Tortoises of the family Testudinidae occur on most continents (except Antarctica and Australia) and on many isolated islands as a result of oceanic dispersal (Bonin et al. 2006, Crumly 2009). Many species, however, have gone extinct since the late Pleistocene. Within the last few millennia, the majority of tortoise extinctions occurred on islands. These recent tortoise extinctions present an opportunity to vet, implement, and evaluate the conservation potential of taxon substitutions. In that spirit, we provide an overview of extant and recently extinct large and giant tortoises, highlight the important roles of extant and extinct tortoises in some ecosystems, and argue that tortoises are a low-risk taxon for substitutions. Finally, we present and discuss several case stories that illustrate how extant tortoises can be suitable analogues for their recently extinct counterparts.
Global distribution and status of large tortoises
At least 36 species of large and giant tortoises have gone extinct since the Pleistocene, with the majority occurring on islands and vanishing in the late Pleistocene (Table 1). At least 32 species are still extant, with the majority of higher-order taxa found on continents (Table 2). The only remaining species of giant tortoises growing to more than one meter carapace length are found on the isolated islands of Galápagos in the Pacific Ocean and the Aldabra Atoll in the Indian Ocean; Geochelone (Centrochelys) sulcata in the African Sahel belt comes close, with lengths of up to 83 cm. Additional extinct tortoise species continue to come to light: sub-fossil specimens have been recently discovered both in the Mediterranean and Caribbean regions (Caloi et al. 1986, Meylan and Sterrer 2000, Chesi et al. 2007, Steadman et al. 2007).
Table 1. Extinct large and giant tortoises from the Pleistocene to Holocene.
|Taxon||Distribution||Island/mainland||Last record||Maximum carapace length (cm)||References|
|Aldabrachelys abrupta||Madagascar||Island||Holocene||115||1, 2, 3|
|Aldabrachelys grandidieri||Madagascar||Island||Holocene||125||1, 2, 3, 4|
|Cheirogaster gymnesica||Minorca, Balearics||Island||Pleistocene|| ||1, 5|
|Cheirogaster sp.||Pituysic Islands, Balearics||Island|| || ||5|
|Chelonoidis cubensis||Cuba, Brazil||Mainland and island||Pleistocene|| ||1, 6|
|Chelonoidis elata||Cuba||Island||Pleistocene|| ||1|
|Chelonoidis elephantopus||Floreana, Galápagos||Island||Holocene|| ||7|
|Chelonoidis phantastica||Fernandina, Galápagos||Island||Holocene||86||7, 8|
|Chelonoidis? sellowi||Uruguay||Mainland||Pleistocene|| ||1|
|Chelonoidis sombrerensis||Sombrero Island||Island||Late Pleistocene||100||1, 6, 9|
|Chelonoidis wallacei||Rabida, Galápagos||Island||Holocene||82||7, 10|
|Chelonoidis sp.||Santa Fe, Galápagos||Island||Holocene|| ||7|
|Chelonoidis sp.||Great Abaco, Bahamas||Island||Holocene||46||11|
|Chelonoidis sp.||Dominican Republic||Island||Holocene||60||12, 13|
|Cylindraspis indica||Reunion, Mascarenes||Island||Holocene||60||2, 15|
|Cylindraspis inepta||Mauritius, Mascarenes||Island||Holocene||“Large”||2, 15|
|Cylindraspis peltates||Rodrigues, Mascarenes||Island||Holocene||42||2|
|Cylindraspis triserrata||Mauritius, Mascarenes||Island||Holocene||“Giant”||2, 15|
|Cylindraspis vosmaeri||Rodrigues, Mascarenes||Island||Holocene||110||15, 16|
|Geochelone burchardi||Canary Islands||Island||Pleistocene|| ||1|
|Geochelone robusta||Malta||Island||Pleistocene||120||1, 17, 18|
|Geochelone sp.||Bahamas||Island|| ||60||6|
|Geochelone sp.||Navassa Island||Island|| ||40||6|
|Geochelone sp.||Barbados||Island||Late Pleistocene||60||19|
|Gopherus donlaloi||Mexico||Mainland||Pleistocene||54 (plastron)||20|
|Hesperotestudo crassiscutata||Southern USA, Central America||Mainland||Late Pleistocene||150||1, 13, 21|
|Hesperotestudo equicomes||Kansas, USA||Mainland||Pleistocene|| ||1|
|Hesperotestudo incisa||Florida, USA||Mainland||Pleistocene|| ||1|
|Hesperotestudo johnstoni||Texas, USA||Mainland||Pleistocene|| ||1|
|Hesperotestudo wilsoni||Southern USA||Mainland||Holocene|| ||1, 22|
|Manouria margae||Celebes, Indonesia||Island||Pleistocene||120–150||1, 23|
|Manouria oyamai||Ryukyu Islands, Japan||Island||Late Pleistocene||“Giant”||24|
|Megalochelys atlas||Java, India||Mainland and island||Pleistocene||180||1, 2|
|Megalochelys cautleyi||India||Mainland||Pleistocene|| ||1|
|Monachelys monensis||Mona Island||Island||Pleistocene||50||1, 6|
Table 2. Extant large and giant tortoises.
|Species||Distribution||Island/mainland||Maximum carapace length (cm)||References|
|Aldabrachelys gigantea||Aldabra, Seychelles||Island||105||1|
|Astrochelys radiata||Southern Madagascar||Island||40||1|
|Astrochelys yniphora||Northwest Madagascar||Island||45||1, 2|
|Chelonoidis carbonaria||Northern South and Central America, introduced to Islands of Caribean||Mainland||70||1, 3|
|Chelonoidis chilensis||Southern South America||Mainland||43||1, 3|
|Chelonoidis denticulata||northern South America and Trinidad||Mainland and island||82||1|
|Chelonoidis abingdoni||Pinta, Galápagos||Island||98||1, 4|
|Chelonoidis becki||Wolf volcano, Isabela, Galápagos||Island||104||1, 4|
|Chelonoidis chatamensis||San Cristobal, Galápagos||Island||90||1, 4|
|Chelonoidis darwini||Santiago, Galápagos||Island||102||1, 4|
|Chelonoidis ephyppium||Pinzon, Galápagos||Island||84||1, 4|
|Chelonoidis guntheri||Sierra Negra, Isabela, Galápagos||Island||102||1, 4|
|Chelonoidis hoodensis||Espanola, Galápagos||Island||75||1, 4|
|Chelonoidis microphyes||Darwin volcano, Isabela, Galápagos||Island||103||1, 4|
|Chelonoidis porteri||Santa Cruz, Galápagos||Island||105||1, 4|
|Chelonoidis vandenburghi||Alcedo volcano, Isabela, Galápagos||Island||125||1, 4|
|Chelonoidis vicina||Cerro Azul, Isabela, Galápagos||Island||110||1, 4|
|Chersina angulata||South Africa, southern Namibia||Mainland||30||5|
|Geochelone elegans||India, Pakistan, Sri Lanka||Mainland and island||38||1|
|Geochelone platynota||Burma||Mainland||30||1, 3|
|Geochelone (Centrochelys) sulcata||Central and North Africa, Sahel-belt||Mainland||83||1, 5|
|Gopherus flavomarginatus||North-central Mexico||Mainland||40 (fossils up to 100)||3|
|Gopherus agassizii||South-western USA, Mexico||Mainland||40||3|
|Gopherus polyphemus||South-eastern USA||Mainland||38||3|
|Indotestudo elongata||Asia (Nepal, India, China, Burma, Malaysia, Thailand, Cambodia, Vietnam)||Mainland||33||3, 6|
|Indotestudo travancorica||Western India||Mainland||30||3, 6|
|Kinixys erosa||Central West Africa||Mainland||40||3, 5|
|Manouria emys||Burma, Thailand, Malay Peninsula, Sumatra, Borneo||Mainland and island||60||3, 6|
|Manouria impressa||Burma, Thailand, Malay Peninsula, Vietnam||Mainland||33||3, 6|
|Stigmochelys pardalis||Eastern to southern Africa||Mainland||70||1, 3, 5|
|Testudo boettgeri||South-eastern Europe||Mainland||34||3|
|Testudo marginata||Greece, southern Balkan||Mainland||40||3|
Since the late Pleistocene, human predation and anthropogenic impacts have been major causes of tortoise extinction and endangerment. This is particularly well-documented for some of the recent extinctions on islands, including Madagascar, the Mascarenes, and the Galápagos (Van Denburgh 1914, Cheke and Hume 2008, Pedrono 2008). There is also ample evidence of early human tortoise-hunting in mainland habitats from the Paleolithic and onwards, including the Mediterranean Rim and southern Africa (Stiner et al. 1999, Klein and Cruz-Uribe 2000, Blasco 2008).
Some tortoise extinctions, however, occurred prior to human contact. For example, the Caribbean tortoise Hesperotestudo bermudae could have been lost due to partial submergence of its low-rise island home during recent interglacials (Meylan and Sterrer 2000, Olson et al. 2006). Similarly, there is evidence that Aldabra was re-colonised by giant tortoises from Madagascar at least three times, following sea-level changes that caused temporal submergence (Taylor et al. 1979). Projected anthropogenic increases in sea level may thus threaten the world's largest remaining population of giant tortoises, Aldabrachelys gigantea, on Aldabra Atoll. Therefore, in some cases taxon substitution cannot be justified based on redressing past anthropogenic extinctions, but could be debated if the introduction of a generalised herbivore is deemed to be facilitating the desired trajectory of an ecosystem restoration project in such places. Indeed, this approach could be a good example of “restoring for the future” (Choi 2007, Macdonald 2009), e.g. maximising future ecosystem resilience.
Few extant tortoises have been studied in sufficient detail to assign an updated IUCN Red List Category. Researchers have argued, however, that almost all extant tortoises are declining, and that many species should be considered endangered (Bonin et al. 2006, Branch 2008). Current threats to tortoises include collection by humans, introduced predators, and climate change (Erasmus et al. 2002, Bonin et al. 2006).
Tortoises as ecological and evolutionary keystone species
True land tortoises (family Testudinidae) arose around 55 million years ago, and are part of the oldest surviving reptile lineage (Auffenberg 1974, Bonin et al. 2006). The slow metabolism of tortoises and their ability to withstand long periods without food or water have enabled them to colonise almost all continents and many islands, with most species found in subtropical and tropical regions. Tortoises are important components of many ecosystems, and often attain high densities and biomass (Iverson 1982). For example, Astrochelys radiata density estimates in Madagascar vary from 1250 to 5400 tortoises km−2 (Leuteritz et al. 2005). On Aldabra, biomass of A. gigantea has been estimated to be between 3.5 and 58 tonnes per square kilometer – more than the combined biomass of various species of large mammalian herbivores in any African wildlife area (Coe et al. 1979). In some African game parks, tortoise biomass outweighs that of several species of large mammalian herbivores (Iverson 1982, Branch 2008). Most extant tortoise species are highly generalised herbivores, frugivores or omnivores (Grubb 1971, Milton 1992, Bonin et al. 2006, Branch 2008). Tortoises do not masticate their food, have a relatively simple digestive system, and many species have flexible digestive responses that are determined by diet (Guard 1980, Bjorndal 1989, Barboza 1995, Hailey 1997, McMaster and Downs 2008). It is likely that extinct tortoises had similarly broad diets.
In many ecosystems, tortoises are thus likely to be or have been keystone species; not in the classical sense as it pertains to ecosystem importance in relation to biomass (Paine 1969), but rather in relation to the topological position and importance of tortoises in interaction- and food webs (Jordán 2009). A good example is the gopher tortoise Gopherus polyphemus, which influences a number of key processes in North American long-leaf pine grasslands and forest ecosystems, including herbivory, seed dispersal, nutrient cycling, and creating and maintaining habitat heterogeneity via trampling or digging of burrows (Kaczor and Hartnett 1990, Carlson et al. 2003, Birkhead et al. 2005, van Lear et al. 2005, Means 2006). Oceanic island ecosystems also offer many examples; given tortoises’ propensity for long-distance oceanic dispersal, they were likely often among the first large, non-volant vertebrates to colonise oceanic islands – thus shaping these isolated ecosystems from early on in their history (Hnatiuk 1978, Arnold 1979, Meylan and Sterrer 2000, Gerlach et al. 2006). The resulting long, shared ecological and evolutionary histories of island tortoises and their plant communities has shaped many plant-tortoise interactions, many of which have since been lost as a result of tortoise decline or extinction (Iverson 1987, Strasberg 1996, Eskildsen et al. 2004, Gibbs et al. 2008, Hansen et al. 2008, Hansen and Galetti 2009, Griffiths et al. 2010). For example, “tortoise turf”, a plant community of endemic grass, herb and sedge species and engineered by continuous tortoise grazing and trampling, is thought to have been common on islands throughout the Indian Ocean before tortoises went extinct; it is now restricted to Aldabra (Merton et al. 1976, Cheke and Hume 2008).
Furthermore, evidence is mounting that tortoises are or were important seed dispersers on continents and islands in ecosystems ranging from coastal shrub and dry deserts to rainforests (Rick and Bowman 1961, Hnatiuk 1978, Milton 1992, Varela and Bucher 2002, Strong and Fragoso 2006, Hansen et al. 2008, Jerozolimski et al. 2009). Tortoises can eat large amounts of fruits and swallow relatively large fruits and seeds. For example, yellow-footed tortoises Chelonoidis denticulata in Brazil with average carapace lengths of only 25–30 cm defecated seeds up to 4.0×1.7 cm in size (Jerozolimski et al. 2009). Variable gut passage times have been reported for tortoises, with average values ranging from a few days to three weeks, allowing for mean dispersal distances of several hundred metres (Rick and Bowman 1961, Hansen et al. 2008, Jerozolimski et al. 2009).
Tortoises represent low-risk, high-impact taxon substitutions
On many islands, tortoise extinction has resulted in dysfunctional ecosystems with respect to seed dispersal and herbivory (Gibbs et al. 2008, Hansen et al. 2008, Hansen and Galetti 2009, Griffiths et al. 2010). On continents, the greater array of extant native herbivores and frugivores has likely helped buffer the ecological losses of tortoises (Hansen and Galetti 2009). Thus, tortoise taxon substitutions are arguably more imperative and appropriate on islands. Indeed, the impact and conservation value of tortoise taxon substitutions on islands is likely to be greater than suggested for mainland scenarios, due to the simpler ecosystems that have only recently been subjected to anthropogenic impacts (Kaiser-Bunbury et al. 2010).
Tortoises can be regarded as low-risk taxon substitutes (Griffiths et al. 2010). Due to their highly generalised diets and relatively minimal reintroduction requirements, it is likely that tortoises introduced as taxon substitutions would be able to reestablish some ecosystem functions of the extinct tortoises and become integral parts of their new ecosystems. We highlight five reasons for large tortoises being particularly well suited for taxon substitutions.
1) Populations of large tortoises have high intrinsic growth rates and are easy to breed or rear in captivity. If juveniles are headstarted in captivity, they have high survival rates even in the presence of introduced predators (MacFarland et al. 1974a).
2) Tortoises are easy and cheap to fence in. This is especially important for their use in the relatively small conservation management areas found on many oceanic islands. Moreover, within fenced areas, it is easy to up- and down-regulate tortoise numbers and size of individuals, even in large areas or on a seasonal basis. Excess individuals can be kept in holding pens elsewhere, or cordoned-off sections of the restoration area, and require comparatively little husbandry. Similar techniques are used for livestock – de facto taxon substitutes for extinct large mammalian herbivores – in large-scale continental grassland restoration projects (Papanastasis 2009).
3) Their versatility enables them to be introduced into a wide range of habitats of varying qualities including highly degraded areas, making tortoises an attractive option for early-stage restoration efforts. There is some evidence that native plant species and communities evolved to withstand tortoise herbivory on islands (Merton et al. 1976, Eskildsen et al. 2004). This can lead to tortoise taxon substitutes actively preferring introduced and invasive plant species, leading to competitive release for the native species and thus further facilitating habitat recovery (Griffiths et al. 2010).
4) The risk of negatively impacting disease dynamics of the native fauna is small. Reptile diseases and parasites are typically species-specific, with little risk of transfer to other reptiles or other vertebrates (Cooper and Jackson 1981). However, several tortoise species and populations are increasingly affected by within-species diseases (Flanagan 2000). Thus, disease screening and quarantine measures are essential before tortoise taxon substitutions, especially if sourcing individuals from several populations.
5) While there are naturalised populations of medium- and large-sized tortoises in several places around the world (e.g. Balearic Islands, Caribbean Islands, Lever 2003), the risk of tortoises becoming invasive pests is remote, given their life history traits. More importantly, the nature of tortoises facilitates management; the removal of a recently introduced population is feasible if deemed necessary.
There are important considerations and risks that will need mitigating before moving forward on any tortoise taxon substitution program. Because of their highly generalised diet, precautions must be taken to avoid tortoises assisting in the spread of invasive plant species via defecated seeds. Giant Aldabra tortoises released on Curieuse Island in the Seychelles have been observed feeding on fruits and seeds of several invasive plant species, and may be a contributing factor to their spread there (Hambler 1994). Similarly, tortoise taxon substitutions in the Galápagos could lead to an increased rate of invasion of some plant species, such as bramble Rubus niveus which tortoises consume (R. Atkinson pers. comm.). Proper quarantine measures that determine passage times for 100% of ingested seeds are critical. When A. gigantea tortoises were quarantined before translocation to Round Island, Mauritius, some seeds took as long as three months to pass through the tortoises' guts (Griffiths unpubl.).
Another point to consider is the length of time required for tortoises to reach full size; while breeding and rearing large tortoises to use in rewilding projects may be straightforward, the time required may be a disadvantage in relation to projects that need a here-and-now capacity for restoring ecosystem function. In Galápagos, for example, there are plenty of small juvenile tortoises in the breeding centre that could be used immediately for taxon substitution projects. Yet with respect to potentially controlling biomass of invasive plants, the impact of one adult tortoise would be much greater than that of dozens of small juveniles. To swiftly reach specific restoration goals it may therefore be preferable to also use translocated adults.
Selection of the taxon to be used for substitution must be strongly supported by ecological history, and balanced between phylogeny and natural history (Martin 1969, Donlan et al. 2006). For taxon substitutions whose goal centers on restoring species interactions or ecosystem function, choosing the genetically closest extant tortoise as a substitute may in some cases not be an appropriate selection criterion (contrary to what the IUCN reintroduction guidelines currently advise; IUCN 1998). This could be the case in an ecosystem where the closest relative of an extinct desert tortoise species is found in a rainforest, or in ecosystems where morphological divergence between species has led to more or less separate diets or feeding behaviours (see the Galápagos case story below for an illustrative example).