Understanding Pyramidal Growth Syndrome (PGS) in Redfoot Tortoises
World Chelonian Trust Newsletter, Vol. 3, No. 1
[Editor's note: Used with permission.]
Pyramiding is the term given to an abnormality in which the scutes of the carapace have a stacked, conical appearance. With few exceptions the severe pyramiding of scutes is a condition found primarily in captive Redfoots, and is more prevalent among those tortoises raised indoors. Even ‘ranch-raised’ Redfoots, grown to legally exportable size, often exhibit a slight degree of PGS. The distorted appearance is something of a stigma to tortoise keepers, and as such is the topic of much discussion. PGS is a visible sign that something has not gone right in the process of growth and development. Aside from appearances, other effects or conditions are poorly understood; tortoises with PGS may continue to grow, reproduce, and seemingly thrive. On the other hand, PGS is often a visible symptom of metabolic bone disease, which is reason enough for keepers to take the issue seriously.
To understand pyramidal growth syndrome, we have to understand the processes underlying shell growth. We must also examine diet and natural history for contributing factors. It is also important to know what Redfoot shells look like under normal conditions- more than one new tortoise keeper has been shocked to discover that stacked scutes are not the normal state of appearance.
Characteristics of normal appearance
In the wild, the shells of Redfoots typically have a smooth, continuous profile. The overall appearance varies somewhat according to region, climate, and diet; shells can be polished and smooth, or they can be slightly raised, with a faceted look to them (1). Growth rings, or annuli, are often evident on each scute, and represent a lateral extension of the scute along the outer edges. The sulci, or seams between the scutes, are usually narrow and shallow in depth. The plastron and bridges typically are worn and polished from the abrasions of plant material, and since Redfoots typically crawl into piles of debris, dense vegetation and animal burrows, the carapace often shows the same effects. This polishing of the scutes can partially obscure the annuli.
Shell growth characteristics
The tortoise shell is typically comprised of three layers of different materials: bony plates on the inside, horny scutes on the outside, with a thin layer of epithelial cells under the scutes. Although characterized as layers, they are not in isolation from each other; vitamin D3, produced in the epidermis via the action of sunlight, is passed into the body via the many blood vessels in the bony plates. Material necessary for scute growth migrate outwards in the same fashion.
During growth periods, all three layers expand laterally, each in concert with the other. New materials are added to the edges, although not equilaterally; depending on the location, new material may be added more on one side than others (2). The areolae, the original neonate scutes, tend to remain attached to the original bone underlying them (3). This anchoring of the natal scute and bone is an indicator of synchronous growth despite differences in material. While the scutes and epithelial layer are primarily derived from protein intake, bone growth primarily requires calcium, phosphorous, and trace minerals. The fact that the shell grows in synchrony, despite the differences in composition, is worth further consideration.
Normal scute growth characteristics
Turtle scutes are essentially the epidermal layer. The scutes are composed of a hard layer of keratin covering the bony plates of the shell. Beneath each scute is a layer of germinal tissue, the epithelium, which produces new scute material (4). During periods of growth, a new layer of keratin is applied to the entire underside of each scute. The new layer is very thin under the center of the scute and thickens towards the edges. This material is soft and plastics, and as it reached the seam and protrudes past the edge of the scutes, it flows upward, forming the new, expanded edge of the scute. The new layer bonds with the old edge and eventually hardens in place. As the scute grows, so does the epithelial layer underlying it.
Under normal conditions in the wild, when bone growth slows or stops, so does scute growth. When scute growth resumes, new material is not added to the last layer produced; once again a new layer of scute material is formed under the entire scute (4).
The original scutes present at hatching are referred to as areolae. In Redfoots the areolae are yellow or yellowish-brown in coloration. On the carapace, the new material added to each scute is heavily pigmented and eventually each areola becomes an isolated light spot on the darker carapace.
Deposition of new growth varies, depending on the location of the scute. This can be characterized as directional growth (2). In the case of vertebral scutes on the midline of the carapace, new growth is deposited evenly around all sides of the scute.
Costal scutes tend [to] have more new material on the lower side. For the marginal scutes around the edge of the carapace (and forming the bridge to the plastron), growth is more advanced along the upper sides. These variances affect the location of the areola within the scute; it lies in the center of the vertebrals, and towards the top on costals. Areolae lie on the lower edge of the marginal scutes, and along the outer edge in plastral scutes, Scutes on the plastron grow in several directions, but primarily towards the center seam that runs head to tail.
It may be possible to determine the approximate age of a wile Redfoot by counting the annuli (1). Annuli indicate periods of growth, and growth occurs during the wet season and slows or stops during the dry season. Growth is tied to nutrient abundance and is reflected in the width of annuli. Much like tree rings, annuli can be thicker in ‘good’ years, and thinner in ‘bad’ years. The age of captive-bred Redfoots cannot be determined by this same yardsticks; the annuli are often very thin and do not correspond to an annual cycle of growth.
Characteristics of abnormal scute growth
With PGS, the deposition of new scute material is altered somewhat. There is much less protrusion beyond the scute edge, and the new growth does not always rise to merge smoothly with the planar edge of the scute. It appears that much of the new material remains underneath the scute, and the scute does not expand laterally in size as normal: by comparison, pyramided scutes tend to be smaller in area (in terms of length and width) than normal scutes. In captivity, the patterns of seasonal growth are usually replaced with a state of constant growth, which means layer after layer of new material is continually added. Over time the scutes rise, taking on the familiar step-pyramid shape. The sulci can deepen and widen with each additional scute layer, but with severe pyramiding they lose all definition as a seam between the scutes. The patterns of directional growth do not seem to be disrupted by pyramiding.
The condition can start developing with the onset of neonate growth, and continue during the rapid growth typical of juveniles. If pyramiding ceases during the development, the visible effects will not disappear, although subsequent growth may smooth things over somewhat, Once a tortoise with PGS reaches adult size, the growth rate slows and the appearance of the shell is nearly immutable, Although severe pyramiding does not generally manifest itself in wild-caught adult tortoises that have been long-term captives, many of these animals exhibit a raising and thickening of the material around the perimeter of the scutes.
A missing factor behind PGS
Since pyramidal growth syndrome could manifest itself from the onset of neonatal growth, an imbalance in one or more growth factors was assumed to be responsible. Excess protein, overfeeding, calcium deficiency, low fiber diet, hydration, lack of exercise and lack of sunlight were all considered to be contributing factors (5, 6). Excessive protein intake received a great deal of attention, being associated with accelerated growth and as a factor in gross deformities in the shell, particularly in herbivorous species, Since the diets of wild herbivorous tortoises are normally low in protein, it made sense to associate PGE with the unnatural levels of dietary protein in captivity.
However, when tortoise keepers adjusted their husbandry, reducing dietary protein and playing close attention to other suspected factors, PGS continued to occur in captive-bred tortoises, although reduction in the severity of stacked scutes was reported in some instances. A number of keepers began to suspect humidity levels and a factor and some recent studies show high humidity to be a key factor in proper shell growth and development in Geochelone sulcata, the African Spurred Tortoise, as well as G. carbonaria, the Redfoot tortoise (7, 8). By providing moist microclimates in the enclosure, a number of keepers are now raising Redfoots and other tortoise normal shell appearances throughout growth and development (8).
Clues in the natural history
It may be easy to understand how low humidity could affect the growth of a tropical tortoise like the Redfoot, but how could it play a role in PGS with dry grassland species such as G. sulcata or G. pardalis? Why aren’t the shells of the wild dry-climate tortoises pyramided? Clearly, PGS is not normally occurring within wild populations, but the mechanism behind it is proving to be complex and rooted in the natural history. Even tortoises from dry environments manage to spend time in moist microclimates- animal burrows or burros they have escalated, ‘scrapes’, where the dry topsoil has been removed, in mud holes and shallow ponds, and in thick stands of vegetation, which tend to hold a higher level of humidity. While humidity is not an issue during the rainy season, Redfoot tortoises also readily use these types of humid microclimates during the dry season (9,10).
The natural history indicates that humidity is but one link in a complex web of factors controlled by the characteristics of the tropical climate and seasons. In the tropics, the season are characterized by the amount of rainfall, rather than temperature. Growth is accelerated during the rainy season, when the food supply is at its peak, and plants contain the most nutrients. During the drier months, plants retain fiber content, while nutritional levels decline, and so growth slows or stops. This season cycle affects growth and development, from beginning when a tortoise emerges from the egg.
Juvenile Redfoots tens to spend much of their time burrowed in leaf litter, in thick vegetation or treefalls, or in animal burrows. In this moist microclimate they pursue the animal and vegetable elements of their diet. During the drier winter months, the nutritional value of plants is greatly reduced; consequently there is little or no growth in Redfoots during these lean months, and their humid microhabitat slowly dried out. The return of the rainy season brings nutrient-rich new plant growth, along with flowers and ripening fruit. Growth resumes, while humidity levels rise, and the substrate contains moisture once again. The record of this cycle is captured in the annuli on the tortoise shell.
How is humidity involved?
In captivity, the normal wet and dry cycles and periods of growth and rest are disrupted. Captive Redfoots are typically kept in drier conditions, on flat surfaces of substrate that do not retain moisture. The low humidity may mimic the dry season, but there is no accompanying reduction of quantity or quality of food. In essence, the tortoises are being kept in a dry season environment, but are fed a wet season diet. Consequently growth continues, and it is under these abnormal conditions that humidity emerges as a factor.
The actual mechanism remains to be determined. The abnormal pyramidal development has been hypothesized to be secondary to the drying of the tissue underlying the sulci, with eventual abnormal ossification (7). The seams between scutes may then become fixed in place as a result, and new growth cannot be deposited laterally along the scute edges and is deposited on the scute under-surfaces instead. This may account for the slightly smaller size (in length and width) of stacked scutes. Under these drier conditions, the new layers of keratin may be less fluid and plastic than usual, and so may not spread laterally in the normal fashion. Mass may also be an issue, relating to the abnormal drying of tissue: small tortoises tend to dehydrate much more quickly than large tortoises.
Can PGS be simply attributed to a change in how new scute material is deposited? While studies decisively identified humidity levels as a factor, they did not eliminate the role of dietary protein, nor the consequences of accelerated growth. Under study conditions, Redfoot tortoises raised in high humidity and given a high protein diet continued to develop slight pyramiding (7). In the U.S. Virgin Islands (St. John), comparisons of wild Redfoots to those raised in outdoor enclosures yielded similar results. Wild Redfoots on the island exhibited normal shell growth, while captive tortoises, fed a more restrictive diet that included cat food or commercial tortoise food, developed pyramided scutes (11).
Although it is not clear whether the deposited layers of keratin are thicker in stacked scutes, it is widely accepted that an abnormal amount of scute material has been produced. In a physical comparison, pyramided carapaces have more surface area than smooth carapaces of equal size. How is this to be interpreted? Has scute growth exceeded normal bone growth, or has bone growth lagged behind? With many tortoises suffering from metabolic bone disease, scute growth continues in stacked fashion, although the scutes are often weak and porous and can sometimes deteriorate and collapse in the center.
What is the condition of the bone underneath pyramided scutes? The tendency to focus on what is visible may take attention away from problems that are developing beneath the skin. The shell in its entirely can be affected by other abnormal conditions in captivity in addition to low humidity. Bone mineralization and growth can be affected by a variety of deficiencies- calcium, vitamin D3, sunlight, exercise, etc.- in a variety of combinations. Calcium absorption is a much more complicated process than the metabolizing of protein and may lag behind under deficient conditions and in cases of overfeeding or excessive dietary protein (5). As a result, the slower bone mineralization may disrupt the synchronous growth of the shell.
If diet, exposure to sunlight, calcium uptake, and other growth factors are ignored, can a healthy tortoise be produced by merely paying attention to humidity? Probably not, but the question brings to light the emphasis placed on appearance, and serves as a reminder that assumptions about heath should not be based on external characteristics.
Proper humidity levels are not a cure-all for proper growth and development of the shell. The practices recommended by workers in the field of tortoise husbandry remain valid and should be followed. The factors behind proper growth and development should be viewed as a complex, interdependent matrix; an imbalance in one factor affects all others. All aspects of captive husbandry should receive equal attention.
Appendix of contributing factors
Tortoises require exposure to the ultraviolet spectrum in sunlight to manufacture vitamin D3, which in turn is necessary for metabolizing calcium. Since reptiles are unable to store vitamin D3, regular exposure to sunlight is essential to proper body functions and bone growth. This can be an issue for Redfoots raised completely indoors; commercial UV bulbs are a poor substitute, as are vitamin D3 supplements. Without adequate exposure to sunlight, calcium deficiency occurs, even when a calcium-rich diet and supplementation are provided. Calcium is inaccessible without vitamin D3.
Calcium is metabolized and absorbed in the intestine, and is pooled for use in the blood plasma. Adequate levels of plasma calcium are vital for all regular biochemical functions with all animals, In the event of a deficiency in plasma calcium, bone mineralization will cease, and the skeleton will release calcium back into the bloodstream for more critical needs. This condition is the precursor to metabolic bone disease. The importance of calcium should not be underestimated; wild Redfoots actively seek out and consume plants with high calcium concentrations, despite their otherwise low biologic value (10). Neonate Redfoots are especially vulnerable to deficiencies in calcium, as the plastral bones are just starting to knit together. Adult females require additional calcium for egg development.
Necessary for proper scute growth. Even in tortoises from dry climates. Providing very high humidity levels for an entire enclosure is impractical and may lead to respiratory issues, and moss or fungus may be an unwelcome side effect. The practical method is to create a humid microclimate within the hide-box or hide-house, which Redfoots use as a sleeping and resting place. The humidity inside a hide house or hide box can be raised by using thick layers of unmilled sphagnum moss, or by attaching a sponge to the underside of the top.
Water is the most vital of all nutrients, essential to all biochemical processes, Redfoot tortoises excrete liquid urine and need to drink fresh water nearly every day. Dehydration affects all soft tissues, including the nasal tissues and the eyes, and may also impact the tissues beneath the scutes. Dehydration also impairs renal function, and a high protein diet may make matters worse (6). Fresh water in a shallow pan or dish should be provided at all times; Redfoots also enjoy soaking in shallow water on a regular basis.
Wild Redfoots have shown growth rates of 2.4cm (1 in) each year until a length of 30cm (11.8 in) is reached; in captivity, this rate is usually accelerated (1). There is a human prejudice that associates fast growth and large size with healthy and vitality, and this can be damaging when applied to slow-growing ectotherms like tortoises. Pyramiding occurs primarily in sub-adult captive tortoises and this may be linked in part to their fast rate of growth. A combination of accelerated growth and lack of proper bone mineralization can make the bones of the shell porous and spongiform (5, 6). Under these unfavorable conditions, it appears that the synchronous growth of bone and scute attempts to continue, and the result is a layer of weak, less dense bone material that does not provide strong shell integrity.
A factor contributing to accelerated growth. ‘More is better’ is a human prejudice that is not necessarily compatible with ectotherms like tortoises. Redfoots have a ‘windfall’ approach to eating- if large quantities of food are available, then eat as much as possible, because there may be no food tomorrow. This is an excellent survival mechanism in nature, but in captivity, each day brings another windfall of food.
Low fiber diets are considered to be a factor for accelerated growth in tortoises (5, 6). The fibrous material in plants are not easily or completely digested as it passes through the digestive tract. Foods low in fiber are more completely digested, and may contribute to accelerated growth when coupled with overfeeding.
Excessive protein intake is another factor contributing to accelerated growth, It is not known what the ‘proper’ levels of protein intake are for growing Redfoots, and differences in how the protein content of foods is measured (dry measure versus included water content) can be confusing and misleading, The diet of juvenile wild Redfoots is poorly understood; it is assumed that animal and plant proteins comprise a significant portions, but not the bulk of the diet.
Many keepers rely solely on prepared foods as a source for proteins, which are typically derived from cereal grains, primarily wheat, corn, rice or soybeans. These grains are not a part of the natural diet of Redfoots, and there is a multitude of reasons as to why they should not be relied upon as a single source for protein. They are deficient in calcium and rich in phosphorous and magnesium, which can retard the absorption of calcium in the gastrointestinal tract. Cereal proteins are typically low in certain essential amino acids such as lysine, methionine, leucine, and tryptophan, which gives them a lower biologic value (expression of the relationship between quantity absorbed and quantity utilized) (12, 13). By comparison, animal proteins have a much higher biologic value, and contain a number of complete proteins not found in plants.
Lack of exercise
With the exception of large adult males, Redfoots are active foragers throughout the year (10). In captivity, they are often kept in small enclosures and are not given enough opportunities for exercise. Exercise aids appetite and adds strength to bone; protein is burned like carbohydrates for energy and is used to build and maintain muscle.Natural abrasion
There is little or no discussion about the effects of mechanical wear on the shell. Wild Redfoots crawl into burrows, logs, piles of debris, and thick tangles of debris, which abrade the plastron and carapace alike. Often the result is a smooth, polished appearance to the scutes. Kept in open enclosures, the carapaces of captive Redfoots do not show this type of wear, and even the plastral scutes may not be smooth. While natural abrasion may not be a direct factor in PRG, it does contribute to the overall appearance of the tortoise.
Revised 11-28-2011 (C) Mike Pingleton