The Cause of Pyramiding Deformity in Tortoises
- tortoisetrust
- 2 hours ago
- 19 min read
A summary of a lecture given to the Sociedad Herpetologica Velenciana Congreso Tortugas on October 30 2010 with additional links and updated practical advice.
A. C . Highfield - Tortoise Trust
English text first published online Nov 1 2010.
We are republishing this here with additional comments by request as it is by far the most complete explanation of the true causes of 'pyramiding' currently available. Some of it is necessarily quite complex and text intensive, but is essential reading if you really want to understand the mechanisms involved. We have added a brief summary at the end if you want to skip the detail (though we strongly recommend reading it in full).
What follows is a brief outline of the major findings of our work in establishing the precise physical and biological mechanisms involved in 'Pyramid Growth Syndrome'. This has been a very complex and demanding piece of research. This is a problem we have addressed continually since around 1990, but from around 2004 we intensified efforts to find some answers. In the course of this, we have conducted extensive fieldwork, have used diagnostic image techniques, and have conducted multiple post-mortem and laboratory examinations of both normal and affected animals. I would stress that at no time was any animal killed or hurt in this process. We relied exclusively upon ‘natural’ casualties from other causes. Key objectives were to look at competing theories, to separate those that had some factual basis from those based upon incomplete or false data, and to conclusively establish the exact mechanisms involved in producing the effect. A further objective was to begin to develop some practical guidelines whereby the problem could be alleviated or prevented.
Two key theories have dominated discussions on this subject:
The abnormal growth is caused by incorrect diet, specifically by high protein, high energy and calcium deficient diets;
The abnormal growth is caused by lack of humidity or by general dehydration or both.
As we shall see, all of these factors play a critical role, with the exception of general dehydration.
One of the major problems with what we will call 'the humidity theory' has been a lack of any biologically credible explanation for it. Some suggestions have been made, but these require us to abandon established physiological science, and grasp at vague concepts of “cellular dehydration” (a condition unknown to science in living organisms) and “tissue collapse” (another pseudo-scientific concept that has no basis in fact) .
The source of most of this confusion and misinformation can be directly linked to one spectacularly poorly conducted and error-filled piece of research that was published in 2003: "Influence of environmental humidity and dietary protein on pyramidal growth of carapaces in African Spurred tortoises (Geochelone sulcata" by Weisner & Iben.
Unfortunately this paper became widely cited by tortoise keepers and was uncritically accepted as fact when even a cursory examination of the methodology used and of the bizarre claims it includes should have set alarm bells ringing immediately. So should the fact that despite constantly referencing various levels of relative humidity, there is absolutely no information on the temperatures involved! This is a truly staggering oversight that renders any 'results' null and void at the outset as simply citing "relative humidity" in the complete absence of temperature data is entirely meaningless. To understand why this is so please see our practical guide "Understanding Humidity for Tortoise Keepers".
For a complete rebuttal and critical analysis of that particular paper see "Pyramiding: Misunderstandings, Misrepresentations and some very strange research methods".
Other theories along the same lines have proved similarly unviable. However, it was clear that many keepers were observing some kind of effect linked to various levels of relative humidity and heat. One of our most important objectives was to try to understand what was really happening.
The first thing to point out is that chelonia are constructed from exactly the same materials as many other animals. Their skeleton, though different in form, is materially virtually identical to that of other species. In a similar manner, the outer keratin scutes are comprised of primarily beta-keratin with some alpha-keratin cells also present. These are well studied materials. What is unique in tortoises (and turtles) is the way in which the skeleton surrounds the body, and the extensive covering of the keratin layer immediately above the skeletal tissue and closely connected to it. Consequently, any disruption of either of these layers will have a profound effect.
If we first examine the bony skeleton, we note that this is vulnerable to exactly the same diseases of deficiency or excess as that of a dog, a horse or a human being. There is absolutely nothing unusual or unique in how a tortoise skeleton develops and is sustained. The process is entirely normal and is completely consistent with established biological and nutritional knowledge.
Suggestions commonly seen that the bone development of chelonia are unique, and are not related to other animals are quite simply entirely false. There is no fundamental difference. The biology has been well understood since 1922 when the role of vitamin D in bone development was finally identified. Later, the role of UV-B from unfiltered sunlight was further discovered as a vital part of bone health in captive reptiles. We discuss this in depth in our other article "Tortoise Shell Deformities: A View from the Inside" which should be studied alongside the current text.
To develop normally, the skeleton requires a supply (carried by the blood, and obtained from the food intake) of essential bone-building trace elements, principally calcium and phosphorus. These trace elements need to be in the correct quantities and proportions. In addition, in order to transport and utilise these materials, the animal’s vitamin-D3 metabolism must also function correctly. Any failure or imbalance, ether of the supply of 'raw materials' or of the transport (D3) mechanism will result in bone formation that lacks normal density and strength.
In reptiles, this condition is widely recognised by keepers as “MBD” or Metabolic Bone Disease. In humans and in other animals it manifests in a range of similar conditions variously known as osteoporosis, fibrous osteodystrophy or rickets.
Bone that lacks adequate density is highly vulnerable to physical stresses and is liable to deformity as a result of conflicting physical forces. This is perhaps best known in humans as the condition called 'Rickets' where the long bones of the legs are bowed and bent by a combination of the effect of gravity (weight) and the pull of muscles.
If we examine the structure of bones affected by Rickets, we find a remarkably similar condition to that seen in tortoises suffering from MBD and so-called 'Pyramiding'. Instead of being hard, thin and dense, the bones are fibrous, thick and porous.
Such bones are extremely easy to deform under conditions of constant stress. In a tortoise, one cause of stress is that of the attached (and very powerful) muscles of the limbs. It is not unusual to see tortoises that suffer from MBD or Pyramiding to also display a depressed pelvic region. The cause of that is muscular tension. Such animals may also display a ‘bulging’ effect at the upper body - caused by lung expansion and contraction and the muscles involved in that process. It is during phases of growth that bone is most vulnerable to such effects as it is at its most plastic. The more rapid the growth is, the greater the potential for absolute or relative deficiencies to occur. This is a well known relationship and affects all animals, and humans too. It can be extremely challenging to obtain good bone density in captive situations on artificial diets. Herbivores are especially sensitive. On greatly accelerated growth regimes achieving normal, healthy bone density is extraordinarily difficult. In fact, so much so that to date I have never seen it. 100% of the animals we have examined that were raised on high growth regimes have MBD present to some extent, whether or not they displayed obvious external symptoms. This is relatively easy to demonstrate by dissecting deceased specimens, or by comparing x-rays of wild tortoises to captive raised examples.
Every tortoise breeder will know that as a hatchling emerges, the bones are extremely soft and flexible. They gradually harden up over the following days, months and years. However, they are never completely fixed, except in extreme old age. They continue to remain sensitive to stresses applied over an extended period. Even relatively slight tensions, applied continually, can have a substantial effect.
A key area where tortoises and most turtles differ from other animals is, as we have noted, the fact that they are largely surrounded by their skeletal structure. The bony, internal layer is overlaid by keratin shields or scutes. Keratin is an interesting material with many unusual properties. It is one of the strongest and toughest biological materials known to science. It is also hygroscopic, and loses and absorbs moisture in an effort to reach equilibrium with the environment. This effect is known to everyone as after a hot bath or shower our fingernails are soft and pliable. After a day hiking in the desert, they are hard and brittle.
Both Alpha and Beta keratins have been studied extensively, and we know quite a lot about how they perform at differing levels of moisture content and in different levels of ambient humidity. One very important feature is the way in which they gain and lose stiffness as they respond to external humidity. These changes are dramatic. They can be measured and quantified. At levels of relative humidity above 80% and when combined with heat, e.g. 30 Celsius, , scute keratin possess only a fraction of the strength and durability that it does at 50% RH. Such changes can be measured and quantified using criteria such as Young’s Modulus (a property of a material that specifies how easily it can stretch and deform). At sustained levels of 90-100% RH and at high temperatures it is essentially saturated as it accumulates water molecules rapidly.
It becomes extremely soft and pliable under such conditions, exerting almost no stress on the underlying skeleton. At the opposite extreme of low humidity, however (below approximately 25% at 30 Celsius) it loses water molecules and becomes very stiff and resistant. At such levels it is exerting a very substantial physical force on the bone beneath. We know from earlier tests we conducted with tortoise vivarium design, that many of these create extremely dry conditions, with sustained relative humidities as low as 12% at typical .basking temperatures. More recent tests have also shown that directly under basking (heat) lamps very low, very localised conditions of humidity well below 20% can occur immediately adjacent to the surface of the scutes of the carapace. This has a profound drying effect, increasing keratin stiffness, driving out water molecules, and at the same time increasing stress forces upon the underlying bony skeleton. It should be noted that there is a vast difference in drying effect between outdoor exposure to solar radiant heat and indoor exposure under a heat lamp. The latter has far more activity upon water molecules due to differences in their infrared spectrum.
This is one reason why the very worst examples of 'pyramided' tortoises that we encounter are typically those that have been raised indoors or under artificial basking lamps. It is rare indeed to see such severe deformities in tortoises raised in outdoor habitats.
It is critically important to address one very common piece of misinformation in this context. It has been claimed that juvenile tortoises (for example, Testudo graeca) spend most of their time in the wild in “humid” microclimates where ambient conditions are in the range of 90-100% RH. This is completely false. One part of our study involved taking many thousands of measurements in the natural habitat to establish the actual conditions experienced. Our methodology involved the use of miniature automatic data loggers that recorded both temperature and humidity with a very high degree of precision. We took recordings over a complete 12-month cycle in several key habitats.
We also attached loggers to tortoises and recovered them later to collect the data. In total, we collected 18,000 data points detailing humidity alone. What we found - in brief - was that juvenile tortoises were not experiencing substantially different levels of humidity than adults.
While it is perfectly true that tortoises make extensive use of selected microclimates, the levels recorded in these were in the range of 34-60% RH at prevailing ambient temperatures. The sole occasions when levels in excess of 90% were recorded were during thunderstorms, in the early morning at the dew point was reached and during episodes of rain. In the semi-arid environments of Almeria and Murcia (which are very similar to those found in most of North Africa) rainfall is not a regular occurrence, even during peak periods of tortoise activity.
In total, we found that tortoises were only exposed to levels of humidity that could reasonably be described at “high” (80%>) for 2% of the total time recorded. While foraging humidity could be as low as 20%, but this was followed by retreat into vegetative microclimates where typical levels averaged well below <50%. Measurements were taken from tortoises in all activity phases, throughout multiple 12-month cycles and included those buried in scrapes.
We have provided very full and detailed field reports that describe these conditions in great depth:
This data accords with that previously recorded (though not in such detail) in Morocco, Turkey and Tunisia. Other workers have also conducted extensive humidity data collection from tortoise burrows of the Desert tortoise, in North America. This data also fails to reveal any evidence whatsoever of the availability of “humid” hides offering relative humidities of “90-100%”. In fact, levels in the arid desert regions of Arizona occupied by Gopherus agassizii are even lower than those we recorded here in Almeria and Murcia. If indeed (as claimed) the main reason why wild tortoises in arid regions do not suffer from “pyramiding” is because they make extensive use of “caves” or “vegetation” offering “90-100% RH” retreats then all of our local Testudo graeca graeca in Spain would be very lumpy and deformed indeed, because no such facilities exist. This is a semi-arid arid habitat with some of the lowest annual rainfall in Europe, with an average precipitation of just 226mm per year (the UK receives almost 600mm).
We have reported separately upon these unfounded "humid hide" claims: The Tortoise Myth-Busters: Episode 6
Important note: We have never disputed that tortoises make extensive use of microclimates. Indeed, we published an article "Understanding microclimates in captivity" as far back as the early 1990's. This stressed that "Microclimates are used by many reptiles and amphibians to sustain themselves in otherwise unfavourable environments, and to regulate body temperature and water balance. Some well-known examples of microclimate utilisation include the burrows used by arid habitat tortoises and lizards, such as Desert tortoises (Gopherus agassizii) and Spiny-tailed lizards (Uromastyx species), or the behaviour of certain toads that encase themselves in mud during the dry In each case, the animal seeks to protect itself from excessively high or low temperatures, and to prevent excessive loss of body fluids from respiration and evaporation that ultimately, would lead to death from dehydration."
The issue at stake here is what precisely is meant by "humid". We need to avoid subjective non-specific terms and instead rely upon objective data gathered in a reliable and accurate manner, preferably using data collected in the natural habitats using precision and calibrated instruments. .
I would also urge all keepers to exercise extreme caution in relying upon generalised “average” figures for relative humidity in tortoise habitats obtained from climate sites. These can create a very misleading impression indeed. The only meaningful, reliable data is that collected at the level occupied by tortoises (not several metres above ground) and in the precise microclimates used. There are massive differences in temperature and humidity at various altitudes, and also conditions inland can vary substantially from those closer to the coast. Tortoises tend to occupy very narrow, very specific biotypes. This needs to be understood when considering climatic data. Data based on an average of all habitats within a region or country is likely to be completely misleading and inappropriate. See our separate article: 'Can you rely upon general climate information to know what your tortoise needs?'
In fact, we recently had a very good demonstration of this when studying Centrochelys sulcata (the African Spurred tortoise) in the field in Senegal. This species occupies a very specific ecological niche within a very restricted range. The temperatures where they occurred were far higher than the 'general' meteorological conditions suggested, while ambient relative humidity was far lower (e.g, 15% at 40 Celsius) than coastal areas which were much more moderate (circa 31 Celsius @ 32% RH).
There is a further important feature of keratin that affects physical stress on the skeleton and the modes by which it proliferates in chelonia. There are two primary methods. Tortoises exclusively rely upon a mode of cell proliferation that deposits new material at the edges of the scute, resulting in the well-known 'tree ring' effect. Aquatic turtles mostly (not all) rely upon a mode where new growth occurs in a horizontal plane only, with new cells growing at an even rate beneath the older material. Many species of aquatic turtle lack 'historical growth rings' for this very reason. Eventually, the older scute is shed (usually entirely) to be replaced with the new, larger scute. In terrestrial tortoises, this pattern of shedding does not occur. The keratin builds up, in a vertical mode, continually.
This vertical and expansive mode of cell proliferation of itself creates an upwards force on the skeleton. Where there is concurrent MBD of any degree, the effect will be substantial. The bone will attempt to conform to the pattern of growth of the scute.
This is the primary mechanism involved in “pyramid” growth syndrome in tortoises and the main reason why it is not observed in those aquatic species that shed whole scutes.
It is further amplified in effect where certain conditions apply:
Where the keratin is excessively stiff as a result of very low humidity.
Where the keratin is unnaturally thickened.
Thickened keratin, with over-proliferation, is a common feature of every severe case of “pyramiding” observed to date. It can often be readily diagnosed by comparing the colour of the keratin to a wild, healthy specimen. In cases of over-proliferation, it is typically much denser and much darker. These animals tend to share some history in common. In the majority of cases, this includes being raised in vivarium systems, under heat lamps, and frequently deprived of adequate fluid intake. We have already noted that many vivarium systems produce incredibly low, sustained levels of ambient humidity, far below that experienced even by tortoises from the most arid habitats. The effect of an overhead heat lamp on a tortoise has been inadequately studied, but it certainly has a very powerful dehydrating influence. Tortoises kept in such conditions also tend to present with other health issues related to generalised dehydration: bladder stones, gout, and renal failure. All of these are associated with sub-optimal hydration. We also have a separate, in-depth article on the causes of bladder stones in tortoises.
One very interesting effect has been demonstrated in laboratory tests with chelonia. As they are subjected to extended periods of dehydration, the epidermis thickens in an attempt to reduce cutaneous evaporative losses. This affects the skin of the limbs, and in particular the proliferation of beta-keratin that comprises the horny scutes. As the animal is subjected to dehydration, the scute growth accelerates, becoming ever thicker. Bone growth however, does not accelerate at the same rate, producing a major differential. This thickened, dry keratin begins to exert an enormously amplified force upon the skeleton (which in such animals is typically of very poor density). This is one other very important reason why we tend to see particularly badly deformed animals that have been raised in conditions of sub-optimal humidity, especially those subjected to the intensely drying effects of heat lamps.
Such animals often also appear much darker than healthy, naturally raised examples, as is very obvious here from these two Astrochelys radiata (Radiated tortoises). The cause of this effect is greatly thickened keratin (this is also obvious on post-mortem samples).
Where accelerated growth (and typically MBD) meets dangerously drying artificial heat the conditions are ideal for producing gross distortions of the carapace due to the conflicting physical stresses of muscular tension and tension resulting from over-proliferation of the thickened keratin scutes.
A further important factor is that wild terrestrial tortoises are continually wearing and abrading excess keratin from the scutes in the course of normal life. Unlike turtles, they do not shed old keratin - they wear it away. They are abraded by coarse vegetation, by impact with rocks, by wind-born sand particles, and by the constant burying, digging and excavating they engage in. While estivating or hibernating they are not motionless. They move, surrounded by highly abrasive particles in the soil. Also, micro-organisms in the soil gradually degrade the outer surface of the scutes. As such, they are subject to continual wearing (and resulting thinning) of the scutes. In the vast majority of captive situations (and especially so in indoor maintenance) this factor is totally overlooked by keepers. One result is that the keratin continues to accumulate even if humidity is not an issue. Where very low humidity is also present, the effect is compounded.
The thicker (and dryer) the keratin, the worse the “pyramiding” becomes. This is not only a consequence of the keratin layer itself, but also of its powerful physical deforming effect on the skeleton immediately beneath.
Some keepers have mitigated these obvious symptoms by essentially “soaking” the animal at high ambient humidity (in the 90%+ range) and at elevated temperatures for long periods. The real effect of this is simply to soften the keratin and reduce stresses. This technique does nothing to address any underlying MBD (it just makes it much less obvious) and in addition it exposes the animal to a high risk of fungal and bacterial infections. The soft, wet keratin is highly vulnerable to such organisms. It lacks structural integrity and damages easily. While the visible 'pyramiding' may be reduced or eliminated by such extreme measures, this is not a very satisfactory answer. It is an artificial solution to an an entirely artificial problem.
If a proposed husbandry method requires us to resort to totally unnatural conditions (extended exposure to 90%+ RH for arid habitat tortoises) to solve a problem created by other totally unnatural conditions (sub-optimal humidity, dehydration and excess growth rates resulting in poor bone density) then I would suggest that something is seriously wrong. It is far preferable to address the fundamental causal issues and not to merely concentrate on trying suppress the most obvious symptoms, which is the sole result of such methods.
In this case, the issues that need to be addressed are:
Obtaining growth that results in comparable bone density to healthy wild examples. This should be tested by routine radiography. By obtaining healthy density maximum resistance to subsequent deformity is achieved.
To ensure that captive environments provide a suitable range of both humidity and temperatures. A safe and appropriate range should be established by reference to reliable data from the natural habitat of the species in question, not by guesswork or by reference to inappropriate and frequently misleading general climatic averages.
Looking again at captive enclosures to develop methods of allowing natural wear and tear of carapace keratin to occur, thus avoiding a continual build-up.
There are challenges in meeting these needs. It is very clear that the design of captive habitats needs to improve. Heat lamps do indeed assist in some ways, but from this study it is also clear they can have a very serious negative effect. Obtaining safe levels of ambient humidity is also not easy for keepers outside the natural range, who must rely on artificial enclosures. Obtaining high-grade bone density and sustainable rates of healthy growth are also very difficult in captive situations. Wild tortoises practice cyclic activity and feeding, with long periods of non-feeding and inactivity. The very nature of their intake also varies seasonally, especially in terms of moisture and fibre content. Practical solutions to these problems are not beyond the bounds of possibility however, and will represent a major step forward in chelonian husbandry. This is especially important in conservation breeding for eventual release or when propagating highly endangered species. It is extremely important that compromised animals must be avoided in such situations.
Quick Summary:
Tortoises and turtles are only unique in that their bony skeleton is almost entirely surrounded by hard, inflexible keratin. All other aspects of their physiology are essentially the same as for other reptiles.
Living bone is plastic and responds over time to physical stresses, including stresses caused by gravity and by muscular tensions. In the case of tortoises, a third major generator of such stress is the effect of the surrounding keratin upon the bony part of the carapace directly beneath it.
If the bone is weak and too soft, as in the case of animals with any of the various forms of metabolic bone disease, this is highly susceptible to being easily deformed by such stresses. This is well-known in mammals where the limb bones are deformed by gravity and muscular stresses resulting in the classic symptoms of rickets.
One very simple way to think of this is to look at it as a "battle of strength" between two layers of material. The bony carapace and the forces exterted by the keratin surrounding it and overlaying it. In nature, these materials develop in a balanced way. In many captive situations that balance is disturbed.
Keratin is softer and more pliable when humid, wet and warm and much stiffer and harder when dry. When saturated and pliable it exerts little stress upon the underlying carapace, but when very dry that stress increases enormously.
Terrestrial tortoises differ from most freshwater aquatic turtles in one critical respect: the way in which the keratin grows. In turtles new cells are added to the base of the scute on a single, flat plane. This is why turtles eventually shed whole scutes as they grow, which tortoises do not. Tortoises scutes grow entirely differently. New cells are added to the edges of the scutes. This is responsible for that 'tree ring' growth pattern. This, however, does result in an 'upward' pressure upon the scute, and in turn, upon the underlying bone. Hence, if the conditions of growth are out of balance, for example, if the underlying bone is weak, or if the keratin itself is too hard, thick or dry, then this is the direct cause of those scutes becoming deformed and raised in that typical 'pyramid' form.
The key to preventing such problems is to ensure healthy, strong bone growth through correct diet and to avoid causing excess stress or thickening in the overlying keratin by causing it to become unnaturally dry or excessively thick. You can indeed prevent obvious 'pyramiding' by keeping the tortoise excessively wet or humid, but this does absolutely nothing to address any underlying issues with poor bone density (indeed, it merely masks it), and in turn it greatly degrades the keratin reducing its intended protective qualities and makes it massively more susceptible to both fungal and bacterial infections.
Acknowledgement
I would like to express my thanks to the late Ed Pirog for many fascinating debates, discussions and indeed heated sometimes arguments on this topic over almost two decades. It is true to say that Ed was as persistent as I have been in trying to understand this problem. Ed had made some important observations on this issue, and also identified the keratin layer and both humidity, heat and hydration as playing an important role in a problem that has plagued keepers ever since captive breeding of tortoises became commonplace. It was, in part, due to Ed’s observations that I set out to examine the role and performance of keratin in different environmental conditions in as much detail as possible and it was these investigations that ultimately led to the results presented here for the first time.
As you can imagine, conducting genuinely original research like this takes a very long time to conduct (months and years), involves a great deal of travel, is very time consuming, and also requires the use of some very expensive equipment indeed. If you would like to see more of this, we really would appreciate it if you could make a donation or subscribe. It really helps. We have been established since 1984 and we continue to provide original research and reliable information to tortoise and turtle enthusiasts worldwide. We also have two excellent online courses available, one for beginners and new keepers and one for advanced and professional keepers. These cover some of the background science that is key to truly understanding and appreciating tortoises and turtles and are also extremely practical. We have taught in colleges and universities around the world, and have trained private enthusiasts, wildlife rangers and conservation staff for many years.