Role of mustelids in the life-cycle of ixodid ticks and transmission cycles of four tick-borne pathogens

Abstract

BackgroundElucidating which wildlife species significantly contribute to the maintenance of Ixodes ricinus populations and the enzootic cycles of the pathogens they transmit is imperative in understanding the driving forces behind the emergence of tick-borne diseases. Here, we aimed to quantify the relative contribution of four mustelid species in the life-cycles of I. ricinus and Borrelia burgdorferi (sensu lato) in forested areas and to investigate their role in the transmission of other tick-borne pathogens. Road-killed badgers, pine martens, stone martens and polecats were collected in Belgium and the Netherlands. Their organs and feeding ticks were tested for the presence of tick-borne pathogens.ResultsIxodes hexagonus and I. ricinus were found on half of the screened animals (n = 637). Pine martens had the highest I. ricinus burden, whereas polecats had the highest I. hexagonus burden. We detected DNA from B. burgdorferi (s.l.) and Anaplasma phagocytophilum in organs of all four mustelid species (n = 789), and Neoehrlichia mikurensis DNA was detected in all species, except badgers. DNA from B. miyamotoi was not detected in any of the investigated mustelids. From the 15 larvae of I. ricinus feeding on pine martens (n = 44), only one was positive for B. miyamotoi DNA, and all tested negative for B. burgdorferi (s.l.), N. mikurensis and A. phagocytophilum. The two feeding larvae from the investigated polecats (n = 364) and stone martens (n = 39) were negative for all four pathogens. The infection rate of N. mikurensis was higher in feeding nymphs collected from mustelids compared to questing nymphs, but not for B. burgdorferi (s.l.), B. miyamotoi or A. phagocytophilum.ConclusionsAlthough all stages of I. ricinus can be found on badgers, polecats, pine and stone martens, their relative contribution to the life-cycle of I. ricinus in forested areas is less than 1%. Consequently, the relative contribution of mustelids to the enzootic cycles of I. ricinus-borne pathogens is negligible, despite the presence of these pathogens in organs and feeding ticks. Interestingly, all four mustelid species carried all stages of I. hexagonus, potentially maintaining enzootic cycles of this tick species apart from the cycle involving hedgehogs as main host species.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-3126-8) contains supplementary material, which is available to authorized users.

Molecular Survey on Vector-Borne Pathogens in Alpine Wild Carnivorans

“…No badgers showed positivity for A. phagocytophilum in The Netherland (68), Czech Republic 71, and Spain (72), where negative results have been obtained also for the wolf (37). Notably, out of 114 badgers only two were found positive during a study on the occurrence of VBPs in mustelids from Belgium and The Netherland (73). The prevalence of A. phagocytophilum obtained in the present study is in line with that reported previously, showing low occurrence of this bacterium in badger and maybe suggesting the poor role of this mustelid species in the epidemiology of Anaplasmataceae.…”

Molecular detection of Anaplasma phagocytophilum in wild carnivores in north-eastern Poland

“…According to the present findings, 18.70% of the tested badgers in north-eastern Poland displayed A . phagocytophilum infection; however, Garcia-Pérez et al [24] reported a prevalence of 1.50% among badgers in Spain, and Hofmeester et al [23] found it to be 1.80% in the Netherlands. While Anaplasma infection was found in two of the four tested European polecats in the present study, previous studies have found the prevalence to be 4.30% in Germany and 4.90% in the Netherlands [22, 23].…”

“…phagocytophilum infection; however, Garcia-Pérez et al [24] reported a prevalence of 1.50% among badgers in Spain, and Hofmeester et al [23] found it to be 1.80% in the Netherlands. While Anaplasma infection was found in two of the four tested European polecats in the present study, previous studies have found the prevalence to be 4.30% in Germany and 4.90% in the Netherlands [22, 23]. Similarly, A. phagocytophilum was found to be more common in pine martens ( Martes martes ) in the present study (41.70%) than in Belgium (22.00%) [23].…”

“…Knowledge about A. phagocytophilum infection in badgers, polecats and martens is still limited. It has been detected in European polecats ( Mustela putorius ) in Germany [22] and in the Netherlands [23], as well as in badgers ( Meles meles ) in the Netherlands and Spain [23, 24]. It has also been identified among pine martens ( Martes martes ) in Belgium.…”

Can Protected Areas Mitigate Lyme Disease Risk in Fennoscandia?

“…The role of top- and mesocarnivores as secondary tick hosts is probably negligible in Europe (Hofmeester et al 2018).…”