The effect of developmental stage on eggshell thickness variation in endangered falcons

Abstract

We compared eggshell thickness of hatched eggs with that of non-developed eggs in endangered falcon taxa to explore the effect of embryo development on eggshell thinning. To our knowledge, this has never been examined before in falcons, despite the fact that eggshell thinning due to pollutants and environmental contamination is often considered the most common cause of egg failure in falcons. Because of the endangered nature of these birds, and the difficulty in gaining access to the nests and their eggs, there is a large gap in our knowledge regarding eggshell thickness variation and the factors affecting it. We used a linear mixed-effects (LME) model to explore the variation in eggshell thickness (n = 335 eggs) in relation to the developmental stage of the eggs, but also in relation to the falcon taxa, the laying sequence and the study zone. Female identity (n = 69) and clutch identity (n = 98) were also included in the LME model. Our results are consistent with the prediction that eggshell thickness decreases during incubation because of the important effect of calcium uptake by the embryo during development. Our results also show that eggs laid later in the sequence had significantly thinner eggshells. In this study, we provide the first quantitative data on eggshell thickness variation of hatched eggs in different falcon taxa that were not subjected to contamination or food limitation (i.e., bred under captive conditions). Because eggshell thickness strongly influences survival and because the species examined in this study are endangered, our data represent a valuable control for future studies on the effects of pollution on eggshells from wild populations and thus are an important contribution to the conservation of falcons.

Introduction

The main functions of the eggshell in birds are protection, and gas and water exchange. In addition, the eggshell provides the embryo with minerals and calcium needed for the development of calcium consuming organs including the skeleton, muscles and brain (Tuan et al., 1991, Blom and Lilja, 2004, Wilkin et al., 2009). Thus, the avian egg provides the developing embryo with an ideal environment for development (Romanoff and Romanoff, 1949, Rahn and Ar, 1974, Solomon, 1991).

Despite the considerable body of research devoted to eggshell characteristics, either in poultry science (Hunton, 1995, Carnarius et al., 1996) or in wild birds (Massaro and Davis, 2004, Massaro and Davis, 2005, Castilla et al., 2007, Castilla et al., 2009b), the effect of developmental stage on eggshell thickness or strength remains unknown for most wild species. Since developing embryos utilize calcium from the eggshell, developmental stage can be expected to cause eggshell thinning (Vanderstoep and Richards, 1970, Bunck et al., 1985, Bennett, 1995, Castilla et al., 2007, Karlsson and Lilja, 2008). Additionally, eggshell thickness appears to be influenced by many factors including genetics, egg colour and size, the time the eggs spend in the uterus, female characteristics (condition, age, stress, health status), and the diet of the females (Kennedy and Vevers, 1973, Nys et al., 1991, Francesch et al., 1997, Ciftci et al., 2003, Boersma et al., 2004, Riczu et al., 2004, Castilla et al., 2007, Castilla et al., 2009b, Birchard and Deeming, 2010). More recent studies have shown that Mycoplasma infection also produced egg abnormalities and eggshell thinning (Feberwee et al., 2009).

Because of the endangered nature of many raptor species (Cramp and Simmons, 1980), eggshell thinning has been the focus of much research in these species (Cade et al., 1971, Peakall and Lincer, 1996, Falk et al., 2006, Castilla et al., 2009b). Population collapse and reproductive failure in raptors have occurred in many parts of the northern hemisphere from about 1950 onwards, and have often been attributed to the use of biocides in agriculture and forestry management (Wegner et al., 2005, Falk et al., 2006, Fernie et al., 2009). Accumulation of toxic persistent compounds causes eggshell thinning and reduction in eggshell strength in eggs laid by falcons and other bird species exposed to toxins (Bunck et al., 1985, Peakall and Lincer, 1996, Falk et al., 2006, Kamata et al., 2006, Jagannath et al., 2008). Falcons are important bird indicator species as they are extremely vulnerable to insecticides and contamination. Consequently, their eggshells are considered to be good indicators of pollution and can be used to monitor the health of populations over long periods (Falk et al., 2006, Castilla et al., 2009a).

To our knowledge, the effect of developmental stage on eggshell thickness variation in falcons has never been examined before. This is remarkable, since pollutants and environmental contamination are often considered the most common cause of egg failure. Yet, without knowing how eggshell thickness is affected by development, a natural process that reduces eggshell thickness, interpretations of other studies on eggshell thickness remain difficult. Because of the difficulty in gaining access to the nests and their eggs, there is a large gap in our knowledge regarding eggshell thickness variation and the factors affecting it.

In this study we therefore examined the effect of developmental stage on eggshell thickness variation in different falcon taxa. We tested the prediction that eggshells from non-developed eggs are thicker than those of hatched eggs. We also tested the prediction that eggs produced later in the laying sequence have thinner shells than eggs laid first.