle with three active stages, larva, nymph and adult. Each stage passively waits for a vertebrate host by questing in the vegetation. Once a host is encountered these ticks feed on the host for several days sucking blood, after which they detach and moult to the next stage or lay eggs. Although these ticks spend the majority of their life in the vegetation, the availability of hosts is an important determinant of tick densities.

In Europe, the Sheep tick (Ixodes ricinus) is the most important vector for tick-borne pathogens. These pathogens include Borrelia burgdorferi sensu lato (s.l.), the causative agent of Lyme borreliosis, Anaplasma phagocytophilum, the causative agent of human granulocytic anaplasmosis, Borrelia miyamotoi, the causative agent of acute febrile illness and Candidatus Neoehrlichia mikurensis, the causative agent of neoehrlichiosis. There are several genospecies within the B. burgdorferi s.l. complex, among which B. afzelii, B. bavariensis, B. garinii, B. lusitaniae, B. spielmanii, and B. valaisiana are found in questing ticks and patients in the Netherlands. All of these pathogens are maintained and amplified by vertebrate hosts. Host species differ in their ability to transmit the different pathogens (reservoir competence), as well as in their competence for ticks. Therefore, it has been hypothesized that changes in vertebrate assemblage composition can change tick-borne pathogen dynamics and thereby tick-borne disease risk, where a decrease in host species diversity might lead to an increased disease risk, the so-called dilution effect of host species richness hypothesis.

In his thesis, Tim Hofmeester describes his research on the role of different vertebrate host species in maintaining I. ricinus populations and in infecting I. ricinus larvae with different tick-borne pathogens. By performing a systematic review, Hofmeester found that for both mammals and birds, there was a positive correlation between host body mass and tick burden for the different stages. Nymphal burden was positively correlated with infection prevalence with B. burgdorferi s.l. in hosts, which was again positively correlated with the average number of larvae that got infected with B. burgdorferi s.l. while feeding on a host. He also showed that the majority of I. ricinus individuals of the three stages (larva, nymph and adult) feed on only a few vertebrate host species (rodents, thrushes and deer, respectively). Using camera traps, Hofmeester showed that the presence of deer, such as Roe deer and Red deer, was a more important determinant of I. ricinus density than the number of deer available to ticks in twenty forested areas in the Netherlands. Ixodes ricinus densities were significantly reduced after two years of excluding deer by fencing four 0.75 ha forest plots in a forest near Apeldoorn, the Netherlands. Therefore, tick-borne disease risk can be reduced by placing fences around small forested areas with a high recreational pressure.

Hofmeester showed that tick burdens on rodents were higher in areas with large numbers of deer, while they were lower in areas with large numbers of carnivores. These differences in tick burden on rodents between areas were strongly correlated to the number of questing nymphs in the vegetation that were infected with tick-borne pathogens that are transmitted by rodents. This implies that changes in vertebrate assemblage can lead to cascading effects on rodent-transmitted tick-borne disease risk, via larval burden on rodents. Furthermore, Hofmeester found that the percentage of ticks infected with a specific pathogen was correlated to the number of animals in an area that could transmit this pathogen, while this percentage decreased with the number of animals that could not transmit this pathogen. These parameters were, however, not correlated to species richness, something that was expected based on the dilution effect of species richness hypothesis. Therefore, there is no support for a dilution effect of species richness on tick-borne pathogens in the Netherlands.

In his synthesis, Hofmeester presents a mathematical model in which the importance of spatial behaviour of hosts for tick-borne pathogens is shown and he proclaims the need for the integration of the field of behavioural ecology into disease ecology to better understand the effect of changes in vertebrate assemblages on pathogen prevalence and ultimately, disease risk. The data presented in this thesis show that it is not host diversity but the presence, abundance and behaviour of specific host species that drives tick-borne pathogen dynamics (identity effect). Vertebrate species change their behaviour in the presence or absence of predators and competitors. Hofmeester shows that this, theoretically, can have a major influence on the density of infected nymphs in the vegetation. Therefore, behavioural changes of reservoir-competent hosts should be taken into account when modelling the effect of changes in vertebrate assemblage composition on tick-borne disease risk.

The behaviour of vertebrate species in Europe is changing, as multiple species have adapted to human-dominated and fragmented landscapes. The adaptation of small mammals, thrushes and deer to fragmented landscapes might be one of the driving factors behind the increase in tick-borne disease incidence in Europe. A further adaptation of important host species to urbanized landscapes might be expected as these are the safest areas for vertebrate species trying to avoid predation. This might result in an increase in population density of reservoir-competent host species in urban areas with a corresponding increase in tick-borne pathogen prevalence and therefore, tick-borne disease risk.

Concluding, our world is changing and as a consequence vertebrate assemblages are also changing. This may lead to changes in I. ricinus density and infection prevalence with tick-borne pathogens. From the studies presented in his thesis Hofmeester concludes that the abundance and behaviour of several host species (e.g., Bank vole, Blackbird, Red deer, Red fox, Roe deer, and Wood mouse) determines tick-borne disease risk. Therefore, studying the drivers of animal abundance and behaviour related to ticks and pathogens will be the next step in better understanding and describing tick-borne disease risk. The ecology of tick-borne pathogens is very complex and targeting vertebrate hosts for intervention strategies will be both inefficient and costly due to the intricate interplay between multiple vertebrate host species. Therefore, Hofmeester concludes that prevention of tick bites is the best way to reduce tick-borne disease incidence.

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