Virulence of recurrent infestations with Borrelia-infected ticks in a Borrelia-amplifying bird

Abstract

Lyme disease cases caused by Borrelia burgdorferi s.l. bacteria is increasing steadily in Europe, in part due to the expansion of the vector, Ixodes ricinus. Wild reservoir hosts are typically recurrently infested. Understanding the impact of these cumulative parasite exposures on the host's health is, therefore, central to predict the distribution of tick populations and their pathogens. Here, we have experimentally investigated the symptoms of disease caused by recurrent infestations in a common songbird (Parus major). Birds were exposed three times in succession to ticks collected in a Borrelia endemic area. Health and immune measures were analyzed in order to investigate changes in response to tick infestation and Borrelia infection rate. Nitric oxide levels increased with the Borrelia infection rate, but this effect was increasingly counteracted by mounting tick infestation rates. Tick infestations equally reduced haematocrit during each cycle. But birds overcompensated in their response to tick feeding, having higher haematocrit values during tick-free periods depending on the number of ticks they had been previously exposed to. Body condition showed a similar overshooting response in function of the severity of the Borrelia infection. The observed overcompensation increases the bird's energetic needs, which may result in an increase in transmission events.

Figure 1. Schematic overview of the study design.

(A) Actions taken during an infestation session (Inf.). “Δ Inf. 1” denotes the acute effect of the tick exposure (17 nymphs) on the birds’ physiology in session 1, i.e. the change in physiological parameters from prior to infestation to the moment that all ticks detached. (B) Schedule of successive infestation sessions. “Δ Cumulative” denotes the change in physiological parameters when birds had the opportunity to recover from the acute tick effects of Inf. 1 and Inf. 2 compared to the initial value in at day 1 (D1). “Δ Acute” denotes the change in acute responses between Inf. 1 and Inf. 3.

Figure 2. Changes in the health measures (Δ Cumulative, see Fig. 1) of great tits in relation to the Borrelia burgdorferis.l. infection rate (A) and overall tick exposure (B).

Least squares regression lines are fitted. Slope differs statistically significantly from zero (solid line) or not (dashed lines). The size of the symbols portrays the actual difference in the acute response between infestation 3 and 1 (Δ Acute, see Fig. 1). Triangles represent the birds that died during infestation 3.

Figure 3. Changes in immune measures (Δ Cumulative, see Fig. 1) of great tits in relation to the Borrelia burgdorferis.l. infection rate (A) and overall tick exposure (B).

Least squares regression lines are fitted. Except for the presented Tick x Borrelia interaction in NOx, slopes that differ statistically significantly from zero are indicated by a solid line. The size of the symbols portrays the actual difference in the acute response between infestation 3 and 1 (Δ Acute, see Fig. 1). Triangles represent the birds that died during infestation 3.