Understanding Pyramidal Growth Syndrome (PGS) in Redfoot Tortoises
By Mike Pingleton
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
scutes is a condition found primarily in captive Redfoots, and is more
prevalent among those tortoises raised indoors. Even ‘ranch-raised’
grown to legally exportable size, often exhibit a slight degree of PGS.
distorted appearance is something of a stigma to tortoise keepers, and
is the topic of much discussion. PGS is a visible sign that something
gone right in the process of growth and development. Aside from
other effects or conditions are poorly understood; tortoises with PGS
continue to grow, reproduce, and seemingly thrive. On the other hand,
often a visible symptom of metabolic bone disease, which is reason
keepers to take the issue seriously.
pyramidal growth syndrome, we have to understand the processes
growth. We must also examine diet and natural history for contributing
It is also important to know what Redfoot shells look like under normal
conditions- more than one new tortoise keeper has been shocked to
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
appearance varies somewhat according to region, climate, and diet;
be polished and smooth, or they can be slightly raised, with a faceted
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
seams between the scutes, are usually narrow and shallow in depth. The
and bridges typically are worn and polished from the abrasions of plant
and since Redfoots typically crawl into piles of debris, dense
animal burrows, the carapace often shows the same effects. This
the scutes can partially obscure the annuli.
Shell growth characteristics
shell is typically comprised of three layers of different materials:
plates on the inside, horny scutes on the outside, with a thin layer of
epithelial cells under the scutes. Although characterized as layers,
not in isolation from each other; vitamin D3, produced in the epidermis
action of sunlight, is passed into the body via the many blood vessels
bony plates. Material necessary for scute growth migrate outwards in the
periods, all three layers expand laterally, each in concert with the
materials are added to the edges, although not equilaterally; depending
location, new material may be added more on one side than others (2).
areolae, the original neonate scutes, tend to remain attached to the
bone underlying them (3). This anchoring of the natal scute and bone is
indicator of synchronous growth despite differences in material. While
scutes and epithelial layer are primarily derived from protein intake,
growth primarily requires calcium, phosphorous, and trace minerals. The
that the shell grows in synchrony, despite the differences in
worth further consideration.
Normal scute growth characteristics
Turtle scutes are
essentially the epidermal layer. The scutes are composed of a hard layer
keratin covering the bony plates of the shell. Beneath each scute is a
germinal tissue, the epithelium, which produces new scute material (4).
periods of growth, a new layer of keratin is applied to the entire
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
reached the seam and protrudes past the edge of the scutes, it flows
forming the new, expanded edge of the scute. The new layer bonds with
edge and eventually hardens in place. As the scute grows, so does the
epithelial layer underlying it.
conditions in the wild, when bone growth slows or stops, so does scute
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
scutes present at hatching are referred to as areolae. In Redfoots the
are yellow or yellowish-brown in coloration. On the carapace, the new
added to each scute is heavily pigmented and eventually each areola
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
midline of the carapace, new growth is deposited evenly around all sides
tend [to] have more new material on the lower side. For the marginal
around the edge of the carapace (and forming the bridge to the
growth is more advanced along the upper sides. These variances affect
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
the marginal scutes, and along the outer edge in plastral scutes, Scutes
plastron grow in several directions, but primarily towards the center
runs head to tail.
It may be
possible to determine the approximate age of a wile Redfoot by counting
annuli (1). Annuli indicate periods of growth, and growth occurs during
season and slows or stops during the dry season. Growth is tied to
abundance and is reflected in the width of annuli. Much like tree rings,
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
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
merge smoothly with the planar edge of the scute. It appears that much
new material remains underneath the scute, and the scute does not expand
laterally in size as normal: by comparison, pyramided scutes tend to be
in area (in terms of length and width) than normal scutes. In captivity,
patterns of seasonal growth are usually replaced with a state of
growth, which means layer after layer of new material is continually
Over time the scutes rise, taking on the familiar step-pyramid shape.
can deepen and widen with each additional scute layer, but with severe
pyramiding they lose all definition as a seam between the scutes. The
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
rapid growth typical of juveniles. If pyramiding ceases during the
the visible effects will not disappear, although subsequent growth may
things over somewhat, Once a tortoise with PGS reaches adult size, the
rate slows and the appearance of the shell is nearly immutable, Although
pyramiding does not generally manifest itself in wild-caught adult
that have been long-term captives, many of these animals exhibit a
thickening of the material around the perimeter of the scutes.
A missing factor behind PGS
growth syndrome could manifest itself from the onset of neonatal growth,
imbalance in one or more growth factors was assumed to be responsible.
protein, overfeeding, calcium deficiency, low fiber diet, hydration,
exercise and lack of sunlight were all considered to be contributing
(5, 6). Excessive protein intake received a great deal of attention,
associated with accelerated growth and as a factor in gross deformities
shell, particularly in herbivorous species, Since the diets of wild
tortoises are normally low in protein, it made sense to associate PGE
unnatural levels of dietary protein in captivity.
tortoise keepers adjusted their husbandry, reducing dietary protein and
close attention to other suspected factors, PGS continued to occur in
captive-bred tortoises, although reduction in the severity of stacked
was reported in some instances. A number of keepers began to suspect
levels and a factor and some recent studies show high humidity to be a
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
now raising Redfoots and other tortoise normal shell appearances
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
the Redfoot, but how could it play a role in PGS with dry grassland
such as G. sulcata or G. pardalis? Why aren’t the shells of
dry-climate tortoises pyramided? Clearly, PGS is not normally occurring
wild populations, but the mechanism behind it is proving to be complex
rooted in the natural history. Even tortoises from dry environments
spend time in moist microclimates- animal burrows or burros they have
escalated, ‘scrapes’, where the dry topsoil has been removed, in mud
shallow ponds, and in thick stands of vegetation, which tend to hold a
level of humidity. While humidity is not an issue during the rainy
Redfoot tortoises also readily use these types of humid microclimates
the dry season (9,10).
history indicates that humidity is but one link in a complex web of
controlled by the characteristics of the tropical climate and seasons.
tropics, the season are characterized by the amount of rainfall, rather
temperature. Growth is accelerated during the rainy season, when the
supply is at its peak, and plants contain the most nutrients. During the
months, plants retain fiber content, while nutritional levels decline,
growth slows or stops. This season cycle affects growth and development,
beginning when a tortoise emerges from the egg.
tens to spend much of their time burrowed in leaf litter, in thick
or treefalls, or in animal burrows. In this moist microclimate they
animal and vegetable elements of their diet. During the drier winter
the nutritional value of plants is greatly reduced; consequently there
little or no growth in Redfoots during these lean months, and their
microhabitat slowly dried out. The return of the rainy season brings
nutrient-rich new plant growth, along with flowers and ripening fruit.
resumes, while humidity levels rise, and the substrate contains moisture
again. The record of this cycle is captured in the annuli on the
How is humidity involved?
In captivity, the
normal wet and dry cycles and periods of growth and rest are disrupted.
Redfoots are typically kept in drier conditions, on flat surfaces of
that do not retain moisture. The low humidity may mimic the dry season,
there is no accompanying reduction of quantity or quality of food. In
the tortoises are being kept in a dry season environment, but are fed a
season diet. Consequently growth continues, and it is under these
conditions that humidity emerges as a factor.
mechanism remains to be determined. The abnormal pyramidal development
hypothesized to be secondary to the drying of the tissue underlying the
with eventual abnormal ossification (7). The seams between scutes may
become fixed in place as a result, and new growth cannot be deposited
along the scute edges and is deposited on the scute under-surfaces
This may account for the slightly smaller size (in length and width) of
scutes. Under these drier conditions, the new layers of keratin may be
fluid and plastic than usual, and so may not spread laterally in the
fashion. Mass may also be an issue, relating to the abnormal drying of
small tortoises tend to dehydrate much more quickly than large
Can PGS be simply
attributed to a change in how new scute material is deposited? While
decisively identified humidity levels as a factor, they did not
role of dietary protein, nor the consequences of accelerated growth.
study conditions, Redfoot tortoises raised in high humidity and given a
protein diet continued to develop slight pyramiding (7). In the U.S.
Islands (St. John), comparisons of wild Redfoots to those raised in
enclosures yielded similar results. Wild Redfoots on the island
normal shell growth, while captive tortoises, fed a more restrictive
included cat food or commercial tortoise food, developed pyramided
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
been produced. In a physical comparison,
pyramided carapaces have more surface area than smooth carapaces of
How is this to be interpreted? Has scute growth exceeded normal bone
has bone growth lagged behind? With many tortoises suffering from
bone disease, scute growth continues in stacked fashion, although the
are often weak and porous and can sometimes deteriorate and collapse in
What is the
condition of the bone underneath pyramided scutes? The tendency to focus
what is visible may take attention away from problems that are
beneath the skin. The shell in its entirely can be affected by other
conditions in captivity in addition to low humidity. Bone mineralization
growth can be affected by a variety of deficiencies- calcium, vitamin
sunlight, exercise, etc.- in a variety of combinations. Calcium
absorption is a
much more complicated process than the metabolizing of protein and may
behind under deficient conditions and in cases of overfeeding or
dietary protein (5). As a result, the slower bone mineralization may
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?
not, but the question brings to light the emphasis placed on appearance,
serves as a reminder that assumptions about heath should not be based on
levels are not a cure-all for proper growth and development of the
practices recommended by workers in the field of tortoise husbandry
valid and should be followed. The factors behind proper growth and
should be viewed as a complex, interdependent matrix; an imbalance in
factor affects all others. All aspects of captive husbandry should
Appendix of contributing factors
Lack of sunlight
Tortoises require exposure to the ultraviolet spectrum in sunlight to
manufacture vitamin D3, which in turn is necessary for metabolizing
Since reptiles are unable to store vitamin D3, regular
exposure to sunlight is essential to proper body functions and bone
This can be an issue for Redfoots raised completely indoors; commercial
bulbs are a poor substitute, as are vitamin D3 supplements. Without
exposure to sunlight, calcium deficiency occurs, even when a
and supplementation are provided. Calcium is inaccessible without
Calcium is metabolized and absorbed in the intestine,
and is pooled
for use in the blood plasma. Adequate levels of plasma calcium are vital
all regular biochemical functions with all animals, In the event of a
deficiency in plasma calcium, bone mineralization will cease, and the
will release calcium back into the bloodstream for more critical needs.
condition is the precursor to metabolic bone disease. The importance of
should not be underestimated; wild Redfoots actively seek out and
plants with high calcium concentrations, despite their otherwise low
value (10). Neonate Redfoots are especially vulnerable to deficiencies
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
may lead to respiratory issues, and moss or fungus may be an unwelcome
effect. The practical method is to create a humid microclimate within
hide-box or hide-house, which Redfoots use as a sleeping and resting
humidity inside a hide house or hide box can be raised by using thick
unmilled sphagnum moss, or by attaching a sponge to the underside of the
is the most vital of all nutrients, essential to all biochemical
Redfoot tortoises excrete liquid urine and need to drink fresh water
every day. Dehydration affects all soft tissues, including the nasal
and the eyes, and may also impact the tissues beneath the scutes.
also impairs renal function, and a high protein diet may make matters
(6). Fresh water in a shallow pan or dish should be provided at all
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
large size with healthy and vitality, and this can be damaging when
slow-growing ectotherms like tortoises. Pyramiding occurs primarily in
sub-adult captive tortoises and this may be linked in part to their fast
of growth. A combination of accelerated growth and lack of proper bone
mineralization can make the bones of the shell porous and spongiform (5,
Under these unfavorable conditions, it appears that the synchronous
bone and scute attempts to continue, and the result is a layer of weak,
dense bone material that does not provide strong shell integrity.
factor contributing to accelerated growth. ‘More is better’ is a human
prejudice that is not necessarily compatible with ectotherms like
Redfoots have a ‘windfall’ approach to eating- if large quantities of
available, then eat as much as possible, because there may be no food
This is an excellent survival mechanism in nature, but in captivity,
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
digested as it passes through the digestive tract. Foods low in fiber
completely digested, and may contribute to accelerated growth when
Excessive protein intake is another factor contributing to accelerated
It is not known what the ‘proper’ levels of protein intake are for
Redfoots, and differences in how the protein content of foods is
measure versus included water content) can be confusing and misleading,
diet of juvenile wild Redfoots is poorly understood; it is assumed that
and plant proteins comprise a significant portions, but not the bulk of
Many keepers rely solely on prepared foods as a source for proteins,
typically derived from cereal grains, primarily wheat, corn, rice or
These grains are not a part of the natural diet of Redfoots, and there
multitude of reasons as to why they should not be relied upon as a
source for protein. They are deficient in calcium and rich in
magnesium, which can retard the absorption of calcium in the
tract. Cereal proteins are typically low in certain essential amino
as lysine, methionine, leucine, and tryptophan, which gives them a lower
biologic value (expression of the relationship between quantity absorbed
quantity utilized) (12, 13). By comparison, animal proteins have a much
biologic value, and contain a number of complete proteins not found in
Lack of exercise
With the exception of large adult males, Redfoots are active
throughout the year (10). In captivity, they are often kept in small
and are not given enough opportunities for exercise. Exercise aids
adds strength to bone; protein is burned like carbohydrates for energy
used to build and maintain muscle.
There is little or no discussion about the effects of mechanical wear on
shell. Wild Redfoots crawl into burrows, logs, piles of debris, and
tangles of debris, which abrade the plastron and carapace alike. Often
result is a smooth, polished appearance to the scutes. Kept in open
the carapaces of captive Redfoots do not show this type of wear, and
plastral scutes may not be smooth. While natural abrasion may not be a
factor in PRG, it does contribute to the overall appearance of the
- Pritchard, Dr. Peter C. H.and Pedro Trebbau. Turtles of Venezuela (Contributions to herpetology)
. Society for the Study of Amphibians and Reptiles, 1984. ISBN 0916984117. P. 207-220
- Magwene, P. M.
2001. “Comparing Ontogenetic Trajectories Using Growth Process Data”.
- Pritchard, Dr. Peter C. H. Encyclopedia of Turtles
. TFH Press. 1979. ISBN 0876669186. P. 30.
- Ernst, C.H. and Roger W. Barbour. Turtles of the World.
Smithsonian Institution Scholarly Press, November 17, 1992. ISBN 1560982128, p. xxiii.
- Senneke, Darrell. “What causes pyramiding?” World Chelonian Trust. 2003.
- Highfield, Andy C. Practical Encyclopedia of Keeping and Breeding Tortoises and Freshwater Turtles
. Kreiger Publishing, 1996. ISBN 1873943067. Pp. 87-108.
- Weisner, C. S. and C. Iben. “Influence of Environmental Humidity and Dietary Protein on the Pramidal Growth of Carapaces of African Spurred Tortoises, Geochelone sulcata.” Journal of Animal Phys. and Nut., 87-2003.
- Fife, Richard. “Pyramiding in Tortoises” Reptiles Magazine. 2005. (From the portal, go to ‘Turtles and Tortoises’, then ‘Tortoise Care’, then look for the article on pyramiding.)
- Vinke, Thomas and Sabine Vinke. “An Unusual Survival Strategy of the Red-Footed Tortoise Geochelone carbonaria in the Chaco Boreal of Paraguay.” Radiata 12(3) 2003.
- Moskovits, Debra.” The Behavior and Ecology of the Two Amazonian Tortoises, Geochelone carbonaria and Geochelone denticulata, in Northwestern Brazil“. (PhD Dissertation) University of Chicago, 1985.
- Blair, Bonnie. Personal communication.
- Cordain, L.,
1999. “Cereal grains: Humanities double edged sword”. In Simpoulos AP
Evolutionary Aspects of Nutrition and Health. Diet, Exercise, Genetics,
Chronic Disease. World Rev Nutr Diet. Basel, Karger, 1999 vol 84, pp
- Lewis, L.
Morris, M. L., & Hand, M. S., 1987. Small Animal Clinical Nutrition
Mark Morris Associates, Topeka, KS. pp 1-12, 12-3
Revised 11-28-2011 (C) Mike Pingleton