Successful interrupted feeding of adult Rhipicephalus appendiculatus (Ixodidae) is accompanied by re-programming of salivary gland protein expression

Abstract

Ixodid female ticks take one comparatively large bloodmeal which they convert to a single large egg mass and then they die. To examine the outcome of interrupted feeding, equal numbers of male and female Rhipicephalus appendiculatus adult ticks were fed on guinea pigs (host 1) for either 2, 4, or 6 days, or to engorgement (8 days). All of the fully engorged (D8) females laid a single large egg mass (80–160 mg/tick), while 85% of the day 6-fed (D6) female ticks (n=20) each laid a small egg mass (6·1 mg/tick). None of the females that had fed for 2 or 4 days oviposited. Ninety percent (n=20) of the day 2-fed (D2) females survived for 4 weeks after their feeding was interrupted, whereas 65% (n=20) of the day 4-fed (D4) females survived. All of the surviving partially fed female ticks (D2 and D4) attached to a second guinea pig (host 2) and attained engorged body weights that were not significantly different from those of the control females (P<0·05). Female ticks that engorged following interrupted feeding layed egg masses comparable to the controls, indicating that engorgement on host 2 was successful. The salivary gland protein profile of female ticks changed constantly during feeding. However, when feeding was interrupted, the protein expression pattern switched back to that of the non-parasitic state, presumably to enable the partially fed ticks to survive and reattach on the new host. This observation indicates that female ixodid ticks have a natural ability to survive and re-establish successful feeding on a new host if the first attempt at feeding is unsuccessful. Such an interrupted feeding mechanism supports the hypothesis that partially engorged ticks may play a role in tick-borne pathogen transmission.