The role of small rodents and shrews as hosts for ticks and reservoirs of tick-borne pathogens in a northern coastal forest ecosystem.

Abstract

Ticks are important vectors for a variety of pathogens of medical and veterinary importance worldwide. Small rodents and shrews are widely distributed, and can harbour several species of ticks and substantial tick burdens. In addition they are considered important competent reservoirs for some of the most adverse tick-borne pathogens, Borrelia burgdorferi sensu lato causing Lyme disease and Anaplasma phagocytophilum causing tick-borne fever in livestock. Despite its importance, current knowledge about the small mammal-tick association from ecosystems at the northern distribution limit of ticks is scarce. In the current study I investigated the role of rodents and shrews as hosts for ticks and reservoir for tick-borne pathogens in a northern coastal forest ecosystem. I predicted that rodents and shrews would host immature life stages of I. ricinus, while they would host all life stages of the rodent specialist, I. trianguliceps. I also predicted that variation in tick burdens would be affected by extrinsic and intrinsic factors. In addition I predicted that rodents and shrews would be detected with B. burgdorferi s.l. and A. phagocytophilum. Questing ticks were sampled, and small rodents and shrews were trapped in two transects in Sogn & Fjordane, Norway, in spring and fall of 2013 and 2014. Tick burdens of different small mammal species were quantified and infestation by pathogens was determined. Distribution of questing I. ricinus ticks and I. ricinus and I. trianguliceps tick burdens were investigated using generalised linear mixed effect models. Rodents and shrews showed relatively high prevalence of tick infestation and some individuals carried high abundance of larvae of both I. ricinus and I. trianguliceps ticks. Both B. burgdorferi s.l. and A. phagocytophilum were detected in small mammal species. There was evidence that tick burdens were affected by extrinsic factors likely linked to local climate. Intrinsic factors were also found to affect tick burdens. Larva and nymph tick burdens were positively correlated with host body size. After controlling for body size, the residual variation in tick burdens for I. ricinus larvae and I. trianguliceps nymphs were attributed to unmeasured qualities of rodent and shrew species. The present study highlights the role of rodents and shrews as important hosts for immature stages of ticks, especially larvae. In addition this study suggests that tick burdens on rodents and shrews are affected by a complex combination of local climate and host factors, making some individuals more likely to contribute to the life cycle of ticks and the enzootic transmission cycle. To better understand tick-borne diseases in relation to climate change, the current study suggests that one must put more emphasis on intrinsic factors, since these may have major impact on the small mammals contribution to the enzootic transmission cycle.

Ticks are important vectors for a variety of pathogens of medical and veterinary importance worldwide. Small rodents and shrews are widely distributed, and can harbour several species of ticks and substantial tick burdens. In addition they are considered important competent reservoirs for some of the most adverse tick-borne pathogens, Borrelia burgdorferi sensu lato causing Lyme disease and Anaplasma phagocytophilum causing tick-borne fever in livestock. Despite its importance, current knowledge about the small mammal-tick association from ecosystems at the northern distribution limit of ticks is scarce. In the current study I investigated the role of rodents and shrews as hosts for ticks and reservoir for tick-borne pathogens in a northern coastal forest ecosystem. I predicted that rodents and shrews would host immature life stages of I. ricinus, while they would host all life stages of the rodent specialist, I. trianguliceps. I also predicted that variation in tick burdens would be affected by extrinsic and intrinsic factors. In addition I predicted that rodents and shrews would be detected with B. burgdorferi s.l. and A. phagocytophilum. Questing ticks were sampled, and small rodents and shrews were trapped in two transects in Sogn & Fjordane, Norway, in spring and fall of 2013 and 2014. Tick burdens of different small mammal species were quantified and infestation by pathogens was determined. Distribution of questing I. ricinus ticks and I. ricinus and I. trianguliceps tick burdens were investigated using generalised linear mixed effect models. Rodents and shrews showed relatively high prevalence of tick infestation and some individuals carried high abundance of larvae of both I. ricinus and I. trianguliceps ticks. Both B. burgdorferi s.l. and A. phagocytophilum were detected in small mammal species. There was evidence that tick burdens were affected by extrinsic factors likely linked to local climate. Intrinsic factors were also found to affect tick burdens. Larva and nymph tick burdens were positively correlated with host body size. After controlling for body size, the residual variation in tick burdens for I. ricinus larvae and I. trianguliceps nymphs were attributed to unmeasured qualities of rodent and shrew species. The present study highlights the role of rodents and shrews as important hosts for immature stages of ticks, especially larvae. In addition this study suggests that tick burdens on rodents and shrews are affected by a complex combination of local climate and host factors, making some individuals more likely to contribute to the life cycle of ticks and the enzootic transmission cycle. To better understand tick-borne diseases in relation to climate change, the current study suggests that one must put more emphasis on intrinsic factors, since these may have major impact on the small mammals contribution to the enzootic transmission cycle.