Annual variation in the reproductive hormone and behavior rhythm in a population of the Asian short-toed lark: Can spring temperature influence activation of the HPG axis of wild birds?

Although a number of studies have demonstrated a correlation between ambient temperature and the timing of reproductive behavior in many bird species, the relationships between temperature, activation of the hypothalamus-pituitary-gonad (HPG) axis, laying, and hatching in free-living birds, remain unclear. We investigated the relationships between spring temperature, reproductive hormones, and behavior, in a population of the Asian short-toed lark (Calandrella cheleensis) on the Inner Mongolian Grasslands in 2014, 2015 and 2016. LH and T levels peaked earliest in the year with the highest April temperature (2014) and latest in the year with the lowest April temperature (2016), and rose faster in 2014 than in 2015 or 2016. Laying and hatching occurred earliest in 2014 and latest in 2016. E2 also peaked earlier in 2014 than in the other two years but there was no significant difference in peak E2 levels among the three years. The peak of hatching only coincided with the peak in grasshopper nymph (the main food of nestlings) abundance in 2015 and the nestling fledging rate in 2015 was significantly higher than that in 2014 and 2016. We also conducted a controlled experiment on the effect of temperature on plasma LH, T and E2 levels in wild-caught larks, which shows that mean plasma LH, T and E2 levels in the 16 °C group all peaked 4 days earlier than in the 13 °C group. All these results suggest that activation of HPG endocrine axis in the Asia short-toed lark population is closely related to ambient temperature, and that this subsequently influences the timing of laying and hatching. The HPG axis' endocrine function is a physiological factor that mediates effects of ambient temperature on the timing of breeding. Temperature induced annual variation in the timing of hatching was, however, insufficient to synchronize the nestling period with the annual peak in grasshopper nymph abundance. Unusually warm, or cold, spring temperatures advanced, or delayed, grasshopper nymph development to an extent that exceeded the Asian short-toed lark's capacity to advance or delay the onset of breeding and reproductive success was lower in the two years of the study in which the nestling period was asynchronous with the peak of grasshopper nymph abundance. Long-term research on the relationship between the timing of reproduction and population demographics of the Asian short-toed lark is required to understand the effects of climate change on this species and on temperate birds in general.