JUNE E. CHATFIELD B.Sc., Ph.D., A.R.C.S,
(Presented at the Symposium at The University of Bristol, 1989)
Professor Bellairs has set the scene for the general functioning of reptiles and the position of the Chelonia within them. The Chelonia comprise an ancient group of reptiles which developed in the Permo-Triassic period some 190 millions of years ago from the stem reptiles or Cotylosaurs. This period of time was one of lowering of sea levels, with Britain then experiencing a hot climate and under desert conditons. Adaptation to a dry environment was necessary for survival and the reptiles, with their thicker horny skin and ability to lay eggs on land, had distinct advantages over the amphibians. During the Permo-Triassic period the plant life differed considerably from the present time. Flowering plants, the staple diet of many present-day tortoises, had not evolved then (they were to come later in the Cretaceous period) so land plants consisted of algae, mosses, ferns, treeferns, horsetails and conifers, which were tough and not a very palatable selection. Animals of various kinds - insects, snails and bodies of dead vertebrates - would have been eaten too. The bony carapace of tortoises and terrapins is likely to survive and fossil chelonia are found in a number of rock strata and they show little change in the overall design over many millions of years. In the Eocene beds outcropping in southern England, as in the Barton Beds on the Hampshire coast, turtle plates of marine and freshwater species are to be found. In the Eocene rocks of Egypt and Madagascar there are recognisable fossil Testudo while larger fossil examples of the same genus are known from the younger deposits of the Lower Pliocene period of India.
The oldest examples of chelonia were unable to withdraw the head into the shell and the jaw was furnished with teeth. It is possible that the horny perpetually growing beak may have developed in response to the toughness and abrasive properties of the plant food at the time. As a group, the Chelonia have shown much adaptive radiation with different examples specialising in life on land, in freshwater and in the sea. They therefore exploit a wide range of feeding opportunities, and in the course of time, this flexible attitude to diet has paid off in survival terms.
European land tortoises (Testudo) feed on leaves, particularly of the clover and daisy families, fruit and, in dry places, succulents. They are essentially vegetarian but take the opportunity to eat dead bodies (carrion) or dung. 1 have observed one of my tortoises (T. graeca) feeding on a dead bird killed and dismembered by a cat.
Many of the North American chelonia are swamp dwellers and this includes the Box Tortoises, which are primarily carnivorous and the Red-eared Terrapins or sliders which take a range of aquatic animal life including snails, insects, fish etc., but they will also eat plants. Recognition of food by these aquatic carnivores is through its movement and some animals need to see their food move before taking it. Chelonia mostly feed on slow-moving bottom dwellers like molluscs and worms and tend not to chase fast-moving prey. The terrapins are amphibious and need both land and aquatic environments in captivity, and like all other chelonia, they come onto land to lay their eggs.
A group we refer to in Britain as the turtles live in the sea and traditionally they feed on eel grass on the coastal fringe. Eel grass is one of the few subtidal flowering plants and would not have been available to the older fossil species.
The diet of chelonia can show variation with season due to availability or absence of certain foods and also to the life cycle of the animal, the growing young often having greater carnivorous tendencies. Knowledge of the precise food plants taken by each chelonia species is very limited and far more research needs to be done in the field in their native lands. Although one species or family, may take a particular staple diet, there is, particularly in the land chelonia, much opportunistic feeding which has had a high survival value.
Food selection and ingestion
In the chelonia there are well developed sense organs and distinct patterns of behaviour. The eyes are prominent and they have reasonable sight. Tortoises will recognise potentially suitable food by sight and then move towards it. Feeding can be impaired by lack of vision, for frost-blinded tortoises are reluctant to feed. Aquatic terrapins also use their eyes to recognise food and they will pounce on anything which wriggles. Food collection in some Chelonia is less active. The Alligator Snapping turtle Macroclemys temmincki lies still on the bottom with its mouth open and its prey (fish) are lured in by the sight of a red lump on the tongue of the turtle which resembles a bloodworm. When they go in to investigate, the turtle closes its mouth on them. A number of terrapins like the Matamata Chelus fimbriatus lie inconspicuous in the mud and ambush their prey when it stumbles across them but such tactics depend on the prey being fairly common. Based on visual information the animal may take a decision to eat or avoid a potential source of food.
Further information on food comes to the animal through the nose. There are two nostrils at the end of the snout and tortoises clearly have a good sense of smell. for they often sniff at strange food for some time before accepting or rejecting it. Food is detected with the eyes, and further examined by its smell. Some foods are eaten more readily than others and most people notice their tortoise having preferences for particular items. T aste also plays a part in deciding whether the animal continues feeding on the food it has sampled or whether it tries elsewhere. On a lawn a tortoise will carefully select the broad-leaved plants like clover and hawkweed and avoid the grass, but if there is no choice they will then eat grass, as Gilbert White observed over two hundred years ago in his Naturalist's Journal There is rnore scope for experirnental work using soluble food extracts presented on a neutral base.
In fruits the animal picks up sharpness and sweetness of taste and in captivity there are different levels of acceptance between the various strains of apples and also between sweet naturally sun-ripened fruit in season compared with forced out-of-season fruit. Leaves of wild plants vary in their palatability throughout the year and overmature ones are often rejected. Wild plants accumulate bitter substances or alkaloids which are the plant's own natural protection against animals and this is why the original wild strains of lettuce are often found unacceptable to the modern human taste as the cultivated varieties normally eaten have had the bitter substances bred out.
Chelonia have hard horny jaws like a parrot's beak in strength and in some individuals it can be very sharp with a serrated edge like a kitchen knife and capable of penetrating the human skin. The horny beak is well adapted to both herbivorous and carnivorous diets. It grows continually so can take the heavy friction and wear associated with feeding on tough plants with a high fibre content. In captivity when the beak gets insufficient wear from too soft a diet, it overgrows and needs trimming artificially.
When a plant is rooted to the ground, the movements of the head of tortoise are sufficient for feeding, but in the case of a dropped fruit moving on the ground, or where leaves are especially large, then the animal uses its front legs to hold it. Gilbert White in his journals noted that Timothy picks out the hearts and stems of the cos lettuce holding the outer leaves back with his feet.
A tortoise grazing on a lawn can have a considerable effect on the grass sward as in the slides of a piece of my lawn before and after tortoise grazing.
Hatchling tortoises feed on clover and much the same plants as the adults and at night, when they are asleep, snails move on to attack the same plants. Gilbert White often compared the functioning of tortoises and garden snails in his writings - both are shell bearers, but from different ends of the animal kingdom but with much similarity in function and both are ectothermic or cold-blooded.
The chelonian jaw is a cutting organ, not one for chewing and these animals will be seen to bolt their food, swallowing it almost entire.
Feeding in chelonia is regulated by temperature and for this reason a tortoise's first priority early in the day is to bask in the sun. This allows the body and internal organs to warm to a temperature where the digestive and other enzymes will work efficiently. Although reptiles are ectothermic or coldblooded, they can control their body temperature to some extent by their behaviour. This involves basking to warm up and shade-seeking to cool off, but they are not independent of temperature since in the warmer months of the year they eat a greater volume of food than in cooler weather. Although zoologists are now aware of the importance of behaviour in regulating body temperature in chelonia, Gilbert White had already discovered this in the eighteenth century for he noted it in his Naturalist's Journal (Chatfield 1986).
Tortoises in their anatomy are typical four-footed vertebrates. They have capacious stomachs and so can feed quickly. Leading from the stomach is a duodenum with a pancreas and pancreatic duct alongside, a large lobed liver , a very long intestine (typical of an animal feeding on bulky plant food) and a broader large intestine which empties into a cloaca. The cloaca is a characteristic structure of the lower vertebrates ( including dogfish of elementary biology courses) and is a sac into which the gut, excretory and reproductive tracts discharge. The opening is in slightly different positions in the male and female tortoises. A description of the anatomy of the tortoise with illustrations of the dissection is given in Thomson ( 1932).
The time taken for food to pass the length of the tortoises gut varies with temperature, but it can take up to a month to pass as demonstrated by Peter Holt (1978) using barium meals. A frost-damaged tortoise which 1 took care of after 7-8 months without food, took 30 days to produce its first faeces after having been hand fed daily on leafy material and fruit.
Digestion and nutrition
During the long passage through the gut, the food is digested by means of enzymes which have an optimal temperature for working, hence the importance of basking. In a diet of leaves and fruit there are carbohydrates: celluloses, starches and sugars. Some of the latter can be absorbed directly (e.g. glucose) as they are soluble in water but others need breaking down into smaller molecules before they can be absorbed. Starches are essentially chains of sugar molecules and certain enzymes will break them down to soluble sugars which can then be absorbed into the bloodstream via blood vessels in the intestine wall. This provides an energy source for day to day action. Sugar is then broken down in the presence fo oxygen to carbon dioxide and water with a discharge of energy which maintains life. Surplus sugars can be stored as glycogen or animal starch in the liver and a store of this is vital to get the animal going again after hibernation. Further food surplus can be condensed as fat which is an efficient storage of energy with many calories stored in a small volume of fat. Cellulose is a complicated large molecule carbohydrate chain (a polymer) which has a molecule size much larger than that of starch and it is less easily digested. Cellulose is abundant in food as it forms the wall of every plant cell. Bacteria in the gut of animals often produce the necessary enzymes to digest cellulose and if this is possible the animal can then make a more efficient use of its food, gaining extra sugars from the breakdown of cellulose.
The much-fragmented nature of tortoise faecal material under the microscope, coupled with the comparatively long duration of time in the gut, suggests that tortoises are able to make use of cellulose. This has particular advantages when an animal is living on a frugal diet in places like the Galapagos Islands.
We often think of meat as the source of protein, which in the largely carnivorous diet of terrapins it obviously is. However vegetarians also need and obtain protein. This is found in the living substance of every single cell, plant or animal and a plant, like the stringing nettle, which 1 have analysed during my research on snail feeding, can have a crude protein content of 28% dry weight. To analyse this, a weighed quantity of leaf is boiled in a strong concentrated acid which breaks down the protein to ammonia. The concentration of ammonia in the solution is then analysed by chemical or colorimetric methods and the crude protein level calculated with a formula. Green leaves are therefore a source of protein.
Proteins are complicated organic chemicals which differ from carbohydrates (consisting of atoms of carbon, hydrogen and oxygen) in including nitrogen as well and being in the form of polyamide chains. All repair work to worn out body cells of the animal require protein as well as growth of the animal. Because proteins are large molecules, they do not dissolve in water and have to be broken down by enzymes into the smaller peptides and animo acids before they can come into solution and be absorbed by the blood vessels of the intestine wall.
Surplus protein, unlike carbohydrate, is not stored but broken down by the kidney and the waste products excreted. It can give rise to harmful toxic waste products and therefore needs to be disposed of or rendered inert. Gross excess protein therefore (in an animal not needing a high protein diet) puts a strain on the kidneys and can lead to kidney failure - which results in a steady poisoning of the body as toxins cannot be eliminated.
Aquatic chelonia convert their nitrogenous waste (worn out cells and excess protein ) into ammonia which dissolves in water and is discharged into the aquatic environment. Tortoises can expel some waste as ammonia dissolved in the urine and this can be detected by its smell.
In terrestrial species of chelonia, most of the excretory waste is precipitated as urate crystals (the white part of the puddle of a tortoise) and this saves the loss of body water in flushing it out in solution or damage from too high a concentration in soluble form. A small amount of urea is also produced - this if the main excretory product of the more advanced group of the mammals.
Although chelonia can build up fat from surplus carbohydrates in their diet, a plant-based diet is low in ready fat and herbivorous species may not be adapted to digesting it. There is a certain amount of fat in meat so the carnivorous species would have a better fat digestion. In any case fat is less necessary in reptiles which live frugally, not having to cope with the energy demands of a central heating system of warm-blooded animals, and because of this they do not have to insulate the body.
Other components of diet
As well as carbohydrates, proteins and fats, a diet also needs to include roughage or fibre, vitamins and mineral nutrients. Roughage comes from the xylem or water-conducting vessels of plants which is composed of lignin, an inert non-carbohydrate polymer that is not broken down in the gut. This helps the healthy passage of food through the gut and has a physical function. Vitamins, which are also needed are complex organic molecules (carbon-based) and they are usually involved in the enzymes which are important in helping the break-down of foods to simple substances at conditions satisfactory to the living body and basic metabolic processes. It is possible to break proteins down with strong chemical acids and heat, but not in the living body. As well as in food digestion, many different enzymes are part of the Krebbs Cycle involved in energy release from sugars as the basis of respiration. Vitamins are essential for different chemical processes in the functioning of the body, often as parts of enzymes and Martin Lawton will have more to say of their deficiency in a later lecture.
Vitamin A molecule is like half of a carotene molecule and derived from carotene pigments which are orange and present in green leaves, although their presence is masked by the more abundant green chlorophyll. In autumn, when chlorophyll breaks down in leaves of trees, the orange pigments are revealed in autumn colour. If a tortoise feeds primarily on green leaves and also eats carrot and tomato, it is unlikely to suffer from Vitamin A deficiency. Terrapins, being more carnivorous are more likely to show deficiency symptoms unless they are offered lettuce, water weed or other green plants, Vitamin A is the one vitamin which can be harmful in excess as demonstrated in a previous paper by Professor Zwart in Testudo, 1987.
Mineral nutrients both basic and as trace elements are important too and in their absence are deficiency symptoms. Calcium and phosphorus are needed in quantity in chelonia for the formation and maintenance of the skeleton and shell as well as egg shell formation and development of the embryo in gravid females. In the wild, tortoises eat a good deal of grit with their food as well as seizing upon empty snail shells and maybe bone. Different species of plants have different levels of efficiency in extracting minerals from the soil, so the different plant leaves have differing levels of concentrations of these minerals in their leaves. This is demonstrated in a table in Cooper and Jackson' s book Diseases of the Reptilia (1981 ).
Vitamins and minerals are a necessary part of the diet of chelonia and they are more likely to be obtained naturally if the animals have a wide choice of very fresh foods (vitamins can deteriorate in storage) as whole leaves rather than cut up, they can have some free-range feeding in a garden rather than total life in a small pen and care is given to include some particularly vitamin and mineral rich foods like watercress. One should aim in husbandry to get the balance right naturally rather than to patch up on deficiency later. In captivity the use of vitamin/mineral supplements like Vionate are recommended.
Maps of the distribution of Testudo graeca and T. hermanni in the Collins Field Guide to Reptiles and Amphibia (Arnold and Burton 1978) show clearly that chelonia are not native to Britain as a breeding species. They have often been kept successfully as pets for long periods of time but they are exotic pets and, because they are not fully adapted to the northern temperate belt, extra care is needed in keeping them in our climate.
Chelonia as a group have a remarkable track record for long term survival. They pre-date the dinosaurs and outlived them by combining a low profile with a frugal physiology. If we allow their habitat to survive, as the American zoologist A S Romer considered. The dinosaurs passed away, and the mammals took their place, but the turtles went calmly on their placid way. NOW man dominates the scene, but the turtles are still with us. And if, in the far distant future, man in turn disappears from earth, very likely there will still be found the turtle plodding stolidly on down the corridor of time. (Romer 1960).
REFERENCES AND FURTHER READING
Arnold, E.N. and Burton, J.A., 1978. A Field Guide to the Reptiles and Amphibians of Britain and Europe. Collins, London
Chatfield, J.E., 1986. Selborne and the tortoise connection. Testudo 2, (4), 1 5-28
Cooper, J.E. and Jackson, O.F ., 1 981 . Diseases of Reptilia. 2 vols. Academic Press
Geissman, T A, 1962. Principles of Organic Chemistry. W.H. Freeman, San Francisco and London
Greenoak, F. and Mabey, R., 1 986, 1 988, 1 989. The Journals of Gilbert White. 3 vols. Century, London
Halliday, T and Adler, K., 1986. The Encyclopaedia of Reptiles and Amphibians. George Allen and Unwin, London
Holt, P ., 1978. Radiological studies of the alimentary tract in two Greek tortoises. Veterinary Record 1 03, 1 98-200
Holt, P., 1978. Barium studies in two Spur-thighed tortoises, Testudo graeca. Testudo 1 (1 ), 7-8
Ministry of Agriculture, Fisheries and Food, 1 986. Manual of nutrition. H.M.S.O., London
Romer, A.S., 1960. Man and the vertebrates Vol. 1. Penguin Books, Middlesex.
Thomson, J.S., 1932. The anatomy of the tortoise. Scientific Proceedings of the Royal Dublin Society 20, 359-46 1
Zwart, P., 1987. Advances in the veterinary care of chelonia over the past 20 years (1967-1987). Testudo 2, (5), 1 -14
Testudo Volume Three Number One 1989