Are the native giant tortoises from the Seychelles really extinct? A genetic perspective based on mtDNA and microsatellite data

The extinction of the giant tortoises of the Seychelles Archipelago has long been suspected but is not beyond doubt. A recent morphological study of the giant tortoises of the western Indian Ocean concluded that specimens of two native Seychelles species survive in captivity today alongside giant tortoises of Aldabra, which are numerous in zoos as well as in the wild. This claim has been controversial because some of the morphological characters used to identify these species, several measures of carapace morphology, are reputed to be quite sensitive to captive conditions. Nonetheless, the potential survival of giant tortoise species previously thought extinct presents an exciting scenario for conservation. We used mitochondrial DNA sequences and nuclear microsatellites to examine the validity of the rediscovered species of Seychelles giant tortoises. Our results indicate that the morphotypes suspected to represent Seychelles species do not show levels of variation and genetic structuring consistent with long periods of reproductive isolation. We found no variation in the mitochondrial control region among 55 individuals examined and no genetic structuring in eight microsatellite loci, pointing to the survival of just a single lineage of Indian Ocean tortoises.     

Transition matrix models and succession after release from grazing on Aldabra atoll

The process of succession after release from grazing by giant tortoises was investigated in three different vegetation types on Aldabra atoll. After four years there was very little change in two vegetation types: a tall mixed scrubland and an open single-species grassland. Probably in the former case grazing had no effect and in the latter case soil nutrients were limiting sward growth and establishment. In the third vegetation type, a patchwork of scrub and low vegetation, analysis of transition matrices showed that the succession was non-independent, non-stationary and depended on more than one past state (high order). This succession was extrapolated by simulation. The results suggested that other vegetation types studied were discrete associations, not merely different stages in the same grazing-mediated sere. The transition matrix approach proved useful in helping to generate initial hypotheses, but became too cumbersome for a realistic model of this succession. An experimental approach will be better for dealing with problems identified from the transition models. We are extremely grateful to the staff of the Seychelles Islands Foundation and of their Aldabra Research Station for permission to work on the island and for their assistance in the field.     

Persistence of distinctive morphotypes in the native range of the CITES‐listed Aldabra giant tortoise

Understanding the extent of morphological variation in the wild population of Aldabra giant tortoises is important for conservation, as morphological variation in captive populations has been interpreted as evidence for lingering genes from extinct tortoise lineages. If true, this could impact reintroduction programmes in the region. The population of giant tortoises on Aldabra Atoll is subdivided and distributed around several islands. Although pronounced morphological variation was recorded in the late 1960s, it was thought to be a temporary phenomenon. Early researchers also raised concerns over the future of the population, which was perceived to have exceeded its carrying capacity. We analyzed monthly monitoring data from 12 transects spanning a recent 15‐year period (1998–2012) during which animals from four subpopulations were counted, measured, and sexed. In addition, we analyzed survival data from individuals first tagged during the early 1970s. The population is stable with no sign of significant decline. Subpopulations differ in density, but these differences are mostly due to differences in the prevailing vegetation type. However, subpopulations differ greatly in both the size of animals and the degree of sexual dimorphism. Comparisons with historical data reveal that phenotypic differences among the subpopulations of tortoises on Aldabra have been apparent for the last 50 years with no sign of diminishing. We conclude that the giant tortoise population on Aldabra is subject to varying ecological selection pressures, giving rise to stable morphotypes in discrete subpopulations. We suggest therefore that (1) the presence of morphological differences among captive Aldabra tortoises does not alone provide convincing evidence of genes from other extinct species; and (2) Aldabra serves as an important example of how conservation and management in situ can add to the scientific value of populations and perhaps enable them to better adapt to future ecological pressures.     

Low‐coverage reduced representation sequencing reveals subtle within‐island genetic structure in Aldabra giant tortoises

Aldabrachelys gigantea (Aldabra giant tortoise) is one of only two giant tortoise species left in the world and survives as a single wild population of over 100,000 individuals on Aldabra Atoll, Seychelles. Despite this large current population size, the species faces an uncertain future because of its extremely restricted distribution range and high vulnerability to the projected consequences of climate change. Captive‐bred A. gigantea are increasingly used in rewilding programs across the region, where they are introduced to replace extinct giant tortoises in an attempt to functionally resurrect degraded island ecosystems. However, there has been little consideration of the current levels of genetic variation and differentiation within and among the islands on Aldabra. As previous microsatellite studies were inconclusive, we combined low‐coverage and double‐digest restriction‐associated DNA (ddRAD) sequencing to analyze samples from 33 tortoises (11 from each main island). Using 5426 variant sites within the tortoise genome, we detected patterns of within‐island population structure, but no differentiation between the islands. These unexpected results highlight the importance of using genome‐wide genetic markers to capture higher‐resolution genetic structure to inform future management plans, even in a seemingly panmictic population. We show that low‐coverage ddRAD sequencing provides an affordable alternative approach to conservation genomic projects of non‐model species with large genomes.     

Plant dispersal by the Aldabran giant tortoise,Geochelone gigantea (Schweigger)

Summary A total of 28 species of grasses, herbs, and woody plants germinated from faeces of Aldabran giant tortoises. It seems likely that all members of the land flora can be ingested by tortoises and so may be dispersed by them over short distances.The tortoises are thought to have derived from a Madagascan stock and reached Aldabra from time to time by transmarine migration until the extermination of the Madagascan tortoises about 1100 years ago. The time taken by a tortoise to void its last meal is much longer than that required to float, at present current speeds, from Madagascar to Aldabra. If neither of these parameters have changed since the tortoise migrations to Aldabra, the tortoises may have been responsible for the introduction of plant species to Aldabra.     

Feeding response of the Aldabra giant tortoise (Geochelone gigantea) to island plants showing heterophylly

Aim Heterophylly is present in many plant species on oceanic islands. Almost all of these plants are island endemics, and heterophylly may have evolved as a response to feeding from large insular browsers such as giant tortoises and flightless birds. We tested this anti‐browser hypothesis by feeding Aldabra giant tortoises (Geochelone gigantea) with leaves of native Mauritian plants to see if they distinguished between juvenile and adult leaves and between heteophyllous and homophyllous species. Location Mauritius. Methods In a choice experiment we recorded feeding response of four captive Aldabra giant tortoises to 10 species of Mauritian plants, of which seven were heterophyllous and three homophyllous. Results In general, juvenile leaves of heterophyllous species showed convergence in shape and midrib coloration. Homophyllous foliage was preferred to heterophyllous, and among heterophyllous species adult foliage was preferred to juvenile. Main conclusions Several Mascarene heterophyllous plants show convergence in morphology of juvenile leaves and these are avoided by giant tortoises. This indicates a strong selection history from large browsers such as the giant tortoises. The Mascarene example is in accordance with several other comparable cases of plant‐large browser interactions from other archipelagos.     

How marine currents influenced the widespread natural overseas dispersal of reptiles in the Western Indian Ocean region

In a recent contribution to this journal, Wilmé et al. (2016) proposed that the giant tortoises of the islands of the Western Indian Ocean (WIO: Aldabra, the Mascarenes, and the Granitic Seychelles) might have originated from translocation by early Austronesian sailors. Prompted by this paper we review recent literature and show that natural overseas dispersal was remarkably widespread in the colonization history of terrestrial reptiles in the WIO region. Almost 90% of the successful colonization events are supported by prevailing marine surface currents. However, these currents may change over geological (and evolutionary) time‐scales, and eddies and counter‐currents may facilitate transport against the main current direction. We review the cases of the extant and extinct WIO giant tortoises and suggest that the current distribution of all lineages can be convincingly explained by overseas dispersal.     

Giant tortoise habitats under increasing drought conditions on Aldabra Atoll—Ecological indicators to monitor rainfall anomalies and related vegetation activity

Aldabra Atoll has the largest population of giant tortoises (Aldabrachelys gigantea) in the world. As such an important biological resource, it is necessary to understand how the effects of climate change will impact this keystone species; in particular the frequency of drought, which is likely to affect tortoise habitat. To assess whether drought frequency has changed over the last 50 years on Aldabra, we calculated the standardized precipitation index (SPI) to identify drought periods using monthly rainfall data collected during 1969–2013. We found that drought frequency has increased to more than six drought months per year today compared with about two months per year in the 1970s (t = 2.884, p = 0.006). We used MODIS normalized difference vegetation index (NDVI) as a proxy for vegetation activity, to determine how vegetation has responded to the changing drought frequency between 2000 and 2013. We found that Aldabra’s vegetation is highly responsive to changes in rainfall: anomalies in long-term mean monthly NDVI across Aldabra were found to decrease below the mean during most drought periods and increase above the mean during most non-drought periods. To investigate the response of tortoise habitat to rainfall, we extracted mean NDVI anomalies for three key habitat types. Open mixed scrub and grasslands, the preferred habitat of tortoises, showed the greatest decrease in vegetation activity during drought periods, and the greatest increase in average greenness during non-drought periods. Recent analysis has shown vegetation changes on Aldabra in recent decades. If these changes are caused by decreased precipitation, then the increased frequency of drought could impact the tortoise population, in both the short and long term, by limiting the quality and quantity of forage and/or shade availability within favoured habitats, and by changing the habitat composition across the atoll.     

The evolutionary origin of Indian Ocean tortoises (Dipsochelys)

Today, the only surviving wild population of giant tortoises in the Indian Ocean occurs on the island of Aldabra. However, giant tortoises once inhabited islands throughout the western Indian Ocean. Madagascar, Africa, and India have all been suggested as possible sources of colonization for these islands. To address the origin of Indian Ocean tortoises (Dipsochelys, formerly Geochelone gigantea), we sequenced the 12S, 16S, and cyt b genes of the mitochondrial DNA. Our phylogenetic analysis shows Dipsochelys to be embedded within the Malagasy lineage, providing evidence that Indian Ocean giant tortoises are derived from a common Malagasy ancestor. This result points to Madagascar as the source of colonization for western Indian Ocean islands by giant tortoises. Tortoises are known to survive long oceanic voyages by floating with ocean currents, and thus, currents flowing northward towards the Aldabra archipelago from the east coast of Madagascar would have provided means for the colonization of western Indian Ocean islands. Additionally, we found an accelerated rate of sequence evolution in the two Malagasy Pyxis species examined. This finding supports previous theories that shorter generation time and smaller body size are related to an increase in mitochondrial DNA substitution rate in vertebrates.     

Patterns of activity and body temperature of Aldabra giant tortoises in relation to environmental temperature

We studied the temperature relations of wild and zoo Aldabra giant tortoises (Aldabrachelys gigantea) focusing on (1) the relationship between environmental temperature and tortoise activity patterns (n = 8 wild individuals) and (2) on tortoise body temperature fluctuations, including how their core and external body temperatures vary in relation to different environmental temperature ranges (seasons; n = 4 wild and n = 5 zoo individuals). In addition, we surveyed the literature to review the effect of body mass on core body temperature range in relation to environmental temperature in the Testudinidae. Diurnal activity of tortoises was bimodally distributed and influenced by environmental temperature and season. The mean air temperature at which activity is maximized was 27.9°C, with a range of 25.8–31.7°C. Furthermore, air temperature explained changes in the core body temperature better than did mass, and only during the coldest trial, did tortoises with higher mass show more stable temperatures. Our results, together with the overall Testudinidae overview, suggest that, once variation in environmental temperature has been taken into account, there is little effect of mass on the temperature stability of tortoises. Moreover, the presence of thermal inertia in an individual tortoise depends on the environmental temperatures, and we found no evidence for inertial homeothermy. Finally, patterns of core and external body temperatures in comparison with environmental temperatures suggest that Aldabra giant tortoises act as mixed conformer–regulators. Our study provides a baseline to manage the thermal environment of wild and rewilded populations of an important island ecosystem engineer species in an era of climate change.     

Human‐mediated dispersals do not explain tortoise distribution on the Indian Ocean's islands

Origins of giant tortoises on the Indian Ocean's islands have been debated, and most recently attributed to human translocation (see Wilmé, Patrick, & Ganzhorn, 2017). To resolve the issue, we analyse all available molecular sequences from extinct and extant Indian Ocean's giant tortoises, along with major clades of the family Testudinidae using phylogenetic methods, Bayesian inference and maximum likelihood, and a relaxed time calibration approach. Our results most strongly support giant tortoises of the genus Cylindraspis evolving in situ in the Mascarene Islands since the early mid‐Miocence, and Aldabra tortoises diverging from a Madagascan lineage in the early Oligocene. The geologic time‐scale of these speciation events and the resulting island endemism for each lineage do not support human translocation, but rather demonstrate the impressive ability of giant tortoises to disperse long distances across oceans.     

The biology of terns nesting at Aldabra Atoll, Indian Ocean, with particular reference to breeding seasonality

Five species of tern breed on Aldabra Atoll (09° 24' S; 46° 20' E). The Caspian tern Sterna caspia and Crested tern S. bergii feed exclusively in very shallow reef/lagoon water, the Fairy tern Gygis alba and Brown noddy Anous stolidus feed out at sea, and the Black-naped tern Sterna sumatrana is intermediate in its foraging. Both of the shallow-water species lay during the south-east monsoon season, the Caspian tern from April to August and the Crested tern from June to August, but the Crested tern also lays in December and January. The remaining three species have extended laying periods largely circumscribed by the north-west monsoon season from November to March. Breeding population size of the Caspian tern is in the low tens and of the Brown noddy in the low thousands, with the other species each numbering in the hundreds. The distribution and abundance of the nine species of tern breeding within the Seychelles ( sensu lato ) vary on the different island groups in a manner interpretable in terms of depth of the surrounding waters. Systematic differences between the central Seychelles and Aldabra groups in timing of breeding by terns which feed out at sea may be associated with seasonal latitudinal movement of the divergence zone between the South Equatorial Current and the Equatorial Counter-current, acting via correlated latitudinal shifts of prey species and game-fish abundance.     

Was there a second adaptive radiation of giant tortoises in the Indian Ocean? Using mitochondrial DNA to investigate speciation and biogeography of Aldabrachelys (Reptilia,Testudinidae)

A radiation of five species of giant tortoises (Cylindraspis) existed in the southwest Indian Ocean, on the Mascarene islands, and another (of Aldabrachelys) has been postulated on small islands north of Madagascar, from where at least eight nominal species have been named and up to five have been recently recognized. Of 37 specimens of Madagascan and small-island Aldabrachelys investigated by us, 23 yielded significant portions of a 428-base-pair (bp) fragment of mitochondrial (cytochrome b and tRNA-Glu), including type material of seven nominal species (A. arnoldi, A. dussumieri, A. hololissa, A. daudinii, A. sumierei, A. ponderosa and A. gouffei). These and nearly all the remaining specimens, including 15 additional captive individuals sequenced previously, show little variation. Thirty-three exhibit no differences and the remainder diverge by only 1-4 bp (0.23-0.93%). This contrasts with more widely accepted tortoise species which show much greater inter- and intraspecific differences. The non-Madagascan material examined may therefore only represent a single species and all specimens may come from Aldabra where the common haplotype is known to occur. The present study provides no evidence against the Madagascan origin for Aldabra tortoises suggested by a previous molecular phylogenetic analysis, the direction of marine currents and phylogeography of other reptiles in the area. Ancient mitochondrial DNA from the extinct subfossil A. grandidieri of Madagascar differs at 25 sites (5.8%) from all other Aldabrachelys samples examined here.     

Reproductive study of Giant tortoises on Aldabra

A population of 150,000 Giant tortoises occurs on the Indian Ocean atoll of Aldabra. During the course of an extensive census and marking programme a preliminary reproductive study was carried out. This paper describes the pattern of seasonal ovarian development and the seasonal cycle of breeding activity that was observed.     

Translocation as a conservation tool for Agassiz's desert tortoises: Survivorship,reproduction, and movements

We translocated 120 Agassiz's desert tortoises to 5 sites in Nevada and Utah to evaluate the effects of translocation on tortoise survivorship, reproduction, and habitat use. Translocation sites included several elevations, and extended to sites with vegetation assemblages not typically associated with desert tortoises in order to explore the possibility of moving animals to upper elevation areas. We measured survivorship, reproduction, and movements of translocated and resident animals at each site. Survivorship was not significantly different between translocated and resident animals within and among sites, and survivorship was greater overall during non-drought years. The number of eggs produced by tortoises was similar for translocated and resident females, but differed among sites. Animals translocated to atypical habitat generally moved until they reached vegetation communities more typical of desert tortoise habitat. Even within typical tortoise habitat, tortoises tended to move greater distances in the first year after translocation than did residents, but their movements in the second or third year after translocation were indistinguishable from those of resident tortoises. Our data show that tortoises translocated into typical Mojave desert scrub habitats perform well; however, the large first-year movements of translocated tortoises have important management implications. Projects that employ translocations must consider how much area will be needed to contain translocated tortoises and whether roads need fencing to prevent the loss of animals. © 2012 The Wildlife Society.     

Giant tortoises spread to western Indian Ocean islands by sea drift in pre‐Holocene times,not by later human agency – response to Wilmé et al. (2016a)

Evidence from DNA phylogeny, Plio‐Pleistocene ocean currents, giant tortoise dispersal, evolution of plant defences, radiocarbon dates and archaeology indicates that the endemic giant tortoises on the Mascarenes and Seychelles colonized naturally and were not translocated there by humans.     

The evolution of island gigantism and body size variation in tortoises and turtles

Extant chelonians (turtles and tortoises) span almost four orders of magnitude of body size, including the startling examples of gigantism seen in the tortoises of the Galapagos and Seychelles islands. However, the evolutionary determinants of size diversity in chelonians are poorly understood. We present a comparative analysis of body size evolution in turtles and tortoises within a phylogenetic framework. Our results reveal a pronounced relationship between habitat and optimal body size in chelonians. We found strong evidence for separate, larger optimal body sizes for sea turtles and island tortoises, the latter showing support for the rule of island gigantism in non-mammalian amniotes. Optimal sizes for freshwater and mainland terrestrial turtles are similar and smaller, although the range of body size variation in these forms is qualitatively greater. The greater number of potential niches in freshwater and terrestrial environments may mean that body size relationships are more complicated in these habitats.     

Resurrecting extinct interactions with extant substitutes

There is increasing evidence that restoration ecologists should be most concerned with restoring species interactions rather than species diversity per se [1]. Rewilding with taxon substitutes, the intentional introduction of exotic species to replace the ecosystem functions of recently extinct species, is one way to reverse ecosystem dysfunction following the loss of species interactions [2]. This is highly controversial [3], in part because of a lack of rigorous scientific studies [4]. Here we present the first empirical evidence of an in situ rewilding project undertaken as a hypothesis-driven ecosystem management option. On Ile aux Aigrettes, a 25-hectare island off Mauritius, the critically endangered large-fruited endemic ebony, Diospyros egrettarum (Ebenaceae), was seed-dispersal limited after the extinction of all native large-bodied frugivores, including giant tortoises. We introduced exotic Aldabra giant tortoises, Aldabrachelys gigantea, to disperse the ebony seeds. Not only did the tortoises ingest the large fruits and disperse substantial numbers of ebony seeds, but tortoise gut passage also improved seed germination, leading to the widespread, successful establishment of new ebony seedlings. Our results demonstrate that the introduction of these exotic frugivores is aiding the recovery of ebonies. We argue for more reversible rewilding experiments to investigate whether extinct species interactions can be restored.     

Feral cats (Felis catus) as predators of hatchling green turtles (Chelonia mydas)

In many parts of the world feral animals have been reported to have severe effects on marine turtle hatchling production. In this study, green turtle ( Chelonia mydas ) hatchlings were shown to be an important component of the diet of the feral cat ( Felis catus ) on Aldabra Atoll, Seychelles, and feral cat activity in the coastal areas was found to be concentrated on the beaches used most intensively by turtles for nesting. The impact of the feral cat's predation on green turtle recruitment could not be determined. However, despite cat predation, the size of the Aldabran green turtle nesting population has increased considerably since human exploitation ceased.