The effect of developmental stage on eggshell thickness variation in endangered 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.
Section snippets
Study animals and eggs
The falcon species examined in this study are protected, rare or endangered and they are included on the CITES list (Tucker and Heath, 1994). Studied species include the peregrine falcon (Falco peregrinus peregrinus; P), the red shaheen falcon (Falco peregrinus babylonicus; B); the intraspecific hybrid peregrine × red shaheen (F. p. peregrinus × F. p. babylonicus; PB); the saker falcon (Falco cherrug; C), the gyr falcon (Falco rusticolus; R), and the interspecific hybrid between the saker falcon
Results
Overall, we found a large and significant variation in eggshell thickness among taxa. Eggs of the peregrine falcons (P, B, PB) had thinner eggshells than those of the larger falcon species (i.e., C, R, CR) independent of developmental stage (ANOVA, developed: F1,208 = 152.54, P < 0.001; undeveloped: F1,167 = 122.19, P < 0.001; Fig. 1). Within the larger falcons no differences were found between taxa irrespective of development (ANOVA, F2,184 = 1.54; P = 0.22). However, within the peregrines, F. p.
Discussion
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), allowing our data to be used as a reference for studies on eggs from natural populations. Our results are consistent with the prediction that eggshell thickness decreases during incubation, and suggest that the effects of calcium uptake by the embryos are as important in
Acknowledgements
We would like to acknowledge the persons in charge and the workers of Roc Falcon, especially Harald Kuespert, Stania Kuespert, Oscar Oliva Piferrer and Sandor Sebestyen, for providing detailed information about the falcons, for helping to collect the eggs and measuring the birds. We are grateful to Benno Böer (UNESCO Office Doha, Qatar) for his support and encouragement to improve our knowledge about the biology and conservation of endangered falcons, and to Eusebio Jiménez Arroyo for
References (44)
- et al.
Relationship of eggshell ultrastructure and shell strength to the soundness of shell eggs
Poult. Sci.
(1996) - et al.
Use of triticale alone and in combination with wheat or maize: effects of diet type and enzyme supplementation on hen performance, egg quality, organ weights, intestinal viscosity and digestive system characteristics
Anim. Feed Sci. Technol.
(2003) - et al.
A long-term increase in eggshell thickness of Greenlandic peregrine falcons Falco peregrinus tundrius
Sci. Total Environ.
(2006) - et al.
Genetic parameters for egg number, egg weight and eggshell color in three Catalan poultry breeds
Poult. Sci.
(1997) - et al.
Eggshell structure, mode of development and growth rate in birds
Zoology
(2008) The effect of embryonic development on the thickness of the eggshells of Coturnix quail
Poult. Sci.
(1972)- et al.
Whitening of brown-shelled eggs: mineral composition of uterine fluid and rate of protoporphyrin deposition
Poult. Sci.
(1991) - et al.
Do PCBs cause eggshell thinning?
Environ. Pollut.
(1996) - et al.
End-of-cycle bone quality in white- and brown-egg laying hens
Poult. Sci.
(2004) - et al.
The changes in eggshell strength during incubation
Poult. Sci.
(1970)
Relative sensitivity of several measures of eggshell quality to the stage of embryonic development
Bull. Environ. Contam. Toxicol.
Avian eggshell thickness: scaling and maximum body mass in birds
J. Zool. Lond.
A comparative study of growth, skeletal development and eggshell composition in some species of birds
J. Zool. Lond.
Why penguin eggshells are thick
Auk
A comparative study of changes in the structure of avian eggshells during incubation
Zool. J. Linn. Soc.
Changes in eggshell thickness during incubation: implications for evaluating the impact of organochlorine contaminants on productivity
Bull. Environ. Contam. Toxicol.
Variation in peregrine falcon eggs
Auk
DDE residues and eggshell changes in Alaskan falcons and hawks
Science
Developmental stage affects eggshell breaking strength in two ground-nesting birds: the partridge (Alectoris rufa) and the quail (Coturnix japonica)
J. Exp. Zool.
Eggshell thickness variation in red-legged partridge (Alectoris rufa) from Spain
Wilson J. Ornithol.
Determinants of egg shell strength in endangered raptors
J. Exp. Zool.
Increase in membrane thickness during development compensates for eggshell thinning due to calcium uptake by the embryo in falcons
Naturwissenschaften
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