An unexpected advantage of insectivorism: insect moulting hormones ingested by song birds affect their ticks

Abstract

Ecdysteroids are important hormones that regulate moulting in arthropods. Three-host ixodid ticks normally moult to the next stage after finishing their blood meal, in the off-host environment. Presumably, three-host ticks that feed on the blood of insectivorous vertebrate hosts can be exposed to high levels of exogenous ecdysteroids causing them to initiate apolysis (the first step of moulting) on the vertebrate host. The aim of the present study was to investigate whether ticks undergo apolysis on insectivorous song birds, and if this phenomenon is associated with the seasonal variation in the availability of moths and with the presence of naturally acquired ecdysteroids in avian blood. During a triannual survey, 3330 hard tick larvae and nymphs were collected from 1164 insectivorous song birds of 46 species. A noteworthy proportion of ticks, 20.5%, showed apolysis. The occurrence of apolytic ticks on birds was correlated with the known seasonality of lepidopteran caterpillars. In addition, 18 blood samples of tick-infested birds were analysed with liquid chromatography - tandem mass spectrometry. Eight samples contained ecdysteroids or their derivatives, frequently in high concentrations, and the presence of these was associated with tick apolysis. In conclusion, naturally acquired ecdysteroids may reach high levels in the blood of insectivorous passerine birds, and will affect ticks (feeding on such blood) by shortening their parasitism.

Figure 1

Haemaphysalis concinna nymphs showing apolysis: (a) when close to full engorgement, (b) at the beginning of engorgement. Compared to nymphs that did not show the signs of apolysis (c), the place of the genital pore (arrow) was more apparent on apolytic nymphs (d).

Figure 2. The monthly regional population density of lepidopterans and the percentage of ticks showing apolysis.

The latter indicates the number of apolytic ticks expressed as the percentage of all ticks removed from birds, calculated for each month.

Figure 3. MRM chromatogram of sample No. 6.

Abbreviations can be found in the legend of Table 2, sample data are shown in Table 1.

Figure 4. Structures of the ecdysteroids tested in the blood samples.