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

Abstract

Protoporphyrin pigment causes the red-brown eggshell colors; however, for many species, the function of this pigment is unknown. It has been proposed that eggshell pigmentation may strengthen the shell or that it may be a sexually selected signal, which advertises the quality of the female and that of her offspring to the male parent. In this study, we aimed to discover whether protoporphyrin-based eggshell pigmentation patterns of Eurasian Great Tits (Parus major) were related to female or egg quality. Additionally, we tested whether different methods of eggshell pigmentation estimation could be reliable predictors of eggshell protoporphyrin levels. We found that spot intensity, spot size, spotting coverage, and brown spot chroma indicated the protoporphyrin pigment concentration of the eggshell. Our results revealed that Eurasian Great Tit females that laid eggs with darker pigmentation had more lymphocytes in their circulation and had paler yellow breast and lower UV plumage reflectance, possibly indicating poorer health and individual quality. However, we did not find evidence that eggshell pigmentation patterns indicated the body condition, body size, or plasma oxidative status of females. Furthermore, we found that eggs with darker spots contained lower concentrations of antioxidants in the yolk. High protoporphyrin levels may be detrimental to females as they may cause oxidative damage, and this may be why birds that laid eggs with darker spots deposited lower amounts of antioxidants into the egg yolk. Shell spot darkness may also indicate territory quality, as females that laid smaller clutches also laid eggs with higher eggshell pigmentation levels. Thus, our results suggest that shell spot darkness may indicate the state of health of the female, egg yolk antioxidant level, and possibly also the quality of the territory. Keywords: eggshell color, female condition, lymphocyte count, plumage coloration, protoporphyrin pigmentation, oxidative status, sexual signalling hypothesis Manchas má s oscuras de la cá scara de huevo indican un nivel má s bajo de antioxidantes y una menor calidad de la hembra en Parus major RESUMEN El pigmento protoporfirina causa el color marrón rojizo de la cáscara de huevo; sin embargo, para muchas especies, la función de este pigmento es desconocida. Se ha propuesto que la pigmentación de la cáscara de huevo fortalece la cáscara o que puede ser una señal seleccionada sexualmente, la cual publicita la calidad de la hembra y la de sus polluelos al macho paterno. En este estudio, nuestro objetivo fue determinar si el patrón de pigmentación de la cáscara de huevo basado en protoporfirina de Parus major estuvo relacionado a la calidad de la hembra o del huevo. Además, evaluamos si diferentes métodos de estimación de la pigmentación de la cáscara de huevo podrían ser predictores confiables del nivel de protoporfirina en la cáscara de huevo. Encontramos que la intensidad de las manchas, el tamaño de las manchas, la cobertura de las manchas y el color marrón de las manchas indica...

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

“…In great tits Parus major, it has been found that females with lower body mass laid eggs with darker eggshell spotting (Stoddard et al 2012). In addition, great tit females laying smaller clutches, an indicator of either lower intrinsic quality or poorer quality territory with lower food availability (Hargitai et al 2016b), and females that bred when caterpillar availability was lower, laid eggs with darker spots (Hargitai et al 2016c). These studies support the view that darker eggshell protoporphyrin pigmentation indicates lower maternal body condition and poorer food availability.…”

“…In great tits, it was reported that females laying smaller clutches, an indicator of either lower intrinsic quality or poorer quality territory with lower food availability (Hargitai et al 2016b), and females that bred early in the breeding season when caterpillar availability was lower, laid eggs with darker spots (Gosler et al 2000, Brulez et al 2014, Hargitai et al 2016c. Moreover, Honza et al (2012) demonstrated that great reed warblers Acrocephalus arundinaceus laid darker eggs in colder weather.…”

Effects of environmental conditions on the egg mass, yolk antioxidant level, eggshell thickness and eggshell spotting patterns of Great Tits (Parus major)

“…We found that birds that bred earlier in the reproductive season laid eggs with darker spots, suggesting higher allocation of protoporphyrin pigments to the eggshell (Brulez et al 2014;Hargitai et al 2016b). Additionally, we found that in colder weather and when breeding in higher density areas birds laid eggs with more spotting.…”

“…The other spotting variables were weakly correlated (size-distribution r = 0.12, N = 268, P = 0.05) or showed no significant correlation (intensity-coverage r = -0.03, P = 0.68; size-coverage r = 0.08, P = 0.20; intensity-distribution r = -0.06, P = 0.34, all N = 268). It has been previously shown that eggshell protoporphyrin concentration in Great Tit eggs positively correlates with spot intensity, spot size, and spotting coverage, but does not correlate with spot distribution (Brulez et al 2014;Hargitai et al 2016b). We decided not to apply a principal component analysis (PCA), but instead to use the original scored variables in the statistical analyses.…”

“…Protoporphyrinbased eggshell pigmentation may help to provide camouflage (Stoddard et al 2011), it may enhance egg mimicry or allow individual egg recognition in species exposed to brood parasites (Stokke et al 1999;Moskát et al 2008), it may reinforce eggshells (Gosler et al 2005;García-Navas et al 2010;Hargitai et al 2013), or it may signal the quality of the female and the egg to the male in order to stimulate more intense paternal care (Moreno and Osorno 2003;Sanz and García-Navas 2009;Stoddard et al 2012;Hargitai et al 2016b). The accumulation of protoporphyrin has been reported to induce oxidative stress, leading to an increase in the activity of antioxidant enzymes to avoid oxidative damage (Afonso et al 1999;Pimentel et al 2013).…”