Desert Tortoise Research Articles

Rates of Food Passage in the Digestive Tract of Young Desert Tortoises: Effects of Body Size and Diet Quality

Diet quality and body size affected passage time of 2 diets (higher and lower in fiber) in hatchling and juvenile desert tortoises (Gopherus agassizii). Mean retention time of the liquid fraction of each diet was significantly shorter than that of the solid fraction, and hatchlings had shorter passage times than juveniles. Habitat disturbances that limit access of hatchlings to diets lower in fiber may negatively impact the physiological and behavioral ecology of young desert tortoises.

The importance of physiological ecology in conservation biology

Many of the threats to the persistence of populations of sensitive species have physiological or pathological mechanisms, and those mechanisms are best understood through the inherently integrative discipline of physiological ecology. The desert tortoise was listed under the Endangered Species Act largely due to a newly recognized upper respiratory disease thought to cause mortality in individuals and severe declines in populations. Numerous hypotheses about the threats to the persistence of desert tortoise populations involve acquisition of nutrients, and its connection to stress and disease. The nutritional wisdom hypothesis posits that animals should forage not for particular food items, but instead, for particular nutrients such as calcium and phosphorus used in building bones. The optimal foraging hypothesis suggests that, in circumstances of resource abundance, tortoises should forage as dietary specialists as a means of maximizing intake of resources. The optimal digestion hypothesis suggests that tortoises should process ingesta in ways that regulate assimilation rate. Finally, the cost-of-switching hypothesis suggests that herbivores, like the desert tortoise, should avoid switching food types to avoid negatively affecting the microbe community responsible for fermenting plants into energy and nutrients. Combining hypotheses into a resource acquisition theory leads to novel predictions that are generally supported by data presented here. Testing hypotheses, and synthesizing test results into a theory, provides a robust scientific alternative to the popular use of untested hypotheses and unanalyzed data to assert the needs of species. The scientific approach should focus on hypotheses concerning anthropogenic modifications of the environment that impact physiological processes ultimately important to population phenomena. We show how measurements of such impacts as nutrient starvation, can cause physiological stress, and that the endocrine mechanisms involved with stress can result in disease. Finally, our new syntheses evince a new hypothesis. Free molecules of the stress hormone corticosterone can inhibit immunity, and the abundance of "free corticosterone" in the blood (thought to be the active form of the hormone) is regulated when the corticosterone molecules combine with binding globulins. The sex hormone, testosterone, combines with the same binding globulin. High levels of testosterone, naturally occurring in the breeding season, may be further enhanced in populations at high densities, and the resulting excess testosterone may compete with binding globulins, thereby releasing corticosterone and reducing immunity to disease. This sequence could result in physiological and pathological phenomena leading to population cycles with a period that would be essentially impossible to observe in desert tortoise. Such cycles could obscure population fluctuations of anthropogenic origin.

ACCURACY AND RELIABILITY OF DOGS IN SURVEYING FOR DESERT TORTOISE (GOPHERUS AGASSIZII)

The desert tortoise (Gopherus agassizii) is federally listed as "threatened" and is afforded protection in several U.S. states including California, Nevada, Utah, and Arizona. Numerous factors ranging from habitat destruction to disease are thought to contribute to the species' decline throughout its range. Data collection on desert tortoises in the wild is challenging because tortoises are secretive, and many age and size classes are virtually undetectable in the wild. Detection dogs have been used for decades to assist humans, and the use of dogs for wildlife surveys is of increasing interest to scientists and wildlife managers. To address the basic question of whether dogs could be used to survey for the desert tortoise, we quantified the reliability and efficacy of dogs trained for this purpose. Efficacy is the number of tortoises that dogs find out of a known population. Reliability is a measure of how many times a dog performs its trained alert when it has found a tortoise. A series of experimental trials were designed to statistically quantify these metrics in the field setting where dogs trained to locate live desert tortoises were tested on their ability to find them on the surface, in burrows, and in mark-recapture surveys. Results indicated that dogs are effective at and can safely locate desert tortoises with reliability on the surface and are capable of detecting tortoises in burrows under a range of environmental conditions. Dogs found tortoises at the same statistical rate at temperatures between 12 degrees and 27 degrees C, relative humidity from 16% to 87%, and wind speeds up to 8 m/s. In both surface and burrow trials, dogs found >90% of the experimental animals. In comparative studies with humans, dogs found tortoises as small as 30 mm, whereas the smallest tortoise located by human survey teams was 110 mm. Although not all dogs or dog teams meet the requirements to conduct wildlife surveys, results from this study show the promise in using dogs to increase our knowledge of rare, threatened, and endangered species through improved data collection methods.

Daily Energy Expenditure in Free-ranging Gopher Tortoises (Gopherus Polyphemus)

Studies of ecological energetics in chelonians are rare. Here, we report the first measurements of daily energy expenditure (DEE) and water influx rates (WIRs) in free-ranging adult Gopher Tortoises (Gopherus polyphemus). We used the doubly labeled water (DLW) method to measure DEE in six adult tortoises during the non-breeding season in south-central Mississippi, USA. Tortoise DEE ranged from 76.7–187.5 kJ/day and WIR ranged from 30.6–93.1 ml H2O/day. Daily energy expenditure did not differ between the sexes, but DEE was positively related to body mass. Water influx rates varied with the interaction of sex and body mass. We used a log/log regression model to assess the allometric relationship between DEE and body mass for Gopher Tortoises, Desert Tortoises (Gopherus agassizii), and Box Turtles (Terrapene carolina), the only chelonians for which DEE has been measured. The slope of this allometric model (0.626) was less than that previously calculated for herbivorous reptiles (0.813), suggesting that chelonians may expend energy at a slower rate per unit of body mass compared to other herbivorous reptiles. We used retrospective power analyses and data from the DLW isotope analyses to develop guidelines for sample sizes and duration of measurement intervals, respectively, for larger-scale energetic studies in this species.

A highway's road-effect zone for desert tortoises ( Gopherus agassizii)

Roads and highways can affect populations of animals directly (e.g. due to road mortality) and indirectly (e.g. due to fragmentation of habitat and proliferation of non-native or predatory species). We investigated the effect of roads on threatened desert tortoise ( Gopherus agassizii) populations in the Mojave Desert, California, and attempted to determine the width of the road-effect zone by counting tortoise signs along transects at 0, 400, 800, and 1600 m from the edge of a highway. Mean sign count was 0.2/km at 0 m, 4.2/km at 400 m, 5.7/km at 800 m, and 5.4/km at 1600 m from the highway edge. The differences between all pairs of distances, except 800 and 1600 m, were statistically significant, suggesting that tortoise populations in our study area are depressed in a zone extending at least 400 m from roadways. We speculate that the major cause for this depression zone is road mortality.

Dominance and environmental correlates of alien annual plants in the Mojave Desert, USA

Land managers are concerned about the negative effects of alien annual plants on native plants, threatened and endangered species such as the desert tortoise ( Gopherus agassizii), and ecosystem integrity in the Mojave Desert. Management of alien plants is hampered by a lack of information regarding the dominance and environmental correlates of these species. The results of this study indicate that alien plant species comprised a small fraction of the total annual plant flora, but most of the annual plant community biomass. When rainfall was high in 1995, aliens comprised 6% of the flora and 66% of the biomass. When rainfall was low in 1999, aliens comprised 27% of the flora and 91% of the biomass. Bromus rubens, Schismus spp. ( S. arabicus and S. barbatus), and Erodium cicutarium were the predominant alien species during both years, comprising 99% of the alien biomass. B. rubens was more abundant in relatively mesic microhabitats beneath shrub canopies and at higher elevations above 800–1000 m, whereas Schismus spp. and E. cicutarium were more abundant in the relatively arid interspaces between shrubs, and, for Schismus spp., at lower elevations as well. Disturbance variables were more reliable indicators of alien dominance than were productivity or native plant diversity variables, although relationships often varied between years of contrasting rainfall. The strongest environmental correlates occurred between dirt road density and alien species richness and biomass of E. cicutarium, and between frequency and size of fires and biomass of B. rubens.

Attributes of desert tortoise populations at the National Training Center, Central Mojave Desert, California, USA

We sampled 21 study plots for desert tortoises ( Gopherus agassizii) at the National Training Center, Fort Irwin, California. Each plot was sampled once between 1997 and 2003 to obtain a snapshot of population attributes, status, and relationships between tortoise densities and human activities. Densities ranged from <1 to 28 tortoises km −2; overall, tortoises were uncommon to rare at 16 of the 21 plots. Tortoise densities were negatively correlated with death rates, infectious disease (mycoplasmosis), surface disturbance and trash. Health status of tortoises was correlated with some anthropogenic uses. The presence of infectious disease in tortoises was negatively correlated with distances from offices, the Ft. Irwin cantonment, and paved roads. Also, significantly more tortoises with shell disease were found on plots with current and recent military use than on plots with no history of military use. Factors contributing to or causing deaths of tortoises included vehicles, vandalism, predation, mycoplasmosis and shell diseases. Annual death rates for subadult and adult tortoises ranged from 1.9% to 95.2% for the 4 years preceding surveys. Deaths from anthropogenic sources were significantly correlated with surface disturbances, trash, military ordnance, and proximity to offices and paved roads—typical characteristics of military training areas.

Abundance and distribution of selected elements in soils, stream sediments, and selected forage plants from desert tortoise habitats in the Mojave and Colorado deserts, USA

A baseline and background chemical survey was conducted in southeastern California, USA, to identify potential sources of toxicants in natural and anthropogenically-altered habitats of the threatened desert tortoise ( Gopherus agassizii). Soil, stream sediment, and plant samples were collected from six tortoise habitat study areas in the Mojave and Colorado deserts and analysed for up to 66 different elements. The chemical analyses provided new information on the abundances and distributions of selected elements in this region. Soil, stream-sediment, and plant analyses showed distinct variations in bulk chemistries from locality to locality. Variations were, in general, consistent with the many types of exposed rock units in the region, their highly variable bulk mineralogies, and chemical contents. Of elements in soils that might have been toxic to tortoises, only As seemed to be anomalous region-wide. Some soil and plant anomalies were clearly anthropogenic. In the Rand and Atolia mining districts, soil anomalies for As, Au, Cd, Hg, Sb, and(or) W and plant anomalies for As, Sb, and(or) W extend as far as ∼15 km outward from the present area of mining; soils containing anomalous Hg were found at least 6 km away from old piles of tailings. The anomalous concentrations of As and Hg may have been the source of elevated levels of these elements found in ill tortoises from the region. In the Goldstone mining district, soil anomalies extended several km from the mining area. These areas probably represented anthropogenic surface contamination of dust redistributed by wind, vehicles, and rainfall. One of two study areas transected by a paved road (Chemehuevi Valley) showed weakly elevated levels of Pb, which extended as far as ∼22 m from the pavement edge and were probably related to vehicle exhaust. No soil or plant samples from historically used military areas (Goldstone, Goffs, Chemehuevi Valley, Chuckwalla Bench) contained anomalous concentrations of the elements As, Cu, Cr, Fe, Pb, or Zn that could be ascribed to military maneuvers, vehicles, or ordnance. For future studies, the distribution and abundance of elements in the tortoise forage plants need to be evaluated for the respective roles of dust and systemic uptake. Additional chemical data from tortoise necropsies and nutritional studies are needed to determine the effects of potentially toxic elements in tortoise habitats on their health.

Ecology of a population of subsidized predators: Common ravens in the central Mojave Desert, California

Human subsidies have resulted in the rapid growth of populations of common ravens ( Corvus corax) in the Mojave Desert. This is a management concern because ravens prey on threatened desert tortoises ( Gopherus agassizii). We conducted weekly counts for 29 months at 10 sites on the US Army's National Training Center, Fort Irwin, California to evaluate factors affecting the distribution of ravens. Raven abundance varied seasonally, diurnally, and with human abundance. It was greatest near resource subsidies, specifically the landfill and sewage ponds. Although other studies have documented heavy use of landfills by ravens, the use of sewage ponds had not been previously reported in the published literature. We suggest that raven management should focus on reducing access to anthropogenic resources.

Seroprevalence of Mycoplasma agassizii and tortoise herpesvirus in captive desert tortoises ( Gopherus agassizii) from the Greater Barstow Area, Mojave Desert, California

Upper respiratory tract disease (URTD) has been implicated as a cause of decline of wild populations of desert tortoises, Gopherus agassizii, in the western Mojave Desert. One explanation for outbreaks of disease may be the release or escape of diseased captive tortoises into naïve wild populations. Because Mycoplasma agassizii and tortoise herpesvirus have surfaced as important pathogens, 179 captive tortoises were evaluated in the greater community of Barstow, San Bernardino County, California during 2000 and 2001 to determine pathogen exposure. An indirect enzyme-linked immunosorbent assay (ELISA) was performed to detect antibodies against Mycoplasma agassizii ( n=179) and tortoise herpesvirus ( n=109). Anti-mycoplasma antibodies were present in 82.7% of the tortoises while anti-herpesvirus antibodies were detected in 26.6%. A positive association was found between tortoises with anti-mycoplasma antibodies and severity of clinical signs of URTD ( p=0.001) and with age categories, with adults being more likely to be positive ( p<0.001). Neither association was found with herpesvirus exposure. No association was found between gender and pathogen exposure or between being positive for exposure to both pathogens. Findings suggest that captive tortoises can be a source of infection for free ranging desert tortoises.

Identification of a novel herpesvirus from a California desert tortoise (Gopherus agassizii)

Herpesviruses are significant pathogens of tortoises, causing upper respiratory tract disease and necrotizing stomatitis, with infections often associated with high mortality rates. Herpesvirus infection in a captive California desert tortoise (Gopherus agassizii) was detected by light microscopic observation of intranuclear inclusion bodies in various tissues followed by transmission electron microscopic observation of herpesvirus-like particles, and amplification of herpesvirus nucleic acid sequences using polymerase chain reaction. Using an indirect enzyme linked immunosorbent assay, anti-tortoise herpesvirus antibodies were detected one month after initial onset of clinical signs. This novel herpesvirus is distinct from the previously described tortoise herpesvirus (tortoise herpesvirus-1, THV-1) sharing 83% sequence identity of 60 amino acids of a portion of the DNA polymerase gene and 79% sequence identity across 120 amino acids of a portion of the ribonucleotide reductase gene. Similar to THV-1, this novel herpesvirus, tortoise herpesvirus-2 (THV-2), also clusters with the alphaherpesviruses.

Mycoplasmosis in Free-ranging Desert Tortoises in Utah and Arizona

Upper respiratory tract disease (URTD) has been associated with major losses of free-ranging desert tortoises (Gopherus agassizii) in the southwestern United States. This prompted a clinical examination of 63 free-ranging desert tortoises for signs of URTD and sampling for Mycoplasma agassizii, the causative agent of URTD. Tortoises were sampled from three sites in the eastern Mojave Desert (1992-93), and from three sites in the Sonoran Desert (1992-94). Plasma samples were tested for antibodies to M. agassizii using an enzyme-linked immunosorbent assay (ELISA). Nasal aspirate samples from 12 Sonoran tortoises were tested using polymerase chain reaction (PCR) test directed at the 16S rRNA gene of M. agassizii. Nasal aspirate samples from all tortoises were cultured for M. agassizii. In the Mojave Desert, nine tortoises had clinical signs of URTD and eight were seropositive for M. agassizii. In the Sonoran Desert, there were no clinical signs of URTD, but two tortoises were seropositive, and two tortoises had positive PCR results.

Correctly Estimating How Environmental Stochasticity Influences Fitness and Population Growth

Increased temporal variance in life-history traits is generally predicted to decrease individual fitness and population growth. We show that a widely used result of stochastic sensitivity analysis that bolsters this generality is flawed because it ignores the effects of correlations between vital rates. Considering the effects of these correlations (although ignoring autocorrelations), we show that the apparently simple relationship between vital rate variance and fitness can be considerably more complex than previously thought. In particular, the previously estimated negative sensitivities of fitness or population growth to variance in a vital rate can be either enhanced by positive correlations between rates or reversed by negative correlations, even to the point that variability in a rate can increase fitness or population growth. We apply this new sensitivity calculation to data from the desert tortoise and discuss its interpretation in light of the factors generating vital rate correlations.

Costs of Growth in Tortoises

The metabolic cost of growth in reptiles has been difficult to detect in many previous studies. We designed experiments to detect and quantify added costs of growth by comparing daily energy expenditures of young, growing Desert Tortoises (Gopherus agassizii) with similar-sized, but adult, Parrot-Beaked Tortoises (Homopus areolatus). We measured both field (outdoors, semicaptive) and standard (20°, 25°, and 30°C) metabolic rates of each species in groups matched for body size to minimize body size effects. Mass-adjusted field metabolic rates of the juvenile tortoises were not higher but were, in fact, significantly lower (by 29%) than in adult tortoises. Standard metabolic rates did not differ between species at any temperature, thus failing to support the hypothesized higher energetic costs of growth in the juvenile tortoises. These results, although contrary to expectations, support a growing body of evidence, suggesting that the cost of growth in juvenile reptiles does not increase their field energy expenditures above those expected for adults.

Regional-Scale Estimation of Density and Habitat Use of the Desert Tortoise (Gopherus agassizii) in Arizona

Abstract Desert Tortoise surveys and management in the Sonoran Desert typically exclude intermountain valleys, where tortoises are generally thought to be absent. Furthermore, few regional-level surveys have been conducted because of difficulties in sampling in the complex landscape of Sonoran Desert upland habitat. We used distance-sampling to document macrohabitat use and regional density of Desert Tortoises across the 76,800-ha Ironwood Forest National Monument in Arizona. We observed 42 tortoises on transects, and distance sampling produced an estimate of 17,997 tortoises ≥ 150 mm carapace length (coefficient of variation = 41.5%) on the monument. Stratification by habitat type (steep topography with boulders, incised washes, or neither of these components) improved precision slightly (37.2%). Detection probability contributed least to density variance, compared to encounter rate and tortoise detectability on the transect line, indicating that assumptions of the technique were met during sampling. We ...

PROBLEMS WITH SAMPLING DESERT TORTOISES: A SIMULATION ANALYSIS BASED ON FIELD DATA

Abstract The desert tortoise (Gopherus agassizii) was listed as a U.S. threatened species in 1990 based largely on population declines inferred from mark–recapture surveys of 2.59-km2 (1-mi2) plots. Since then, several census methods have been proposed and tested, but all methods still pose logistical or statistical difficulties. We conducted computer simulations using actual tortoise location data from 21-mi2 plot surveys in southern California, USA, to identify strengths and weaknesses of current sampling strategies. We considered tortoise population estimates based on these plots as “truth” and then tested various sampling methods based on sampling smaller plots or transect lines passing through the mile squares. Data were analyzed using Schnabel's mark–recapture estimate and program CAPTURE. Experimental subsampling with replacement of the 1-mi2 data using 1-km2 and 0.25-km2 plot boundaries produced data sets of smaller plot sizes, which we compared to estimates from the 1-mi2 plots. We also tested di...

Mycoplasmosis in Free-ranging Desert Tortoises in Utah and Arizona

Mycoplasmosis in Free-ranging Desert Tortoises in Utah and Arizona

Survival during Early Life Stages of the Desert Tortoise (Gopherus agassizii) in the South-Central Mojave Desert

Early age classes of the Desert Tortoise (Gopherus agassizii) are particularly vulnerable to predation by several mammal and bird species. We studied tortoise survival at the Sand Hill Training Area of the Marine Corps Air Ground Combat Center, Twentynine Palms, California, from 1998 to 1999. We radiographed and thread-spooled 25 females to determine reproductive and nesting ecology. Predators consumed 11 of 42 monitored nests during the first 70 days of incubation. Ninety-one of 132 eggs in nests fenced after 70 days developed into healthy neonates. We recorded 0.84 and 0.91 neonate survival probability during dispersal in 1998 and 1999, respectively. Applying neonatal survival to egg success, we predict that 40% of individuals survived from oviposition to hibernation. Our findings support other chelonian life-history models indicating relatively high mortality early in life. Our data also suggest that neonatal Desert Tortoises are less susceptible to predation than was previously thought, perhaps because of their cryptic coloration and secretive habits. The Common Raven (Corvus corax) was not found to be a source of neonate mortality during this study.

METHODOLOGICAL INSIGHT: Linking management changes to population dynamic responses: the transfer function of a projection matrix perturbation

Summary An important task in applied population ecology is to understand how changes to individual life‐history parameters, such as survival, growth and fecundity, affect population dynamics. Parameter changes, or perturbations, may be caused by deliberate attempts to manage populations (e.g. in pest control, harvesting or conservation) or they may be side‐effects of pollution, genetic modification and climate change. For organisms with complicated life cycles, links between individual life histories and population dynamics are made using population projection matrix (PPM) modelling. Changes to individual, or groups of, life‐history transition rates within a PPM have a nonlinear impact on the resulting eigenvalues. Conventional sensitivity analysis calculates the derivative of the perturbation‐eigenvalue curve to provide tangential linear extrapolation. Until now, only the simulation of perturbed PPMs has captured nonlinear perturbation effects. Here we describe the transfer function of a matrix perturbation. The transfer function captures analytically the true relationship between perturbation magnitude and PPM eigenvalues. This analytical link extends easily to multi‐transition and multiple perturbations, promotes an understanding of matrix properties, and provides a simple method to predict the perturbation required to achieve a desired population rate of increase. We use the transfer function approach to analyse a PPM for the desert tortoise Gopherus agasizzii Cooper, in the context of conservation management decisions. Synthesis and applications. The transfer function offers a novel and powerful framework for the analysis of population projection matrices (PPMs), giving precise predictive power and analytical understanding of population‐level responses to life‐history perturbations, for example in the design of conservation, pest control and population harvesting strategies, prediction of population effects of pollution in ecotoxicology, and in ecological risk assessment. A useful focus is to set a target for the desired rate of increase (or decline) of a population, and use the transfer function to determine how best to achieve this rate.

Laser ablation ICP-MS profiling and semiquantitative determination of trace element concentrations in desert tortoise shells: documenting the uptake of elemental toxicants

The outer keratin layer (scute) of desert tortoise shells consists of incrementally grown laminae in which various bioaccumulated trace elements are sequestered during scute deposition. Laser ablation ICP-MS examination of laminae in scutes of dead tortoises revealed patterns of trace elemental distribution from which the chronology of elemental uptake can be inferred. These patterns may be of pathologic significance in the case of elemental toxicants such as arsenic, which has been linked to both shell and respiratory diseases. Laser ablation transects, performed along the lateral surfaces of sectioned scutes, offered the most successful means of avoiding exogenous contamination that was present on the scute exterior. Semiquantitative determination of elemental concentrations was achieved using sulfur, a keratin matrix element, as an internal standard. The results presented here highlight the potential of laser ablation ICP-MS as a diagnostic tool for investigating toxic element uptake as it pertains to tortoise morbidity and mortality.