Fiber digestibility in juvenile Galapagos tortoises (Geochelone nigra) and implications for the development of captive animals

Digestive strategies have been recognized to be a key factor for healthy growth in juvenile Galapagos giant tortoises (Geochelone nigra). The aim of present study was to investigate digestive coefficients with special regard to fiber fractions. Four captive bred Galapagos giant tortoises 4–5 years of age were fed a controlled diet for 32 days. The diet consisted of 77% hay, 15% tortoise pellets, and 8% apples on a dry matter basis. On a dry matter basis diet analysis showed: 95.7% organic matter, 11.3% crude protein, 20.5% crude fiber, 22.6% acid detergent fiber, 5.0% acid detergent lignin, and 17.6% cellulose. Based on total fecal collection during 7 days average dry matter digestibilities were calculated: 65% for dry matter, 67% for organic matter, 63% for crude protein, 55% for crude fiber, 49% for acid detergent fiber, 41% for acid detergent lignin, 54% for cellulose. An increase in crude fiber content resulted in a reduced digestibility in comparative evaluations of data for different tortoise species, and in a comparison of tortoises and mammalian hindgut fermenters. Compared to some mammalian hindgut‐fermenting herbivore species (domestic horses, Asian elephants, Indian rhinoceroses) on a diet of hay and concentrates, the juvenile Galapagos giant tortoises showed a digestion of similar efficiency. If a reduction in dietary digestibility is warranted in juvenile Galapagos giant tortoises, it is concluded that dietary fiber levels should be increased and it is proposed that crude fiber levels of 30–40% on a dry matter basis should be achieved. Zoo Biol 24:185–191, 2005. © 2005 Wiley‐Liss, Inc.     

Isolation and characterization of eight microsatellite loci for the study of gene flow between Testudo marginata and Testudo weissingeri (Testudines: Testudinidae)

The taxonomic status of the Greek Testudo species, marginated tortoise (Testudo marginata Schoepff, 1793) and dwarf marginated tortoise (Testudo weissingeri Bour, 1995), is controversed. In order to study the gene flow among these Greek Testudo species, eight polymorphic microsatellite markers were characterized and screened for 32 individuals. The number of alleles observed per locus ranged from two to 19. Observed heterozygosities varied from 0.235 to 0.830. These microsatellite loci were also successfully tested on seven closely related species of Testudinidae. This set of microsatellites offers an efficient tool to investigate genetic differentiation among testudinid species.     

Flexibility of digestive responses in two generalist herbivores,the tortoises Geochelone carbonaria and Geochelone denticulata

Summary To test the prediction that digestive responses digestibility, intake and passage time-of generalist herbivores vary with different diets, feeding trials were conducted in Venezuela with two sympatric tortoise species, Geochelone carbonaria and G. denticulata. Three single-species diets (two fruit, one foliage) were fed to both species. For a given diet, digestibility, mass-specific intake and passage time did not differ between the two tortoise species, nor did they vary by sex or body mass within each species. However, the digestive parameters varied for tortoises feeding on the different diets. The responses ranged from nearly abandoning cell wall fermentation and depending entirely on extraction of cell contents to relying heavily on cell wall fermentation. Therefore, these generalist herbivores have flexible digestive responses that are influenced by diet, not fixed digestive responses that limit the diet, as previously observed in other generalist herbivores. A three-part classification of herbivores (specialist, specialized mixed feeder and opportunistic mixed feeder) is suggested as an approach to understanding flexible and inflexible digestive strategies in herbivores.     

Life cycle of tortoise tick <Emphasis Type="Italic">Hyalomma aegyptium</Emphasis> under laboratory conditions

The tortoise tick Hyalomma aegyptium has a typical three-host life-cycle. Whereas its larvae and nymphs are less host-specific feeding on a variety of tetrapods, tortoises of the genus Testudo are principal hosts of adults. Ticks retained this trait also in our study under laboratory conditions, while adults were reluctant to feed on mammalian hosts. Combination of feeding larvae and nymphs on guinea pigs and feeding of adults on Testudo marginata tortoises provided the best results. Feeding period of females was on average 25 days (range 17–44), whereas males remain after female engorgement on tortoise host. Female pre-oviposition period was 14 days (3–31), followed by 24 days of oviposition (18–29). Pre-eclosion and eclosion, both together, takes 31 days (21–43). Larvae fed 5 days (3–9), then molted to nymphs after 17 days (12–23). Feeding period of nymphs lasted 7 days (5–10), engorged nymphs molted to adults after 24 days (19–26). Sex ratio of laboratory hatched H. aegyptium was nearly equal (1:1.09). The average weight of engorged female was 0.95 (0.72–1.12) g. The average number of laid eggs was 6,900 (6,524–7,532) per female, it was significantly correlated with weight of engorged female. Only 2.8% of engorged larvae and 1.8% of engorged nymphs remained un-molted and died. Despite the use of natural host species, feeding success of females reached only 45%. The whole life-cycle was completed within 147 days (98–215).     

Hyalomma aegyptium as dominant tick in tortoises of the genus Testudo in Balkan countries, with notes on its host preferences

Collection of 1327 ticks sampled throughout Greece, Bulgaria, Romania and Croatia, from 211 tortoises belonging to three species, Testudo marginata Schoepff, T. graeca Linnaeus, and T. hermanni Gmelin, revealed the presence of four species of ixodid ticks, namely Hyalomma aegyptium (Linnaeus), Haemaphysalis sulcata Canestrini and Fanzago, H. inermis Birula and Rhipicephalus sanguineus (Latreille). Study confirmed the strong dominance of all life stages of H. aegyptium among ticks parasitizing west Palaearctic tortoises of genus Testudo Linnaeus. Furthermore, a considerable portion of ticks collected from tortoises in southwestern Bulgaria represent larvae and nymphs of H. sulcata. At the same area we collected as exception one larva and one nymph of H. inermis from a single specimen of T. hermanni. Our findings of four adults of R. sanguineus is the first record of this species from reptilian host. According to our results achieved on localities with syntopic occurrence of two tortoise species, T. marginata and T. graeca represent in the Balkans the principal hosts of H. aegyptium, whereas T. hermanni serves only as an alternative host in the areas close to range of either T. marginata or T. graeca.     

Tick prevalence and species diversity on Aldabran giant tortoises (Dipsochelys dussumieri) in relation to host range and host size in a restored ecosystem, Kenya

Tick species density and diversity on Aldabran tortoises was investigated in relation to the habitat range and size of each tortoise. Identification of tick infestation patterns forms an important aspect of effective tick control. Ten Aldabran tortoises were de‐ticked and monitored over the course of 2 months. Tick species found were Amblyomma sparsum, Amblyomma nuttalli, Amblyomma hebraeum and Boophilus decoloratus, with the most prevalent species found being A. sparsum. Tick loads varied considerably from 20 to 214 ticks per tortoise, with most ticks collected from the head/neck region. Tortoises ranging outside Haller Park had higher tick loads (70–214) compared with tortoises ranging within Haller Park (20–99). Tick load was not correlated with tortoise size. Results indicate that tick loads are related to the habitat range of the tortoises and may indirectly also be related to food preference and host food availability. Implications of the findings and appropriate tick control measures are discussed.     

Seed dispersal by Galápagos tortoises

Aim Large‐bodied vertebrates often have a dramatic role in ecosystem function through herbivory, trampling, seed dispersal and nutrient cycling. The iconic Galápagos tortoises (Chelonoidis nigra) are the largest extant terrestrial ectotherms, yet their ecology is poorly known. Large body size should confer a generalist diet, benign digestive processes and long‐distance ranging ability, rendering giant tortoises adept seed dispersers. We sought to determine the extent of seed dispersal by Galápagos tortoises and their impact on seed germination for selected species, and to assess potential impacts of tortoise dispersal on the vegetation dynamics of the Galápagos. Location Galápagos, Ecuador. Methods To determine the number of seeds dispersed we identified and counted intact seeds from 120 fresh dung piles in both agricultural and national park land. To estimate the distance over which tortoises move seeds we used estimated digesta retention times from captive tortoises as a proxy for retention times of wild tortoises and tortoise movement data obtained from GPS telemetry. We conducted germination trials for five plant species to determine whether tortoise processing influenced germination success. Results In our dung sample, we found intact seeds from > 45 plant species, of which 11 were from introduced species. Tortoises defecated, on average, 464 (SE 95) seeds and 2.8 (SE 0.2) species per dung pile. Seed numbers were dominated by introduced species, particularly in agricultural land. Tortoises frequently moved seeds over long distances; during mean digesta retention times (12 days) tortoises moved an average of 394 m (SE 34) and a maximum of 4355 m over the longest recorded retention time (28 days). We did not find evidence that tortoise ingestion or the presence of dung influenced seed germination success. Main conclusions Galápagos tortoises are prodigious seed dispersers, regularly moving large quantities of seeds over long distances. This may confer important advantages to tortoise‐dispersed species, including transport of seeds away from the parent plants into sites favourable for germination. More extensive research is needed to quantify germination success, recruitment to adulthood and demography of plants under natural conditions, with and without tortoise dispersal, to determine the seed dispersal effectiveness of Galápagos tortoises.     

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.     

Desert Tortoises (Gopherus agassizii) Are Selective Herbivores that Track the Flowering Phenology of Their Preferred Food Plants

Previous studies of desert tortoise foraging ecology in the western Mojave Desert suggest that these animals are selective herbivores, which alter their diet according to the temporal availability of preferred food plants. These studies, however, did not estimate availability of potential food plants by taking into account the spatial and temporal variability in ephemeral plant abundance that occurs within the spring season. In this study, we observed 18 free-ranging adult tortoises take 35,388 bites during the spring foraging season. We also estimated the relative abundance of potential food plants by stratifying our sampling across different phenological periods of the 3-month long spring season and by different habitats and microhabitats. This methodology allowed us to conduct statistical tests comparing tortoise diet against plant abundance. Our results show that tortoises choose food plants non-randomly throughout the foraging season, a finding that corroborates the hypothesis that desert tortoises rely on key plants during different phenological periods of spring. Moreover, tortoises only consumed plants in a succulent state until the last few weeks of spring, at which time most annuals and herbaceous perennials had dried and most tortoises had ceased foraging. Many species of food plants—including several frequently eaten species—were not detected in our plant surveys, yet tortoises located these rare plants in their home ranges. Over 50% of bites consumed were in the group of undetected species. Interestingly, tortoises focused heavily on several leguminous species, which could be nutritious foods owing to their presumably high nitrogen contents. We suggest that herbaceous perennials, which were rare on our study area but represented ~30% of tortoise diet, may be important in sustaining tortoise populations during droughts when native annuals are absent. These findings highlight the vulnerability of desert tortoises to climate change if such changes alter the availability of their preferred food plants.     

Motivational Aspects of Desert Tortoise Caretaking

ABSTRACT

This study (n=490) investigates the motives of humans who maintain desert tortoises in a captive setting. Using data from previously published surveys, a species-appropriate instrument, the Tortoise Caretaking Questionnaire (TCQ), utilizing 20 Likert-type questions was developed to examine ten motives for caretaking. The TCQ also contained a brief demographic section. Each motive was analyzed with respect to strength, age, gender and tortoise rank (compared with other household pets). Two thousand three hundred and seventy-eight questionnaires were distributed and 496 were returned (20.8%); of these, 490 were deemed usable. All motives were shown to be significant and with one exception, females expressed stronger levels of each than did males. Younger respondents tended to rank tortoises higher than other pets whereas older respondents ranked them lower. Future research should investigate longitudinal and other aspects of tortoise caretaking.     

The Dominance of Introduced Plant Species in the Diets of Migratory Galapagos Tortoises Increases with Elevation on a Human‐Occupied Island

The distribution of resources and food selection are fundamental to the ecology, life history, physiology, population dynamics, and conservation of animals. Introduced plants are changing foraging dynamics of herbivores in many ecosystems often with unknown consequences. Galapagos tortoises, like many herbivores, undertake migrations along elevation gradients driven by variability in vegetation productivity which take them into upland areas dominated by introduced plants. We sought to characterize diet composition of two species of Galapagos tortoises, focussing on how the role of introduced forage species changes over space and the implications for tortoise conservation. We quantified the distribution of tortoises with elevation using GPS telemetry. Along the elevation gradient, we quantified the abundance of introduced and native plant species, estimated diet composition by recording foods consumed by tortoises, and assessed tortoise physical condition from body weights and blood parameter values. Tortoises ranged between 0 and 429 m in elevation over which they consumed at least 64 plant species from 26 families, 44 percent of which were introduced species. Cover of introduced species and the proportion of introduced species in tortoise diets increased with elevation. Introduced species were positively selected for by tortoises at all elevations. Tortoise physical condition was either consistent or increased with elevation at the least biologically productive season on Galapagos. Santa Cruz tortoises are generalist herbivores that have adapted their feeding behavior to consume many introduced plant species that has likely made a positive contribution to tortoise nutrition. Some transformed habitats that contain an abundance of introduced forage species are compatible with tortoise conservation.     

The Role of Endangered Species Reintroduction in Ecosystem Restoration: Tortoise–Cactus Interactions on Española Island, Galápagos

We evaluated the role that endangered species reintroduction efforts can play in the larger context of ecosystem restoration. To do so, we examined interactions between endangered giant tortoises (Geochelone nigra hoodensis), currently being reintroduced to Isla Española, Galápagos, and an arboreal cactus (Opuntia megasperma var. megasperma), which is itself endangered and a keystone resource for many animals on the island. We collected information on spatial patterns of occurrence of cacti, tortoises, and woody vegetation and compared recruitment of juvenile cacti in areas occupied versus unoccupied by tortoises. Reintroduced tortoises appeared to suppress cactus recruitment near the few remaining adult cacti at the study site, but facilitate it at longer distances, with tortoise–cactus interactions mediated by the presence of woody vegetation, which likely alters tortoise movements and thereby patterns of cactus seed dispersal. The net effect of tortoises on cacti appeared to be positive insofar as tortoise presence was associated with greater recruitment of juveniles into cactus populations. Our study provides support for reintroducing endangered reptiles and other animals to aid ecosystem restoration in areas where they might once have played an important role in grazing upon and dispersing plants.     

Body size development of captive and free‐ranging Leopard tortoises (Geochelone pardalis)

The growth and weight development of Leopard tortoise hatchings (Geochelone pardalis) kept at the Al Wabra Wildlife Preservation (AWWP), Qatar, was observed for more than four years, and compared to data in literature for free‐ranging animals on body weight or carapace measurements. The results document a distinctively faster growth in the captive animals. Indications for the same phenomenon in other tortoise species (Galapagos giant tortoises, G. nigra; Spur‐thighed tortoises, Testudo graeca; Desert tortoises, Gopherus agassizi) were found in the literature. The cause of the high growth rate most likely is the constant provision with highly digestible food of low fiber content. Increased growth rates are suspected to have negative consequences such as obesity, high mortality, gastrointestinal illnesses, renal diseases, “pyramiding,” fibrous osteodystrophy or metabolic bone disease. The apparently widespread occurrence of high growth rates in intensively managed tortoises underlines how easily ectothermic animals can be oversupplemented with nutrients. Zoo Biol 29:517–525, 2010. © 2009 Wiley‐Liss, Inc.     

Changes in the status of tortoise populations in Greece 1984–2001

Three species of tortoise (Testudinidae) occur in Greece (Testudo hermanni, T. graeca and the endemic T. marginata), all of which have been listed as rare or vulnerable. This paper describes the current situation of 75 populations that were last observed in the 1970s and 1980s and described in 1989. Twenty-nine populations had declined in density and/or status (significantly more than had improved), 10 of which were functionally extinct. A particularly notable loss was a dense population of T. marginata at Gytheion in the Peloponnese due to a widespread fire. Declining populations were significantly associated with identified high threat in 1989 and with close proximity to human settlement. There were no significant effects of tortoise species, area of site, characteristics of surrounding areas or original density on these changes. Declines were less associated with agriculture than predicted in 1989, reflecting changing economic conditions in Greece in the 1990s. Continuing threats to tortoise habitats make their long-term future appear bleak outside of protected areas. The risk of extinction from stochastic variation in small populations was also assessed, using the VORTEX program. This risk was much lower than that from habitat loss; 60–96% of populations of 100 tortoises would survive for 1000 years, depending on adult body size, compared to only 0–0.02% of habitats. The high survival potential of small populations would facilitate conservation of the high intraspecific diversity of tortoises in Greece.     

Using motion-sensor camera technology to infer seasonal activity and thermal niche of the desert tortoise (Gopherus agassizii)

Understanding the relationships between environmental variables and wildlife activity is an important part of effective management. The desert tortoise (Gopherus agassizii), an imperiled species of arid environments in the southwest US, may have increasingly restricted windows for activity due to current warming trends. In summer 2013, we deployed 48 motion sensor cameras at the entrances of tortoise burrows to investigate the effects of temperature, sex, and day of the year on the activity of desert tortoises. Using generalized estimating equations, we found that the relative probability of activity was associated with temperature (linear and quadratic), sex, and day of the year. Sex effects showed that male tortoises are generally more active than female tortoises. Temperature had a quadratic effect, indicating that tortoise activity was heightened at a range of temperatures. In addition, we found significant support for interactions between sex and day of the year, and sex and temperature as predictors of the probability of activity. Using our models, we were able to estimate air temperatures and times (days and hours) that were associated with maximum activity during the study. Because tortoise activity is constrained by environmental conditions such as temperature, it is increasingly vital to conduct studies on how tortoises vary their activity throughout the Sonoran Desert to better understand the effects of a changing climate.     

Sighting frequency and food habits of the leopard tortoise, Geochelone pardalis, in northern Tanzania

Sighting frequency and food habits of the leopard tortoise (Geochelone pardalis) were studied in northern Tanzania from October 1993 to June 1996. Sighting frequency varied significantly between protected (0.22 mhr^?1) and unprotected sites (0.59 mhr^?1), and between Arusha (0.27 mhr^?1) and Serengeti sites (0.56 mhr^?1). The tortoise diet comprised mostly plants (97.8%) and rarely inorganic matter (2.2%). A total of 47 plant species from 21 families was eaten. Forbs made up 74.5% of the plant items and monocots the remainder. Succulents contributed 51.0% of the plant items eaten while grasses and legumes accounted for 16.8% and 13.5%, respectively. Some plant items were eaten more frequently than their occurrence in the habitats.     

Tracing Genetic Lineages of Captive Desert Tortoises in Arizona

Abstract: We genotyped 180 captive desert tortoises (Gopherus agassizii) from Kingman (n = 45), Phoenix (n = 113), and Tucson (n = 22), Arizona, USA, to determine if the genetic lineage of captives is associated with that of wild tortoises in the local area (Sonoran Desert). We tested all samples for 16 short tandem repeats and sequenced 1,109 base pairs of mitochondrial DNA (mtDNA). To determine genetic origin, we performed assignment tests against a reference database of 997 desert tortoise samples collected throughout the Mojave and Sonoran Deserts. We found that >40% of our Arizona captive samples were genetically of Mojave Desert or hybrid origin, with the percentage of individuals exhibiting the Mojave genotype increasing as the sample locations approached the California, USA, border. In Phoenix, 11.5% were Sonoran–Mojave crosses, and 8.8% were hybrids between desert tortoise and Texas tortoise (G. berlandieri). Our findings present many potential implications for wild tortoises in the Sonoran Desert of Arizona. Escaped or released captive tortoises with Mojave or hybrid genotypes have the potential to affect the genetic composition of Sonoran wild populations. Genotyping captive desert tortoises could be used to inform the adoption process, and thereby provide additional protection to native desert-tortoise populations in Arizona.     

Distribution,status and biology of the tortoise,Geochelone chilensis,in Río Negro Province,Argentina

Morphometric and meristic data from 32 specimens from Río Negro Province do not allow differentiation between G. donosobarrosi and G. chilensis. The significance of morphological and genetic differentiation among Argentinian tortoises is yet to be determined; southern Chaco tortoises undergo ontogenetic and sexual dichromatism. Geochelone chilensis has an extensive latitudinal range (Map 1). Field investigations indicate that Chaco tortoises occupy, and apparently excavate, burrows in the southern portion of the range, prior reports of the species’ southern limit are evaluated and the link between tortoise distribution and “monte”; vegetation is discussed. The season of reproduction and clutch size are noted. Extensive internal pet traffic has markedly affected tortoise populations in some areas; near the southern limit of the range, however, there is little commercial collecting.     

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.     

Invertebrate prey and predatory behaviour of the omnivorous African tortoise Kinixys spekii

Invertebrates form an important part of the diet in the omnivorous African tortoises of the genus Kinixys. Millipede prey of Kinixys spekii in Zimbabwe had a mean volume of 0.9 ml, and made up 64.7% of invertebrate food by volume; beetles made up most of the remainder and had a mean volume of 1.4 ml. The mean mass of invertebrate prey was 0.19% of tortoise mass, a similar value of relative prey mass to many insectivorous lizards. Tortoises preferentially attacked moving millipedes at or just behind the head, but predatory behaviour was otherwise unspecialized, with tortoises killing millipedes by ingesting them in pieces. Handling times of millipede prey varied significantly with relative prey mass, defensive behaviour, and direction of ingestion. The profitability (mass intake/handling time) of millipedes was maximal at a relative prey mass of 0.2%; the basis on which prey are selected is discussed.