High atmospheric temperatures and ‘ambient incubation’ drive embryonic development and lead to earlier hatching in a passerine bird

Abstract

Tropical and subtropical species typically experience relatively high atmospheric temperatures during reproduction, and are subject to climate-related challenges that are largely unexplored, relative to more extensive work conducted in temperate regions. We studied the effects of high atmospheric and nest temperatures during reproduction in the zebra finch. We characterized the temperature within nests in a subtropical population of this species in relation to atmospheric temperature. Temperatures within nests frequently exceeded the level at which embryo’s develop optimally, even in the absence of parental incubation. We experimentally manipulated internal nest temperature to demonstrate that an average difference of 6°C in the nest temperature during the laying period reduced hatching time by an average of 3% of the total incubation time, owing to ‘ambient incubation’. Given the avian constraint of laying a single egg per day, the first eggs of a clutch are subject to prolonged effects of nest temperature relative to later laid eggs, potentially increasing hatching asynchrony. While birds may ameliorate the negative effects of ambient incubation on embryonic development by varying the location and design of their nests, high atmospheric temperatures are likely to constitute an important selective force on avian reproductive behaviour and physiology in subtropical and tropical regions, particularly in the light of predicted climate change that in many areas is leading to a higher frequency of hot days during the periods when birds breed.

Embryonic heart rate predicts prenatal development rate, but is not related to post‐natal growth rate or activity level in the zebra finch (Taeniopygia guttata)

“…This suggestion is consistent with the hypothesis that different selection pressures and priorities at different life stages promote shifts in the regulation of behaviour and development (White et al, ). However, we acknowledge that in our study of wild, “desert dwelling” zebra finches, we were unable to control for the effects of ambient incubation (Griffith et al, ) and differential provisioning (and other parental effects) within and between nests that may have influenced our estimations of “intrinsic” prenatal and post‐natal developmental rate. Indeed, embryonic metabolism and growth rates are known to be correlated in commercial poultry (where food intake is more controlled) (Tona et al, ).…”

Egg size is unrelated to ambient temperature in the opportunistically breeding zebra finch

“…Our sample of clutches certainly included a wide range of climatic conditions, and ecological variation. A good number of clutches were sampled across conditions in which ambient incubation is unlikely (<20°C) and many clutches were sampled in ambient conditions (>30°C), in which, given the relationship between atmospheric temperature and nest temperature in this species in both the wild and captivity (Griffith et al , Mariette and Buchanan 2016), ambient incubation would have occurred to some degree. Given that temperature varies considerably over the period during which zebra finches breed, and that the advancing season leads to very predictable increases in temperature right across Australia, the cues should be sufficient for a facultative response to have evolved.…”

“…These findings are consistent with the proposal by Groothuis et al () that biased investment across the laying sequence in birds could be explained by the ‘hatching asynchrony adjustment hypothesis’, with patterns of biased resource allocation evening out the consequent competition between offspring developing from early and later laid eggs across the laying sequence. Although not explicitly discussed by Groothuis et al (), the effect of ambient incubation is potentially one of the likely environmental determinants of a greater need for adjustment of investment across the laying order (Griffith et al , ). If females adjust egg size to counter the potential advantage that first laid eggs get through the effect of ambient incubation on hatching asynchrony, we predict that egg size variation across the laying sequence will be more pronounced at high ambient temperatures.…”

Variation in the timing of avian egg‐laying in relation to climate

“…In the desert biome, the hoary-headed grebe Poliocephalus poliocephalus breeds when the observed temperatures are well above the 2-yr average in contrast to the majority of other species in this biome (Fig. In desert regions, eggs can reach their thermal limits rapidly when exposed to direct sunlight (Carey 2002) and when eggs are exposed to very warm temperatures, 'ambient' incubation can occur, reducing incubation time and decreasing hatch synchrony (Griffith et al 2016). Historically this species did not breed in the arid interior of Australia, but it now breeds in artificial water bodies indicating that human Table 3.…”