Table Of ContentTropical Natural History 21(1): 61–78, April 2021
©2021 by Chulalongkorn University
The Evolutionary Ecology of the African Pancake Tortoise
Malacochersus tornieri (Siebenrock 1903): A Review and Synthesis
Based Upon Current Knowledge
DON MOLL1*, LAUREN E. BROWN2 AND EVAN S. BROWN3
1Department of Biology, Missouri State University, 901 S. National Ave., Springfield, Missouri 65897, USA
2School of Biological Sciences, Illinois State University, Campus Box 4120, Normal, Illinois 61790, USA
3Joliet Junior College, 1215 Houbolt Rd., Joliet, Illinois 60431, USA
Present address of corresponding author: N16356 Lakeshore Drive, Butternut, Wisconsin 54514 USA
*Corresponding author. Don Moll ([email protected])
Received: 8 July 2020; Accepted: 25 January 2021
ABSTRACT.– The pancake tortoise Malacochersus tornieri (Siebenrock 1903) of East Africa is morphologically,
behaviourally and ecologically unique among extant land tortoises of the family Testudinidae. Recent studies
suggest it shares a common ancestor with the Indotestudo – Testudo group, but the selective pressures and
evolutionary pathway that produced the single extant species, Malacochersus tornieri, are poorly understood. We
propose that intense predation pressure and competition initiated the process of change from an ancestral,
generalized tortoise form by driving Malacochersus into rocky areas and subsequently rock crevices, where
predation and competition were reduced. This change in habitat led to rapid changes in morphology, ecology, and
behaviour in order to better adapt to the crevice environment, and to enhance its safety within from predators.
These changes in turn led to strict limits to the extent and duration of out-of-crevice activity. The changes in
morphology also allowed greater mobility, agility, and speed to enhance safety when tortoises left their crevices to
forage, mate, defecate, or colonize new habitats. Padlopers, an extant clade of small, southern African tortoises
may provide insight into the pancake tortoise’s ancestral evolution toward its modern form, lifestyle, and
reproductive characteristics. Both the pancake tortoise and padlopers also inexplicably display an unusually large
amount of anomalous variation in scute and/or shell characteristics.
KEY WORDS: East Africa, crevice fauna, competition, tortoise predation, tortoise evolution
attempts using molecular techniques (i.e.,
INTRODUCTION
Le et al. 2006; Parham et al. 2006; Fritz and
Bininda-Emonds 2007). The consensus
The pancake tortoise, Malacochersus
opinion based mainly on the studies of Le et
tornieri (Siebenrock 1903) is the only extant
al 2006 and Fritz and Bininda 2007 is that
species of its genus, and it is morpho-
Malacochersus is derived from the Indotestudo
logically, behaviourally and ecologically the
– Testudo – Malacochersus clade. This view
most unique, and distinctive extant member
has recently been generally supported by
of the land tortoises of the family
Kehlmaier et al. (2019). Unfortunately, there is
Testudinidae (Fig. 1). Mautner et al. (2017)
no known fossil record for Malacochersus
provided a concise summary of efforts to
at this time; therefore, a significant time and
understand the evolutionary origins of the
knowledge gap exists between the origin of
pancake tortoise. They described the earliest
the pancake tortoise ancestor(s) and the
attempts using morphological characters
unique extant form present in East Africa
(i.e., Loveridge and Williams 1957; Crumly
today.
1984; Gaffney and Meylan 1988) and later
2 TROPICAL NATURAL HISTORY 21(1), APRIL 2021
FIGURE 1. Pancake tortoise, Malacochersus tornieri, captive specimen from East Africa. Note extreme
dorso-ventral flattening, a characteristic of this crevice-dwelling species. Photo by F.J. Obst
Malacochersus has a wide, but disjunct Ernst and Barbour (1989), Lovich and Ernst
distribution in suitable habitats (i.e., crevice- (1989); and Mautner et al. (2017). When
rich rocky hillsides and kopjes [Fig. 2A]) emergence is necessary to forage, seek
across East Africa with naturally occurring mates, defecate and colonize new habitats,
populations known from Kenya, Tanzania or when rapid return to the crevice is required
and (marginally) Zambia (Moll D. and to escape or avoid dangerous situations (e.g.,
Klemens 1996; Mwaya et al. 2018a). It spends predation, trampling, unfavourable environ-
most of its time in rock crevices with suitable mental conditions) these tortoises can move
dimensions and structural characteristics swiftly, turn over quickly if they fall on their
where it can tightly wedge itself between backs, and climb rocks in an almost lizard-
crevice walls and ceilings (Fig. 2B). It’s like manner. These behaviours may be
extremely dorso–ventrally flattened, thin shell facilitated by morphological changes that
and scutes, and extensive skeletal fenestration have lightened the shell (Kabigumila 2002),
enhance this capability. Additionally, it has and have been further enhanced by greater
the ability to inflate itself slightly, or brace suppleness in the wrists and ankles than
itself against the crevice ceiling to wedge seen in most testudinids (see also Procter
itself even more tightly when threatened 1922; Honegger 1968; Ireland and Gans
within the crevice (Moll D. and Klemens 1972; Wilke 1984; Moll D. and Klemens
1996; Mwaya et al. 2018a). More detailed, 1996; Wood and MacKay 1997; Kabigumila
basic morphological studies related to these 2002; Malonza 2003; Schmidt 2006; Mwaya
capabilities include those of Siebenrock et al. 2018a).
(1904), Procter (1922), Loveridge and The objectives of this paper are to
Williams (1957), Pritchard (1979, 2007), elucidate a plausible evolutionary scenario
MOLL ET AL. — THE EVOLUTIONARY ECOLOGY OF THE AFRICAN PANCAKE TORTOISE 3
FIGURE 2. Pancake tortoise macrohabitat in northern Tanzania's Yaedachini Game Reserve (2A), and
microhabitat near Mbulu, Tanzania (2B). A pair of pancake tortoises (not visible) are present in the diagonal
crevice in the rock at the right foreground of photo (2B). Photos by D. Moll
and relevant selective forces that may have as they may provide insight into some of the
been involved in shaping the unique evolutionary stages undergone by the
morphology, behaviour and ecology of the pancake tortoise’s ancestors. Reproductive
extant pancake tortoise. The morphological, characteristics, as well as scute and shell
behavioural and ecological characteristics of anomalies in the pancake tortoise and
the southern African padloper tortoises padlopers are also briefly discussed.
(genera Homopus and Chersobius, Family
Testudinidae) will also be briefly discussed
4 TROPICAL NATURAL HISTORY 21(1), APRIL 2021
MATERIALS AND METHODS molecular evidence, Le et al. (2006),
Parham et al. (2006), Fritz and Bininda-
Literature search Emonds (2007), and Kehlmaier et al. (2019)
The methodology of Brown et al. (2008) suggested Malacochersus was derived from
was employed to obtain a maximum number the Indotestudo – Testudo – Malacochersus
of relevant references concerning the subject group of species within the Testudinidae.
matter of this paper. Searches employing Available evidence suggests this group
numerous combinations of search words, originated in the Palearctic Region (i.e.,
and the search engines Google, Google Scholar Eurasia) as recently as the late Miocene (~5-
(Advanced Scholar Search), and JSTOR 15 myo). An invasion of Africa by members
Advanced Search were conducted. We also of this group, perhaps via land bridge(s)
used traditional library-based searches of paper present in the late Miocene (Rögl 1999),
sources at Illinois State University’s Milner occurred somewhat later. This is much
Library, and DM’s and LEB’s personal younger than the oldest known African
herpetological and paleontological libraries to tortoises (e.g., Gigantochersina ammon at
obtain pertinent references. Detailed field 35.4-35.6 myo – Holroyd and Parham
notes by one of us (DM) concerning his 2003). Parham et al. (2006) point out that
1992 Tanzanian field studies of the pancake the clade containing the ancestral pancake
tortoise’s ecology were also consulted and tortoise; therefore, must have invaded
cited in this paper. Africa after other tortoises, including the
Scientific names follow those designated diverse and widespread Geochelone complex
by the Turtle Taxonomy Working Group were already well established on the
(2017). No original DNA sequencing was continent.
conducted in our research related to the The ancestral Malacochersus that arose
preparation of this manuscript. However, within this clade would probably have been
DNA sequence registration information and a habitat generalist and would have been
DNA sequencing methodology employed distributed across a variety of habitats which
are provided in the papers by Parham et al. provided suitable foods (mainly vegetation),
(2006), Le et al. (2006), Fritz and Bininda- shelter from environmental stresses, suitable
Emonds (2007), and Kehlmaier et al. (2019) reproductive sites, and at least some
that we referred to in our Results and protection from predators. We assume
Discussion section. predator diversity and predation pressure
would have been important selective forces
on prey species in ancient Africa as they are
RESULTS AND DISCUSSION
today. A diverse array of mammalian, avian
(probably underestimated in importance)
Into the crevice: selective pressures and
and reptilian predators would have preyed
morphological change
on tortoises of all ages and sizes along with
We envision the earliest ancestral
their eggs much as they do today (Moll D.
Malacochersus to be a small to medium-
and Klemens 1996; Mwaya et al. 2018a).
sized tortoise with a typical hard-shelled
Interspecific competition with already
testudinid morphology (e.g., similar to
established tortoises and other vertebrate
extant Indotestudo or Testudo or Homopus
herbivores would also have been an
tortoises). Considering both fossil and
important selective force.
MOLL ET AL. — THE EVOLUTIONARY ECOLOGY OF THE AFRICAN PANCAKE TORTOISE 5
Parham et al. (2006) suggested that given caves, rock slabs, and other semi-enclosed
the great length of time that tortoises were rock structures for shelter and protection
present in the Ethiopian Region before the from predators, and from inclement weather
group containing the ancestor(s) of and other unfavourable environmental
Malacochersus colonized there, it is likely conditions outside. Loehr (2002) stated that
that one or more radiations may have the characteristic thin shell and large
occurred before their arrival (e.g., the fenestrae of pancake tortoises could just as
evolution of the diverse Geochelone well have been “a reduction of unnecessary
complex-Hofmeyr et al. [2016]). If so, the investment in shell, replaced by protection
niches available for newly arriving, by rocks” rather than necessarily being an
herbivorous tortoises would likely have adaptation which allowed them to inflate
been limited, and competition for resources themselves in rock crevices to avoid being
could have been intense. pulled out by predators. We agree that the
The generalized ancestral Malacochersus protection afforded by the rock crevice
would likely have been more vulnerable to allowed the luxury of shell reduction and
predation and competition pressure in some softening to proceed, but we envision a
habitats than in others, depending on more complex series of specific adaptive
ecological factors referred to above, and the morphological and behavioural changes
diversity and effectiveness of potential occurring at this stage. We do not think the
tortoise predators and competitors present. reduction and change in shell structure was
Habitats that reduced the tortoises’ just the result of random atrophy (and which
effectiveness in defense and niche use may be analogous to the reduction in wing
against resident predators and competitors structure leading to flightlessness in island-
would result in lower population sizes, or colonizing birds and insects freed from
perhaps even extirpation, while habitats that predation [Carlquist 1965]). In the case of
more effectively supported and protected the pancake tortoise the extensive fenestration
resident tortoises would provide refugia and thinning of the scutes and underlying
from predators and competitors. bone led to greater flexibility and even
We suggest that tortoises inhabiting slight inflation capability while still
rocky habitats were able to benefit from maintaining specific sturdier areas
greater opportunities for shelter, crypsis, and (especially its hard, ossified vertebral/neural
protection from predators and competitors section at the dorsal rear location of the
compared to tortoises in other habitat types. carapace [Fig. 1]) for protection from
An ability to shift in diet to low-growing predators and for bracing against the crevice
plants associated with rocky areas (as ceiling (see below for a more detailed
utilized by extant pancake tortoises [Moll description of morphological and behavioural
and Klemens 1996; Mwaya 2009; Mwaya et adaptations for crevice life).
al. 2018a]) would have helped in adapting to We suggest the hard-shelled pancake
the new niche. As a result, the tortoise tortoise ancestor(s) began entering rock
populations in these rocky habitats were shelters (e.g., caves, fissures, larger crevices,
able to survive and thrive while those in etc.) mainly for protection from predators
other habitats did not. and other external threats. This behaviour
Presumably, tortoises in rocky habitats was effective against larger mammalian and
would have begun using rock crevices, avian predators, but it left the pancake
6 TROPICAL NATURAL HISTORY 21(1), APRIL 2021
tortoise ancestor vulnerable to agile small continued to better adapt the pancake
and medium-sized mammalian predators tortoises’ ancestral form to these new
such as herpestids (e.g., mongooses), specialized habitats, and 5) associated
viverrids (e.g., genets and civets) and also changes in ecology and behavior continued
reptilian predators (e.g., varanid lizards). in the ancestral pancake tortoise’s lineage
These predators still prey on pancake until the extant form evolved.
tortoises, and other tortoises in East Africa Parham et al. (2006) researched the
today, and routinely enter crevices in search phylogeny of a number of species of
of prey (Moll D. and Klemens 1996, Moll tortoises (including M. tornieri) using
D. pers. obs.; Mwaya et al. 2018a). This mitochondrial genome sequences. Their
type of predation served as a strong results implied a higher mtDNA rate of
selective force precisely guiding profound, evolution for M. tornieri than the other
specific behavioural and morphological tortoises examined. This may be associated
changes that promoted the utilization of with the rapid effects of natural selection on
ever-smaller and narrower crevices. behaviour and morphology, which must
Utilization of these new habitats could be have been progressing at essentially the
considered analogous to the first attempts to same time, and would have enhanced the
take to the air by bird-like, maniraptoran adaptive value of each trait in a positive
theropod dinosaurs (i.e., entering a new feedback loop. The Parham et al. (2006) and
adaptive zone). Once the utilization of the new Omland (1997) studies (see below) also
zone was initiated, a cascade of adaptations suggested that the changes could have taken
that better adapt the organisms to the new place very rapidly, perhaps in just a few
niche would occur. Modifications in generations.
morphology, behaviour and ecology occurred The processes described above represent
which changed the tortoise into a form evolutionary stages we envision where
possessing the characteristics of, and eventually crevice selection became very specific, and
becoming, the extant pancake tortoise, was based upon the requirements for
Malacochersus tornieri. maximum protection (according to Moll and
The proposed, critical, formative Klemens 1996: where the crevice ceiling is
processes influencing the ancestral pancake <5 cm above the floor and where,
tortoise’s evolution can be summarized in preferably, this crevice section is somewhat
the following event sequence: 1) dispersal removed from the crevice entrance). Indeed,
from Palearctic origins into the Ethiopian if suitable crevices are not present or very
Biogeographic Region by the pancake scarce in a particular kopje or rock outcrop,
tortoise ancestor(s) ~5 – 15 myo in the late pancake tortoises are unlikely to be found
Miocene, 2) the selective pressures of there (Moll D. and Klemens 1996; Mwaya
predation and competition led to the et al. 2018a). Crevice dimension preferences
utilization of rocky habitats for shelter and are very precise, and this is because the
protection, by the ancestral pancake tortoise, unique behaviours of wedging, bracing, and
3) the continued selective pressure of inflating, accomplished in different ways
smaller to medium-sized predators (e.g., depending upon the configuration of the
mongooses) led to the pancake tortoises’ use crevice, are apparently very important in
of increasingly smaller and narrower preventing dislodgement of resident tortoises
crevices, 4) changes in morphology by potential predators (Moll D. and Klemens
MOLL ET AL. — THE EVOLUTIONARY ECOLOGY OF THE AFRICAN PANCAKE TORTOISE 7
1996). Morphological specializations are also results in the expansion of a large underlying
involved in wedging effectively (i.e., part of plastral fontanelle (Fig. 3), and produces a
the suite of unique morphological changes slightly larger body circumference for the
characterizing pancake tortoises, and tortoise in the crevice, again enhancing the
especially, affecting their shell structure [see capability for tighter wedging (Moll D. and
references concerning morphological studies Klemens 1996).
cited in the Introduction]). Briefly, the main
morphological modifications for crevice life Leaving the crevice
in conjunction with those behaviours The benefits of shell reduction and
referred to below as inflation and bracing greater thinness are obvious in a crevice-
include: 1) the shell is dorso-ventrally dwelling tortoise with the ecological and
flattened (Fig. 1), so that the tortoise can behavioural specializations of Malacochersus,
more easily squeeze into narrow crevices, 2) but they also come at significant cost.
the plastron and carapace are soft and Emergence from the crevice is much more
widely fenestrated to facilitate compression, perilous than it was previously due to the
3) the scutes on the shell are thin facilitating reduced protection provided by the greatly
flexion and compression, and 4) the bones modified shell. Predators outside the crevice
of the shell are connected by thin flexible are the main concern, but there may be other
cartilage, again enhancing the flexion and dangers as well. Trampling by hooved,
compression of the shell. These shell mammalian herbivores has not yet been
characteristics collectively allow the tortoise documented by observation to our knowledge,
to mold its body into the contours of the but Malacochersus lives in areas known for
crevice (i.e., simple wedging) and enhance large herbivore herds and the great size and
its capacity to resist dislodgement. When sharp hooves of individuals composing
crevice dimensions and configurations some of these herds pose a threat (Mwaya et
allow, bracing and/or inflation may be al. 2018a). One of us (DM) has observed
employed also to provide even more effective large herds of African buffalo (Sincerus
mechanisms to avoid dislodgement. caffer) foraging just outside rock crevices
The presence of a solid hump of scute containing pancake tortoises in Tarangire
and underlying bone on the dorsal rear of National Park, Tanzania. Excessive heat
the carapace (Fig. 1), allows a threatened experienced while foraging or in other
tortoise to brace itself tightly against the outside activity could also be dangerous to
ceiling of the crevice. This is accomplished pancake tortoises or their ancestors that
by extending and straightening the hind legs wandered too far from the crevice with its
in order to thrust the hump into the rock often more moderate and/or stable internal
ceiling. As pancake tortoises often wedge environment (Honegger 1968; Wilke 1984;
themselves into crevices with their posterior Moll D. and Klemens 1996; Schmidt 2006).
shell facing toward the crevice entrance Although time spent within the relative
(Moll, D. pers. obs.), the hardened rear of safety of the crevice is considerable in the
their carapace may also physically shield extant pancake tortoise (and presumably its
them from injury by intruding predators. immediate ancestor[s]) certain out-of-
Inflation is caused by retracting the limbs, crevice activities are essential for survival
and head into the shell while the tortoise and reproduction within the species, such as
inhales and holds its breath. This behaviour foraging, seeking mates and mating, nesting
8 TROPICAL NATURAL HISTORY 21(1), APRIL 2021
FIGURE 3. Adult pancake tortoise showing the large light-coloured area of the plastron covering the central
fenestrated area in the underlying bony layer. Photo by D. Moll
and oviposition, basking, and defecating. al. (2018a) suggested male pancake tortoises
One of us (DM) has observed and collected may move overland to reside with females
considerable amounts of pancake tortoise in crevices for a time, but whether mating
scat outside crevices and inside, near the occurs there is unknown. The social
entrances, but little within the crevices behaviour of pancake tortoises remains
themselves. All of these activities have been largely unstudied (Moll D. and Klemens
observed outside crevices, but some may 1996; Mwaya et al. 2018a). Single eggs
occur within as well – the ability to observe have been observed within crevices in the
activity inside a crevice is obviously limited. wild and in captive conditions (Loehr 2002;
Moll D. and Klemens (1996) and Mwaya et Schmidt 2006; Mwaya et al. 2018a), but the
MOLL ET AL. — THE EVOLUTIONARY ECOLOGY OF THE AFRICAN PANCAKE TORTOISE 9
normal method of oviposition is usually the duration (although some individuals may be
standard chelonian method of digging a immobile outside for a longer period of
shallow hole, laying an egg in it and burying time), and may occur throughout the day.
the (usually single egg) clutch (Mwaya et Branch (2012) observed that ~50% of the
al. 2018a). Oviposition in the crevice would pancake tortoise’s movements he observed
initially seem to be a favourable and safer are between crevices on the same rock
way to reproduce, but pancake tortoises outcrop although considerable movement
often share their crevices with a variety of between outcrops may sometimes occur.
reptilian and other usually commensal Mwaya (2002) also noted occasional longer
residents (Moll D. and Klemens 1996; Mwaya movements between crevices, especially by
et al. 2018a). The regular movements of males. During these forays, including the
periods of immobility, the plain horn colour
pancake tortoises and the other crevice
(usually in older individuals) and “sunburst”
dwellers could damage the egg(s) inside and
carapacial scute patterns and varied
some of the crevice dwellers could possibly
also eat some (e.g., varanid lizards). In carapacial colours displayed in other
individuals may serve a cryptic function for
addition, the crevices usually have a rock
both juveniles and adults (Fig. 4A, B). It is
floor so burying the egg(s) would be
impossible. Exposure to the crevice notable also that the diurnal activity patterns
displayed by tortoises engaging in external
environment over the long incubation period
activities contrast with the predominantly
could also be detrimental to egg
development. As Malacochersus is a TSD nocturnal activity of their main mammalian
predators, the herpestids and viverrids. To
species (i.e., has temperature-dependent sex
our knowledge, there are no recorded
determination [Ewert et al. 2004]) the
observations of pancake tortoises active
normal population sex ratio of eggs could be
outside their crevices at night. However, the
disrupted if too many individuals oviposit
potential for nocturnal movements by
within crevices, rather than in outdoor
Malacochersus has not been thoroughly
substrates in a more normal chelonian
investigated. Moll D. and Klemens (1996)
manner.
counted at least seven mutilated pancake
The solution to the problems imposed by
tortoise carcasses in close proximity to
outside activity of extant pancake tortoises
crevices (within 2 meters) in Tarangire
(and presumably their immediate ancestor[s])
National Park, Tanzania. The three freshest
is to prolong their stay in their crevices as
long as possible before emergence. Once carcasses were discovered in early morning
surveys, and clearly displayed wounds
outside they curtail the time spent engaging
resembling those made by mammalian teeth
in outside activities by limiting the distance
(Moll D. unpubl. field notes). Mwaya R.
traveled from the nearest suitable crevice
(unpubl. observ.) also found several
(Moll D. and Klemens 1996; Branch 2012;
predated pancake tortoises outside of
Mwaya et al. 2018a).
crevices in Tarangire National Park, but the
Observations of foraging pancake
predators involved, and distance from
tortoises (by Njalale A. in [Moll D. and
crevices, are unknown. No tortoises or other
Klemens 1996] and in Mwaya et al. ([2018a])
signs of predation were observed, despite
suggest that most activity occurs near the
intensive searches at more distant locations
crevice entrance, is of relatively short
(i.e., beyond several meters from crevices
10 TROPICAL NATURAL HISTORY 21(1), APRIL 2021
FIGURE 4. Adult pancake tortoises displaying cryptic colouration against backgrounds of lighter coloured
rock (4A) and black rock with orange lichens (4B). Photos by D. Moll
[Moll D. unpubl. field notes]). Pancake tortoises and other reptiles, such as secretary
tortoises may have been surprised and birds (Sagittarius serpentarius), ground
pulled from their crevices during the night hornbills (Bucorvus leadbeateri), white-
and consumed just outside before dawn. A necked ravens (Corvus albicollis) and pied
few dead tortoises (i.e., four in ~two months crows (Corvus albus) would still be a threat
of fieldwork) were found within crevices, to both juvenile and adult pancake tortoises
but they displayed no signs of predation outside the crevices during the day, perhaps
(Moll D. unpubl. field notes). Avian diurnal reduced by the cryptic behavior and colour
predators known to prey upon small patterns mentioned above (Uys 1966;
