Demographic Consequences of Disease in Two Desert Tortoise Populations in California, USA

Proceedings: Conservation, Restoration, and Management of Tortoises and Turtles—An International Conference, pp. 91–99
© 1997 by the New York Turtle and Tortoise Society.

Demographic Consequences of Disease
in Two Desert Tortoise Populations in California, USA

 

KRISTIN H. BERRY

 

U.S. Department of the Interior, Bureau of Land Management,
6221 Box Springs Blvd., Riverside, CA 92507-0714, USA
Current Agency: U.S. Geological Survey, Biological Resources Division (same address)

 

        ABSTRACT: Disease is a causal factor in declines of desert tortoise, Gopherus agassizii, populations at two locations in California. In the interior of the Desert Tortoise Research Natural Area (DTNA), population densities of all sizes of tortoises declined 76% from 75/km² in 1979 to 18/km² in 1992. Densities of adults followed the same pattern and declined 90% from 61/km² in 1979 to 6/km² in 1992. Declines of adult tortoises are attributed primarily to an upper respiratory tract disease (URTD) caused by the pathogen Mycoplasma agassizii. Additional disease-related mortalities are expected to occur, because 25–38% of four samples of adult tortoises from an adjacent site within the DTNA tested positive for antibodies to M. agassizii in 1992. This disease may have been introduced to the DTNA through release of ill captive tortoises.
A second disease, cutaneous dyskeratosis, is present at another reserve, the Chuckwalla Bench Area of Critical Environmental Concern, and is linked to population declines. Between 1982 and 1988 the incidence of cutaneous dyskeratosis increased and lesions became more severe. Between 1982 and 1992 the total tortoise population (all size classes) declined 54% from 153 tortoises/km² to 70 tortoises/km². The adult population declined 61% from 87 tortoises/km² to 34 tortoises/km². The cause(s) of cutaneous dyskeratosis remain uncertain, but possibilities include deficiency diseases or environmental toxicosis.
Diseases, especially if introduced to a native population or if environmentally caused, can have serious consequences for threatened chelonians and will complicate conservation and recovery efforts. Of the two diseases, URTD is of the greatest immediate concern because of its potential to harm tortoise populations on a global scale.

 

Desert tortoise, Gopherus agassizii, populations have declined substantially in the past two decades due to a wide variety of causes, including collecting, vandalism, predation, and habitat loss and deterioration (U.S. Fish and Wildlife Service [USFWS], 1994). Declines became so precipitous that in August 1989, the USFWS listed the species as “Endangered” under the emergency provisions of the Endangered Species Act of 1973, as amended. Disease was a factor in the emergency listing. Subsequently, in April 1990 the USFWS permanently listed the desert tortoise as “Threatened.”
Disease was first implicated as having a significant role in mortality of wild desert tortoises in the 1980s, when remains of tortoises from the Beaver Dam Slope of Arizona and Utah were found to have osteopenia, indicative of malnutrition (Jacobson, 1994). Disease was documented as the major cause of mortality in a wild desert tortoise population in 1988, when ill tortoises with upper respiratory disease were observed by field-workers at a long-term permanent study plot in the interior of the Desert Tortoise Research Natural Area (DTNA) in the western Mojave Desert of California (Berry, 1990; Jacobson et al., 1991). Further research in 1989 and 1990 (e.g., Knowles, 1989; Berry, 1990) confirmed that many tortoises at the DTNA were ill, dying, or had recently died. The signs of disease (nasal discharge, lassitude, cachexia) were similar to signs observed in an often fatal upper respiratory disease of captive desert tortoises throughout southern California (W. Rosskopf, DVM, pers. comm.). Prior to 1988 upper respiratory disease had not been observed in wild, free-living tortoises at the DTNA (Berry and Nicholson, 1984; Berry et al., 1986).
Upper respiratory disease was considered a threat to wild populations of the desert tortoise in the 1970s, long before the disease appeared. When the DTNA was established in 1972, the author and the U.S. Bureau of Land Management (USBLM) expressed concerns about the potentially infectious nature of the disease. We suspected wild populations may become infected through release of ill captive tortoises, which were numerous throughout southern and central California (St. Amant, 1977; Berry and Nicholson, 1984). Because of the potential threat, the USBLM provided funds to Dr. Murray Fowler and his students to conduct research on the disease (Fowler, 1977; Snipes and Biberstein, 1982). No specific bacterial organism was identified as causing respiratory disease. Fowler (1977) concluded that the disease was not caused by a single organism and was not infectious. Stress, especially from malnutrition, was considered the prime predisposing factor.
By the mid-1970s the USBLM, the California Department of Fish and Game (CDFG), the Desert Tortoise Preserve Committee, Inc., and the California Turtle & Tortoise Club distributed literature and issued public statements warning that captive tortoises should not be released to wild lands because of the potential for spreading disease, contaminating genetic stock, and adversely affecting the behavior of wild resident populations (e.g., St. Amant, 1979, 1980; Berry and Nicholson, 1984).
When several wild tortoises with respiratory disease were discovered at a long-term permanent study plot in the DTNA interior in 1988, the CDFG and USBLM provided financial support to initiate research on the pathogenesis of the disease. Within two years research scientists at the University of Florida described the disease as an upper respiratory tract disease (URTD) associated with a new and undescribed mycoplasma (Jacobson et al., 1991). Shortly thereafter a transmission study demonstrated that a new mycoplasma, M. agassizii, is a highly infectious pathogen and causes URTD (Brown et al., 1994). An enzyme-linked immunosorbent assay (ELISA) test for M. agassizii was developed (Schumacher et al., 1993) and was used to determine whether wild desert tortoises carried antibodies to the pathogen (Brown et al., 1994b; Jacobson et al., 1995).
Within weeks of the time that ill tortoises were discovered at the DTNA in 1988, tortoises at another long-term study site in the Chuckwalla Bench Area of Critical Environmental Concern (ACEC), in the eastern Colorado Desert of Riverside County, were discovered to have shell lesions. An abnormally high number of tortoises, many of which were previously marked, were discovered dead (Berry, 1990). Research on the pathogenesis of shell lesions was initiated by Jacobson et al. (1994).
In this paper, I describe the demographic consequences of disease on desert tortoises at the long-term permanent study sites in the interior of the DTNA and on the Chuckwalla Bench, and the evidence linking disease to deaths. I also review the status of the populations as of 1992, discuss the implications of the two diseases for chelonian populations, and outline actions taken to cope with diseases within the two preserves and elsewhere.

 

METHODS

Desert tortoise study site localities
Figure 1. Locations of two protected areas for the desert tortoise: the Desert Tortoise Research Natural Area in the western Mojave Desert, eastern Kern County, California, and the Chuckwalla Bench Area of Critical Environmental Concern in the eastern Colorado Desert, Riverside County, California.

Description of the Two Long-Term Permanent Study Sites for Desert Tortoise Populations

        Desert Tortoise Research Natural Area (DTNA). The DTNA is a 100 km² reserve established in 1972 in the western Mojave Desert to protect high-density tortoise populations and their habitats (Figure 1) (USBLM and CDFG, 1988). Formally designated as a Research Natural Area and Area of Critical Environmental Concern in 1980, the DTNA is protected from recreational vehicle use and sheep grazing by a hog wire fence of which the lower edge is approximately 25 cm above the ground (USBLM, 1980; USBLM and CDFG, 1988). The raised fence permits wild animals to move into and out of the DTNA unimpeded. Since 1972 federal and state governments and the Desert Tortoise Preserve Committee, Inc. have invested considerable effort in establishing and securing habitat in the DTNA to create a viable reserve. To date, more than 8,000 km² of private inholdings have been acquired. The USBLM took action to eliminate all livestock grazing and hardrock mineral mining and also established long-term stewardship and education programs.
Two research study sites on the DTNA were sources of information: (1) a long-term study plot (2.8 km²), established in 1973 in the central interior to monitor changes in populations and habitat (Berry, 1984, 1990); and (2) a short-term, adjacent study plot, established in 1988 for research on health profiles (Christopher et al., 1993, this volume), physiology (water balance and energy flow), and epidemiology of diseases (Brown, 1994b). Habitats within the study plots are typical of diverse creosote bush (Larrea tridentata) scrub plant communities in the western Mojave Desert. Joshua trees (Yucca brevifolia) are widely scattered; creosote bushes are the predominant shrub; and more than three dozen perennial species of shrubs and grasses are present in the understory, e.g., burrobush (Ambrosia dumosa), goldenhead (Acamptopappus sphaerocephalus), cheesebush (Hymenoclea salsola), Anderson thornbush (Lycium andersonii), Nevada joint fir (Ephedra nevadensis), desert needle grass (Achnatherum speciosum), Indian rice grass (A. hymenoides), and one-sided blue grass (Poa secunda ssp. secunda). Elevations range from 853 to 914 m.
Chuckwalla Bench ACEC. In 1980 the USBLM established the Chuckwalla Bench ACEC in the eastern Colorado Desert in recognition of unique wildlife and vegetation values, including high densities of desert tortoises (Figure 1) (USBLM, 1980, 1986). The 371 km² protected area is long (approx. 60 km) and narrow (2.4–12 km) and is a raised bench between the Orocopia, Chocolate, and the Chuckwalla mountains. The bench drains into Milpitas Wash, which has the largest known populations of ironwood, Olneya tesota. In 1980, 35% of the ACEC was in numerous scattered privately owned parcels. Since that time, the USBLM has acquired most of these inholdings (S. Eubanks, pers. comm.) through land acquisition and mitigation programs.
The 2.8 km² long-term study plot (elev. 640 m) contains areas of desert pavement cut by rocky gullies and microphyll woodland washes. The predominant vegetation on the pavements and flat areas is diverse creosote bush scrub typical of the eastern Colorado Desert. It contains burrobush, white rhatany (Krameria grayi), California joint fir (Ephedra californica), cheesebush, ocotillo (Fouquieria splendens ssp. splendens), silver cholla (Opuntia echinocarpa), and Mojave yucca (Yucca schidigera). Washes are dominated by blue palo verde (Cercidium floridum), smoke tree (Psorothamnus spinosus), desert willow (Chilopsis linearis ssp. arcuata), ironwood, and catclaw (Acacia greggii).Collecting Data on Population Densities of Desert Tortoises
Data for estimates of densities were collected during 60 day spring surveys conducted in 1979, 1982, 1988, and 1992 (Berry, 1984, 1990), according to the following procedure established for these ongoing studies: Each study site was divided into a grid of quadrats, each of which was 0.0259 km², and was permanently marked by rebar (iron reinforcing rods). Between late March and early June, one or two field-workers walked transects on each quadrat in search of tortoises. The plot was thoroughly and evenly covered twice, with each coverage requiring about 30 person days of effort. Each coverage constituted a census, with a total of two censuses conducted in each survey year. Surveys were conducted over a minimum of 45 and a maximum of 90 calendar days to minimize the effects of immigration and emigration of tortoises. For each tortoise located, the following data were collected for density estimates: date, unique identification number assigned to each tortoise, size (carapace length at the midline or MCL), sex, capture type (i.e., first capture of a previously unmarked tortoise, first capture in a given year of a previously marked tortoise, second or subsequent capture of a previously marked tortoise in a given year), location, and survey type (first or second census).

Analyzing Data on Population Densities of Desert Tortoises
The Stratified Lincoln Index (Overton, 1971) was selected as the density estimator because it satisfies two critical criteria for estimating densities of long-lived species such as the tortoise: (1) the population data can be stratified into size classes based on capturability, and (2) the equations allow for growth of individual tortoises and their shift from a smaller to a larger size-age class between the first and second censuses (Berry, 1990). The stratification is of particular importance, because larger tortoises are much easier to find than smaller tortoises.
Samples were sorted for analysis by study site, year, and census period (Berry, 1990). For each census within a year, each tortoise was assigned to one of five strata based on MCL: juveniles 1 and 2 (<100 mm MCL), immature 1 (100–139 mm MCL), immature 2 (140–179 mm MCL), small or young adults (180–208 mm MCL), and adult (>208 mm MCL). Tortoises were placed in three groups based on time of capture: (1) tortoises captured during the first census, (2) tortoises captured during the second census, and (3) tortoises captured during both the first and second censuses. Capture-recapture data were arranged in matrices to allow for growth of individual tortoises from one size group to another between censuses. The 95% Confidence Interval (CI) was used to establish level of significance for changes in population densities. An additional source of data was the number of individual tortoises encountered and marked during the 60-day survey for each sample year. If CIs did not overlap from one survey year to the next, the changes in the density estimates were considered statistically significant.

Evaluating Effects of Diseases on the Populations
Data on health status was gathered in detail on the two plots in 1992, including information on presence or absence and type of nasal discharge, patency of the nares, appearance of eyelids and eyes, condition of chin glands, presence or absence of ocular discharge, presence of active or healed injuries, presence and extent of lesions on the shell and limbs, and other signs of disease. In all survey years, 35 mm slide transparencies were taken of the plastron and carapace of most tortoises (Berry, 1984, 1990). These slides document the presence and extent of shell lesions.
Data were also available from necropsies of ill and dying tortoises salvaged from or adjacent to the plots (Jacobson et al., 1991, 1994; J. Klaassen, pers. comm.) from the ELISA tests of tortoises in the research program on epidemiology of URTD at the DTNA (Brown et al., 1994b) and from mortality rates of tortoises in the health profile research program at the DTNA (Christopher et al., 1993). The latter program began in May 1989 with ten adult males and ten adult female tortoises, each fitted with radio transmitters. The tortoises were monitored four times annually (Christopher et al., 1993). Over the next 35 months—through March 1992—as tortoises died, new individuals were added to the program.

 

RESULTS

Desert tortoise density at the DTRNA
Figure 2. Estimates of population densities of desert tortoises at the Desert Tortoise Research Natural Area in Kern County, California in 1979, 1982, 1988, and 1992. Density estimates are presented for all sizes of tortoises and for the adult tortoises (greater than or equal to 180 mm carapace length at midline). The histogram shows the midpoint of the density estimates, and the brackets enclose the 95% Confidence Intervals for the population estimates.
The DTNA
In the 13 years between 1979 and 1992, both the total population and the adult component of the tortoise population experienced statistically significant declines in densities (Figure 2). The total population density, which included all sizes of tortoises, steadily decreased 76%, from a high of 149 tortoises/km² (95% CI = 115–195) in 1979 to a low of 18 tortoises/km² (95% CI = 8–44) in 1992. The pattern of decline of adults differed. First, the adult population component rose in density from 59 tortoises/km² (95% CI = 43–78) in 1979 to 92 tortoises/km² (95% CI = 71–119) in 1982 as a result of recruitment of immature tortoises into the adult size class (Berry, 1990). However, the adult component then steadily declined to 61 tortoises/km² (95% CI = 47–79) in 1988 and thence to 6 adults/km² (95% CI = 2–15) in 1992. The 13-year decline resulted in a 90% loss of adults, during which the total of number of tortoises registered per survey year declined from 189 to 25 individuals.
The deaths of tortoises and the population declines are attributable to several causes (Berry, 1990), including predation by common ravens on the juvenile and small immature size classes. However, between 1988 and 1992 the declines of adults are clearly attributable to URTD caused by M. agassizii. The evidence is from several sources. Prior to 1988 wild, free-ranging tortoises at the DTNA and other long-term tortoise study plots in California were not observed with signs of URTD, and very few were observed with signs of illness or in a dying state (Berry and Nicholson, 1984; Berry et al., 1986). In contrast, many ill, dying, and dead tortoises (remains of animals dead <2 years), most of which were previously marked during censuses, were found on the DTNA plot in 1988, 1989, and 1990, and many dead animals were discovered in 1992 (Berry, unpubl. data). Ill tortoises showed classic signs of URTD (Jacobson et al., 1991; Brown et al., 1994a). In May 1989, 12 tortoises (11 males and 1 female), all of which showed signs of advanced and chronic URTD, were removed from the DTNA for observation and necropsies during the initial research on URTD (Jacobson et al., 1991). The tortoises had chronic inflammatory changes in the upper respiratory tract. A mycoplasma-like organism was seen on the surfaces of the macroepithelial cells (Jacobson et al., 1991). Subsequently, a transmission research program demonstrated that M. agassizii was the causative pathogen (Brown et al., 1994a).
Tortoises with signs of URTD were not confined to a single part of the DTNA but were present throughout the DTNA and in adjacent areas of the Fremont Valley and Rand Mountains (Knowles, 1989; Berry, unpubl. data). In spring 1989, 13 sample plots (1.3–2.6 km² each) were established in the 100 km² DTNA and in adjacent lands within the Fremont Valley and Rand Mountains to determine distribution and frequency of ill tortoises (Knowles, 1989). The sample plots totaled 31.2 km². Four hundred sixty-eight live tortoises were found, of which 202 (43%) showed signs of URTD. From 9.4% to 66.7% of tortoises on 12 of the 13 sample plots showed signs of URTD.
The DTNA experienced a catastrophic epidemic that is not yet over. In 1992 from 12 to 14 adult tortoises in the research program for epidemiology of URTD were tested for antibodies to M. agassizii (Brown et al., 1994b) using the ELISA test (Schumacher et al., 1993). The tortoises were tested during late winter, spring, summer, and fall and were in a study area immediately adjacent to the long-term plot. From 25 to 38 percent of the tortoises in the four seasonal samples tested positive for M. agassizii, indicating that the tortoises had been exposed to the pathogen, or were currently ill, or had been ill and were recovered. Between 1993 and 1995, from 7 to 62% of the tortoises in the four samples taken each year have produced positive ELISA tests, indicating that the population is in a chronic disease state (M. B. Brown et al., pers. comm.)
Of the 27 tortoises in the health profile research program between May 1989 and March 1992, six died between late 1989 and mid-1991. An additional 11 tortoises disappeared and have not been found as of October 1995. The death rate for adults is abnormally high, compared to approximately 2% per year in stable populations (Turner et al., 1987). The disappearance rate is also high and unusual for tortoises fitted with radio transmitters. Many of the missing animals should be considered dead.
Desert tortoise density at Chuckwalla Bench
Figure 3. Estimates of population densities of desert tortoises at the Chuckwalla Bench Area of Critical Environmental Concern in Riverside County, California in 1979, 1982, 1988, and 1992. Density estimates are presented for all sizes of tortoises and for the adult tortoises (greater than or equal to 180 mm carapace length at midline). The histogram shows the midpoint of the density estimates, and the brackets enclose the 95% Confidence Intervals for the population estimates.
Chuckwalla Bench ACEC
Between 1979 and 1992 both the total population and the adult component of the tortoise population exhibited statistically significant declines (Figure 3). The total population density, which included all sizes of tortoises, steadily decreased from a high of 223 tortoises/km² (95% CI = 177–283) in 1979 to a low of 64 tortoises/km² (95% CI = 46–92) in 1988 (Berry, 1990). The 1992 census figures were slightly higher but not significantly different from the figures recorded for 1988: 70 tortoises/km² (95% CI = 48–102). The pattern of decline of adults was similar. There were no statistically significant differences in the adult population component in the 1979 and 1982 censuses; in 1979 density estimates were 75 tortoises/km² (95% CI = 56–98), whereas in 1982 estimates were 87 tortoises/km² (95% CI = 68–112). By 1988 census figures showed statistically significant declines with 42 tortoises/km² (95% CI = 29–62). The 1992 estimates were lower still, 33 adults/km² (95% CI = 22–49), but not significantly different from the 1988 figures.
During the 13-year time frame, the total number of tortoises registered per survey year on the study site also declined, from 265 individuals in 1979 and 262 in 1982 (Berry, 1990) to 107 individuals in 1992 (Berry, unpubl. data). Of considerable concern is the differential loss of adult females. In 1979, 74 adult females and 79 adult males were registered. The numbers of registered tortoises increased to 98 adult females and 80 adult males in 1982 and then declined to 42 adult females and 44 adult males in 1988. By 1992 female numbers had further declined to 26 individuals, while male numbers remained similar at 42. As of mid-1992 (the end of the 1992 field survey season), deaths of adults continued to occur at a rate higher than the 2% annualized death rate estimated for stable populations in the Mojave Desert (Turner et al., 1987). The remains of 20 adults, all of which had been captured in previous years, were found during the 1992 survey. Of the 20, eight had died within the last year and ten had died within the last one to two years. Of the 20 adults, 15 were females.
The population decline appears to be linked to the appearance of shell lesions on the tortoises. In a retrospective analysis of the 35 mm slides taken during surveys conducted between 1979 and 1990, the disease was evident in 1979 but affected only 56% of the tortoises and was generally of limited extent (mild) on the shell (Jacobson et al., 1994). Between 1982 and 1988 the percentage of tortoises affected increased to 90%, and the severity of the lesions on the shells likewise increased. The lesions, which were on the scutes of the plastron and carapace and on the scales of the forelimbs, consisted of white-gray or sometimes orange flaky areas. They appeared at the seams, spreading outward in irregular patterns onto the scutes. In severe cases, bone was exposed. The lesions were described as cutaneous dyskeratosis, but the exact cause could not be determined. The locations on the shell and body and histology of the lesions were suggestive of either a deficiency disease or toxicosis. Both deficiency diseases and environmental toxicants are known to affect keratin in other vertebrates. A wide variety of toxicants are responsible for lesions in the epidermal hard parts of domestic hoofstock, for example (Blood et al., 1989).
Subsequent to the study of the shell and limb lesions in tortoises at the Chuckwalla Bench, 32 ill or damaged tortoises (including some with similar shell lesions) were salvaged for necropsy from the Mojave and Colorado deserts of California and the Sonoran Desert of Arizona (Homer et al., 1994, 1996a, 1996b). The salvaged tortoises with cutaneous dyskeratosis had elevated concentrations of toxicants in the liver, kidney, or plasma (e.g., barium, calcium, cadmium, chromium, magnesium, molybdenum, nickel, phthalates, and selenium in plasma), and/or nutritional deficiencies (e.g., low copper, zinc, selenium, plasma vitamin A). The toxicants and/or nutritional deficiencies may be the cause of the shell disease. Tortoises with cutaneous dyskeratosis may be more vulnerable to bacterial and fungal infections, other diseases, and predation because of the thin scutes and loss of laminae.

DISCUSSION

        Desert tortoises are slow-maturing animals that require 15–20 years to reach reproductive maturity (Woodbury and Hardy, 1948). Once reproductive maturity is reached, wild females generally produce relatively small and few clutches of eggs (Turner et al., 1986, 1987; Henen, 1994). During a six-year study of egg production in the eastern Mojave Desert, females produced from 0 to 3 clutches per year. Mean clutch sizes ranged from 3.53 ±0.26 to 5.15 ±0.34 eggs and clutch frequency from 1.06 ±0.06 to 1.89 ±0.11 per year. Eggs and hatchlings are vulnerable to many predators and pre-adult mortality is generally high (Turner et al., 1987). However, under normal conditions, adult survivorship is about 98% per year. Populations cannot rapidly recover from catastrophic losses of adults, such as the 90% decline experienced at the DTNA or the 50–60% losses at the Chuckwalla Bench because recruitment of young adults requires so many years. These populations face serious threat of extinction (USFWS, 1994). According to analyses prepared by the Desert Tortoise Recovery Team, desert tortoise populations that have declined to 4 adults/km² would require three doublings, or 210 years, to reach a density of 31 adults/km²—if the population is able to grow at an average rate of 1% per year (USFWS, 1994). Using these projections, the adult population at the DTNA would require 280 years to reach the 1979 level of 61 adults/km². One of the more serious aspects of the population declines for the DTNA and the Chuckwalla Bench is that the declines may not have reached the lowest point and recovery may not be underway. Furthermore, the long-term effects of the two diseases on reproduction, viability of eggs, and general health of young are not yet known.
One of the diseases, URTD, is highly infectious (Brown et al., 1994a) and has demonstrated its potential for producing catastrophic impacts on populations at the DTNA. Captive tortoises are implicated in the spread of this disease to wild populations of both desert and gopher tortoises, G. polyphemus (Jacobson, 1993a; Jacobson et al., 1995). In the last five years the number of desert tortoise populations with clinical signs of URTD has increased and the disease appears to be spreading. Wild tortoises that have positive ELISA tests and show clinical signs of disease have been identified throughout the Mojave Desert in California (Brown et al., 1994b; Homer et al., 1994), Nevada (Jacobson et al., 1995), northern Arizona (Dickinson et al., 1995), and Utah (Dickinson et al, 1995; Jacobson et al., 1991).
In California, government agencies have taken measures to prevent release of captive turtles and tortoises since the late 1970s (e.g., St. Amant, 1979, 1980). In 1993 more than 7,500 copies of a booklet with information about wild and captive desert tortoises, URTD, and adoption programs for captives (Berry, 1993) were distributed to people perceived to be authorities on management of wild and captive tortoises (government agencies, librarians, humane societies, police departments and county sheriffs, and veterinarians). The booklet focuses on why captive tortoises should not be released, what one should do when encountering desert tortoises in wild settings, and whom to contact when a tortoise is found in a city or town. A four-page brochure that addresses scientific and medical aspects of URTD, including treatment and guidelines for care and husbandry of tortoises, (Jacobson, 1993b) was also distributed with the booklet. These materials were prepared and distributed not only to educate the public but also to protect the considerable investment by both government and the Desert Tortoise Preserve Committee in existing reserves and legally designated Critical Habitat (USFWS, 1994) for the desert tortoise.
Will education reduce the threat of captive releases and better protect the tortoise? Education is likely to reduce but not entirely eliminate the threat. Data are available on behavior of the general public from the monitoring reports of naturalists at the DTNA (Howland, 1989; Ginn, 1990; Jennings, 1992; Ogg and Gallant, 1992; Kidd, 1993; Boland, 1994, 1995). Since spring 1989 the Desert Tortoise Preserve Committee and the USBLM have sponsored naturalists at the DTNA. Naturalists, who are generally present five to seven days per week for three months in spring at the Interpretive Center, a single site on the 57.5 km fenced boundary of the reserve, have reported that visitors arrive from throughout the state with the intention of releasing captives for various reasons. These reasons include the belief that the DTNA is the appropriate place to release tortoises or that public officials have told them to do so. Some of these captives showed signs of URTD. The naturalists also reported that visitors bring wild tortoises from nearby areas to the DTNA, believing it to be a place that is safe from the hazards of vehicles and other land uses. The 31 illegal incidents summarized in Table 1 occurred at a rate of 2.4 incidents/1000 visitors over a seven-year period. The documented incidents are a minimum number; they represent only incidents of which the naturalists were aware and only at a single point along the DTNA boundary. Certainly, such illegal activities occur more widely in the Southwest (USFWS, 1994).
The second disease, cutaneous dyskeratosis, is also widespread in desert tortoise populations (Berry, unpubl. data; Homer et al., 1994, 1996a, 1996b), with some populations more affected than others. Cutaneous dyskeratosis may have multiple causes and be associated with the presence of environmental toxicants and/or nutritional deficiencies. Field-workers and research scientists need to be taught to identify and describe the lesions. The sources of the environmental toxicants need to be identified, and the link of toxicants to cutaneous dyskeratosis and to the high mortality rates needs to be established. Ultimately, the cause(s) of the disease must be identified and actions taken to reduce the deaths in wild populations.

 

Recommendations

  1. Because our knowledge of infectious diseases in tortoises is limited (Jacobson, 1993a), research scientists and government biologists should take precautions to prevent transmission of known and unidentified diseases from one tortoise to another in the laboratory and field. The field-worker should use a separate pair of disposable gloves for each tortoise; sterilize equipment (e.g., calipers, scales) after use with each animal; sterilize probes used to measure or view burrows after use at each burrow; and ensure that the tortoise does not touch or contaminate the field worker’s clothing, day pack, or other equipment. Equipment should be sterilized or properly disinfected between uses at different sites. If the field-worker is visiting more than one study site, consideration should be given to sterilizing clothing and shoes before traveling to the second site. Where an infectious disease is known to occur in a population, protocols must be established to prevent spread to unexposed populations (including cleaning field vehicles and camping equipment). Sites where infectious diseases are known to occur should be visited last on field trips.
  2. Field-workers should keep detailed records on the health of each wild tortoise in research programs, including 35 mm slides of both healthy and ill individuals.
  3. Ill, dying, and recently dead (but not autolyzed) wild tortoises should be salvaged for necropsies (especially if the tortoise is ill or is a victim of trauma from a vehicle or predator). Where possible, necropsies should be performed by a licensed veterinary pathologist, or a professional pathologist with expertise in reptile pathology. A complete necropsy can provide invaluable information on diseases of tortoises.
  4. Legally designated “Natural Areas” and reserves can appear as attractive, natural, and safe places for release of unwanted captive or illegally collected tortoises. Government employees, research scientists, and the general public must be educated about the hazards of releasing captive tortoises or translocating wild tortoises to a reserve. As a minimum precautionary measure, Natural Areas and reserves should be posted with signs to reduce the likelihood of release. Costs for patrols by recreation specialists and law enforcement personnel should be included in management plans.
  5. Persons with unwanted captive tortoises must have ready access to facilities (e.g., adoption centers) or groups that will accept and properly care for the unwanted animals. Such facilities and organizations serve as deterrents to illegal releases.

 

ACKNOWLEDGMENTS

        C. Knowles, P. Knowles, and P. Gould contributed to the fieldwork at the DTNA study site, and A. P. Woodman, J. Howland, and T. Shields made significant contributions at the Chuckwalla Bench study site. The following people provided constructive comments on the manuscript: B. Homer, M. Brown, V. Dickinson, E. R. Jacobson, and J. Oldemeyer. The USBLM at Riverside, California supported all long-term research efforts on desert tortoise study plots. Research on pathogenesis and epidemiology of URTD was supported by USBLM contracts to E. R. Jacobson at the University of Florida (Contract No. CA-950-CT9-28) and M. B. Brown (Contract No. B950-C2-0046), respectively. Research on cutaneous dyskeratosis was supported through USBLM contracts to E. R. Jacobson and T. J. Wronski (No. CA951-CT0-046) and to B. Homer and E. R. Jacobson (No. CA 950-C1-0062), as well as a National Biological Service Research Work Order to B. Homer and E. R. Jacobson.

 

LITERATURE CITED

Berry, K. H. 1984. A description and comparison of field methods used in studying and censusing desert tortoises. Appendix 2. In K. H. Berry (ed.), The Status of the Desert Tortoise (Gopherus agassizii) in the United States. Desert Tortoise Council report to U.S. Fish and Wildlife Service, Order No. 11310-0083-81, Sacramento, California.
Berry, K. H. 1990. The status of the desert tortoise (Gopherus agassizii) in California in 1989. Draft report to the U. S. Fish and Wildlife Service, Portland, Oregon.
Berry, K. H. 1993. Answering questions about desert tortoises: A guide for people who work with the public in California. Report No. BLM-CA-PT-93-003-6840, U.S. Bureau of Land Management and California Department of Parks and Recreation. 43 pp.
Berry, K. H. and L. L. Nicholson. 1984. A summary of human activities and their impacts on desert tortoise populations and habitat in California. Chapter 3. In K. H. Berry (ed.), The Status of the Desert Tortoise (Gopherus agassizii) in the United States. Desert Tortoise Council report to U.S. Fish and Wildlife Service, Order No. 11310-0083-81, Sacramento, California.
Berry, K. H., T. Shields, A. P. Woodman, T. Campbell, J. Roberson, K. Bohuski, and A. Karl. 1986. Changes in desert tortoise populations at the Desert Tortoise Research Natural Area between 1979 and 1985. Proc. Desert Tortoise Council Symp. 1986:100–123.
Blood, D. C., O. M. Radostits, J. H. Arundel, and C. C. Gay. 1989. Veterinary Medicine. A Textbook of the Diseases of Cattle, Sheep, Pigs, Goats, and Horses. 7th ed. Bailliere Tindall, London. 1502 pp.
Boland, C. 1994. Observations and activities of the naturalists at the Desert Tortoise Research Natural Area, Kern County, California: 1 March through 31 May 1994. Prepared for the Desert Tortoise Preserve Committee, Inc., in cooperation with the U.S. Bureau of Land Management, Riverside, California. 39 pp.
Boland, C. 1995. Observations and activities of the naturalists at the Desert Tortoise Research Natural Area, Kern County, California: 1 March through 31 May 1995. Prepared for the Desert Tortoise Preserve Committee, Inc., in cooperation with the U.S. Bureau of Land Management, Riverside, California. 45 pp.
Brown, M. B., I. M. Schumacher, P. A. Klein, K. Harris, T. Correll, and E. R. Jacobson. 1994a. Mycoplasma agassizii causes upper respiratory tract disease in the desert tortoise. Infection and Immunity 62(10):4580–4586.
Brown, M. B., P. A. Klein, I. M. Schumacher, and K. H. Berry. 1994b. Health profiles of free-ranging desert tortoises in California: Results of a two-year study of serological testing for antibody to Mycoplasma agassizii. Final Report. U. S. Bureau of Land Management, Contract. No. B950-C3-0046, Riverside, California. 54 pp.
Christopher, M. M., I. Wallis, K. A. Nagy, B. T. Henen, C. C. Peterson, B. Wilson, C. Meienberger, and I. Girard. 1993. Laboratory health profiles of free-ranging desert tortoises in California: Interpretation of physiologic and pathologic alterations (March 1992–October 1992). Report to the U.S. Dept. of the Interior, Bureau of Land Management, Contract No. B950-C1-0060, Riverside, California.
Christopher, M., K. A. Nagy, I. Wallis, and K. H. Berry. 1997. Laboratory health profiles of desert tortoises in the Mojave Desert: A model for health status evaluation of chelonian populations. In J. Van Abbema (ed.), Proceedings: Conservation, Restoration, and Management of Tortoises and Turtles—An International Conference, pp. 76-82. July 1993, State University of New York, Purchase. New York Turtle and Tortoise Society, New York.
Dickinson, V. M., T. Duck, C. R. Schwalbe, and J. L. Jarchow. 1995. Health status of free-ranging Mojave desert tortoises in Utah and Arizona. Arizona Game and Fish Department Tech. Rept. 21, Phoenix. 70 pp.
Fowler, M. E. 1977. Respiratory disease in desert tortoises. In Annual Proceedings of the American Association of Zoo Veterinarians, pp. 79–99.
Ginn, S. 1990. Observations and activities of the naturalist for the Desert Tortoise Natural Area, Kern County, California: March 18–June 2, 1990. Report. to the Desert Tortoise Preserve Committee, Ridgecrest, California and the U. S. Bureau of Land Management, Riverside, California. 37 pp.
Henen, B. T. 1994. Seasonal and annual energy and water budgets of female desert tortoises (Xerobates agassizii) at Goffs, California. Ph.D. dissertation, University of California, Los Angeles.
Homer, B. L., K. H. Berry, M. M. Christopher, M. B. Brown, and E. R. Jacobson. 1994. Necropsies of desert tortoises from the Mojave and Colorado deserts of California and the Sonoran Desert of Arizona. Final report to U.S. Dept. of the Interior, Bureau of Land Management, Contract No. B950-C1-0062, Riverside, California.
Homer, B. L., K. H. Berry, and E. R. Jacobson. 1996a. Necropsies of eighteen desert tortoises from the Mojave and Colorado deserts of California: 1994–1995. Final Report for U.S. Dept. of Interior, National Biological Service Work Order No. 131. 120 pp.
Homer, B. L., K. H. Berry, F. Ross, C. Reggiardo, and E. R. Jacobson. 1996b. Potentially toxic metals and minerals in liver and kidney of desert tortoises in California. In Abstracts from the Twenty-first Annual Meeting and Symposium of the Desert Tortoise Council, pp 19–20. Held 29 March–1 April 1996, Las Vegas, Nevada.
Howland, J. 1989. Observations and activities of the naturalist for the Desert Tortoise Natural Area, Kern County, California: March 12–July 12, 1989. Report from the Desert Tortoise Preserve Committee, Inc., Ridgecrest, California to U.S. Bureau of Land Management, Contract No. CA950-CT9-44, Riverside, California. 59 pp.
Jacobson, E. R. 1993a. Implications of infectious diseases for captive propagation and introduction programs of threatened/endangered reptiles. J. Zoo Wildl. Med. 24(3):245–255.
Jacobson, E. R. 1993b. The desert tortoise and upper respiratory tract disease. Prepared for the Desert Tortoise Preserve Committee, Inc., and U.S. Bureau of Land Management, Report No. BLM-CA-PT-93-004-6840, Riverside, California. 4 pp.
Jacobson, E. R. 1994. Causes of mortality and disease in tortoises: A review. J. Zoo Wildl. Med. 25(1):2–17.
Jacobson, E. R., J. M. Gaskin, M. B. Brown, R. K. Harris, C. H. Gardiner, J. L. LaPointe, H. P. Adams, and C. Reggiardo. 1991. Chronic upper respiratory tract disease of free-ranging desert tortoises (Xerobates agassizii). J. Wildl. Dis. 27(2):296–316.
Jacobson, E. R., T. J. Wronski, J. Schumacher, C. Reggiardo, and K. H. Berry. 1994. Cutaneous dyskeratosis in free-ranging desert tortoises, Gopherus agassizii, in the Colorado Desert of Southern California. J. Zoo Wildl. Med. 25(1):68–81.
Jacobson, E. R., M. B. Brown, I. M. Schumacher, B. R. Collins, R. K. Harris, and P. A. Klein. 1995. Mycoplasmosis and the desert tortoise (Gopherus agassizii) in Las Vegas Valley, Nevada. Chelon. Conserv. Biol. 1(4):279–284.
Jennings, W. B. 1992. Observations and activities of the naturalists for the Desert Tortoise Natural Area, Kern County, California: March 2–May 27, 1991. Report to the Desert Tortoise Preserve Committee, Inc., Ridgecrest, California, in cooperation with the U.S. Bureau of Land Management, Grant No. B950-A1-0034, Riverside, California. 40 pp.
Kidd, J. 1993. Observations and activities of the naturalists at the Desert Tortoise Research Natural Area, Kern County, California: 1 March through 31 May 1993. Prepared for the Desert Tortoise Preserve Committee, Inc., San Bernardino, California, in cooperation with the U.S. Bureau of Land Management, Riverside, California.
Knowles, C. 1989. A survey for diseased desert tortoises in and near the Desert Tortoise Natural Area. Spring 1989. Report for the U.S. Bureau of Land Management, Contract No. CA950-CT9-23, Riverside, California. 26 pp.
Ogg, S. and R. Gallant. 1992. Observations and activities of the naturalists for the Desert Tortoise Natural Area, Kern County, California: 3 March–31 May, 1992. Report to the Desert Tortoise Preserve Committee, Inc., San Bernardino County, California, in cooperation with the U.S. Bureau of Land Management, Grant No. B950-A1-0034, Riverside, California. 53 pp.
Overton, W. C. 1971. Estimating the numbers of animals in wildlife populations. In R. G. Giles (ed.), Wildlife Management Techniques, pp. 403–456. The Wildlife Society, Washington, D.C.
Schumacher, I. M., M. B. Brown, E. R. Jacobson, B. R. Collins, and P. A. Klein. 1993. Detection of antibodies to a pathogenic mycoplasma in desert tortoises (Gopherus agassizii) with upper respiratory tract disease. J. Clin. Microbiol. 31:1454–1460.
Snipes, K. P. and E. L. Biberstein. 1982. Pasteurella testudinis sp. nov.: A parasite of desert tortoises (Gopherus agassizi). International Journal of Systematic Bacteriology 32(2):201–210.
St. Amant, J. 1977. State Report—California. In M. Trotter (ed.), Proc. 1977 Symposium of the Desert Tortoise Council, pp. 21–22. Desert Tortoise Council, San Diego, California.
St. Amant, J. 1979. State Report—California. In E. St. Amant (ed.), Proc. 1979 Symposium of the Desert Tortoise Council, pp. 75–77. Desert Tortoise Council, Long Beach, California.
St. Amant, J. 1980. State Report—California. In K. A. Hashagen (ed.), Proc. 1980 Symposium of the Desert Tortoise Council, pp. 68–69. Desert Tortoise Council, Long Beach, California.
Swingland, I. R. and M. W. Klemens (eds.). 1989. The Conservation Biology of Tortoises. Occasional Papers of the IUCN Species Survival Commission (SSC) No. 5. IUCN, Gland, Switzerland. iv + 202 pp.
Turner, F. B., K. H. Berry, D. C. Randall, and G. C. White. 1987. Population ecology of the desert tortoise at Goffs, California, 1983–1986. Report to Southern California Edison Co., Rosemead, California. 101 pp.
Turner, F. B., P. Hayden, B. L. Burge, and J. B. Roberson. 1986. Egg production by the desert tortoise (Gopherus agassizii) in California. Herpetologica 42:93–104.
U.S. Bureau of Land Management. 1980. The California Desert Conservation Area Plan. U.S. Dept. of the Interior, Bureau of Land Management, Desert District, Riverside, California. 173 pp.
U.S. Bureau of Land Management. 1986. Chuckwalla Bench Area of Critical Environmental Concern: Management Plan and Environmental Assessment. U.S. Dept. of the Interior, Bureau of Land Management, California Desert District, Indio Resource Area, California. 40 pp. + appendices.
U.S. Bureau of Land Management and California Dept. of Fish and Game. 1988. A Sikes Act management plan for the Desert Tortoise Research Natural Area and Area of Critical Environmental Concern. U. S. Dept. of the Interior, Bureau of Land Management, California Desert District, Ridgecrest Resource Area, California. 43 pp. + unpaginated appendices.
U.S. Fish and Wildlife Service. 1994. Desert Tortoise (Mojave Population) Recovery Plan. U.S. Dept. of the Interior, Fish and Wildlife Service, Portland, Oregon. 73 pp. + appendices.
Woodbury, A. M. and R. Hardy. 1948. Studies of the desert tortoise, Gopherus agassizi. Ecol. Monogr. 81:146–200.

 

TABLE 1Number of attempts to release captive and illegally translocated desert tortoises at or adjacent to the Desert Tortoise Research Natural Area, eastern Kern County, California, between 1989 and 1995.
Number of incidents regarding tortoises: Number of illegal incidents
Year Captive releases Translocations per 1000 visitors Reference

1989 5 0 2 Howland, 1989
1990 1 4 5 Ginn, 1990
1991 2 2 2 Jennings, 1992
1992 3 4 4 Ogg and Gallant, 1992
1993 0 3 1 Kidd, 1993
1994 2 2 2 Boland, 1994
1995 1 2 1 Boland, 1995
Totals 14 17

This article was reprinted with permission from the New York Turtle and Tortoise Society

Leave a Reply