Eggshell coloration reflects both yolk characteristics and dietary carotenoid history of female mallards

Abstract

Summary1. Avian eggshell coloration has frequently been examined in a functional context (e.g. mimicry, camouflage), but in recent years, an interest has emerged in identifying the mechanisms that drive eggshell colour variation. 2. Eggshell coloration is predominately caused by pigment deposition; one such pigment is the antioxidant biliverdin, and deposition of biliverdin into eggshells may be costly to mothers due to depletion of their antioxidant reserves. Previous work has shown that dietary supplementation during laying with another type of antioxidant -carotenoid pigments -induces females to produce more biliverdin-rich eggshells. However, the impact of pre-laying nutrition -including the developmental period early in life -on eggshell coloration has not been investigated. 3. Here, we raised female mallards (Anas platyrhynchos) from hatching, supplemented their diets with carotenoids during early-, mid-or late-developmental periods, and at adulthood measured female circulating carotenoid levels, yolk carotenoid levels, and eggshell coloration. We found that carotenoid supplementation during the late stages of development (transitional period from juvenile to adult plumage) promoted the laying of eggs with more biliverdin-rich eggshells. Independent of developmental dietary treatment, females with higher circulating carotenoid levels at the time of egg laying produced more biliverdin-rich eggshells and more carotenoid-rich yolks. When controlling for female identity, we found that more biliverdin-rich eggshells were associated with more carotenoid-rich, but smaller, yolks. We also detected a laying order effect; later-laid eggs had larger, less carotenoid-rich yolks and less biliverdin-rich eggshells. 4. Taken together, these results demonstrate that eggshell coloration reveals carotenoid status of both mothers and yolks and that diet quality more than 1 month prior to laying can affect eggshell coloration in a waterfowl species. As mallards are considered to be capital breeders in terms of lipid stores, our findings provide a new developmental perspective on the carryover of lipid-soluble and antioxidant nutrient reserves for breeding.

Darker eggshell spotting indicates lower yolk antioxidant level and poorer female quality in the Eurasian Great Tit (Parus major)

“…In several previous studies on blue-green eggshell coloration, a positive association between shell biliverdin concentration and yolk antioxidant level was detected , Navarro et al 2011, Butler and McGraw 2013. So far, to our knowledge, only one study has tested the association between protoporphyrin-based eggshell spotting and yolk antioxidant level.…”

“…For example, it has been reported that biliverdin-based eggshell coloration may signal egg yolk antioxidant , Navarro et al 2011, Butler and McGraw 2013, yolk immunoglobulin (Morales et al 2006), and yolk testosterone (López-Rull et al 2008) levels. For protoporphyrin-based shell coloration, to our knowledge there have been only 2 studies to date that have tested the association between eggshell pigmentation and the concentrations of biomolecules in the egg.…”

Effects of food limitation on the intensity of blue‐green and brown eggshell coloration: an experimental study with the canary

“…However, if females experience a food limitation before and during egg-laying, this relationship may disappear. Previously, it has been reported in various bird species that antioxidant supplemented (Morales et al 2011, Butler and McGraw 2013, Hargitai et al 2016a) and nutrient supplemented (Moreno et al 2006) female birds lay eggs of more intense blue-green eggshell coloration, while food-limited birds lay eggs with lower concentration of biliverdin in the eggshells (Duval et al 2013a). These studies suggest that antioxidant and nutrient availability could influence bluegreen eggshell coloration, and our study partly supports these findings, as female canaries experiencing food limitation were not able to produce an eggshell colour reliably indicating their body condition.…”

“…These findings suggest that birds with higher level of oxidative stress and lower level of energy would produce more biliverdin. However, an opposite pattern was generally found for eggshell biliverdin level, as females in better condition and better antioxidant status laid eggs with more intense blue-green colour (Siefferman et al 2006, Butler and McGraw 2013, Hargitai et al 2016a. Plasma biliverdin is mainly produced in the spleen from degrading erythrocytes, and then released into the circulation, and transferred to the liver (Murray 2003).…”

“…Furthermore, females in better body condition may have elevated levels of compounds with antioxidant properties, such as antioxidant enzymes (Feoli et al 2006, Rindler et al 2013) and uric acid (Cohen et al 2009, Alan andMcWilliams 2013). Therefore, birds in better body condition may have higher general antioxidant capacity, and thus could lay eggs with more intense blue-green chroma (Hanley et al 2008, Morales et al 2008, 2011, Butler and McGraw 2013, Hargitai et al 2016a). However, limitation in antioxidant and protein availability due to food restriction treatment may have weakened the correlation between body condition and antioxidant capacity, and therefore, females in better body condition could not lay eggs of more intense blue-green eggshell chroma.…”