Tortoise Testudo Research Articles

Multiple paternity and sperm storage in captive Hermann's tortoises, Testudo hermanni boettgeri determined from amniotic fluid adhering to the eggshell

We identified multiple paternity in 52.9% of the clutches of Hermann's tortoise Testudo hermanni boettgeri using polymorphic microsatellite markers. In addition we demonstrated sperm storage across seasons. DNA was extracted from the amniotic fluid adhering to the eggshell's inner surface, a procedure suitable for easy, non-invasive DNA sampling in conservation and breeding programs. To improve the informative value of monomorphic single tandem repeat (STR) markers we additionally analyzed single nucleotide polymorphism (SNP) variability.

Ticks imported to Europe with exotic reptiles

It is known that traded exotic animals carry with them an immense number of associated symbionts, including parasites. Reptiles are no exception. Most of the imported reptiles originate from tropical countries and their possibility to carry potentially dangerous pathogens is high. According to CITES, Europe is currently the main reptile importer in the world. Despite this, there is no review or analysis available for the risk related to the importation of tick-borne diseases with traded reptile to the EU. The main aim of the manuscript is to provide a review on the available literature on ticks introduced to and exchanged between European countries via the live reptile trade. So far, the published reports of ticks imported on reptiles are limited to few European countries: Italy, Poland, Spain, Netherlands, Belgium, Slovenia and UK. The following species have been reported: Hyalomma aegyptium, Amblyomma dissimile, Amblyomma exornatum, Amblyomma flavomaculatum, Amblyomma fuscolineatum, Amblyomma latum, Amblyomma quadricavum, Amblyomma marmoreum, Amblyomma nuttalli, Amblyomma sparsum, Amblyomma sphenodonti, Amblyomma transversale and Amblyomma varanense. The majority of species are of African origin, followed by American and Asian species. All groups of reptiles (chelonians, snakes, lizards, crocodiles, tuataras) were involved. However, it seems that certain groups (i.e. tortoises of genus Testudo, monitor lizards of genus Varanus, snakes of genus Python) are more important as host for imported ticks, but this may be related to higher levels of international trade. Even fewer are the reports of tick-borne pathogens associated with imported reptile ticks. Despite the diversity of tick species reported on imported reptiles, the situations of truly invasive species are atypical and are limited in natural environments to maximum two cases where H. aegyptium was involved. Otherwise, the risk associated with reptile trade for introduction of invasive tick to Europe is low. Nevertheless, veterinary control is still to be reinforced for collecting more data.

Individualistic response to past climate changes: niche differentiation promotes diverging Quaternary range dynamics in the subspecies of Testudo graeca

Understanding how species have responded to past climate changes might inform how current climate change may affect species. However, current perspectives on species’ response to Quaternary cycles mainly stem from studies on mid and high latitudes and limited information is available at lower latitudes. In these systems a greater variation in individual species’ responses to glacial cycles has been suggested, but we lack of clear case studies of such variations. Here, by means of ecological niche modelling, we characterized the niche differentiation of the five subspecies of the tortoise Testudo graeca in north Africa and described the range dynamics suffered by each of the subspecies since the Last Glacial Maxima. Molecular data was employed to infer past population dynamics.The five subspecies present a clear niche differentiation, particularly in relation to rainfall, covering a range from semiarid to humid species. The ecological differentiation among subspecies promotes very different, even opposite, post‐glacial range dynamics. Since the Last Glacial Maxima, the ranges have either expanded (T. g. graeca), contracted (T. g. marokkensis), shifted northwards (T. g. soussensis) or remained stable (T. g. cyrenaica and T. g. nabeulensis). Molecular data supported the majority of these range dynamics. Our work exemplifies how, in a climate change scenario, phylogenetically very close taxa (i.e. at the subspecies level) might experience strikingly different biogeographical dynamics due to former niche differentiation. Our work supports an individualistic response to glacial cycles, which can be particularly strong in lower latitudes. In these areas precipitation changes during glacial periods may have strongly affected distribution ranges in idiosyncratic ways. We hypothesize that in those species limited by precipitation the response to glacial cycles (and climate changes) is more unpredictable than in those limited by temperature.

Captive breeding the Critically Endangered Egyptian tortoise Testudo kleinmanni Lortet, 1883, for an in situ recovery project in Egypt

The Egyptian tortoise Testudo kleinmanni (Family Testudinidae) is a small‐sized tortoise with a carapace length of up to 140 mm that inhabits an arid to semi‐arid range extending over the coastal regions of Egypt and Libya, and some interior desert areas of Israel. The species is almost completely herbivorous. Population sizes have been under severe pressure for decades. Causes of the decline are overgrazing by cattle, intensification of agriculture and overcollecting for the international pet trade. In Egypt the species is virtually extinct. Since 2000, the breeding programmes of both the European Association of Zoos and Aquaria and the European Studbook Foundation have been coordinated. In the northern Sinai desert, a recovery project has been established, supported by the local Sweirki Bedouin tribe and coordinated by Nature Conservation Egypt. Linking the in situ project to the ex situ breeding programmes forms the basis for the conservation and recovery of the Egyptian tortoise in Egypt.

Computational aspects of N-mixture models.

The N-mixture model is widely used to estimate the abundance of a population in the presence of unknown detection probability from only a set of counts subject to spatial and temporal replication (Royle, 2004, Biometrics 60, 105–115). We explain and exploit the equivalence of N-mixture and multivariate Poisson and negative-binomial models, which provides powerful new approaches for fitting these models. We show that particularly when detection probability and the number of sampling occasions are small, infinite estimates of abundance can arise. We propose a sample covariance as a diagnostic for this event, and demonstrate its good performance in the Poisson case. Infinite estimates may be missed in practice, due to numerical optimization procedures terminating at arbitrarily large values. It is shown that the use of a bound, K, for an infinite summation in the N-mixture likelihood can result in underestimation of abundance, so that default values of K in computer packages should be avoided. Instead we propose a simple automatic way to choose K. The methods are illustrated by analysis of data on Hermann's tortoise Testudo hermanni.

Sighting frequency decreases over two decades in three populations of Testudo hermanni from central Italy

Sighting frequency of tortoises (Testudo hermanni), standardized by the number of person-hours of field effort, was studied between 1992 and 2013 at three different study areas in central Italy. Although the frequency of tortoise sightings fluctuated substantially across years and among study areas, there was a significant declining trend in all the three areas, with GLM analyses showing also a significant interaction between study area and sampling year. The decreasing trend was higher in Castel Fusano than in the other two sites, with yearly frequency of sightings being independent of search effort in all of the study areas. These trends may indicate population declines, because no other explanations seem plausible. Total rainfall from previous autumn to the study period was positively correlated to tortoise sightings in only one locality. The yearly frequency of sightings of juvenile tortoises did not vary significantly among study areas and across years, thus indicating that simple differences in detectability cannot explain the observed patterns. Summer fires and forest overgrowing seem to explain the tortoise decline in two study areas (Castel Fusano and Oriolo) whereas we were not able to identify any specific reason for tortoise decline in the third study area (Manziana).

Explorations in anatomy: the remains from Royal London Hospital

This paper considers the faunal remains from recent excavations at the Royal London Hospital. The remains date to the beginning of the 19th century and offer an insight into the life of the hospital's patients and practices of the attached medical school. Many of the animal remains consist of partially dissected skeletons, including the unique finds of Hermann's tortoise (Testudo hermanni) and Cercopithecus monkey. The hospital diet and developments in comparative anatomy are discussed by integrating the results with documentary research. They show that zooarchaeological study of later post-medieval material can significantly enhance our understanding of the exploitation of animals in this period

The injuries on tortoise shells as a depository of past human impact

The spur-thighed tortoise Testudo graeca has a wide distribution encompassing southern Europe and the Middle East through to northern Africa. The populations at the northern limit of T. graeca’s range in the province of Dobrogea (Romania) are sparsely distributed across the entire area, with higher densities found in the hilly forested areas. Although strictly protected, the spur-thighed tortoise was and continues to be impacted by human activities. This study investigated the presence and characteristics of scars from past injuries on their shells. We studied three populations from protected areas, situated along a north–south gradient of approximately 150 km: Măcin Mountains National Park (northernmost limit of T. graeca’s range), Cetatea Histria, located within the Danube Delta Biosphere Reserve, in the central part of the region, and the Dumbrăveni Forest Natural Reserve in the south. All three populations had individuals with scars from past injuries on their shells. The highest numbers of injured tortoises were in Dumbrăveni Forest (35.78%) and Măcin Mountains (35%) while the population from Cetatea Histria (11.26%) was less affected. Carapace injury frequency was higher in the Măcin Mountains whilst the Dumbrăveni Forest population had a higher frequency of plastron injuries. Human-caused injuries were observed mainly in the anterior and dorsal zones of the carapace and the anterior zone of the plastron. Natural injuries were located on the posterior zone of the carapace, mainly on marginal scutes. Our study showed that the scars of turtle shells proved to be an excellent depository of past and recent human impacts and may offer insights for better conservation and management strategies.

Factors determining the abundance and occurrence of Hermann’s tortoise Testudo hermanni in France and Spain: Fire regime and landscape changes as the main drivers

Major landscape transformations have occurred in the northern Mediterranean over the last decades, including urbanization, agricultural intensification and land abandonment, which, in turn, increase the risk of the propagation of fire. We used repeated-count surveys conducted at 369 sites in France and Spain to jointly model the effects of environmental covariates on the abundance, occupancy and detection of Hermann’s tortoise, a long-lived and endangered species, using a novel zero-inflated approach. We also employed a large dataset of presence-only data collected in Provence to model environmental influences on occurrence probability using maximum entropy models. In both France and Spain, sites that experienced wildfires over the last 50years hosted 31% fewer individuals than unburned sites. In Provence, higher wildfire frequency decreased this species’ occurrence probability, from 50% when 0–1 fire had occurred over the last 50years, to 7% in areas that had burned at least 3 times. We also showed that abundance required a long recovery time (more than 25years) after wildfires. In Provence, the highest occurrence probability for this species was found in patchy landscapes and scrub and/or herbaceous vegetation. The lowest species occurrence was found in extensive artificial areas, vineyards and arable lands. These results suggest a high risk of population extinction in the future if these types of habitats continue to expand in plains and coastal areas to the detriment of scrublands. Higher wildfire frequency predicted by climate change scenarios in the Mediterranean is also likely to increase the risk of extinction for some populations.

Endoscopic assisted orchiectomy in Herman's tortoises (Testudo hermanni sp.).

Male tortoises in captivity are often aggressive against other males or females, in particular during mating season related to hormonal influences (testosterone). Castration in males is the treatment of choice in many vertebrate species. A novel technique of minimal invasive castration is presented for Herman's tortoises (Testudo hermanni). The procedure was performed in ten mature males. An endoscope (2.7 mm/30° angled) was inserted into a prefemoral incision on each side. The testicle was resected after ligation of the gubernaculum testis and the spermatic cord using hemoclips. Each testicle could be removed in approximately 20 minutes. Complications like hemorrhage or damage of adjacent tissue did not occur and all animals recovered uneventfully. Using the bilateral prefemoral entrance offers an alternative option for orchiectomy in Herman's tortoises without dissection of the shell. Thus complications like hemorrhage or impaired wound healing followed by sequestration of the bone flap are prevented. Because of the anatomical settings and the risk of tissue damage and time consumption, a unilateral approach is not recommended. Fasting the animals is necessary due to the voluminous gastrointestinal tract of this herbivorous tortoise and emptying the urinary bladder provides more space for manipulations in the coelomic cavity and prevents clipping and cutting of adjacent organs. The magnification via the endoscope is beneficial for orientation in the coelomic cavity, which is formed by the extremely convex carapace. Without this equipment it is challenging to visualize the dorsocaudally located gonads through the relatively small incision and the inserted instruments might block the view at the surgical field. Administration of hemoclips achieved a good hemostasis and the testicles could be resected without major blood loss. The described technique is a gentle method for resection of the testicles in this species and can be adapted to other European tortoise species of equal size.

Taxonomic and functional response of a Mediterranean reptile assemblage to a repeated fire regime

Wildfires are common disturbances that have a major impact on ecosystems. Recent decades have seen an increase in fire frequency and extension due to the combined effects of climate change and land-use history. We studied the taxonomic and functional response of a reptile assemblage to repeated fires in southern France to understand shifts in dominant species and diversity, as well as the mechanisms that underlie responses according to functional traits of species. In the spring of 2010, we sampled reptiles in areas with three types of fire regime: unburned, burned once (2003) and burned 4–5 times (last fire in 2003) along a fire history of 51-years period. With this field sampling design, we examined the intermediate disturbance hypothesis and the habitat accommodation model of succession as methods to predict reptile responses to natural fire regimes. We also compared habitat structure at the study area between 1944 and 2006 to certify that repeated-fire regimes have modified the habitat for reptiles. The comparison of the habitat structure between both periods demonstrated that repeated-fire regimes modified the landscape from a homogeneous sparse forest to a contrasted heterogeneous mixture of scrubland and dense forest. We found a loss of reptile diversity after one and multiple fires, a result that contradicts the intermediate disturbance hypothesis. Reptile composition differed among the three fire regimes: there was a shift in dominant species and a reduction of beta diversity related to an increase in the number of fires. We also observed a functional response to repeated fires, with an increased frequency of insectivorous reptiles, which live in open areas, are specialists in their ecological niche, and have a short lifespan. These results suggest that reptile replacement according to fire regime accounts for a habitat accommodation model following particular traits of species. Our study indicated that areas subjected to repeated fires have a more strictly Mediterranean reptile assemblage than unburned areas, due to the ability of Mediterranean species to survive thermal environments in open (burned) areas. At a regional scale, changes in dominant species between unburned and repeatedly burned areas might be an argument for maintaining a patchwork of areas burned at variable intervals. However, the increase in fire frequency and extension suggests a future scenario of extinction for species negatively impacted by fire, such as the endangered Hermann’s tortoise Testudo hermanni, for which the study area is home to one of the last native populations in the western Mediterranean.

Wildlife DNA forensics against crime: Resolution of a case of tortoise theft

A paternity test was used to investigate a robbery case involving captive individuals of Greek tortoise (Testudo graeca). Six tortoises were allegedly stolen from a private breeder and offered for sale on the web by the supposed thief. The stolen tortoises were confiscated by the rangers of the State Forestry Corps (CFS). A panel of 14 autosomal microsatellite loci was used to genotype the seized tortoises and ten individuals assumed to be legally owned by the breeder. Kinship analyses reliably reconstructed the tortoise pedigree, demonstrating parent-offspring relationships among the owned and the stolen tortoises. As correctly declared by the breeder, four of the six stolen individuals belonged to the same family group of the ten legally owned tortoises. Results indicate that genetic identification procedures can provide valuable evidence and give useful support against illegal wildlife traffic.

Maintained effects of fire on individual growth and survival rates in a spur-thighed tortoise population

Fires strongly influence the ecology of reptiles and have both direct and indirect effects on population dynamics as they affect life history traits. Here, we examine the effects of fire on individual growth patterns and on the survival rates of a tortoise Testudo graeca population in south-eastern Spain. We compare the biometric data from recaptures 4 years before and after a fire which burned 31 % of our study area. The von Bertalanffy and Gompertz growth models best describe the individual growth patterns for males and females. In males, but not females, fire significantly decreased the time required to reach their asymptotic size (k parameter). However, adult survival analyses reveal that the local survival rates lowered for both sexes after fire. Our work evidences that the effects of fire can be complex and maintained over time, affecting different life history traits.

Bilateral Bronchial Collapse in a Hermann's Tortoise (Testudo hermanni boettgeri)

Abstract A 45-year-old Hermann's tortoise (Testudo hermanni boettgeri) was presented for therapy-resistant respiratory tract disease of several months duration. On presentation, the animal showed severe inspiratory distress and produced wheezing sounds on inspiration. Computed tomography and tracheobronchoscopy revealed bilateral bronchial collapse. Histopathology showed cartilaginous lesions comparable to those of tracheobronchomalacia described in dogs and humans.

Comparative Morphology of Three Populations of Testudo graeca Linnaeus, 1758 from the Western Taurus Mountains, Turkey

We examined a total of 65 specimens of the Mediterranean spur-thighed tortoise Testudo graeca Linnaeus, 1758 from three distinct localities in the western Taurus Mountains of the Mediterranean region of Turkey: Kalkan (12 ♀, 14 ), Ciglikara (6 ♀, 7 ♂), and Akseki (7 ♀, 19 ♂). For morphological comparisons 15 morphometric characters and 17 ratios developed by combination of characters were investigated. Post-ANOVA pairwise analysis (Tukey’s) across all groups verified sexual dimorphism in the Kalkan and Ciglikara populations in terms of the following ratios: plastron length/plastron width 2 ( p = 0.02) and straight carapace length/femoral suture length ( p = 0.04), respectively. Females in all three populations are larger than males, and in the Ciglikara population individuals are larger than those from other populations (ANOVA F (2.22) = 16.28, p < 0.0001). The maximum straight carapace length measured was of a female in the Ciglikara population (295 mm). This is a new record size for Turkish tortoises. Discriminant analysis based on 13 ratios confirms that the Kalkan population tends to differ from the other two populations. This difference was more clear between Akseki and Kalkan.

THE DIET OF VARANUS GRISEUS IN THE SOUTHERN COASTAL PLAIN OF ISRAEL (REPTILIA: SAURIA)

ABSTRACT Fecal pellets were collected and analyzed microscopically during a two-year study of the desert monitor (Varanus griseus) in a sand-dune area south of Holon. V. griseus was found to be a predator-scavenger carnivore type, eating almost any animal of appropriate size. Although 92.2% of the fecal pellets contained invertebrates (mainly arthropods), the higher frequency of occurrence of the smaller species among the invertebrates is probably due to secondary predation. The main prey items included rodents (mostly gerbils, Gerbillus sp., and jirds, Meriones sp.), bird eggs (presumably chukar partridge, Alectoris chukar eggs), birds (mainly partridge chicks), skinks (Chalcides sp.), fringe-toed lizards (Acanthodactylus sp.), chameleons (Chamaeleo chamaeleon), elegant geckos (Stenodactylus sthenodactylus), tortoises (Testudo graeca) and snakes (including the venomous Vipera xanthina palaestinae). Less frequent were: hedgehogs (Hemiechinus auritus), leverets (Lepus europaeus), Sanis pygmy shrew (Suncus ...

URBANIZATION AND SAND DUNES IN ISRAEL: DIRECT AND INDIRECT EFFECTS

ABSTRACT Considerable attention has been given lately to the effects of habitat fragmentation and destruction on wildlife. Here, we summarize their effects on animal abundance and plant cover during a three-year study period (1987–90) of the sand dunes of the coastal plain of Israel. Populations of the gray monitor Varanus griseus, the spur-thighed tortoise Testudo graeca, and the mountain gazelle Gazella gazella in the study area declined markedly and plant cover increased significantly. Habitat destruction and fragmentation, introduced animals (especially dogs and carrion crows), a continuing change in the native herbivore fauna, and blockage of wind-borne sand are all believed to be responsible for the observed changes. We recommend that small areas, unsuitable for full protection, be declared “city reserves,” to be used for educational and recreational purposes. Nature reserves need to be managed in order to maintain the existing fauna and flora.

Protein Electrophoresis in Hermann's Tortoises (Testudo hermanni): A First Step in Reference Value Determination

In veterinary medicine, protein electrophoresis has become a routine test. However, its use in exotic animals remains controversial because of a lack of reference values for many species. Establishing protein electrophoresis reference values of healthy Hermann's tortoises (Testudo hermanni) could prove to be a very useful tool for assessing the health status of this endangered species. The aim of this study was to establish a preliminary reference interval for the protein fractions of Hermann's tortoises under normal conditions. Serum samples from healthy adult Hermann's tortoises (n = 22) were analyzed by cellulose acetate electrophoresis. Total protein concentration (min–max: 2.10–6.20 g/dl) was measured by the biuret method. Four protein fractions were identified: albumin, α-globulins, β-globulins, and γ-globulins. The reference intervals for healthy tortoises were determined by parametric methods as recommended by the American Society of Veterinary Clinical Pathologists Quality Assurance and Laboratory Standards Committee. Furthermore, differences between sexes (15 females, 7 males) were evaluated and a statistical difference was noted. To our knowledge, this is the first study to determine reference intervals for the protein profile of Hermann's tortoise using parametric methods.

Modeling road mortality hotspots of Eastern Hermann’s tortoise in Romania

Road-associated mortality can lead to local declines of wildlife populations, and management agencies are actively implementing mitigation measures, especially focused on potential road mortality hotspots. In this study we used a spatially-explicit simulation modeling approach to estimate the hotspots of road mortality for the Eastern Hermann’s tortoise (Testudo hermanni boettgeri) within its distribution range in Romania. Using a field experiment, we first evaluated velocities while crossing roads. Adult male tortoises moved faster than females (3.98 m/min vs. 2.51 m/min) which led to higher individual probabilities for females being killed on high-traffic roads (0.61 for females vs. 0.44 for males at traffic levels of 7000 vehicles/day). Both males and females had similar road mortality probabilities for traffic levels &lt;1000 and &gt;35 000 vehicles/day. Our spatially explicit model suggests that, within the entire Romanian distributional range, the tortoises have an overall risk of road mortality 1.6%, which may have a negative impact on tortoise populations. Using the Getis-Ord Gi statistic, we identified road mortality hotspots with mortality rates of 5-30%, in areas bisected by high-traffic national and European-level roads. Our research is timely in that many low-traffic roads are predicted to have increased traffic associated with tourism activities, thus increasing the overall risk of mortality. We suggest that mitigation measures such as signage and roadside fences associated with underpasses have the potential to limit road mortality of this threatened species within predicted current mortality hotspots.

Using digital images in the study of fluctuating asymmetry in the spur-thighed tortoise Testudo graeca

Fluctuating asymmetry has been proposed as a useful noninvasive tool for detecting the influence of the environment on body development. In the present study, we used digital images to estimate the fluctuating asymmetry of the plastron in an isolated Testudo graeca population in Dobrogea, Romania. We extracted data from the photos regarding the area, height, and width of 3 plastron scutes. A total of 155 adult tortoises analysed showed reduced variation in plastron asymmetry and no significant relationship was detected between fluctuating asymmetry and sex or body size. We suggest that fluctuating asymmetry may be an individual trait, with no predictive value at the population level.