Surface texture heterogeneity in maculated bird eggshells

Abstract

Many of the world's 10 000 bird species lay coloured or patterned eggs. The large diversity of eggshell patterning among birds, achieved through pigment, has been attributed to a few selective agents such as crypsis, thermoregulation, egg recognition, mate signalling, egg strength and protecting the embryo from UV. Pigmentation may influence the texture of eggshells, which in turn may be important for dealing with water and microbes. We measured surface roughness (S_a, nm), surface skewness (S_sk) and surface kurtosis (S_ku), which describe different aspects of surface texture, across 204 bird species with maculated (patterned) eggs and 166 species with immaculate (non-patterned) eggs. Using phylogenetically controlled analyses, we tested whether maculated eggshells have different surface topography between the foreground colour and background colour, and between the background colour of maculated eggshells and the surface of immaculate eggshells. Secondly, we determined to what extent variation in eggshell pigmentation of the foreground and background colour is determined by phylogenetic relatedness, and whether certain life-history traits are important predictors of eggshell surface structure. We show that the surface of maculated eggs consists of a rougher foreground pigment compared to the background pigment across 71% of the 204 bird species (54 families) investigated. Species that lay immaculate eggs showed no difference in surface roughness, kurtosis or skewness compared to background pigment of maculated eggs. The difference in eggshell surface roughness between foreground and background pigmentation was greater among species that occupied dense habitats, such as forests with closed canopies, compared to those that nest in open and semi-open habitats (e.g. cities, deserts, grasslands, open shrubland and seashores). Among maculated eggs, foreground texture was correlated with habitat, parental care, diet, nest location, avian group and nest type, while background texture was correlated with clutch size, annual temperature, development mode and annual precipitation. Surface roughness among immaculate eggs was greatest for herbivores, and species that have larger clutch sizes. Together, this suggests that multiple life-history traits have influenced the evolution of eggshell surface textures in modern birds.

Keywords: bird; eggshell; maculation; roughness; surface texture; topography.

Figure 1.

Schematic visualizing relative values of S_sk and S_ku. (a) Sine wave; S_sk = 0.00; S_ku = 1.50; immaculate example: ruby-throated hummingbirds, Archilochus colubris (S_sk = −0.02, S_ku = 2.80). (b) Spikes; S_sk = 0.61; S_ku = 2.11; immaculate examples: wood storks, Mycteria americana (S_sk = 0.56, S_ku = 3.59) or black-necked stilts, Himantopus mexicanus (S_sk = 0.62, S_ku = 3.92). (c) Inverted spikes; S_sk = −0.61; S_ku = 2.11; immaculate example: barred cuckoo-doves, Macropygia unchall (S_sk = −0.61, S_ku = 3.27) or red-shouldered hawks, Buteo lineatus (S_sk = −0.60, S_ku = 3.62). (d) Tall humps; S_sk = −1.04; S_ku = 2.85; immaculate example: brown pelicans, Pelecanus occidentalis (S_sk = −1.02, S_ku = 4.87). (e) Medium humps; S_sk = −1.23; S_ku = 3.38; immaculate example: firewood-gatherers, Anumbius annumbi (S_sk = −1.08, S_ku = 6.16). (f) Short humps; S_sk = −1.32; S_ku = 3.63; immaculate example: Manx shearwaters, Puffinus puffinus (S_sk = −1.48, S_ku = 7.09). All of the values are dimensionless. The dashed line indicates the average height of the line section. All figures are generated from equations and are not the actual species examples mentioned.

Figure 2.

Eggshell surface roughness (S_a, nm) of foreground and background pigment of 204 bird species with maculated eggs. Dotted line has a slope of 1, with mean species S_a values above the line having rougher foreground versus background pigment surface. Species are colour coded based on avian clade (pink = Passeriformes; blue = non-Passeriformes) and a subset of species are labelled. The data in the figure are not corrected for phylogenetic relatedness.

Figure 3.

Surface topography of maculated eggshells from a selection of species included in this study. Greyscale two-dimensional images of the surface topography are shown for the foreground and background pigment. Digital elevation models of the foreground and background pigment for one specimen per species (1 µm resolution, dimensions 200 µm × 200 µm). Bird art by Scott Partridge and egg photos by the Western Foundation of Vertebrate Zoology. The egg photos are not to scale. More information can be found in the electronic supplementary material.

Figure 4.

(a) Phylogenetic tree showing significant predictors of surface heterogeneity (ΔS_a) among maculated eggs. Branch colours depicts ΔS_a (nm) for each species. Scientific names are shown as tip labels and avian family is separated using black bars. (b) Boxplot and violin plot showing the difference in foreground to background roughness as a function of habitat. Species that occupy dense habitats had higher ΔS_a than those in semi-open and open habitats. A single asterisk (*) signifies significant (p < 0.05) differences for pairwise comparisons. Panel (b) is not corrected for phylogenetic relatedness. Silhouette illustrations came from PhyloPic (http://phylopic.org) and SVG Silh (https://svgsilh.com/), contributed by various authors under public domain licence (see electronic supplementary material).

Figure 5.

Significant predictors of eggshell surface kurtosis (S_ku) and skewness (S_sk) for background pigment among species that lay maculated eggs. Background S_ku is plotted as a function of (a) annual precipitation and (c) clutch size. Background S_sk is plotted as a function of (b) annual temperature, (d) clutch size and (e) mode of development. Three asterisks (***) signify p < 0.001 for pairwise comparisons. The data in the figures are not corrected for phylogenetic relatedness. None of the life-history traits were significant for background surface roughness (S_a) in conditionally averaged models. Silhouette illustrations came from SVG Silh (https://svgsilh.com) under public domain licence (see electronic supplementary material).

Figure 6.

Significant predictors of foreground surface roughness (S_a, nm), kurtosis (S_ku) and skewness (S_sk) among species that lay maculated eggs. Foreground S_a is plotted as a function of (a) habitat, (b) parental contact, and (c) diet. Foreground S_ku is plotted as a function of (d) nest location, while foreground S_sk is plotted as a function of (e) nest location, (f) avian group and (g) nest type. The data in the figures are not corrected for phylogenetic relatedness. Significant differences between categorical variables based on conditionally averaged models are given in asterisks with ***p < 0.001, **p < 0.01 and *p < 0.05. Silhouette illustrations came from PhyloPic (http://phylopic.org) and SVG Silh (https://svgsilh.com/), contributed by various authors under public domain licence (see electronic supplementary material).

Figure 7.

Significant predictors of surface texture among species that lay immaculate eggs. Surface roughness (S_a) is plotted as a function of (a) diet and (b) clutch size. Significant differences between categorical variables based on conditionally averaged models are given in asterisks with ***p < 0.001, **p < 0.01 and *p < 0.05. Silhouette illustrations came from the authors or Silh (https://svgsilh.com) under public domain licence (see electronic supplementary material).