How avian incubation behaviour influences egg surface temperatures: relationships with egg position, development and clutch size

Abstract

While understanding heat exchange between incubating adults and their eggs is central to the study of avian incubation energetics, current theory based on thermal measurements from dummy eggs reveals little about the mechanisms of this heat exchange or behavioural implications for the incubating bird. For example, we know little about how birds distribute their eggs based on temperature differences among egg positions within the nest cup. We studied the great tit Parus major, a species with a large clutch size, to investigate surface cooling rates of individual eggs within the nest cup across a range of ambient temperatures in a field situation. Using state‐of‐the‐art portable infrared imaging and digital photography we tested for associations between egg surface temperature (and rate of cooling) and a combination of egg specific (mass, shape, laying order, position within clutch) and incubation specific (clutch size, ambient temperature, day of incubation) variables. Egg surface temperature and cooling rates were related to the position of the eggs within the nest cup, with outer eggs being initially colder and cooling quicker than central eggs. Between foraging bouts, females moved outer eggs significantly more than centrally positioned eggs. Our results demonstrate that females are capable of responding to individual egg temperature by moving eggs around the nest cup, and that the energy cost to the female may increase as incubation proceeds. In addition, our results showing that smaller clutches experience lower initial incubation temperatures and cool quicker than larger clutches warrant further attention for optimal clutch size theory and studies of energetic constraints during incubation. Finally, researchers using dummy eggs to record egg temperature have ignored important elements of contact‐incubation, namely the complexity of how eggs cool and how females respond to these changes.

The behavioural and physiological strategies of bird and reptile embryos in response to unpredictable variation in nest temperature

“…Nonetheless, nest temperatures vary from about 30 to 40 • C among avian species (Webb, 1987), and can drop to as low as 10 • C for several hours daily if brooding parents leave to forage (Lill, 1979;Jia et al, 2010). Thermal environments may even differ among different layers in a large clutch of eggs, or between the centre and periphery of the nest, due to disparities in proximity to the sunwarmed soil surface in reptiles and the brood patch in birds, or to metabolic heat produced by embryonic metabolism of adjacent eggs (Caldwell & Cornwell, 1975;Thompson, 1988;Zbinden, Margaritoulis & Arlettaz, 2006;Boulton & Cassey, 2012). For example, thermal differentials of up to 6 • C between eggs occur within field nests of the freshwater turtle Emydura macquarii, and up to 9 • C in the Australian brush-turkey Alectura lathami (Thompson, 1988;Goth, 2007).…”

Thermoregulatory Behavior Is Widespread in the Embryos of Reptiles and Birds

“…Heat for avian egg incubation mainly comes from the brood patch of the parent (Lea and Klandorf 2002), which may deliver heat to only a part of an egg, creating a thermal gradient inside a nest or even within an egg (Caldwell and Cornwell 1975;Turner 2002;Boulton and Cassey 2012). Eggs at the center of a bird nest are likely to be warmer than those at the periphery of the nest (Boulton and Cassey 2012) due to the three-dimensional temperature fields created by differential warming (brood-patch contact) and cooling (environmental contact;Turner 2002).…”

How does an increase in minimum daily temperatures during incubation influence reproduction in the great tit Parus major?

“…Mothers can influence the developmental temperature of their offspring by modulating incubation behaviour in birds (Webb 1987, Durant et al 2013. Incubation behaviour may buffer egg temperature variation (Boulton andCassey 2012, Durant et al 2013) and is thus crucial in the reproduction of egg-laying species. In species where incubation is mainly provided by the female, incubation temperature depends on the allocation trade-off of energy between heating eggs and self-maintenance, depending on ambient temperature (Amininasab et al 2016) and on their mate's ability to feed them during incubation (Kluijver 1950, Gosler 1993.…”

“…Then, although females do not let their eggs cool down to the 'physiological zero' (i.e. temperature below which no developmental process occurs) (Haftorn 1988), more energy is needed to reheat the clutch than when male feeding is sufficient (Bryan and Bryant 1999, Reid et al 2000, Cresswell et al 2004, Ardia et al 2009, Boulton and Cassey 2012. In the great tit, egg temperature when the female returns to the nest depends on clutch size, duration of female's absence, initial egg temperature when the female left the nest and environmental temperature (Boulton and Cassey 2012).…”