Massively accelerated captive growth in a young Testudo horsfieldii (Russian tortoise).
Metabolic bone disease (MBD) occurs if a tortoise has abnormal calcium, phosphorus, and vitamin D3 levels, caused by a poor diet or incorrect environment (lack of UV-B, for example). It is especially prevalent in tortoises where unnaturally high growth rates occur. The reasons for this are fairly simple in some ways, but rather complex in others, however, at it’s most basic it is very difficult to ensure that dense and strong bone is generated, especially on captive diets, during sustained periods of rapid growth. This is illustrated very clearly here, where we compare two plastron sections:
Left: Plastron from captive-raised tortoise on a highly digestible, relatively calcium-deficient diet that promoted excessive growth rates. Right: Plastron from a healthy wild example of similar size and age.
For this reason metabolic bone disease is most commonly seen in young, rapidly growing animals, though extended periods of deficiency can cause even established adults to develop problems over time.
The effects of metabolic bone disease are devastating, and normally, are irrevisible. Some examples of what this means in practice are shown here.
There are two primary factors involved in promoting unnaturally, and unhealthy, rates of growth in captive tortoises.
1) Digestibility of the diet
Highly digestible, high energy diets inevitably promote rapid growth. This property is widely exploited in commercial animal feeds. It applies not just to tortoises but other animals too. Captive Marmoset monkeys and Green Iguanas for example are also highly susceptible to developing vitamin-D related rickets and relative calcium deficiencies if subjected to rapid growth regimes. Arid habitat tortoises are adapted to function optimally on diets of very low digestibility: coarse, ultra-high fibre plant stems and arid-habitat, drought-resistant plant material for example. In the case of Testudo species, only for very short periods throughout an entire 12-month cycle are they able to access lush, fresh, green and more digestible grazes. These two ‘flushes’ of new vegetation occur in early spring, and following the autumn rains. Even this is a low digestible diet compared to typical, carbohydrate-rich captive diets. Some quite recent research (2022) looked at the effects of fibre content, dietary digestibility, growth and bone health in Chelonoidis carbonaria (the Redfoot tortoise). The general findings were as follows (the most critical observations are highlighted in red):
Fibre content and digestibility efficiencies are negatively correlated in tortoises (e.g., high fibre diets result in lower digestible efficiency and slower, more even growth).
Diets with low fibre content and rich in starch are related to accelerated growth.
Accelerated growth is linked with lack of proper bone mineralisation (MBD).
A high fibre diet produced lower mass-specific intake of digestible DM, Da, and growth rate.
Animals fed with a high starch diet presented lower bone mass content and density.
These are highly important findings and confirm exactly what the Tortoise Trust has been saying for many years. Highly digestible starch-rich diets a) Promote high growth rates and b) Result in poor bone density.
There are of course, other factors implicated in generating excess growth. In addition to the digestibility of the diet, the amount of food consumed over a 12-month cycle is key among these.
2) Annual feeding cycles
Tortoises from temperate climates do not consume food each and every day, all year round. Even tortoises from tropical climates experience some days when the weather is not conducive to feeding. In some cases these ‘non-feeding’ periods are very extended indeed. For example, Russian tortoises (Testudo horsfieldii) might only be active in the wild for a total of 90 days out of 365. Yet, in captivity, these same animals are often kept in controlled environments and are fed every day (and usually on totally unsuitable diets that contribute to excessive growth in their own right). As we noted in our article on Russian tortoises "Because this species is only active for such a short period every year, it is 'programmed' to eat as much as possible during that short period in order to build up reserves to survive the 'barren' and innactive remainder (the majority) of the year". In the wild that is a very good strategy and helps them to survive. In captivity with an endless supply of food continually offered, it backfires badly.
It is therefore no surprise at all that there is an incredibly high incidence of unhealthy, excess growth and severe metabolic bone disease observed in the vast majority of individuals of this species kept in captivity.
Other members of the Testudo group may not be quite as extreme in terms of limited activity periods as this, but when we look at the combined effects of brumation (hibernation), aestivation (summer dormancy) and randomised days when weather conditions are not conducive to activity, we find that these tortoises often spend more of the year inactive and not feeding than they do active and feeding. Again, in captivity, many keepers do not allow natural brumation, very few provide facilities for aestivation, and on days with unseasonable cold weather, for example, the reaction of many keepers is to immediately bring the animals indoors under a heat lamp to encourage continous feeding! The net effect is that very often these tortoises are over-fed to a massive extent in quantity terms compared to their counterparts in the wild. This too is then translated into unnaturally rapid high growth rates and consequently, into a very high incidence of metabolic bone disease and other related problems such as fatty infiltration of internal organs, and renal stress. Take a look at these charts. They indicate ‘feeding days’ vs. ‘non-feeding days’ for two representative species: Testudo horsfieldii and Testudo graeca graeca in the wild.
Typical activity and feeding days of Testudo horsfieldii in the wild.
Typical activity/feeding days of Testudo graeca graeca in the wild.
These are, of course, variable and do depend upon geographical location and general variables due to local weather conditions, but they do give a fair, typical approximation of the vast differences between food intake in the wild over a 12-month period compared to the expectations and totally artificial forced near-constant activity and feeding days so typical of these same species in captivity.
Typical percentage of active/feeding days of Testudo graeca maintained in a controlled vivarium environment.
Typical activity/feeding days of Testudo graeca housed in a mainly outdoor environment with some supplemental light and heat in Northern Europe where brumation (but not aestivation) is permitted.
Combine this with the previously-described differences in digestibility and energy between the wild diets and captive diets, and it is very clear just why ‘supercharged growth syndrome’ is such a major problem for captive tortoises.
By contrast, the combination of fewer days of activity and feeding, plus the much lower digestibility of the wild diet results in far slower rates of growth in wild tortoises. At the same time, the bone density and strength is outstanding and the shell development is perfectly smooth and even.
Slow growth evident in a wild, male Testudo graeca graeca at the end of the spring feeding cycle, just prior to entering aestivation.
It is important to recognise that this perfectly smooth growth is achieved in extremely arid, desert-like habitats and without any kind of access whatever to microclimates providing continual 'high humidity'. That notion (widely propagated on uneducated 'tortoise keeper' forums and social media groups) is complete nonsense.
Because it is such a widespread myth, it is important to understand what is really happening, and to understand the links between bone growth, keratin and humidity. We have explained it all at great length elsewhere, but the physiology of 'pyramiding' is quite complex on one hand, quite simple on the other. The outer scutes are keratin. This is hygroscopic. It is softer wet than when dry. When dry, it is an incredibly strong, resistant material. Chelonia are unique in having their skeleton (the carapace) surrounded by keratin. The keratin on tortoises (not on aquatic turtles) also has a unique mode of growth (cell proliferation) that places specific stresses upon the underlying bone. This leads to 'upwards' forces being applied continually as the animal grows. If the bone is weak - it deforms in accordance with these forces. Hence: 'pyramiding'. It is important to note that this is like a 'battle of strength' between the underlying bone and the overlying keratin. Many things affect this, including bone density, growth rates, keratin thickness and keratin hydration status. All of these things are involved. It is also really important to understand that a lack of 'pyramiding' is not by any means the sole criteria for healthy growth. You can have perfectly 'smooth' tortoises with disastrously deficient bone density, for example. Interior muscular forces also affect shell shape for the same reasons, with classic examples being depressed pelvic regions.
Many of these keepers rely upon continual levels of super high (80-90%) humidity to effectively soften and weaken the keratin so that it does not exert the same stresses that dry keratin exerts on the underlying bone despite dangerously high growth rates.
To the extent that this prevents visible 'pyramiding' - it works.
However, this ignores several critical things. The first is that this is a totally unnatural method that bears no relationship whatever to actual conditions in nature. Another is that ir merely prevents weakened, poor density bone from being visibly deformed by keratin stresses. It does nothing at all to prevent poor density bone from ocurring in the first place. It is rather like papering over cracks in a wall. It might look better superficially, but the real problem remains. Finally, tortoises manage perfect growth in the wild without this kind of bizarre approach. There is something seriously wrong when keepers are subjecting arid habitat and desert species to conditions even more damp and humid than would be experienced by true rainforest dwellers.....
Keratin, hard keratin, exists for a reason on tortoises. It is highly protective and it also helps to reduce internal fluid losses via evapouration. If we soften and degrade it (leaving it far more suseptible to fungal diseases in the process), then we are undermining the animal's natural defences.
On the correct diet, and in environmental conditions similar to that encountered in the wild, perfectly good growth in captivity is entirely achievable. This is possibly by controlling growth rates, ensuring a safe calcium-phosphorous balance, and by provision of adequate UV-B.
Perfect smooth, strong growth in a wild female Testudo graeca graeca in an extremely arid habitat: No 'humid hides'. Just a very high calcium content, super-high fibre diet and optimal UV-B.
In Practice
How do we prevent excess growth rates in captivity? The first thing is to learn to recognise the (very obvious) signs that it is happening. There are some very clear illustrated examples of this in our article on Russian tortoises (but note that this applies to ALL species). There are several ways that we can influence this. With a brumating (hibernating) species - let it do what it does in the wild. You will immediately effectively 'remove' at least 3 months, or 25% of 'feeding days' from the activity cycle. That alone will have a major effect upon annual growth. Achieving aestivation in captivity is also possible, but not everyone will have the necessary facilities. We used a large plastic polytunnel. Tortoises buried down into the dry substrate there through the heat of summer, only emerging again in early autumn. Our 'Climate Frame' design can achieve similar results, but this will depend on exactly how it is set up and your location. If this is done, however, you then 'lose' another 60-90 'feeding days' on average. That too will have a big impact upon the annual growth rate.
One very common mistake is to assume that tortoises from temperate habitats must be kept 'warm' continually, even overnight. This is entirely false. We recently studied wild Testudo hermanni hermanni and recorded overnight temperatures in the habitat of 2 degrees Celsius. Sometimes it gets even lower than that. This overnight temperature reduction is actually important. It slows up the metabolism and allows for the fermentation-based digestive system to avoid running at 'full speed' around the clock. That is another contributory factor to excess growth rates and consequent MBD. Another recent study (2016) confirmed that excess overnight heat for Centrochelys sulcata (African Spurred tortoise) directly correlated with both higher growth rates and an increased degree of carapacial deformity.
Some keepers also only feed once every 48 hours. That too will have a very large impact with growth rates and is a method that also works very well with non-brumating species such as those from tropical zones (even if the tortoise is active all year, this instantly reduces feeding days and food intake by 50%). Provided they are fed an adequate amount every two days, and their body mass is monitored carefully, this is a perfectly viable approach. For tortoises living in outdoor enclosures planted with edible graze, there is no need to interfer here, as typically, they self-regulate very well and do experience non-feeding days due to weather effects. Tortoises take quite a while to digest what they have eaten and breaks from daily feeding causes no harm whatever. By far the worst cases of overfeeding and excess growth in any event are invariably found in tortoises kept in indoor enclosures with artificial light and heat. Far more harm is done through overfeeding. You can, even here, for example, provide some 'quiet days' , just as happens in the wild. Not every day is 'perfect weather', even in the natural habitat.
Finally, be guided by the natural diet. Avoid over-processed 'commercial' foods which are often packed with highly digestible and grossly unsuitable ingredients.
Many of these 'diets' also include probiotics to further increase digestibility. This is the exact opposite of what is really needed. Try to provide a diet as close as possible to that in the wild, and also take note of seasonal fluctuations in both digestibility and availability.
One approach that that can also help is to get the fibre content super-high. This would be much closer to a wild diet, and is far, far less digestible than fresh weeds, and certainly fresh 'salad' items. It 'bulks them up' internally so they do not tend to feel so much like eating constantly. Wild diet fibre intake is typically 35%+ compared to an average captive diet of <15%. This alone can make quite a difference. In Europe there is a product from Agrobs called 'Testudo Fibre' that works extremely well for this. It has no artificial additives, no added maize starches or other cereal by-products (which do the exact opposite of what is needed) and can be fed both 'wet' and dry.
By a combination of these approaches, excellent healthy growth at near-natural rates can be achieved.
References and Further Reading
Mark L. Heinrich, Kaleb K. Heinrich (2016) Effect of Supplemental Heat in Captive African Leopard Tortoises (Stigmochelys pardalis) and Spurred Tortoises (CENTROCHELYS sulcata) on Growth Rate and Carapacial Scute Pyramiding,Journal of Exotic Pet Medicine, Volume 25, Issue 1.
Pierina Mendoza, Camila Furuta, Beatriz Garcia, Lucas A. Zena, Silvana Artoni, Ellen S. Dierenfeld, Kênia C. Bícego, Aulus C. Carciofi (2002), Starch and fiber intake effects on energy metabolism, growth, and carapacial scute pyramiding of red-footed tortoise hatchlings (Chelonoidis carbonaria), Comparative Biochemistry and Physiology: Molecular & Integrative Physiology, Volume 265, 2022.
Ragna Franz, Jürgen Hummel, Dennis W.H. Müller, Martin Bauert, Jean-Michel Hatt, Marcus Clauss (2011) Herbivorous reptiles and body mass: Effects on food intake, digesta retention, digestibility and gut capacity, and a comparison with mammals. Comparative Biochemistry and Physiology: Molecular & Integrative Physiology, Volume 158.
(c) 2024 The Tortoise Trust/A. C. Highfield
As usual a great read