Ineffective humoral anti-tick IgY-response in birds: reaction against pathogen constituents?

Background: Variation in parasite burdens among hosts is typically related to differences in adaptive immunity. Comprehension of underlying mechanisms is hence necessary to gain better insights into endemic transmission cycles. Here we investigate whether wild songbirds that have never been exposed to ticks develop adaptive humoral immunity against endemic Ixodes ricinus ticks. Methods: Blue tits were exposed three times in succession to wild Ixodes ricinus ticks. For each infestation, serum samples were obtained. An enzyme-linked immunosorbent assay was developed, using tick salivary antigens, in order to quantify the bird's IgY response against ticks. In addition, at every sampling occasion the birds' body weight (corrected for body size) and haematocrit level was determined. Results: Individual IgY levels against the ticks' salivary proteins increased over three consecutive tick infestations, and large among-individual variation was observed. The responses were specifically directed against I. ricinus; cross-reactivity against the congeneric tree-hole tick Ixodes arboricola was negligibly low. IgY responses did not impinge on tick feeding success (engorgement weight and attachment success). Yet, those birds with the highest immune responses were more capable to reduce the acute harm (blood depletions) by compensating erythrocyte loss. Furthermore, at the end of the experiment, these birds had gained more body weight than birds with lower IgY levels. Conclusions: Latter observations can be considered as an effect of host quality and/or tolerance mechanisms. Birds anticipate the (future) costs of the activation of the immune system by ticks and/or ongoing tick-borne pathogen infections. Furthermore, although unsuccessful against tick feeding, the IgY responses may indirectly protect birds against tick-borne disease by acting against salivary protein secretions on which pathogens rely for transmission.