A C Highfield
This is the original article, based upon early Tortoise Trust research, that literally revolutionised the way people thought about feeding tortoises in captivity. When this was published, in the mid-late 1980's, almost all books, veterinary texts and articles were recommending diets that were high in protein and promoted fast growth. The vast majority of captive bred tortoises at this time developed shell deformities, and died within a few years. This article changed perceptions, and made a major contribution to advancing the whole concept of dietary management for captive chelonians.
Dietary related disorders represent a major cause of mortality in captive bred hatchlings and juveniles (Highfield 1986, Zwart 1987). Lambert (1986, 1988) reports that the median survivorship of UK captive bred Testudo graeca is 1.5 years, that of T. hermanni 1.75 years and T. marginata 2.3 years but does not provide any clinical reason for such mortalities other than to indicate that growth rates are more rapid than those attained in the wild, and that carapace deformities are characteristic of such animals. These median survivorship figures agree with those recorded by the present author from submissions made by members of the public and other inexperienced keepers. Detailed examination of the affected living and deceased specimens reveals that a combination of recognised clinical factors are invariably present, principally acute secondary nutritional osteodystrophy resulting from and inadequate dietary Ca:P ratio (Wallach and Hoessele, 1968) frequently combined with hepatic dysfunction and renal dysfunction urea and deposits of uric acid within the renal tubules. The latter condition is most often observed in cases where artificially high protein diets have been imposed by keepers upon herbivorous species which in their native habitat would experience much lower levels of dietary protein. High incidences of renal and hepatic disease have been noted for some time both in veterinary reports and necropsy surveys of long-term captive chelonians. Keymers survey of 1978 which details the result of 144 pathological examinations reports that G.I. tract, hepatic and renal disease accounted respectively for 27%, 1 1% and 9.7% of mortalities with miscellaneous nutritional disorders contributing a further 22.2% of the total. 77.8% of the study group had been housed in the London Zoo, the remainder being drawn from animals belonging to members of the public (Keymer, 1978).
The disorders may be usefully divided into two main groups consisting of:
a) diseases of excess
b) diseases of deficiency.
Clinically, combinations of the two groups are common, e.g., acute carapace distortion due to lack of dietary calcium and concurrent hepatic and renal dysfunction resulting from dangerously high consumption of saturated fats, proteins and nitrates.
The calcium requirement of chelonians is variable and increases during growth phases and in the case of females during egg formation. Given that a 100% growth-weight increase frequently occurs during the first eight weeks of life, it is clear that this period is especially critical. The calcium requirement is also dependent upon external factors such as the quantity of dietary phosphorous. Vitamin D3 availability is also of relevance. In the wild, tortoises from desert habitats typically experience a calcium to phosphorous ratio of between 5: 1 to 8: 1. The greater proportion of plants consumed are considerably
richer in calcium than they are in phosphorous, are comparatively low in protein and are also very
high in fibre. Furthermore, additional trace elements are consumed as soil, sand and grit particles. Zwart (1987) notes that a critical Ca:P deficiency ratio of 1.2:1 is typical and that at this level osteoporosis and osteomalacia (softshell syndrome) together with other deformities of the scutes recorded by Lambert (1983) manifest. Supplementation with Vionate (Ciba-Geigy) is frequently inadequate, as this product itself contains both calcium and phosphorous in the ratio of 2:1, and excess phosphorous in the principal diet rapidly reduces the ratio actually attained to critical deficiency levels. Certain food items used by some captive breeders are particularly disruptive of the calcium balance, especially legumes, sprouting seeds and processed cat or dog food of animal origin. This latter frequently has a negative Ca:P ratio by as much as 1:44 or more (Collins, 1971), whilst lOOg of peas typically contains 42mg Ca to 127mg P, broad beans 27mg Ca to 160mg P and mung sprouts 19mg Ca to 64mg P.
Vitamin D and Ultraviolet Light
Animals in their natural habitat are extremely unlikely to suffer hypovitaminosis-D3. Deficiencies are possible in captive animals which are deprived of access to sunlight or a suitable artificial U.V. source of sufficient intensity, e.g., True-lite @ (Durolite Corporation) or blacklight. Symptoms of deficiency include poor locomotion, osteomalacia and osteoporosis. Plant foods contain nil vitamin D. The skin of tortoises is however, extremely rich in oils containing sterols which react with U.V. to produce the vitamin and provided adequate U.V. exposure is attained oral supplementation is not necessary (Kauffield, 1969; Wagner, 1977). It is common for herpetologists to over estimate D3 demand and to grossly overdose orally. One possible consequence of this practice is metastatic mineralisation of the soft tissues (Barten, 1982; Wallach and Hoessle, 1966). Vitamin D3 is highly toxic and extreme caution should be exercised whenever oral supplementation is employed (Finlayson and Woods, 1977). If calcium and phosphorous are provided in suitable ratios and sufficient quantity and quality of U.V. are available, hypovitaminosis D3 is not at all likely. Human demand is for 10 micrograms (400iu) per day which can be obtained from as little as 3 hours exposure to sunlight. The requirements of tortoises are not known in detail, although Zwart (1987) suggest that 10-20,000 iu of D3 per Kg of general vitamin-mineral supplement dosed routinely at 2% food volume is an effective prophylactic measure where exposure to U.V. is inadequate.
B complex deficiencies have been recorded by the author in both hatchling and adult T. graeca and T. kleinmanni where animals have been maintained by owners on what amount to lettuce-only diets. The B group includes thiamine riboflavin, pyridoxine, nicotinic acid, pantothenic acid, biotin, folic acid and cobalamin. Clinical signs of deficiency include lack of neuromuscular coordination and pernicious anaemia. In the wild, it is probable that tortoises are able to obtain adequate levels of B12 to interact with dietary folic acid by gut microflora activity involving trace dietary cobalt. B12 is absent in vegetation, but essential to life. Although it has been recommended by some herpetologists (Reid, 1982; Engberg, 1980) raw fish is categorically not suitable dietary constituent for terrestrial chelonians due to its thiaminase content which prevents synthesis and absorption of B-group vitamins. Deficiency is particularly common following severe colitis and malabsorption syndrome resulting from pathogenic flagellate infection of the G.I. tract.
Fibrous goitre or hypothyroidism is commonplace among captive herbivorous chelonians, particularly Geochelone elephantopus and Megalochelys gigantea maintained in zoological collections and which have been fed diets rich in vegetables containing high levels of anionic goitrogens (e.g. glucosinolates and thiocyanates) such as cabbage and kale. The condition has also been observed in hatchling T. graeca and T. marginata subjected to an identical dietary regime. The consumption of the responsible class of vegetables needs to be limited and in addition a multi-mineral supplement containing traces of iodine at a suggested dose rate of 6-10mg per Kg of supplement should by routinely provided with every meal. Vegetation from mountainous areas, or from soil rich in limestone may be lower than average in dietary iodine.
A disease of excess, steatitis or fatty infiltration of the liver is encountered frequently in captive chelonians and is an established cause of mortality in both hatchlings and in adults (Will, 1975; Rosskopf, 1981). Herbivorous chelonians are poorly equipped to metabolize saturated fats (Tammar, 1974), and when subjected to high fat content diets develop serious hepatosis resulting in jaundice and the inability to retain vitamin-A; hence hypovitaminosis-A is often concurrent clinically with steatitis. In the wild, virtually no saturated fats whatsoever are consumed, yet in captivity many keepers habitually provide dietary sources which are extremely rich in these substances. Tinned cat and dog foods are undoubtedly the worst offenders in this respect. Taking into account the normally reduced metabolic rate of most captive animals compared with wild specimens due to reduced temperatures and photo-periods, it is therefore not surprising that many mortalities are found post mortem to be suffering from obesity and gross fatty lesions of the liver. Botanical analysis of the native diet of T. graeca and G. agassizzii which may be assumed typical for species inhabiting similar biotypes, indicate that an average level of polyunsaturated fat consumption is 0.35g per lOOg of raw vegetation. Existing cases of steatitis may respond to veterinary treatment with thyroxine and vitamin-E.
Captive chelonians are frequently placed on diets richer in useable protein by a factor of several magnitudes greater than they would possibly be able to attain in the wild, and this, combined with a lack of dietary calcium is a major direct cause of mortalities in the median of 1.5 to 1.75 age group. The growth of such specimens is greatly accelerated, and full sexual maturity has been observed by the author in one captive bred male T. ibera at just 19 months of age. This animal weighed 565g and had a carapace length of 148mm. There was marked carapace deformity and overgrowth of keratin, the beak being extremely overgrown to the extent of interfering with normal feeding. Similar observations have been made in respect of Gopherus agassizzii hatchlings captive-bred in
the USA, when calcium deficient protein-rich diets of vegetable origin were employed to rear hatchlings by amateur herpetologists instead of a diet of designed to replicate as closely as possible the naturally occurring diet of the species (Jackson and Trotter, 1976; Hansen, Johnson, Van Devender 1976). The photographs illustrating the first reference show grossly deformed carapaces typical of the most acute form of nutritional osteodystrophy fibrosa.
The Role of Symbiotic Digestive Microflora
The intestinal microflora of herbivorous chelonians is geared to processing relatively large quantities of fibrous, carbohydrate-rich cellulose matter. There is reason to suppose that protozoans and ciliate organisms play a role in this process together with the more unusual bacterial agents (See Fenchel, McRoy, Ogden, Parker and Rainey, 1979). Non-specific enteritis is common in captive collections (Keymer, 1978; Hunt, 1957) ac counting for up to 40% of total mortalities in some cases. Deficiencies of dietary fibre are certainly one factor (Shaw, 1961; Throp, 1969; Bacon, 1980) and an adequate intake of dietary fibre may also be of importance in controlling populations of potentially pathogenic parasites. An additional factor responsible for the high incidence of gastrointestinal disease noted may be inclusion of food items of animal origin to which the slow fermentation process of the herbivores digestive system appears ill suited (Bellairs, 1969; Holt, 1978; Dandifrosse, 1974; Sokol, 1967; Skoczylas, 1978).
The dietary requirements of captive herbivorous chelonians are far more complex than has previously been assumed by many keepers. The interaction and interdependence between the mineral, vitamin and protein metabolisms have rarely been studied in sufficient detail and much work remains to be done in this field. The role of the endocrine system in relation to the mineral metabolism is yet another area where currently much awaits discovery. It is apparent that the simplistic approach of providing a high quality diet in mammalian terms is totally inadequate to meet the real needs of chelonians which have a completely different set of requirements. Indeed, that which may represent a high quality diet for a mammal or carnivorous reptile may have entirely negative consequences when presented to a chelonian herbivore.
©1997 The Tortoise Trust/A. C. Highfield