Tortoise Populations Research Articles

SalmonellaInfection in Illegally Imported Spur‐Thighed Tortoises (Testudo graeca)

The prevalence of Salmonella infection was determined in a group of spur-thighed tortoises (Testudo graeca) seized during two smuggling attempts and in a population of captive Hermann's tortoises (Testudo hermanni) sheltered in a wildlife rescue centre. Salmonella spp. was isolated in 81 of 220 (36.8%) and in 17 of 67 (25.4%) cloacal swabs collected from the T. graeca and T. hermanni tortoises respectively. Overall, a total of 21 different Salmonella serotypes were found. Some of these serotypes are common to terrestrial chelonians while others have never been reported. All cultured serotypes were non-typhoidal but nonetheless many of these have been previously reported as source of human outbreaks of reptile-related salmonellosis. Eighty-two per cent and 5.3% of the isolates were resistant to two and three anti-microbial agents respectively. However, the isolates were highly susceptible to the anti-microbials of choice for the treatment of salmonellosis such as cephalosporins and fluoroquinolones. Our findings confirm that tortoises can be considered a reservoir for Salmonella and that care should be employed when handling and breeding these animals. Tight surveillance should be enforced to avoid illegal importation and prevent the trading of live tortoises, carriers of zoonotic pathogens.

Impacts of a wildfire on the mortality rate and small-scale movements of a Hermann's tortoise Testudo hermanni hermanni population in southeastern France

AbstractBecause they have high longevity and a weak dispersal capacity, chelonians are known to be highly impacted by fire. We investigated the immediate demographic consequences of a wildfire occurring in 2009 on a population of Hermann's tortoises Testudo hermanni in the Plaine des Maures in southeastern France using the multistate capture–recapture method. Over two years (2009 and 2010), 108 adult individuals were marked. Survival probability was higher in the unburned (0.99) than in the burned area (0.43). The inter-annual transition probability from the burned to the unburned area was high (0.72). These results show that fire affects survival by immediately killing individuals and by inducing small-scale movements from burned to unburned areas.

PCR Prevalence of Ranavirus in Free-Ranging Eastern Box Turtles (Terrapene carolina carolina) at Rehabilitation Centers in Three Southeastern US States

Ranaviruses (genus Ranavirus) have been observed in disease epidemics and mass mortality events in free-ranging amphibian, turtle, and tortoise populations worldwide. Infection is highly fatal in turtles, and the potential impact on endangered populations could be devastating. Our objectives were to determine the prevalence of ranavirus DNA in blood and oral swabs, report associated clinical signs of infection, and determine spatial distribution of infected turtles. Blood and oral swabs were taken from 140 eastern box turtles (Terrapene carolina carolina) that were presented to the wildlife centers at the University of Tennessee (UT; n=39), Wildlife Center of Virginia (WCV; n=34), and North Carolina State University (NCSU; n=36), as well as a free-ranging nonrehabilitation population near Oak Ridge, Tennessee (OR; n=39) March-November 2007. Samples were evaluated for ranavirus infection using polymerase chain reaction (PCR) targeting a conserved portion of the major capsid protein. Two turtles, one from UT and one from NCSU, had evidence of ranavirus infection; sequences of PCR products were 100% homologous to Frog Virus 3. Prevalence of ranavirus DNA in blood was 3, 0, 3, and 0% for UT, WCV, NCSU, and OR, respectively. Prevalence in oral swab samples was 3, 0, and 0% for UT, WCV, and NCSU, respectively. Wildlife centers may be useful in detection of Ranavirus infection and may serve as a useful early monitoring point for regional disease outbreaks.

The Relationship Between Burrow Abundance and Area as a Predictor of Gopher Tortoise Population Size

Because gopher tortoises (Gopherus polyphemus) occupy high-value lands in the southeastern United States, are declining throughout their range, and stir public passion when they are entombed through currently legal take, refined conservation measures for this species are needed. Of particular interest is a determination of how many individuals constitute a population and what sized areas are required by such populations so that animals currently in harm's way might be moved to designated reserve areas. We use surveys of burrows of gopher tortoises from a large sample of areas of differing sizes to test for a relaxation of the linear relationship between area and number of burrows expected at the edge of a population of gopher tortoises. For measures of burrow abundance, some of our data are from sites on which estimates were based on transect samples; on other sites, complete counts were made. The relationship between area and abundance was elevated for transect samples compared to similar data from complete counts, indicating that transect data yield inflated counts when extrapolated over large areas. For complete counts, our data indicate a threshold point at which a linear relationship between area and abundance ends and a loss of this relationship for larger areas begins. This threshold point suggests that, on average, populations of gopher tortoises consist of 444 burrows, cover 755 ha, and contain 240 tortoises. These figures describe features of tortoises inhabiting a variety of lands that differ in current management goals and past land-use history. Our results suggest that many current reserve areas for gopher tortoises are likely to be too small. Our results also provide an example of how key conservation variables can be generated for long-lived species.

Desert Tortoise Microhabitat Selection on the Florence Military Reservation, South-Central Arizona

We examined Desert Tortoise microhabitat selection on the Florence Military Reservation (FMR) in south-central Arizona where National Guard training and other activities, such as motorized recreation and grazing, are permitted. Previous research on the FMR indicated that Desert Tortoise home ranges overlapped with firing boxes, areas where most of the National Guard's training activity was concentrated. Our objective was to examine Desert Tortoise microhabitat selection within, and adjacent to, these firing boxes in an effort to guide future management for restoring degraded tortoise habitat on the installation. Desert Tortoises selected habitat that was characterized by a higher percentage of canopy cover, absence of cattle activity, and closer proximity to roads and washes than was available within their home range. Canopy cover had the highest calculated parameter importance and was included in each of the supported microhabitat selection models. Areas with sufficient canopy cover most likely provided shade for escaping the desert heat during periods of high tortoise activity. Our results suggest that management prescriptions that maintain, or increase, the amount of vegetative cover and that protect desert washes will have positive impacts on Desert Tortoise populations.

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.

Total Counts Versus Line Transects for Estimating Abundance of Small Gopher Tortoise Populations

Abstract: Status and trends of gopher tortoise (Gopherus polyphemus) populations are a critical information need for natural resource managers, researchers, and policy makers. Many tortoise populations are small and isolated, which can present challenges for deriving population estimates. Our objective was to compare abundance and density estimates for a small tortoise population derived using a total burrow count versus estimates obtained with line transect distance sampling (LTDS) using repeated surveys. We also compared results of the 2 survey methods using standard burrow‐to‐tortoise correction factors versus assessing occupancy of all burrows with a camera scope. In addition, we compared LTDS data obtained using a compass and measuring tape to define transects to those obtained using a Global Positioning System (GPS) and Personal Data Assistant (PDA) field computer to navigate transects. Line transect distance sampling with repeated surveys (both with a measuring tape and compass and with a GPS—PDA) yielded sufficient observations of tortoises to calculate population estimates. From 18% to 31% of burrows were occupied by tortoises as determined with the burrow camera. We found 25 burrows during the LTDS survey that we did not find in the total count survey, which demonstrated that the assumption of 100% detection for the total count was not met; hence, density or abundance measurements derived with this method were underestimates. We recommend using GPS—PDA technology, scoping all burrows detected, and using LTDS with repeated surveys to estimate abundance and density for small gopher tortoise populations.

Total Counts Versus Line Transects for Estimating Abundance of Small Gopher Tortoise Populations

Total Counts Versus Line Transects for Estimating Abundance of Small Gopher Tortoise Populations

EFFECTS OF MYCOPLASMAL UPPER RESPIRATORY TRACT DISEASE ON MORBIDITY AND MORTALITY OF GOPHER TORTOISES IN NORTHERN AND CENTRAL FLORIDA

Gopher tortoise (Gopherus polyphemus) populations on four tracts of public lands in northern and central Florida were studied from 1998 to 2001 to assess the effects of mycoplasmal upper respiratory tract disease (URTD). Adult gopher tortoises (n=205) were marked for identification, serum and nasal flush samples were obtained for mycoplasmal diagnostic assays, and clinical signs of URTD (nasal discharge, ocular discharge, palpebral edema, and conjunctivitis) were evaluated. A subset of tortoises (n=68) was radio-instrumented to facilitate repeated sampling and document potential mortality. Presence of serum antibody to Mycoplasma agassizii was determined by enzyme-linked immunosorbent assay (ELISA), and mollicutes species were detected in nasal flushes by polymerase chain reaction (PCR). Antibody prevalence varied among sites and years but was highest in 1998, exceeding 70% at two sites. Only 11 tortoises (5%) were positive by PCR, and three species (M. agassizii, M. testudineum, and a nonpathogenic Acholeplasma) were identified in nasal flush specimens. Nasal discharge, though rare (6% of tortoises), was significantly correlated with higher ELISA ratios, study site, and positive PCR status. Mortality events (n=11) occurred on two of the three M. agassizii-positive sites; no mortality was observed on the M. agassizii-negative control site. However, none of the tested variables (ELISA result, study site, year, sex, presence of clinical signs, or carapace length) showed significant ability to predict the odds of death. Mycoplasmal URTD is believed to be a chronic disease with high morbidity but low mortality, and follow-up studies are needed to detect long-term effects.

Population and Thermal Ecology of Testudo hermanni hermanni in the Tolfa Mountains of Central Italy

Herman's tortoise, Testudo h. hermanni, is an endangered subspecies in Italy, France, and Spain. We studied a Herman's tortoise population in the Riserva Naturale Regionale Monterano in the Tolfa Mountains of central Italy. We found that, unlike most other studies of this and related species, sex ratios were 1:1, and half the population was made up of juveniles. Sexual maturity was reached at 12 years in males and 12-13 years in females, and females were significantly larger. Tortoises greatly preferred open maquis habitat over other habitat types and thermoregulated so that body temperatures stayed consistently above ambient temperatures, especially under low ambient temperature conditions. Presence of ticks was significantly associated with an index of thermoregulatory behavior. We suggest that maintenance of open maquis habitat in this reserve is essential to high hatchling production and effective thermoregulation.

Health and Reproductive Assessment of a Free-Ranging Gopher Tortoise (Gopherus polyphemus) Population Following Translocation

ABSTRACT In 2004, a subset of a translocated population of gopher tortoises (n = 14; Gopherus polyphemus) were captured to determine the overall health of individuals and to investigate the prevalence of selected pathogens. Additionally, ultrasonography and endoscopic visualization of the reproductive tract were compared as methodologies to accurately determine sex and reproductive status. Tortoises were premedicated with butorphanol and induced with propofol. The hematology and biochemical profile values obtained were within the reference ranges previously reported for gopher tortoises. Tortoises were parasitized with Alaeuris spp. of pinworms and trichostrongyles. Ten of the tortoises (71%) were also parasitized by hemogregarines. None of the animals had clinical signs indicative of acute upper respiratory disease (URTD); however, six animals had signs consistent with previous upper respiratory infections. One tortoise had an antibody titer against Mycoplasma agassizii, considered to be positive, while ...

Social behavior drives the dynamics of respiratory disease in threatened tortoises

Since the early 1990s, morbidity and mortality in tortoise populations have been associated with a transmissible, mycoplasmal upper respiratory tract disease (URTD). Although the etiology, transmission, and diagnosis of URTD have been extensively studied, little is known about the dynamics of disease transmission in free-ranging tortoise populations. To understand the transmission dynamics of Mycoplasma agassizii, the primary etiological agent of URTD in wild tortoise populations, we studied 11 populations of free-ranging gopher tortoises (Gopherus polyphemus; n = 1667 individuals) over five years and determined their exposure to the pathogen by serology, by clinical signs, and by detection of the pathogen in nasal lavages. Adults tortoises (n = 759) were 11 times more likely to be seropositive than immature animals (n = 242) (odds ratio = 10.6, 95% CI = 5.7-20, P < 0.0001). Nasal discharge was observed in only 1.4% (4/296) of immature tortoises as compared with 8.6% (120/1399) of adult tortoises. Nasal lavages from all juvenile tortoises (n = 283) were negative by PCR for mycoplasmal pathogens associated with URTD. We tested for spatial segregation among tortoise burrows by size class and found no consistent evidence of clustering of either juveniles or adults. We suggest that the social behavior of tortoises plays a critical role in the spread of URTD in wild populations, with immature tortoises having minimal interactions with adult tortoises, thereby limiting their exposure to the pathogen. These findings may have broader implications for modeling horizontally transmitted diseases in other species with limited parental care and emphasize the importance of incorporating animal behavior parameters into disease transmission studies to better characterize the host-pathogen dynamics.

Low Genetic Diversity in Several Gopher Tortoise (Gopherus polyphemus) Populations in the Desoto National Forest, Mississippi

Gopherus polyphemus has experienced severe population declines, especially in the western portion of its range. As a consequence, G. polyphemus may have experienced population bottlenecks that resulted in a decrease in genetic diversity and an accumulation of deleterious alleles. The importance of genetic diversity has been well-documented for several fitness parameters (e.g., survival, disease resistance, growth and developmental rates, and developmental instability). Western populations of G. polyphemus in south Mississippi (USA) have lower hatching success (16.7–48%) than that found in eastern populations (67–97%). Even under laboratory conditions, approximately 40% of the eggs still failed to hatch, suggesting that intrinsic (egg quality) factors may be affecting development. Using nine microsatellite loci, we genotyped individuals from four populations in south Mississippi and one eastern population (Fort Benning, GA) and compared several genetic diversity indices (e.g., allelic richness, expected heterozygosity, and percent polymorphic loci) with published data from populations in the eastern portion of the range, such as populations east of the Mobile and Tombigbee rivers. We found significantly lower genetic diversity in the four Mississippi populations than in the eastern populations. However, these findings only demonstrate that these populations have low genetic diversity, and establishing any causal relationship between low genetic diversity (or other intrinsic factors; e.g., female condition) and reduced reproductive success should be further investigated.

A quantitative reassessment of morphology-based taxonomic schemes for Turkish tortoises (Testudo graeca)

AbstractIn the last decade, Asian populations of Testudo graeca were split into as many as 10 species based on morphology and morphometry and then subsequently synonymized based on genetic evidence. We generate new morphometric data for six of these disputed species from Turkey, a major center of morphological and genetic diversity for Asian T. graeca. We test the concordance of our data with previous morphological assignments. Our morphometric data and analyses do not support all of the results of previous morphometric studies. Instead we find that putatively named taxa from the Mediterranean coast (“antakyensis”, “anamurensis”, and “terrestris”) are not morphometrically distinct. On the other hand, some inland populations from eastern Turkey (“armeniaca” and “perses”) are morphometrically distinct as previously claimed. Tortoise populations from northern and southern Turkey, which may correspond to the ibera and terrestris mt clades, also appear to be morphometrically distinct. In this respect, the morphometric data reflects the emerging genetic pattern, although the picture is complicated by a lack of genetic sampling within Turkey and morphometric studies outside of Turkey.

Effects of subsidized predators, resource variability, and human population density on desert tortoise populations in the Mojave Desert, USA

Understanding predator-prey relationships can be pivotal in the conservation of spe- cies. For 2 decades, desert tortoise Gopherus agassizii populations have declined, yet quantitative evidence regarding the causes of declines is scarce. In 2005, Ft. Irwin National Training Center, California, USA, implemented a translocation project including 2 yr of baseline monitoring of desert tortoises. Unusually high predation on tortoises was observed after translocation occurred. We conducted a retrospective analysis of predation and found that translocation did not affect the proba- bility of predation: translocated, resident, and control tortoises all had similar levels of predation. However, predation rates were higher near human population concentrations, at lower elevation sites, and for smaller tortoises and females. Furthermore, high mortality rates were not limited to the National Training Center. In 2008, elevated mortality (as high as 43%) occurred throughout the listed range of the desert tortoise. Although no temporal prey base data are available for analysis from any of the study sites, we hypothesize that low population levels of typical coyote Canis latrans prey (i.e. jackrabbits Lepus californicus and other small animals) due to drought conditions influenced high predation rates in previous years. Predation may have been exacerbated in areas with high levels of subsidized predators. Many historical reports of increased predation, and our observation of a range- wide pattern, may indicate that high predation rates are more common than generally considered and may impact recovery of the desert tortoise throughout its range.

A Second Specimen of the Pleistocene Bermuda Tortoise, Hesperotestudo bermudae Meylan and Sterrer

A fragmentary radius of Hesperotestudo bermudae from an underwater cave deposit in Bermuda is only the second known specimen of the species. The exact provenance and age of the specimen have been lost, but the record provides additional evidence that there was a population of endemic tortoises on Bermuda in the Pleistocene.

Seroprevalence of Mycoplasma agassizii in Wild Caught and Rescued Texas Tortoises (Gopherus berlanderi) in South Texas

The Texas tortoise (Gopherus berlanderi) is one of four native tortoise species found in North America. All four Gopherus species receive some form of government protection because of recent population declines. The Texas tortoise is considered threatened within the state of Texas and is of major conservation interest. As a result of human encroachment into Texas tortoise habitats, there has been an increase in the dissemination of infectious disease into native populations. One of the most important diseases studied in North American tortoises is Mycoplasma agassizii. Seroprevalence studies have been performed in the California desert tortoise (Gopherus agassizii) and Gopher tortoise (Gopherus polyphemus) but have yet to be performed in the Texas tortoise. The purpose of this study was to measure the seroprevalence of Mycoplasma agassizii using an ELISA in two populations of Texas tortoises, a wild population (N = 39) and a population in a wildlife rehabilitation facility (N = 15). Tortoises in the wild population were all seronegative (95% confidence intervals [CI]: 0–7.6%), whereas 80% (12/15; 95% CI: 60–100) of the tortoises from the rehabilitation facility were seropositive. The results of this study suggest that Texas tortoises are exposed to and can mount an immunoglobulin response to Mycoplasma agassizii, which may influence the status of this species in North America. This pilot study suggests that further research is needed to determine the epidemiology of mycoplasmosis in Texas tortoises from the wild and in captivity.

Detecting trends in desert tortoise population growth: elusive behavior inflates variance in estimates of population density

Assessing the recovery of the federally listed Mojave population of desert tortoises Gopherus agassizii requires detecting subtle changes in population size over a period of many years. The methods that have been employed by the US Fish and Wildlife Service to estimate population density of desert tortoises are inadequate for detecting modest trends in population density, partly due to a hidden variance in a parameter (g0) that corrects for the proportion of tortoises that are inactive and thus unavailable for sampling when population density is being assessed. We used small dataloggers to record the activity of tortoises throughout their active season, and derived daily esti- mates of g0, which we compared with the 2004 estimate published by the US Fish and Wildlife Ser- vice. Due to the substantial variation in animal activity that we found within and among days during the active season, we used a daily method to estimate density. We found that this method, while pro- viding a more accurate assessment of g0, translates into estimates of density with coefficients of vari- ation that are 4 larger than previously reported due to the variation in g0 and n (number of animals encountered). This discrepancy could adversely influence managers' perceptions of population recovery for desert tortoises, and could undermine any ability to monitor the efficacy of recovery actions for populations.

Morphometrics Parallel Genetics in a Newly Discovered and Endangered Taxon of Galápagos Tortoise

Galápagos tortoises represent the only surviving lineage of giant tortoises that exhibit two different types of shell morphology. The taxonomy of Galápagos tortoises was initially based mainly on diagnostic morphological characters of the shell, but has been clarified by molecular studies indicating that most islands harbor monophyletic lineages, with the exception of Isabela and Santa Cruz. On Santa Cruz there is strong genetic differentiation between the two tortoise populations (Cerro Fatal and La Reserva) exhibiting domed shell morphology. Here we integrate nuclear microsatellite and mitochondrial data with statistical analyses of shell shape morphology to evaluate whether the genetic distinction and variability of the two domed tortoise populations is paralleled by differences in shell shape. Based on our results, morphometric analyses support the genetic distinction of the two populations and also reveal that the level of genetic variation is associated with morphological shell shape variation in both populations. The Cerro Fatal population possesses lower levels of morphological and genetic variation compared to the La Reserva population. Because the turtle shell is a complex heritable trait, our results suggest that, for the Cerro Fatal population, non-neutral loci have probably experienced a parallel decrease in variability as that observed for the genetic data.

Habitat Use by Sonoran Desert Tortoises

ABSTRACT The distribution of desert tortoises (Gopherus agassizii) spans a wide range of biotic and abiotic conditions in the southwestern United States and northwestern Mexico, with physical and behavioral differences distinguishing tortoises inhabiting the Mojave Desert from those inhabiting the Sonoran Desert. Relative to tortoise populations in the Mojave Desert, populations in the Sonoran Desert have not been well‐studied. To assess how habitat use of desert tortoises in the Sonoran Desert was influenced by topography, vegetation, geomorphology, and soil, we surveyed 40 randomly located 3‐ha sites for presence of adult tortoises within a site‐occupancy framework. We modeled both occupancy and detection probability as a function of environmental features, and compared those results with a logistic regression model that assumed detection probability was equal to 1. Results from both approaches agreed, suggesting that habitat selection of tortoises in the Sonoran Desert was influenced primarily by topographic and geomorphologic features rather than by vegetation. Specifically, tortoises were more likely to occupy sites that were steep (we detected tortoises on 29% of sites with mean slope &lt;5° and 92% of sites with mean slope &gt;15°) and predominantly east‐facing (53% of sites with &lt;5% of site facing E and 92% of sites with &gt;20% facing E), and less likely to occupy north‐facing slopes (100% of sites with &lt;10% of site facing N and 14% of sites with &gt;60% facing N). Our results contrast with patterns of habitat use in the Mojave Desert where tortoises primarily occupy valley bottoms. Habitat use of tortoises in Sonoran and Mojave Desert populations differ considerably, contributing to the mounting body of evidence suggesting that these geographically distinct populations may represent separate species.