Monitoring Rarity: The Critically Endangered Saharan Cheetah as a Flagship Species for a Threatened Ecosystem

Deserts are particularly vulnerable to human impacts and have already suffered a substantial loss of biodiversity. In harsh and variable desert environments, large herbivores typically occur at low densities, and their large carnivore predators occur at even lower densities. The continued survival of large carnivores is key to healthy functioning desert ecosystems, and the ability to gather reliable information on these rare low density species, including presence, abundance and density, is critical to their monitoring and management. Here we test camera trap methodologies as a monitoring tool for an extremely rare wide-ranging large felid, the critically endangered Saharan cheetah (Acinonyx jubatus hecki). Two camera trapping surveys were carried out over 2–3 months across a 2,551km² grid in the Ti-n-hağğen region in the Ahaggar Cultural Park, south central Algeria. A total of 32 records of Saharan cheetah were obtained. We show the behaviour and ecology of the Saharan cheetah is severely constrained by the harsh desert environment, leading them to be more nocturnal, be more wide-ranging, and occur at lower densities relative to cheetah in savannah environments. Density estimates ranged from 0.21–0.55/1,000km², some of the lowest large carnivore densities ever recorded in Africa, and average home range size over 2–3 months was estimated at 1,583km². We use our results to predict that, in order to detect presence of cheetah with p>0.95 a survey effort of at least 1,000 camera trap days is required. Our study identifies the Ahaggar Cultural Park as a key area for the conservation of the Saharan cheetah. The Saharan cheetah meets the requirements for a charismatic flagship species that can be used to “market” the Saharan landscape at a sufficiently large scale to help reverse the historical neglect of threatened Saharan ecosystems.     

Phylogeography, genetic structure and population divergence time of cheetahs in Africa and Asia: evidence for long-term geographic isolates

The cheetah (Acinonyx jubatus) has been described as a species with low levels of genetic variation. This has been suggested to be the consequence of a demographic bottleneck 10 000–12 000 years ago (ya) and also led to the assumption that only small genetic differences exist between the described subspecies. However, analysing mitochondrial DNA and microsatellites in cheetah samples from most of the historic range of the species we found relatively deep phylogeographic breaks between some of the investigated populations, and most of the methods assessed divergence time estimates predating the postulated bottleneck. Mitochondrial DNA monophyly and overall levels of genetic differentiation support the distinctiveness of Northern‐East African cheetahs (Acinonyx jubatus soemmeringii). Moreover, combining archaeozoological and contemporary samples, we show that Asiatic cheetahs (Acinonyx jubatus venaticus) are unambiguously separated from African subspecies. Divergence time estimates from mitochondrial and nuclear data place the split between Asiatic and Southern African cheetahs (Acinonyx jubatus jubatus) at 32 000–67 000 ya using an average mammalian microsatellite mutation rate and at 4700–44 000 ya employing human microsatellite mutation rates. Cheetahs are vulnerable to extinction globally and critically endangered in their Asiatic range, where the last 70–110 individuals survive only in Iran. We demonstrate that these extant Iranian cheetahs are an autochthonous monophyletic population and the last representatives of the Asiatic subspecies A. j. venaticus. We advocate that conservation strategies should consider the uncovered independent evolutionary histories of Asiatic and African cheetahs, as well as among some African subspecies. This would facilitate the dual conservation priorities of maintaining locally adapted ecotypes and genetic diversity.     

Social and genetic population structure of free-ranging cheetah in Botswana: implications for conservation

Once widely distributed throughout Africa, cheetahs (Acinonyx jubatus) occur today within fragmented populations and are listed as vulnerable by the IUCN. Botswana currently hosts the second largest cheetah population throughout the species’ range. This study initiated a molecular genetic survey of wild Botswana cheetah populations. It focused on the relatedness within presumed social groups using 14 microsatellite markers and revealed a higher proportion of unrelated male coalitions than was expected. Based on the unrelated cheetahs only, the estimation of the genetic variation corresponded with results from recent studies on different African populations. The analysis of unrelated individuals indicated limited genetic differentiation between cheetahs from different regions of Botswana. This suggests that the Botswana cheetah population might represent a unique panmictic population as long as sufficient levels of gene flow are maintained within the distribution range. This baseline information will now be incorporated to develop management strategies and set priorities for cheetah conservation in Botswana.     

The critically endangered Asiatic cheetah <Emphasis Type="Italic">Acinonyx jubatus venaticus</Emphasis> in Iran: a review of recent distribution,and conservation status

Considerable effort has been put into conservation of the critically endangered Asiatic cheetah Acinonyx jubatus venaticus in Iran during the past few decades, and a thorough review of the species’ status, demography, range and conservation is provided here. We collated a large dataset of all verified occurrence data, photographic records and mortality cases since 1980 throughout the species’ range in Iran. Currently, the cheetah is distributed throughout the arid landscapes of the eastern half of Iran, but the limits of its current and past range as well as population trends are uncertain. Surveys of nearly 40 different areas resulted in 18 localities with confirmed presence of cheetahs in recent years. Camera trapping has been an effective tool to provide evidence of presence and status of cheetahs, revealing the species’ extremely low density and long inter-reserve movements. Together with photographic records, a total of 82 different cheetahs were detected during the 2000s in Iran. Protection status in most areas has been elevated by the Iran government. Asiatic cheetahs are highly vulnerable to extinction, mainly due to causalities mediated by herder persecution, poaching and road collisions as well as prey and habitat loss. Some efforts have been made to address these threats, but range expansion in recent years is a result of greater survey effort, rather than population recovery. We suggest that, despite conservation investment of the last 15 years, the species remains critically endangered on the verge of extinction.     

Camera trapping mammals in the scrubland’s of the Cape Floristic Kingdom—the importance of effort,spacing and trap placement

As a non-invasive monitoring method camera traps are noted as being an effective, accurate and rapid means of compiling species richness estimates of medium to large terrestrial mammals. However, crucial elements of camera trap survey design are rarely empirically addressed, which has raised the need for both a standardised and optimised camera trapping protocol. Our study confirms that an appropriate camera placement buffer and targeting areas of animal activity, contributes to more complete species richness estimates as well as significantly reducing the rate of false trigger events. However, attaining the required survey effort in terms of camera days was the most important factor in providing accurate species richness estimates. Our results suggest that reliable estimates of species richness can be achieved in open scrubland when cameras are spaced 1 × 1 km apart and left in the targeted area until a survey effort of a 1000 camera days is realised.     

Regional variation in the cheetah (Acinonyx jubatus) revisited: Morphology of wild and captive populations

The cheetah (Acinonyx jubatus) is listed as a vulnerable species by the International union for the conservation of nature (IUCN), including two critically endangered subspecies, the Saharan cheetah, and the Iranian cheetah, so it is imperative that we understand variation in cheetah morphology to make good decisions regarding the conservation of this species. Here, we aim to determine whether northeastern African cheetahs have smaller body sizes than southern African cheetahs. This study also adds to our knowledge of cheetah morphology from two cheetah populations that do not yet have comprehensive published data: Kenya, and northeastern Africa, including captive individuals. We calculated means and standard deviations on cranial and body measurements of live or in few cases, freshly dead, cheetahs from the aforementioned populations, plus previously published data on Namibian and Botswanan cheetahs and compared them to one another using multivariate analysis of variance. Results show that northeastern African cheetahs have smaller body sizes than southern and eastern African populations. We also found that captive cheetahs retain the morphological characteristics of their ancestral population- captive cheetahs from southern Africa have similar body sizes to wild southern African cheetahs and larger body sizes than captives from northeastern Africa. Other analyses regarding cheetah growth agree with previous studies on Namibian and Botswanan cheetah populations rates. As such, this study can serve as a baseline for the care of captive cheetah populations to maintain healthy weights and body proportions.     

Focal palatine erosion in captive and free-living cheetahs (Acinonyx jubatus) and other felid species

We examined 1,092 skulls of captive and free-living individuals, representing 33 felid species, to determine the prevalence of focal palatine erosion (FPE). FPE was detected in 3.2% of cats evaluated, including cheetah (Acinonyx jubatus) and 14 other felid species. The prevalence of FPE between cheetah (9.4%; n = 64) and non-cheetah species (2.8%; n = 1,028) (χ(2) test; P = 0.004) and between captive (5.7%; n = 246) and free-living (2.4%; n = 824) individuals (χ(2) test; P = 0.010) were significantly different, with prevalence between captive (19%; n = 21) and free-living (2.9%; n = 34) cheetahs approaching significance (Fisher's exact test; P = 0.064). FPE was diagnosed with equal prevalence in skulls from individuals in which the lower molars did not meet the palatine bone (60.6%) and individuals in which it did (39.4%; n = 33) (χ(2) test; P = 0.139). In cheetahs with FPE, one was a captive animal in Germany, one a free-living cheetah from Mali, one captive cheetah from Kenya, and three captive cheetahs of unknown origin. Additionally, we evaluated the medical records of 49 captive cheetahs in Namibia. Of these cheetahs, 48 (98.0%) had clinical signs consistent with FPE, although only 16 of these 48 (39.6%) had perforation of the palatine bone. Based on physical examinations, FPE was diagnosed in two caracals (Caracal caracal) and one fishing cat (Prionailurus viverrinus) from a North American Zoo. Results from this study confirm FPE in cheetahs outside of Namibia, in a minimum of 15 felid species, and a higher FPE prevalence in captive individuals than free-living ones. Clinical implications of these findings and recommendations for future studies are provided.     

Trends in cheetah Acinonyx jubatus density in north-central Namibia

Assessing trends in abundance and density of species of conservation concern is vital to inform conservation and management strategies. The remaining population of the cheetah (Acinonyx jubatus) largely exists outside of protected areas, where they are often in conflict with humans. Despite this, the population status and dynamics of cheetah outside of protected areas have received relatively limited attention across its range. We analyzed remote camera trapping data of nine surveys conducted from 2005 to 2014 in the Waterberg Conservancy, north-central Namibia, which included detections of 74 individuals (52 adult males, 7 adult females and 15 dependents). Using spatial capture–recapture methods, we assessed annual and seasonal trends in cheetah density. We found evidence of a stable trend in cheetah density over the study period, with an average density of 1.94/100 km² (95% confidence interval 1.33–2.84). This apparent stability of cheetah density is likely the result of stable and abundant prey availability, a high tolerance to carnivores by farmers and low turnover rates in home range tenure. This study highlights the importance of promoting long-term surveys that capture a broad range of environmental variation that may influence species density and the importance of nonprotected areas for cheetah conservation.     

Molecular genetic insights on cheetah (Acinonyx jubatus) ecology and conservation in Namibia

The extent and geographic patterns of molecular genetic diversity of the largest remaining free-ranging cheetah population were described in a survey of 313 individuals from throughout Namibia. Levels of relatedness, including paternity/maternity (parentage), were assessed across all individuals using 19 polymorphic microsatellite loci, and unrelated cheetahs (n = 89) from 7 regions were genotyped at 38 loci to document broad geographical patterns. There was limited differentiation among regions, evidence that this is a generally panmictic population. Measures of genetic variation were similar among all regions and were comparable with Eastern African cheetah populations. Parentage analyses confirmed several observations based on field studies, including 21 of 23 previously hypothesized family groups, 40 probable parent/offspring pairs, and 8 sibling groups. These results also verified the successful integration and reproduction of several cheetahs following natural dispersal or translocation. Animals within social groups (family groups, male coalitions, or sibling groups) were generally related. Within the main study area, radio-collared female cheetahs were more closely interrelated than similarly compared males, a pattern consistent with greater male dispersal. The long-term maintenance of current patterns of genetic variation in Namibia depends on retaining habitat characteristics that promote natural dispersal and gene flow of cheetahs.     

Conservation of severely fragmented populations: lessons from the transformation of uncoordinated reintroductions of cheetahs (<Emphasis Type="Italic">Acinonyx jubatus</Emphasis>) into a managed metapopulation with self-sustained growth

We document and evaluate the use of metapopulation management to conserve a declining population of 217 cheetahs in 40 subpopulations. Metapopulation management resembles a natural metapopulation, but dispersal success, demographic rescue effects and genetic viability are enhanced by moving suitable individuals to selected habitat fragments. Unfortunately, history and results of metapopulation management are rarely published. Cheetahs, extirpated from 85% of South Africa, were reintroduced from Namibian and South African ranches into fenced reserves. During 1965–2009 343 cheetahs were reintroduced, yet reserves held only 289 in 2009. Then translocations of free-roaming cheetahs were halted, and numbers dropped to 217 on 40 reserves by 2012. A metapopulation project was launched, and key conservation problems indentified from interviews and records. Thirty-five percent of reserves had no breeding cheetahs, 13% were inbreeding, fence quality was erratic, 3% of cheetahs were sold into captivity annually, and 28% of cheetah mortalities were anthropogenic. Lions accounted for 31% of mortality, perhaps elevated by lion-inexperienced cheetahs and high lion densities. These problems were addressed, and cheetahs were translocated between reserves. Although the median reserve size was only 125 km² holding four cheetahs, and 80% of reserves were privately owned, in 6 years the metapopulation grew by 51% to 328 cheetahs on 51 reserves, while genetic diversity was managed and monitored. Thus, using metapopulation management, low density species and associated key processes, including carnivory or mega-herbivory, can be conserved in relatively small reserves in regions with dense human populations precluding  natural gene flow.     

Evaluating the Status of and African Wild Dogs Lycaon pictus and Cheetahs Acinonyx jubatus through Tourist-based Photographic Surveys in the Kruger National Park

The Kruger National Park is a stronghold for African wild dog Lycaon pictus and cheetah Acinonyx jubatus conservation in South Africa. Tourist photographic surveys have been used to evaluate the minimum number of wild dogs and cheetahs alive over the last two decades. Photographic-based capture-recapture techniques for open populations were used on data collected during a survey done in 2008/9. Models were run for the park as a whole and per region (northern, central, southern). A total of 412 (329–495; SE 41.95) cheetahs and 151 (144–157; SE 3.21) wild dogs occur in the Kruger National Park. Cheetah capture probabilities were affected by time (number of entries) and sex, whereas wild dog capture probabilities were affected by the region of the park. When plotting the number of new individuals identified against the number of entries received, the addition of new wild dogs to the survey reached an asymptote at 210 entries, but cheetahs did not reach an asymptote. The cheetah population of Kruger appears to be acceptable, while the wild dog population size and density are of concern. The effectiveness of tourist-based surveys for estimating population sizes through capture-recapture analyses is shown.     

Ecological niche of the Asiatic Cheetah (Acinonyx jubatus venaticus) in the arid environment of Iran (Mammalia: Felidae)

The Asiatic Cheetah, Acinonyx jubatus venaticus, is a species of global conservation concern and a small population occurs in Iran in fragmented habitats located in the central parts of the country with a continental, arid climate. Naybandan Wildlife Refuge (NWR) holds the largest population in Iran. To understand better the factors which determine the occurrence of cheetahs in these areas, we applied an Ecological Niche Factor Analysis (ENFA) to assess the relationship between occurrences of cheetahs across the NWR and topographic, biological, and anthropogenic factors. ENFA analysis results suggested that cheetahs have a tendency to inhabit areas different from the mean conditions of the study area and live in a narrow set of conditions. They prefer mountainous habitats far from flat areas, habitats near to water resources, and habitats with high prey densities. 13% of the NWR can be classified as suitable habitat for the cheetah, indicating a high conservation value of this reserve for the species.     

Spoor density as a measure of true density of a known population of free-ranging wild cheetah in Botswana

Knowledge of the abundance of animal populations is essential for their management and conservation. Determining reliable measures of abundance is, however, difficult, especially with wide-ranging species such as cheetah Acinonyx jubatus . This study generated a correction factor to calculate true cheetah density from spoor survey data and subsequently tested its accuracy using the following season's data. Data were collected from October 2005 to December 2006 on a known population of wild, free-ranging cheetah in the Jwana Game Reserve, Botswana. The cheetahs in the area were captured, tagged and photographed. The reserve was divided into twelve 9 km transects covering all vegetation types and prey densities. The total sampling distance was 8226 km, with a spoor density of 2.32 individual cheetah spoor per 100 km². To determine a precise and accurate spoor density, it was necessary to sample for a longer period during the dry season (April–September) than during the wet season (October–March). This difference may be due to cheetah behavioural changes with seasonal variations in habitat and prey. The true density was 5.23 cheetahs  per 100 km² ranging from 3.33 to 7.78 at the low and high points of the population, respectively. A positive linear correlation between spoor and true density was observed. This relationship differed in the wet and dry season and required refinement with the following season's data. Correction factors may be viable, but require further testing taking the behavioural responses to seasonal, habitat and prey variations into consideration.     

How Small is too Small? Camera Trap Survey Areas and Density Estimates for Ocelots in the Bolivian Chaco

Studies on carnivores, which are generally difficult to observe directly because they are elusive and nocturnal, are carried out through indirect methods, e.g. , camera trapping and radiotracking. The first method has been used to estimate population densities of species that can be differentiated as individuals using unique pelage patterns. However, the use of capture–recapture methodology has raised doubts regarding the estimation of the sampling area around the camera traps, which is obtained using maximum distances traveled by individuals photographed at two or more different locations. In this paper, the results from camera traps are compared with a radiotracking study carried out simultaneously with ocelots ( Leopardus pardalis ) to confirm whether maximum distances observed in camera traps coincide with ranging patterns determined from radio telemetry, and in turn whether the sampling areas estimated from camera traps are appropriate for estimating density. Mean maximum distance moved was 2880 m according to camera trap records during a 60-d survey period while, with radiotracking, the maximum distance moved was 3176 m during the same period. The difference is not significant, and the sampling areas estimated with camera traps to assess ocelot density are reliable. However, if the area covered by cameras is reduced to less than three to four times average home range for the target species, then density estimates from camera trapping are exaggerated because of the reduced observed distances and the fact that multiple individuals can overlap in relatively small areas.     

Can Camera Traps Monitor Komodo Dragons a Large Ectothermic Predator?

Camera trapping has greatly enhanced population monitoring of often cryptic and low abundance apex carnivores. Effectiveness of passive infrared camera trapping, and ultimately population monitoring, relies on temperature mediated differences between the animal and its ambient environment to ensure good camera detection. In ectothermic predators such as large varanid lizards, this criterion is presumed less certain. Here we evaluated the effectiveness of camera trapping to potentially monitor the population status of the Komodo dragon (Varanus komodoensis), an apex predator, using site occupancy approaches. We compared site-specific estimates of site occupancy and detection derived using camera traps and cage traps at 181 trapping locations established across six sites on four islands within Komodo National Park, Eastern Indonesia. Detection and site occupancy at each site were estimated using eight competing models that considered site-specific variation in occupancy (ψ)and varied detection probabilities (p) according to detection method, site and survey number using a single season site occupancy modelling approach. The most parsimonious model [ψ (site), p (site*survey); ω = 0.74] suggested that site occupancy estimates differed among sites. Detection probability varied as an interaction between site and survey number. Our results indicate that overall camera traps produced similar estimates of detection and site occupancy to cage traps, irrespective of being paired, or unpaired, with cage traps. Whilst one site showed some evidence detection was affected by trapping method detection was too low to produce an accurate occupancy estimate. Overall, as camera trapping is logistically more feasible it may provide, with further validation, an alternative method for evaluating long-term site occupancy patterns in Komodo dragons, and potentially other large reptiles, aiding conservation of this species.     

Toward reliable population density estimates of partially marked populations using spatially explicit mark–resight methods

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To Kill,Stay or Flee: The Effects of Lions and Landscape Factors on Habitat and Kill Site Selection of Cheetahs in South Africa

Understanding how animals utilize available space is important for their conservation, as it provides insight into the ecological needs of the species, including those related to habitat, prey and inter and intraspecific interactions. We used 28 months of radio telemetry data and information from 200 kill locations to assess habitat selection at the 3^rd order (selection of habitats within home ranges) and 4^th order (selection of kill sites within the habitats used) of a reintroduced population of cheetahs Acinonyx jubatus in Phinda Private Game Reserve, South Africa. Along with landscape characteristics, we investigated if lion Panthera leo presence affected habitat selection of cheetahs. Our results indicated that cheetah habitat selection was driven by a trade-off between resource acquisition and lion avoidance, and the balance of this trade-off varied with scale: more open habitats with high prey densities were positively selected within home ranges, whereas more closed habitats with low prey densities were positively selected for kill sites. We also showed that habitat selection, feeding ecology, and avoidance of lions differed depending on the sex and reproductive status of cheetahs. The results highlight the importance of scale when investigating a species’ habitat selection. We conclude that the adaptability of cheetahs, together with the habitat heterogeneity found within Phinda, explained their success in this small fenced reserve. The results provide information for the conservation and management of this threatened species, especially with regards to reintroduction efforts in South Africa.     

Challenges and opportunities in population monitoring of cheetahs

Population monitoring is key to wildlife conservation and management but is challenging at the spatial and temporal extents necessary for understanding changes. Noninvasive survey methods and spatial capture–recapture (SCR) models have revolutionized wildlife monitoring by providing the means to acquire data at large scales and the framework to generate spatially explicit predictions, respectively. Despite opportunities for improved monitoring, challenges can remain in the study design and model fitting phases of an SCR approach. Here, we used a search-encounter design with multi-session SCR models to collect spatially indexed photographs and estimate changes in density of cheetahs between 2005 and 2013–2016 in the Masai Mara National Reserve (MMNR) in Kenya. Our SCR models of cheetah encounters suggested little change in cheetah density from 2005 to 2013–2016, with some evidence that density fluctuated annually in the MMNR. The sampling period length (5 vs. 10 months) and timing (early, late, full year) over which spatial encounters were modeled did not alter inferences about density when sample sizes were adequate (>20 spatially distinct encounters). Our average density estimate of ~1.2 cheetahs/100 km² is consistent with the impression that the MMNR provides important cheetah habitat in Africa. During most years, spatial distribution of vegetation greenness (proxy for ungulate habitat quality) accounted for important variation in encounter rates. The search-encounter design here could be applied to other regions for cheetah monitoring. While snapshot estimates of population size across time are useful for wildlife monitoring, open population models may better identify the mechanisms behind temporal changes.     

cameratrapR: An R package for estimating animal density using camera trapping data

• 1.Camera trapping plays an important role in wildlife surveys, and provides valuable information for estimation of population density. While mark-recapture techniques can estimate population density for species that can be individually recognized or marked, there are no robust methods to estimate density of species that cannot be individually identified.
• 2.We developed a new approach to estimate population density based on the simulation of individual movement within the camera grid. Simulated animals followed a correlated random walk with the movement parameters of segment length, angular deflection, movement distance and home-range size derived from empirical movement paths. Movement was simulated under a series of population densities. We used the Random Forest algorithm to determine the population density with the highest likelihood of matching the camera trap data. We developed an R package, cameratrapR, to conduct simulations and estimate population density.
• 3.Compared with line transect surveys and the random encounter model, cameratrapR provides more reliable estimates of wildlife density with narrower confidence intervals. Functions are provided to visualize movement paths, derive movement parameters, and plot camera trapping results.
• 4.The package allows researchers to estimate population sizes/densities of animals that cannot be individually identified and cameras are deployed in a grid pattern.

     

Estimating Abundance of an Unmarked,Low-Density Species using Cameras

Estimating abundance of wildlife populations can be challenging and costly, especially for species that are difficult to detect and that live at low densities, such as cougars (Puma concolor). Remote, motion-sensitive cameras are a relatively efficient monitoring tool, but most abundance estimation techniques using remote cameras rely on some or all of the population being uniquely identifiable. Recently developed methods estimate abundance from encounter rates with remote cameras and do not require identifiable individuals. We used 2 methods, the time-to-event and space-to-event models, to estimate the density of 2 cougar populations in Idaho, USA, over 3 winters from 2016–2019. We concurrently estimated cougar density using the random encounter model (REM), an existing camera-based method for unmarked populations, and genetic spatial capture recapture (SCR), an established method for monitoring cougar populations. In surveys for which we successfully estimated density using the SCR model, the time-to-event estimates were more precise and showed comparable variation between survey years. The space-to-event estimates were less precise than the SCR estimates and were more variable between survey years. Compared to REM, time-to-event was more precise and consistent, and space-to-event was less precise and consistent. Low sample sizes made the space-to-event and SCR models inconsistent from survey to survey, and non-random camera placement may have biased both of the camera-based estimators high. We show that camera-based estimators can perform comparably to existing methods for estimating abundance in unmarked species that live at low densities. With the time- and space-to-event models, managers could use remote cameras to monitor populations of multiple species at broader spatial and temporal scales than existing methods allow. © 2020 The Wildlife Society.