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Tropical 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