Distribution, status, and conservation of radiated tortoises (Geochelone radiata) in Madagascar

The radiated tortoise, Geochelone radiata, one of Madagascar’s four endemic tortoises, occupies a narrow band of xeric spiny forest along the island’s southwest coast. Traditionally avoided by indigenous tribes, these tortoises are now routinely harvested for food. An accurate assessment of human exploitation remains problematic, however, hindered by limited, dated statistics available on tortoise populations. To update the radiated tortoise’s status and distribution, we established a series of line transects at seven localities across its range and implemented a mark-recapture study at one of these localities (Cap Sainte Marie). Tortoises currently range from south of Tulear to east of Cap Sainte Marie, at density estimates spanning 27-5744 tortoises/km². The mark-recapture estimate for Cap Sainte Marie (1905-2105 tortoises/km²) was substantially higher than its transect estimate (654 tortoises/km²) though comparable to actual tortoise captures (1438) there. Thus, our transect density values probably err as underestimates, and from these data, we calculate a conservative total population size of 12 million radiated tortoises. We also examined mitochondrial DNA sequences (ND4 gene) for two individuals/locality in a preliminary assessment of genetic variation across the species’ range. Only two ND4 haplotypes were recovered, the more common haplotype representing 13 of the 14 individuals. We offer several conservation recommendations in light of our survey results.     

Return to the wild: Translocation as a tool in conservation of the Desert Tortoise (Gopherus agassizii)

Translocation could be used as a tool in conservation of the threatened Mojave Desert Tortoise (Gopherus agassizii) by moving individuals from harm’s way and into areas where they could contribute to conservation of the species. Numerous factors may affect the success of translocations, including the conditions experienced by tortoises in holding facilities while awaiting translocation. The tortoises available for our translocation study had been provided supplemental water during their years spent in a captive holding facility, potentially inducing carelessness in water conservation. In addition to generally investigating the efficacy of translocation, we compared the effects of continuing with the effects of ceasing the holding facility’s water supplementation regimen. After exposure to one of the two water regimens, all tortoises were given the opportunity to hydrate immediately prior to release. We examined behavior, body mass, carapace length, movement, and mortality of tortoises for two activity seasons following release to the wild. Water supplementation was correlated with high rates of carapace growth and distant movements by males after release. Lengthy movements following translocation may be problematic for conservation planning, but this should be evaluated in light of the goals and circumstances of each translocation project. Although the mortality rate was 21.4% in 1997, data suggest that drought conditions at the site rather than the translocation itself negatively affected the tortoises. None of the tortoises died during their second season at the site. Our results indicate that translocation should be considered a useful tool in conservation of the Desert Tortoise.     

Long-term apparent survival of translocated gopher tortoises: A comparison of newly released and previously established animals

Most turtle species require high adult survivorship to maintain stable populations. Translocations are often implemented to conserve turtle populations but may cause demographic disturbance as a result of increased mortality or dispersal of released animals. The gopher tortoise (Gopherus polyphemus) is one of the most frequently translocated turtle species. Short-term monitoring indicates that dispersal by released tortoises is common, but few long-term data are available to determine if losses of translocated animals continue for multiple years. We used 12 years of mark-recapture data to investigate long-term apparent survival of two groups of gopher tortoises translocated during separate periods to St. Catherines Island, Georgia, USA. We analyzed capture histories in program MARK to compare apparent survival of newly released tortoises and previously established translocated tortoises and also to determine whether apparent survival varied with sex or maturity. Apparent annual survival did not vary between adult males and females (0.98 ± 0.01), but was lower in sexually immature tortoises (0.84 ± 0.05). We documented a temporary reduction in apparent survival of newly released adult (0.75 ± 0.06) and immature tortoises (0.45 ± 0.26) during the first year after release that may be attributed in part to permanent dispersal. However, for both maturity classes, apparent survival of newly released tortoises was consistently high and matched that of previously established animals during the remainder of the study. Additional long-term studies of both translocated and naturally-occurring populations are needed to improve management of remaining tortoise populations.     

The use of shell morphometrics for the management of the endangered malagasy radiated tortoise (Geochelone radiata)

The radiated tortoise (Geochelone radiata) is an endangered species endemic to the spiny forest of southern Madagascar. The main threat that this species faces is illegal harvesting for both local consumption and foreign markets. Large numbers of live individuals are often confiscated and their population of origin is in most cases unknown. Previous work has identified three genetically distinct units across the current distribution of the species. The objective of the present study was to develop a method of assigning G. radiata individuals to their original population based on the analysis of morphometric characters. We measured 39 variables on the shell of tortoises sampled at seven locations across the species range in order to assess differentiation. We employed a PCA-based method to analyze morphometric data and found three distinct groups of populations based solely on shape variation. Discriminant functions allowed for the correct classification of 83% of individuals among these groups. The abundance of tortoises, a variable strongly linked to the level of human exploitation at each site, was correlated with the morphometric differentiation of populations. Our results thus suggest that humans may have played a role in the recent evolution of radiated tortoises. The outlined methodology could become a useful tool for the management of radiated tortoises, and could theoretically be applied to any chelonian species.     

The Galápagos giant tortoises (Geochelone elephantopus) Part I: Status of the surviving populations

Eleven of the original 15 races of Galápagos tortoises are known to survive. The populations of three of these may be self-replacing. The other eight are threatened with extinction, each by one or more of the following: (1) greatly decreased population size, (2) predation on nests and/or young by introduced pigs, dogs, cats, or black rats, and (3) competition for food resources with feral populations of goats or donkeys. Human exploitation of the tortoise populations has become relatively unimportant in the past few years for a number of reasons, including more wide-spread acceptance of protective laws and the increasing activity of the Servicio del Parque Nacional Galápagos and the Charles Darwin Research Station. Data on population sizes and sex structures, reproductive potential, and natural mortality rates suggest that all but two of the endangered populations could remain stable or even increase in size if the effects of introduced mammals were eliminated or greatly lessened.     

Vital rate sensitivity analysis as a tool for assessing management actions for the desert tortoise

Sensitivity analyses of population growth in desert tortoise (Gopherus agassizii) have shown no consensus on the limiting vital rate. More importantly, the most sensitive vital rate might not be the most readily manipulated by management, so it begs the question of what actions would be most effective. We compared 13 management alternatives using a vital rate sensitivity analysis that is valid regardless of age structure, and is sensitive to initial population size and time frame, to determine the efforts required for equivalent population growth. We evaluated three time frames, each with five initial population sizes and three initial age distributions. To achieve equivalent population growth, mortality of older females needed to be reduced less than did mortality of other age classes. Similarly, fewer adults needed to be introduced to a population to have the same effect as releasing juveniles, but differences among adult age classes were trivial. A single release (headstarting) required fewer total individuals than did annual releases to achieve the same population growth. Also, the same population growth was more easily achieved when the initial age structure was deficient of young animals. Interestingly, because small tortoises are difficult to survey, some management alternatives could result in increased population size but decreased numbers of countable individuals over short to intermediate (25 years) time frames. Our paper demonstrates an approach to determine what constitutes equivalent management actions for population growth, thus allowing managers to more directly compare expected gains toward population recovery achieved by their resource-allocation decisions.     

Coexisting with fire: The case of the terrestrial tortoise Testudo graeca in mediterranean shrublands

Fire and fire management are recognized as important factors in biodiversity conservation. Measuring species-level demographic, behavioural and population responses to different fire regimes is essential for designing adequate management policies. Here we assessed the impact of fire on survival rates, reproduction and movement patterns in Testudo graeca, an endangered terrestrial tortoise inhabiting the Mediterranean region, a system in which fire plays a relevant role in the functioning of their ecosystems. Then we predicted the probabilities of quasi-extinction of T. graeca under several fire regimes and population sizes by means of stochastic population models. Our results showed that fire caused direct and delayed reductions in local survival, young individuals being the most affected. There were not differences in fecundity and movement patterns of tortoises between burned and unburned areas. Population models showed a strong variation in the probability of quasi-extinction of populations depending on the fire regime and the population size. Under fire frequencies similar to those occurring in the wild (<1 fire every 20–30 years) most tortoise populations seemed to buffer the effects of fires. However, when this threshold value of fire frequency was surpassed, the probability of quasi-extinction of populations exploded for all populations, except for those with the largest sizes. T. graeca populations may be able to cope with natural current fire frequencies, but the effects of more recurrent fires may severely threaten the species. Our results have straightforward applications for fire management purposes in those areas of the Mediterranean region where this endangered species is present.     

The ecology of the mediterranean tortoise Testudo hermanni in northern Greece (the effects of a catastrophe on population structure and density)

Two large, dense and viable populations of Testudo hermanni inhabiting adjacent sites in northern Greece were studied over three years. One site experienced severe habitat destruction by fire during the course of the study, and the other may either have been seriously disturbed in a single event several years previously, or is suffering from a continual low level of disturbance. In the stable situation average population density was estimated as 45 tortoises ha ⁻¹ and in parts may have reached 100 ha⁻¹ The adult sex ratio was biased 2:1 in favour of males, due to higher female mortality. Most animals were sedentary, but there were some seasonal movements between vegetation types for feeding. The immediate effect of the fire was an estimated 40% population reduction, with juveniles being most severely affected. Subsequently the growth rate of immature animals rose sharply. This study demonstrates the relative resistance of tortoise populations to a sudden and temporary catastrophe, and their high potential for recovery if left undisturbed.     

Sampling on private property to evaluate population status and effects of land use practices on the gopher tortoise, Gopherus polyphemus

Although private properties are predicted to play an increasingly significant role in conservation, surveys of species of special concern are rare on these lands. We created a template for a multi-county survey of randomly selected sites and sampled for burrows of the gopher tortoise (Gopherus polyphemus) in south-central Georgia, USA. Current land use was strongly correlated with tortoise population condition. The highest densities of tortoise burrows were found on lands with open-canopied pine stands that were managed with prescribed fire, a practice associated with types of selection forestry and/or wildlife management. Agricultural sites and unburned areas provided poor habitat and pine plantations were only slightly better. Our estimates of tortoise population densities indicated that the current landscape supports less than 20% of the animals present before implementation of modern land use practices. In addition, our estimate for density of active burrows was approximately one third of that projected for the entire state range 20 years ago by Auffenberg and Franz [Auffenberg, W., Franz, R., 1982. The status and distribution of the gopher tortoise (Gopherus polyphemus). In: Bury, R.B. (Ed.), North American Tortoises: Conservation and Ecology (US Fish and Wildlife Service Wildlife Research Report 12). pp. 95-126]. However, some good sites for gopher tortoises remain in south Georgia and our data also suggested that extraordinary conservation actions may not be required if ways can be developed to retain traditional land management practices on private property.     

Hatch size, somatic growth rate and size-dependent survival in the endangered ploughshare tortoise

Successful conservation requires a good understanding of both the direct and indirect causes of any decline in population size. Harvests of wild populations often target the largest, oldest individuals that have the greatest economic value. If these individuals contribute disproportionately more to recruitment than conspecifics, the harvest will cause a greater reduction in population viability than initially anticipated. The ploughshare tortoise, endemic to Madagascar, has been reduced to <600 individuals due to exploitation and habitat loss. A trial release of captive-bred juveniles has been carried out but the relative suitability of individuals for release, in terms of body size, was not considered. Using data from a long-term mark-recapture study of an unharvested wild population of ploughshare tortoises, we found that larger juveniles were significantly more likely to survive their first year of life than smaller tortoises. Juveniles that survived beyond their first year of life generally grew at the same rate, but had a significantly larger hatch size (mean = 41.7 mm), compared with juveniles that did not survive (mean = 39.3 mm). The conservation implications of these results are that release of captive-bred ploughshare tortoises is likely to be more successful if larger individuals are released. Previous studies have reported larger female ploughshare tortoises laying larger eggs which hatch larger juveniles. This study shows individuals with a larger hatch size retain their size advantage over smaller conspecifics and are more likely to survive their first year of life. This suggests a harvest that targets the largest females in the ploughshare tortoise population could be highly detrimental to population viability.     

Non-commercial collection of spur-thighed tortoises (Testudo graeca graeca): a cultural problem in southeast Spain

Collecting tortoises for the pet trade is one of the factors threatening species of Testudo in the Mediterranean area. The collection of Testudo graeca graeca for pets is described in southeast Spain, where the main European population of this subspecies coincides with an area where keeping tortoises in captivity is a long-established custom. This present paper, based on inquiries made to children, reveals that this practice continues to be a common activity, and estimates a captive population in the order of tens of thousand of tortoises. Tortoises are collected as a result of chance encounters with wild animals by local inhabitants, and without any commercial objectives. The captive breeding and the release of tortoises without any institutional control is also common. These activities could be an important threat for the species. Implications for conservation are discussed and a critical review of the conservation strategies developed in relation to this threat (trade control and re-introduction programmes) are presented. We suggest that environmental education programmes are necessary to reduce casual collection and to change the social perception of tortoises as pets.     

Phenotype management: a new approach to habitat restoration

The goal of habitat restoration is to provide environmental conditions that promote the maintenance and growth of target populations. But rarely is it considered how the allocation of resources influences the diversity of phenotypes in these populations. Here we present a framework for considering how habitat restoration can shape the development and expression of phenotypes. We call this approach phenotype management as it entails restoring the resources in a habitat to manage phenotypic diversity. Phenotype management is achieved by manipulating the spatial and temporal distribution of resources to alter the degree of competition among individuals. Differences in competition, in turn, lead to changes in phenotypic and life history expression that affect population parameters including demography and effective population size (N_e). To illustrate how phenotype management can be applied, we explore how resource distributions shape variation in phenotypes in two imperiled fishes, Pacific salmon and desert pupfish. In both examples, modulating male reproductive phenotypes changes the allocation of reproductive success among population members to subsequently affect N_e. These examples further demonstrate that whether to increase or decrease phenotypic diversity depends on the primary conservation pressures faced by the species.     

Temperature,activity and field sighting in the mediterranean spur-thighed or common garden tortoise Testudo graeca L

Daylight observations on NW African and W Turkish populations of the Mediterranean spur-thighed tortoise Testudo graeca L. showed that activity, depending upon maturity, sex and size, is influenced by air temperature and sunshine. Tortoises are active above 18°C while refuge from sunshine during the middle of the day occurs above 28°C. Morning basking increases body temperature, which under glass in S England was shown to be thermoregulated at about 35°C. With movements in and out of sunshine, most heat is dissipated through the plastron. Field sighting frequency (no.man-h^?1) as a relative index of abundance in low density populations is influenced by activity and behaviour type. This is discussed with regard to tortoise detection being increased by locomotory rustling and mating sounds in thick vegetation.     

Exposure of coelomocytes from the earthworm Eisenia hortensis to Cu,Cd, and dimethylbenz[a]anthracene: An in vitro study examining reactive oxygen species production and immune response inhibition

The principal aims of this study were to investigate the in vitro effects of copper (Cu), cadmium (Cd) and the polycyclic aromatic hydrocarbon (PAH) dimethylbenz[a]anthracene (DMBA) on reactive oxygen species (ROS) production and the effect of DMBA on immune function (phagocytosis) in coelomocyte samples isolated from the earthworm Eisenia hortensis. Using a fluorogenic indicator of ROS, dihydrorhodamine 123, we show that earthworm coelomocytes are induced to produce significant increases in ROS when exposed to Cu or Cd at 32–250 μM, an effect diminished by the chelator ethylenediaminetetraacetic acid (EDTA). DMBA also induced significant ROS production in the range of 20–400 μM compared to controls. Testing the effect of DMBA on cellular immune mechanisms, we used a phagocytosis assay to reveal an immunosuppressive effect of DMBA (50–200 μM) on the capacity of hyaline amoebocytes to ingest fluorescent Escherichia coli. These studies illustrate the relative ease and efficiency of these in vitro procedures for testing the toxicological effects of environmental pollutants, including heavy metals and PAHs, using earthworm coelomocytes as indicators of oxidative stress and immune response impairment.     

Mating system in a gopher tortoise population established through multiple translocations: Apparent advantage of prior residence

Population manipulations such as translocation are becoming increasingly important tools in the management of rare and declining species. Evaluating the effectiveness of such manipulations requires comprehensive monitoring of population processes, including dispersal, survivorship, and reproduction. We investigated the mating system of a translocated population of gopher tortoises (Gopherus polyphemus) established through multiple releases, which occurred primarily during 1987–1994. During 2006–2007, we sampled and genotyped 27 candidate males (candidate sires), 34 candidate females (candidate dams), and 121 offspring from 19 clutches at five polymorphic microsatellite loci to determine the relative frequency of multiple paternity and to estimate individual reproductive success. Multiple paternity was detected in 57% of clutches genotyped, and females of single-sire clutches and females of multiple-sire clutches were of similar size. Reproductive success varied among male tortoises, and successful sires were significantly larger than males to which no offspring were attributed. Among successful sires, previously established males sired a disproportionate number of the offspring sampled, despite being significantly smaller than subsequently released males. The high variance in individual reproductive success and the apparent reproductive advantage associated with prior residence observed in this gopher tortoise population has important implications for the design of future translocation projects.     

Wild-captive metapopulation viability analysis

We developed an interactive management model for wild and captive populations of the ploughshare tortoise or angonoka, Geochelone yniphora. Interactive management is based on the translocation of individuals between wild and captive populations to simulate a metapopulation. Demographic parameters of one captive and two wild populations of this rare tortoise were used to conduct a metapopulation viability analysis (MVA). The effectiveness of the conservation strategy proposed for this species was then evaluated by modifying the probability of extinction and growth of the metapopulation over a fixed period of time. Several alternative scenarios of interactive management were then tested and ranked in terms of their effect on the viability of the metapopulation. The model predicted that catastrophic events such as bush fires would likely have a negative effect on the future of remaining wild populations. However, the model also predicted that the use of captive-born offspring to establish additional wild populations would decrease the risk of extinction of the metapopulation as a whole. We believe that, when supported by sound knowledge of the demographic parameters of a species, the use of MVA as part of an interactive management program can be an effective conservation tool that allows assessment of the probable response of both captive and wild populations to different management alternatives. One of the most interesting aspects of this interactive management approach is the link between in situ and ex situ conservation.     

The impact of harvester ants on decomposition, N mineralization, litter quality, and the availability of N to plants in the Mojave Desert

In arid areas of North America, nests of the seed-harvesting ant Pogonomyrmex rugosus tend to be elevated in mineral nitrogen and other soil nutrients relative to other microhabitats. We investigated the roles of decomposition, N mineralization, and plant nutrient uptake in maintaining high standing stocks of nutrients in P. rugosus ant nests. Decomposition rates of standard cellulose substrates placed on the surface of ant nests and other desert microhabitats suggest that conditions found in ant nests and bare areas are conducive to higher rates of decomposition than conditions under shrubs. In laboratory incubations of moist soil, net N mineralization rates were significantly higher in soil from ant nests than from bare areas and under two of three plant species. Net N mineralization rates measured in situ were much lower than those measured in laboratory incubations, but ant nest soil still exhibited higher rates at one of two sites. Litter collected from ant mounds, composed chiefly of seed chaff, was similar in N content to litter collected from underneath the dominant plant species, but had a significantly higher mean δ¹⁵N. Using this distinctive isotope signature as a tracer, we found no evidence that large perennial shrubs tap ant nests as a source of N. An invasive, annual grass species was significantly enriched in ¹⁵N, had higher leaf %N, and produced more seeds when growing on the mound than when growing several meters away; however P. rugosus nest surfaces are typically free of such annuals. We conclude that both high rates of nutrient cycling relative to other Mojave Desert microhabitats and low N utilization by the surrounding vegetation contribute to high standing stocks of mineral N in P. rugosus nests.     

Giant tortoise and vegetation interactions on Aldabra atoll—Part 2: Coastal

Grazing by a large population of giant tortoises on Aldabra atoll in the western Indian Ocean may be linked to apparent changes taking place in the coastal grass and scrub lands. This paper presents a circumstantial case for the involvement of the tortoise population in a change from coastal, maritime, scrub-tussock vegetation to one of short, turf grassland.     

A survey of the Aldabra giant tortoise population introduced on Curieuse Island,Seychelles

The Zoological Society of London carried out a field study in the Republic of the Seychelles to obtain biomedical data from the Aldabra giant tortoise population on Curieuse island and assess the progress of the colony within the context of the Curieuse experiment. The biomedical data will be published in full detail elsewhere, but brief details of the sampling methods are included as an integral part of the handling procedure to which the tortoises were subjected. From evidence gathered in the field it appears that the tortoises have adapted well to the environment, are causing little damage and represent a major tourist attraction.The impact of the tourist industry on the Curieuse experiment was assessed and found to be a source of concern in relation to the successful management of the island.A total of 144 post hatchlings, 1 juvenile and 17 hatchlings were found, distributed in 6 out of 9 designated areas on Curieuse. These represent less than 50% of the total of tortoises re-introduced as part of the Curieuse experiment.There is strong evidence of poaching and theft, probably by local inhabitants.     

Impact of introduced honey bees on native pollination interactions of the endemic Echium wildpretii (Boraginaceae) on Tenerife, Canary Islands

The aim of this study was to investigate effects of introduced honey bees (Apis mellifera) on native pollination interactions of Echium wildpretii ssp. wildpretii in the sub-alpine desert of Tenerife. We selected two study populations, one dominated by honey bees, while the other was visited by many native insects. During peak activity period of insects, nectar was nearly completely depleted in flowers of the first, but not the latter population. Thus, a high abundance of honey bees may have suppressed visitation by native animals due to exploitative competition. Honey bees stayed longer and visited more flowers on the same inflorescence than native bees, thus potentially promoting self-pollination of the plants. Level of seed set and viability was similar in the two study populations. However, we cannot rule out long-term changes in genetic population structure due to changes in gene-flow patterns caused by foraging behaviour of honey bees vs. native flower-visitors.