Understanding Pyramidal Growth Syndrome (PGS) in Redfoot Tortoises
By Mike Pingleton

World Chelonian
Trust Newsletter, Vol. 3, No. 1

[Editor’s note: Used with permission.]

Introduction

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.

 

Discussion

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.

 

Recommendations

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

Lack of sunlight

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 deficiency

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.

Humidity

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.

Hydration

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.

Accelerated growth

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.

Overfeeding

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.

Dietary fiber

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.

Protein intake

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.

Protein sources

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.

Literature Cited:

1. 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
2. Magwene, P. M.
   2001. “Comparing Ontogenetic Trajectories Using Growth Process Data”.
   Systematic
   Biology 50(5):640-656.
3. Pritchard, Dr. Peter C. H. Encyclopedia of Turtles
   . TFH Press. 1979. ISBN 0876669186. P. 30.
4. Ernst, C.H. and Roger W. Barbour. Turtles of the World.
   Smithsonian Institution Scholarly Press, November 17, 1992. ISBN 1560982128, p. xxiii.
5. Senneke, Darrell. “What causes pyramiding?” World Chelonian Trust. 2003.
6. Highfield, Andy C. Practical Encyclopedia of Keeping and Breeding Tortoises and Freshwater Turtles
   . Kreiger Publishing, 1996. ISBN 1873943067. Pp. 87-108.
7. 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.
8. 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.)
9. 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.
10. 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.
11. Blair, Bonnie. Personal communication.
12. Cordain, L.,
    1999. “Cereal grains: Humanities double edged sword”. In Simpoulos AP
    (ed):
    Evolutionary Aspects of Nutrition and Health. Diet, Exercise, Genetics,
    and
    Chronic Disease. World Rev Nutr Diet. Basel, Karger, 1999 vol 84, pp
    19-73
13. Lewis, L.
    D.,
    Morris, M. L., & Hand, M. S., 1987. Small Animal Clinical Nutrition
    III
    Mark Morris Associates, Topeka, KS. pp 1-12, 12-3