Trade-off between the risk of overheating and camouflage on eggs of ground-nesting birds

Abstract

Many Charadriiform birds (shorebirds and allies) nest on the ground in sites with no vegetative cover, which receive direct solar radiation. When incubating adults depart from nests, the eggs may reach critical temperatures for embryos if they receive direct solar radiation. Nest predation is an important cause of breeding failures, so that to have well camouflaged nests may be critical to reduce the risk of predation while the nests are unattended. Eggshell pigmentation and spottiness have been suggested to improve camouflage, but by making the eggs darker they may increase the rates of overheating when eggs receive direct solar radiation. So, this may lead to a trade-off between both factors (camouflage and egg temperature) on eggshell coloration. The aim of this thesis was to show whether there is such a trade-off, and to analyse whether ground-nesting birds mitigate the adverse thermal conditions of their nesting sites in hot environments by means of biophysical mechanisms (e.g., egg colour and spottiness, nest materials with favourable thermal properties), as well as by behavioural mechanisms (e.g., risk-taking by incubating birds in relation to nest camouflage, choice of sites where eggs are better camouflaged).

First, we show that darker eggs of shorebirds (plovers Charadrius spp. and stilts Himantopus spp.) were better camouflaged when the nests were not attended by adults, but suffered quicker overheating than light-coloured eggs due to direct solar radiation, and also that, after controlling for environmental temperatures, eggs overheated more in the Tropics, likely because of a more intense solar radiation, than in the Mediterranean region. Thus, the benefits of increasing pigmentation and spottiness to improve camouflage are counteracted by the increased risks of overheating when eggs remain exposed to direct solar radiation.

We expected a similar trade-off at a specific level across latitudinal ranges, as at higher latitudes solar radiation is less intense that at lower latitudes. Indeed, we found that eggshell reflectance in the Kentish plover (Charadrius alexandrinus) is primarily determined by latitudinal variations in solar radiation, with eggshells of lower reflectance (darker) found in higher latitudes. However, in the southernmost localities (nearer to the equator), where solar radiation is very intense, eggshells are of dark coloration in spite of high ambient temperatures, likely to protect embryos from UV radiation. Therefore, differential effects of solar radiation on functions of coloration of eggshells may shape latitudinal variations in egg appearance in the Kentish plover.

Then, we analysed whether eggshell coloration and spottiness are related to pigment contents in the Kentish plover. As expected, we found that protoporphyrin was more abundant than biliverdin in eggshells. However, eggshell coloration was not related to pigment concentrations, which may be due to a different allocation of pigments either between eggshell¿s background and spots, or between different eggshell¿s layers. Interestingly, there was a positive relationship between the fractal dimension of eggshell spottiness and the amount of protoporphyrin. Likely, the fractal dimension of spottiness may be related to the mechanical function of protoporphyrin (e.g. by strengthening eggshells to interfere with a potential fractal structure of fractures), and/or it may have a functional role if it affects the resulting egg camouflage. If this is generalised among species, the fractal dimension of spottiness could be used as a proxy of protoporphyrin content in spotted avian eggshells.

In addition to eggshell coloration, the use of nest materials may be another biophysical mechanism with which to counteract the adverse effects of high ambient temperatures on egg overheating. Kentish plovers added into their nests lighter materials (pebbles) than those available around nest sites. Because light materials are thermally reflective, the microclimate of nests was likely improved. However, light materials worsened nest camouflage. We showed experimentally that rates of egg heating on lighter materials were lower than on darker materials. Yet, in a field experiment the plovers removed most of the experimental materials independently of their thermal properties, so that egg camouflage returned to the original values within a week of the experimental treatments. Although the thermal environment may affect the choice of nest materials by the plovers, at our study sites it was not too stressful as to determine the acceptance of the lightest experimental materials.

Beyond those biophysical mechanisms, ground-nesting birds may use behavioural strategies to enhance egg camouflage and mitigate the risk of overheating when eggs are not attended. By applying predator visual models to images of nests, we analysed whether microhabitat and nest material selection by three ground-nesting birds (pied avocet Recurvirostra avosetta, Kentish plover, and little tern Sternula albifrons) facilitated camouflage. Plovers and avocets selected microhabitats and nest materials that matched their individual egg appearance. In contrast, the lighter and less spotted eggs of the terns did not as effectively match nest microhabitats and nesting material, despite choosing lighter substrates, and their eggs were an inferior match to their background than eggs of the other two species. The paler eggs and poor camouflage of tern eggs could reflect a trade-off between thermal protection and camouflage, because terns breed later in the season than the other two species, when there is a greater risk of egg overheating. Thus, by simulating predator vision systems we show that wild birds select their laying substrates at an individual level according to their eggshell appearance. The apparent need to respond to other selective drivers that may compromise embryo survival, such as the risk of overheating, may explain why the camouflage of little tern eggs was worse than that of the other species.

Leaving eggs unattended during predator disturbance may expose embryos to potentially harmful factors, to which parent birds should respond when making decisions about when to leave or return to their nest. In an experimental study, we showed that diurnal changes in flushing behaviour of incubating little terns from nests during predator approach were affected by egg camouflage, the terns allowing closer approaches to individual nests in midday, when the eggs appeared better camouflaged, than in the morning. Return times to the nests were affected by ambient temperature, with the terns shortening such times at high ambient temperatures (i.e., in midday), thus diminishing the risk of egg overheating. As a whole, our results show that the decisions of the birds on when to leave or return to their nests depended on shifting payoffs, as a consequence of diurnal variations in both the thermal risks incurred by embryos and egg camouflage.

In conclusion, our observational and experimental studies allowed us to understand trade-offs among factors that affect embryo performance in the evolution of coloration and patterning of eggshells of ground-nesting birds. This may be useful to predict the responses of ground-nesting birds under a scenario of global warming.