Richard N. Smith, PhD., D.Sc., F.R.C.V S.
School of Veterinary Science,
University of Bristol.
Based on a talk given to the British Chelonia Group, 22nd January 1984
The commonest tortoise kept in this country is Testudo graeca, the Spur thighed Tortoise, and all the chelonian material in this paper refers only to that species.
The female scrapes out a nest in the soil when she is ready to lay, deposits a clutch of from four to ten eggs (approximately), and then covers them with the soil. She may do this twice (even three times) in one summer with an interval of a few weeks between. In the British climate it is essential to take up the eggs and transfer them to an incubator or equivalent arrangement to keep the ambient temperature about 25.3°C. It is customary to keep the eggs buried in sand.
The usual instruction is to mark the upper surface of the eggs and transfer them from the nest to the sand without turning them. In my experience this is unnecessary. I have purposely inverted eggs and have had as good a hatching rate from these as from eggs kept the original way up. I wouId emphasise that I can only vouch for this in the early days of incubation, but at all times the egg should be handled deliberately and with care. Rotating would certainly seem to be not appropriate when blood vessels have formed (approximately 3 weeks after lay).
There is also some doubt as to whether eggs can be transported. Several of the eggs that I have incubated successfully have travelled by car in a box of sand well over a hundred miles within their first few days of incubation. Although the tortoise has been a common pet (recent legislation may make this more unusual) there seems to have been few data published about the eggs. The book, Turtles - Perspectives and Research, by Harless and Morlock (1979) does not give much detail on T. graeca eggs. This is an American book and so despite the title it does include also tortoises and terrapins. Most writers on tortoise eggs refer to the paper by Young ( 1950). For his data on T. graeca, he obtained four clutches each of three eggs from the oviducts of tortoises and stored them before use in air-tight bottles at 4°C. More recently Cooper (1983) has produced some data based on eggs that had been laid in captivity but had failed to hatch.
It is interesting to compare tortoise eggs with those of birds. I have used the standard text of Romanoff and Romanoff (1949) for this since, although old, it is still constantly used as a reference for articles on birds' eggs. My own figures are based on tortoise eggs collected from a variety of sources over several years and I am extremely grateful to the donors. Some eggs have been examined at intervals during incubation and the successful hatchlings are apparently still quite normal tortoises. Many eggs have been studied within twenty-four hours of being laid. For some measurements, e.g. shell thickness, it has been possible to include also eggs that were proved infertile or that did not hatch successfully.
General surface characteristics
The eggs of Testudo graeca are hard-shelled. They are not pigmented but are slightly creamy, sometimes white, when laid. They do become dirty if left in the soil. NO harm is done if the dirt is removed with a damp swab before transferring the egg to the incubator.
The shape varies, even within a clutch. Although some are almost perfect spheres most are 'prolate spheroids' (i.e. an ellipse rotated about its major axis). The major axis is often referred to as the length, the minor, at right angles to this, is then called the width. Measurements of the minor axis do vary slightly depending on where they are taken since the egg is often slightly flattened- The ends are rounded and similar in size. There is no large end and small end, nor is either cone-shaped as with most birds' eggs.
The structure of the eggs of Testudo graeca is similar, but not identical, to that of the birds' egg. The surface is covered by a thin transparent coating or cuticle which is tightly adherent to the shell. Wiping with a damp tissue to clean the egg does not remove the cuticle- It is removed by boiling fragments of the shell in sodium hydroxide solution, a technique that is also used to remove the membranes lining the inside of the shell. These membranes are fibrous and separate the shell from the fluid components, i.e. the yolk and its surrounding albumen.
Measurements of length and width have been taken using vernier calipers. The greatest measurement at right angles to the length has been taken as the width. Other axes may be about a millimetre smaller. Sixty-nine eggs from eleven different clutches had a mean length of 33.3 mm (standard deviation 2.4) and width 28.2 mm (s.d- 1 .2). (Cooper, 1983) of 1.1 1g per c.c. This compares with 1 .09, the figure given by Romanoff and Romanoff (1949) for a standard hen's egg.
The hard egg shells of birds and reptiles consist mainly of crystals of calcium carbonate. (Many reptiles lay soft-shelled eggs.) In birds the calcium carbonate is in the form of calcite, in reptiles it is aragonite. Another difference between the egg-shell of the bird and that of T. graeca is that the basis of organic material in which the crystals are embedded in birds' eggs is absent from those of the tortoise. In other words, the aragonite crystals of the tortoise egg are held in place apparently by being wedged tightly together, whereas in the bird's egg there is a permeating material that acts as a scaffolding.
Thirty-one eggs weighed within 24 hours of lay totalled 472.802g. The eggs were then cut by a rotary emery disc and the shell split to evacuate the contents. When the weight of the removed yolk and albumen was deducted from the original, that of the shell and membranes was 77.021 g. (This would include a very slight amount of albumen left in the shell when the contents were separated.) The shell and membranes of this sample thus represented 16.29% the weight of the eggs.
Compared to birds' eggs this is a very high proportion of shell to egg. The highest quoted by Romanoff and Romanoff ( 1949) is the ostrich at 14. 1 %. The domestic chicken has a percentage of 12.3. These authors consider that in proportion to total egg weight, the shells are considerably heavier in the eggs of precocial birds (those capable of looking after themselves when newly hatched). This description certainly fits the tortoise.
To remove the membranes the shells were fragmented and boiled for five minutes in 5% sodium hydroxide (NaOH). They were then rinsed in hot tap water and left to dry at room temperature. (This is the usual technique for preparing avian egg shells for examination (Tullett 1975). This also removed most of the cuticle. Pieces of shell were then measured between hemispherical anvils using a dial gauge reading to 0.01 mm.
At first, measurements were made of fifty pieces taken at random from the crushed shell. Later the eggs were divided into approximately equal thirds (two ends and a middle piece). Seventeen pieces of each of these thirds were measured giving a total of fifty-one pieces of each of these eggs. The mean thickness of over two-thousand pieces taken from forty eggs of nine clutches was 0.27 mm (s.d. 0.01 ).
Cooper (1983) gives a mean thickness of 0.28 mm from 24 eggs, having discarded two '' abnormals", but does not say how many pieces from each egg were measured nor how the pieces were prepared.
There is variation within the clutch; as an example, mean thicknesses for seven eggs of one clutch were 0.25, 0.26, 0.26, 0.26, 0.27, 0.27 , 0.28. The eggshells of birds vary greatly in thickness but it does appear to be a species characteristic. The thickness of these tortoise eggshells is similar to that of bantams (0.26mm according to figures used by Romanoff and Romanoff (1949) ; this is slightly thinner than for other breeds of chickens). When the measurementS for the shell from the middle third of the egg were separated from those of the ends it was found that the middle section was almost invariably slightly thicker. The mean measurements of 25 eggs prepared in this way gave a middle section of 0.28 mm (s.d. 0.01 ) and ends 0.26 mm (s.d. 0.0 1 ). Whether this is a physiological occurrence due to the way the egg is formed or a physical arrangement to give certain regions a mechanical advantage (or both) it is not at present possible to say. It is, nevertheless, a remarkably constant occurrence.
There was no correlation between mean shell thickness and the total weight or volume of the egg.
There is a thick fibrous layer between the shell and the albumen. A short time after the egg of T. graeca is laid an air cell appears. I have found a convenient way to record this is by radiographing the egg. The celI is not present at lay and sometimes does not develop for one or two days. If it is formed in the same way as that of the bird (and this seems quite reasonable) the egg contents are thought to contract when they leave the higher temperatures inside the mother's body. Since the shell will contract only minimally a space forms between the shell and the contents. In the tortoise egg this space can appear in almost any position although it is commonly at one end.
The albumen of the freshly laid T.graeca egg is stiff and when tipped out of the broken egg it tends to stay in one mass. Closer examination shows that parts are very gelatinous whereas some are almost water-like. The albumen is transparent. So far I have found no satisfactory method of causing it to coagulate. There are no chalazae, the twisted strings found in the aIbumen of hens' eggs between the yolk and the ends of the egg.
Although the yolk can be 'shelled-out' of the enclosing albumen it still retains its globular shape. This is presumably maintained by yolk membranes similar to those of the bird's egg. Certainly there is a transparent 'bag' that has to be ruptured to free the yolk When released, the yolk is quite stiff and thin layers coagulate fairly rapidly.
Measurements of egg contents
In the following measurements it should be noted that after tampering with eggs none of the measurements can be exact; some loss invariably occurs however careful the manipulation. It has been mentioned that a slight covering of albumen remains inside the shell when the contents are tipped out. The yolk and albumen can be separated, but it is difficult to ensure that the division is complete. Strands of albumen remain attached to the yolk in its membranes. The components of 23 eggs have been measured. The mean weights were:
- complete egg 15.794g
- yolk 6.253g
- albumen 6.950g
- shell (plus membranes) 2.502g
The densities were also established; that of the yolk was 1 .16g per c.c., albumen 1 .00 g per c.c.
When the contents of all 23 eggs are totalled the relative proportions are:
- albumen 44.00%
- yolk 39.59%
- shell (plus membranes) 15.81%
These can be rounded off as albumen 44%, yolk 40%, shell (plus membranes) 16%.
The proportion of shell has already been commented on. There is also a high proportion of yolk when compared to birds' eggs. In these tortoise eggs, yolk provided 47% of the weight of the fluid contents. The bird with the nearest percentage to this (according to figures in Romanoff & Romanoff ( 1949) ) is the plover with a proportion of approximately 45%. The yolk of the domestic chicken is only about 36% of the fluid contents, Romanoff & Romanoff ( 1949) show that birds laying eggs with a high yolk content are precocial (as well as those that have a high proportion of shell). The newly hatched tortoise is immediately capable of an independent existence and it could be that the high yolk content of its egg has a similar purpose to the same phenomenon in birds.
In conclusion, it should be noted that I have excluded several eggs from this survey. These are ones with excrescences on the surface. The projections may be few and restricted in location, But sometimes they are quite extensive, covering almost all the egg. They appear to be extra crystals of aragonite that somehow or other have formed on the surface of an otherwise normal shell. In some areas they do actually form another layer of shell. Naturally, such extra material would affect measurements, especially of shell thickness. The excrescences and the detailed structure of the shell are subjects of further investigation.
Cooper, J.E. ( 1983) Preliminary studies on the eggs of three species of chelonians. Testudo 2(2), 33-35.
Harless, M.& Morlock H. ( 1 979) Turtles - Perspectives and Research. New York John Wiley & Sons.
Romanoff, AL & Romanoff, AJ. (1949) The avian egg. New York John Wiley & Sons.
Tullett, S.G. (1975) Regulation of avian eggshell porosity. J. 2001., Lond. 1 77, 339-348.
Young J.D. ( 195O) The structure and some physical properties of the testudian eggshell. Proc. 2001. Soc., London. 120, 455-469.
Testudo Volume Two Number Three 1984