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Egg Shell Composition and Structure
Reptiles (Lepidophores and Testudines)
A mineralized egg shell membrane evolved as a synapamorphy for reptilia (1). The mineral content and structure of eggshells vary among reptilian species. Egg shells of many reptiles consist of a fibrous shell membrane connected to the albumen, as well as a calcareous layer attached to the outer surface of the membrane. The inorganic content of the reptilian shell involves mainly the outer portion and is comprised of calcium carbonate in the form of calcite (5). Reptilian eggs can be separated into three separate groups based on the structure of their shells: flexible shells with no calcareous layer, flexible shells with a thick calcareous layer, and rigid shells with a well-developed calcareous layer. Egg shell structures can be examined and studied with the use of a Scanning Electron Microscope (SEM). The SEM analysis of eggshells is used to differentiate important taxonomic characters to determine relationships among taxa.
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Squamate reptiles mainly lay eggs with flexible shells. In fact, all squamate eggs are flexible except for two subfamilies of keggonid lizards (1). Some of these flexible shells, such as those of Diposaurus doralis, Anolis auratus, Anolus limiforns and Natrix natrix contain no calcareous layer, only a shell membrane. This fibrous membreane is organized into an irregular series of ridges and a finely woven mat of fibers on the outer surface.
In other squamates, the outer surface of the flexible shell contains a relatively thin calcareous layer. This can be shown in the network of spheres found in the SEM pictures of Figure 3A and B (3). This type of shell is found in Anolis carolinensis and Callisaurus draconoides (3). Pogona barbata is a squamate with a unique egg shell structure; it is the only flexible shell squamate egg in which the calcite crystals form columns that penetrate into the fibrous layer. This type of egg shell is also typical for the lepidosaurian sphenodon punctuates, or Tuatara (5). A study done by Osborne and Thompson on the chemical composition and structure of the eggshell of three oviparous lizards analyzes the typical flexible eggshells of squamates including the scincid lizards Lamprophois guichenoti and Laprophois delicate, as well as anagamid Physignathus lesuerurri. This study used SEM to determine that the structure of the shells of L. guichenoti, L. delecata and P. lesueurii were very similar. Their shell structure consisted of an outer calcareous layer, a fibrous shell membrane and an inner boundary layer. The calcareous layer appeared uneven at low magnification, but showed a surface consisting of protruding calcareous segments which touch to form a smooth appearance at higher magnifications. Also visible were pore like structures and fibers that were laid down in layers with alternating direction. Osborne and Thompson’s study also did an x-ray analysis using an Energy Dispersive Analysis by X-ray (EDAX) to determine the distribution of ions within the eggshell. This study showed that most of the inorganic content of the shell, including magnesium, sodium and potassium occurred in the calcareous layer.
Some turtles also have flexible shelled eggs. These eggs are made of a defined calcareous layer that is as thick as the shell membrane. This calcareous layer is variable however. For example, the eggs of sea turtles have a poorly ordered, open matrix calcareous layer with undefined shell components and pores. In the flexible shelled eggs of Emydids and chelydrids, however, the calcareous layer is highly structured with well defined shell componants and pores (3). Rigid-shelled eggs (laid by crocodilian, some chelonians, dibamids and gekkonids) have a well developed calcareous layer that makes up most of the eggshell and a thin shell membrane. These eggshells are organized into shell units that fit together tightly and interlock. Turtles do not have only flexible eggs however; shell structure can be described as pliable, hard-expansible or brittle (1).
Birds generate heavily mineralized, rigid egg shells (2). The shell of avian eggs consists of shell membranes along with an external layer of calcite crystals (A). Avian egg shells are composed of mostly inorganic materials with an organic matrix. The shell is made of two separate layers, the palisade and the cone layer, which make up the bulk of the shell. The palisade and the cone layer are comprised of calcite. The outer part of the palisade layer is formed from dense crystalline material. Magnesium and phosphate are minor constituents to the avian eggshell. Magnesium levels are thought to increase outwards from the inner shell toward the palisade layer and a relationship between the magnesium content and strength and hardness of the eggshell of the domestic hen has been found by a study completed by Board and Scott (c). Surrounding the true shell are shell accessory materials comprised of a distinct cover and cuticle made of organic and inorganic material. Pore canals are present connecting the cones and extend across the palisade layer to the external surface of the shell. The type of pore canals is a major variation in avian eggs. There are five types of pore systems found in avian eggshells: open, occluded, plugged, capped and reticulate. Most pores are non-branched; exceptions to this are mainly in thick shells such as those of swans, ratites, and ostriches. The simplest open pore systems can be found in the in the eggshells of pigeons and doves. Occluded pore systems have accessory materials that form a skin on the outer surface of the shell but are considered to be a variant of the simple shell form. Plugged pore systems are found in Rhea Americana, Micropara capensi, and Cuculus canorus ©. The plugs themselves are made of variable materials. Capped pore systems have pores covered with accessory materials in the form of sphere like layers. Capped pore systems include the eggshells of Guira guira, Crotophagia ani, Podiceps cristatus and Numidia meleagris ©. The reticulate pore system includes a pore in which the outer part of the palisade layer is extensively modified. This type of pore system can be found in Casuarius casuarius, and Dromaius nouvaehollandiea. ( c).
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The eggs of currently living oviparous mammals are composed of soft, leathery, flexible shells. The monotreme egg shell is not mineralized and lacks a calcareous covering. The parchment- like egg shell is white in color, soft and compressible (9). Little studies have been done on the egg shell composition and structure and therefore will not be mentioned.
Although it is known that reptiles ovulate all eggs at the same time, the process of shell formation in reptiles is not well studied. For example, a study of the prolonged egg retention in the turtle Deirochelys reticularia in South Carolina by Buhlmann, Lynch, Gibbons and Greene were not able to determine if eggshell formation begins sequentially on each egg or if formations begins only when all of the eggs are in the oviduct. (11) It is known that formation of the shell membrane and the calcareous layer happens in the uterus. In order to form the egg shell a supersaturated solution of ions needs to be present along with a site of nucleation which acts to overcome the free energy barrier of crystal growth. These nucleators differ depending on the egg type.
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