Aspects of Cheetah (Acinonyx jubatus) Biology, Ecology and Conservation Strategies on Namibian Farmlands by Laurie L. Marker Thesis submitted for the degree of Doctor Of Philosophy Lady Margaret Hall, University of Oxford Trinity Term 2002 ASPECTS OF CHEETAH (ACINONYX JUBATUS) BIOLOGY, ECOLOGY AND CONSERVATION STRATEGIES ON NAMIBIAN FARMLANDS Summary In an increasingly human-dominated environment, the task of successfully conserving large carnivores, such as cheetahs, is difficult due to real or perceived threats resulting in conflict and often their local extirpation. This research describes the causes and potential solutions to this conflict in Namibia. Cheetah biology and ecology were studied through physical examination, laboratory analysis, radio-tracking and human perceptions using survey techniques. Between 1991 and 2000 data collected on over 400 live-captured and dead cheetahs showed that a perceived threat to livestock or game was the reason for 91.2% (n = 343) of cheetahs captured and 47.6% (n = 30) of wild cheetah deaths. Both were biased towards males, with 2.9 males being captured for every female, despite an apparent equality of sex ratio. Human-mediated mortality accounted for 79.4% (n = 50) of wild deaths reported, of which the majority involved prime adult animals, with a peak at around 5-6 years of age. Polymorphic microsatellite loci were used to assess 313 Namibian cheetahs’ variation, gene flow, paternity and behavioural ecology. Genetic analysis showed limited regional differentiation supporting a panmictic population and that persistence in Namibia depends on dispersal from regions throughout the country; therefore efforts of connectivity throughout the country should continue. Relatedness values confirmed family groups, and 45 new potential sire/dam offspring and 7 sibling groups were identified, providing information on dispersal and the success of translocation. Sera from wild cheetah were assessed for exposure to feline and canine virus antibodies to CDV, FCoV/FIP, FHV1, FPV, and FCV; antibodies were detected in 24%, 29%, 12%, 48%, and 65%, respectively, showing infection occurs in wild cheetahs; although there was no evidence of disease at time of capture, these diseases are known to cause serious clinical disease in captive cheetahs. Neither FIV antibodies nor FeLV antigens were present in any wild cheetahs tested, however, the first case of FeLV in a non-domestic felid is described in a captive Namibian cheetah. Concern for contact with domestic animals is discussed. Focal Palatine Erosion (FPE), a dental abnormality found in captive cheetahs, was discovered in over 70% of the wild cheetahs and was correlated with dental malocclusions, and is of concern to the long-term health of wild cheetahs. Namibian cheetahs have a mean 95% kernel home range of 1642.3 km2 (+ 1565.1 km2), the largest home ranges yet defined. Habitat type significantly affected the cheetah’s spatial distribution and prey density. Radio-collared female cheetahs were more closely related to other cheetahs in the study area than males, indicating male dispersal. Continual cheetah perturbation may partially explain the unusually low density of cheetahs in this area (estimated at only 2.5 cheetahs per 1000km2) despite the apparent abundance of prey. Namibian farmers originally surveyed revealed a mean removal of 19 cheetahs per year/farm, even when not considered a problem, and higher removals occurred on game farms. Evidence for actual livestock depredation was negligible, only 3% of reported captures. Scat analysis revealed cheetahs’ selection for indigenous game, however 5% of scats contained evidence of livestock. Research conducted on methods of conflict resolution showed that placing Anatolian Shepherd livestock guarding dogs proved to be effective, with 76% of farmers reporting a large decline in livestock losses since acquiring an Anatolian. Such solutions appear effective in increasing farmer’s tolerance for cheetahs, and by the end of the study period cheetah removals dropped to a mean of 2.1 cheetahs/farm/year. Implementing strategies such as these could be significant for reducing human-carnivore conflict in the many other places in which it occurs. ii To Khayam, who showed me the path and provided the vision Here with Loaf of Bread beneath the Bough, A Flask of Wine, a Book of Verse - and Thou Beside me singing in the Wilderness – And Wilderness is Paradise enow. In: Rubaiyuat of Omar Khayyam iii ACKNOWLEDGEMENTS Although only one name appears on the cover, this thesis would not exist without all those who have given so generously of their time and energy over the last several years. In particular, Amy Dickman, my research assistant, who worked diligently by my side for three years and who shares my interest in science, finding answers through analysis, and good red wine! Also thanks to Bruce Brewer for managing and building the Cheetah Conservation Fund’s (CCF) Research and Education Centre while I worked on this Thesis, and Richard Jeo for his invaluable guidance, and to my International Science Advisory Board members who gave me continued encouragement during this process and have mentored me along the way, in particular Linda Munson and Steve O’Brien. I am indebted to my major supervisors, David Macdonald and Gus Mills who taught me more than they will know just from this thesis. I am also very grateful to CCF team of staff and volunteers, in particular Bonnie Schumann, Don Muroura, Matti Nghkembua, and Susan Deshaies for their valuable input and continued moral support, and to Jack Imbert our radio-tracking pilot for all the safe hours of flying. In addition, I’m grateful to Warren Johnson, Christine Breitenmoser-Wursten, and Ruth Feber for their assistance and editorial comments, and my friends and colleagues at WildCRU who made Oxford stimulating. In addition, many thanks to my board of directors of CCF-USA, CCF- Namibia, and CCF-UK for their supporting my time, both financially and morally, while working on my Thesis, in particular Vance Martin, Cathryn and Carl Hilker, Bill and Pat Miller, and Charlie Knowles. This research was conducted with the generous support of the Namibian farmers who provided access to cheetahs and allowed their release back into the wild, and who spent hours answering questions about the Namibian farmlands. In particular, Dr. Arthur Bagot- Smith for first showing me the problems facing the Namibian cheetah, the Kruger’s for making me apart of their family, and the Waterberg Conservancy farm families for being great neighbours with a great conservation vision for the future. I am thankful to the Namibian Government, particularly the Ministry of Environment and Tourism, which supported this research. And, to His Excellency, Dr. Sam Nujoma, the President of Namibia and the International Patron for the Cheetah Conservation Fund, for his interest learning about the Namibian cheetah In addition, I’d like to acknowledge the various foundations, organisations and individuals that have supported the work encompassed in this Thesis, particularly major donors of the Cheetah Conservation Fund in the United States. Partial funding for this research was provided by the African Wildlife Foundation, the Angel Fund, the American Zoo Association Conservation Endowment Fund, the Bay Foundation, the Chase Foundation, Cheetah Conservation Fund Namibia and USA, Cincinnati Zoo, Columbus Zoo, Earthwatch Institute, the Mazda Wildlife Fund, Philadelphia Zoo, Total SA, the Weeden Foundation, the WILD Foundation, White Oak Conservation Center and the WWF SA Green Trust. On a more personal note, I would like to thank my parents Marline and Ralph Bushey for teaching me that the world is an open door and one is only constrained to venture into the world by one’s own fears. They told me I could do anything I put my mind to. L.M. - Sept 2002 iv Table of Contents CONTENTS ASPECTS OF CHEETAH (ACINONYX JUBATUS) BIOLOGY, ECOLOGY AND CONSERVATION STRATEGIES ON NAMIBIAN FARMLANDS Abstract………………………………………………………………………… ii Acknowledgements……………………………………………………………. iii Contents………………………………………………………………………... iv List of Tables…………………………………………………………………… vii List of Figures………………………………………………………………….. x Foreword………………………………………………………………………... xiv Chapter 1 General Introduction……………………………………………………. 1 Chapter 2 Study Area……………………………………………………………… 24 Chapter 3 Aspects of the Management of Cheetahs Trapped on Namibian Farmlands………………………………………………………………. 49 Chapter 4 Morphology, Physical Condition and Growth of Namibian Cheetahs…. 75 Chapter 5 Patterns of Molecular Genetic Variation in Namibian Cheetahs………. 92 Chapter 6 A Serosurvey of Antibodies to Viral Diseases in Wild Namibian Cheetahs………………………………………………………………... 118 Chapter 7 Lymphosarcoma Associated with Feline Leukaemia Virus Infection in a Captive Namibian Cheetah…………………………………………… 131 Chapter 8 The Incidence of Dental Abnormalities in Wild-Caught Namibian Cheetahs………………………………………………………………... 138 Chapter 9 Demography of the Namibian Cheetah………………………………… 153 Chapter 10 Notes on the Diet and Feeding Ecology of the Cheetah on Namibian Farmlands………………………………………………………………. 178 Chapter 11 Movements and Spatial Organisation of Cheetahs on North-Central Namibian Farmlands: The Influence of Prey Base, Competition and Perturbation…………………………………………………………….. 199 Chapter 12 Factors Influencing Perceptions and Tolerance towards Cheetahs on Namibian Farmlands…………………………………………………… 243 v Table of Contents CONTENTS (continued) Chapter 13 Evaluating the Effectiveness of Using Livestock Guarding Dogs as a Method of Conflict Resolution…………………………………………. 283 Chapter 14 General Discussion and Conservation Implications……………………. 328 Appendices Appendix I Current Status of the Cheetah…………………………………… 345 Appendix II 2000/2001 International Cheetah Studbook: Summary…………... 376 Appendix III Bush Encroachment and Ungulate Density on Commercial Farmlands in North-Central Namibia……………………………... 397 Appendix IV Morphometric Protocols Used while Measuring Cheetahs……… 418 Appendix V Morphometric Data for Cheetahs Published from Various Studies. 419 Appendix VI Sample Population of Cheetahs used for Genetic Analyses……… 420 Appendix VII Allele Frequencies for all Loci and Subpopulations……………… 424 Appendix VIII LOD Scores for Known Dams and Offspring, Showing Mismatchings and Probability of Non-Exclusion………………… 431 Appendix IX Questionnaires Used to Interview Farmers……………………….. 433 Appendix X Questionnaire Used to Evaluate Performance of Livestock Guarding Dogs……………………………………………………. 435 vi List of Figures List of Tables 2.1 Farm sizes in the survey area……………………………………. 30 2.2 Livestock numbers reported in the survey area………………….. 30 2.3 Numbers of wildlife reported in the survey area………………… 31 2.4 Game densities (animals/km2) and estimated biomass (kg/km2) by habitat type (sparse, medium, thick) using bush canopy……... 37 2.5 Population estimates for three major game species in Namibia…. 41 2.6 Utilisation of cheetah in Namibia 1980 – 1991………………….. 43 3.1 Description of the physical factors used to age cheetahs in this study……………………………………………………………... 53 3.2 Breakdown of capture events, necropsies and fates of examined cheetahs…………………………………………………………... 57 3.3 Number of social groups captured and reported each year………. 58 3.4 Demographic composition of cheetahs captured and examined…. 61 3.5 Demographic breakdown of cheetahs examined, separated by farm type…………………………………………………………. 62 3.6 Frequency of physical or behavioural problems observed in cheetahs captured and examined………………………………… 63 4.1 The numbers of male and female cheetahs examined, categorised by age group, during the study period…………………………… 80 4.2 Morphometric data for the wild adult cheetahs (aged over 30 m at capture, and held in captivity for <30 days), collected using the protocol shown in Appendix IV……………………………… 82 5.1 Heterozygosity and number of alleles by district………………... 104 5.2 Population pairwise F and R estimates using the combined st st data from the regions…………………………………………….. 108 5.3 Relatedness value used to identify possible sire/dam and sibling relationships within research population of cheetahs……………. 111 6.1 Prevalence of antibodies to selected feline and canine viruses in free-ranging Namibian cheetahs sampled between 1992-1998….. 125 8.1 Sample population of cheetahs examined for dental abnormalities……………………………………………………... 144 8.2 Focal palatine erosion scores assigned to captive and wild cheetahs examined of different ages…………………………….. 144 8.3 Overall frequency of missing premolars, crowded incisors and perforated FPE in the cheetahs examined………………………... 145 9.1 Annual demographic breakdown into social groups of the cheetahs captured and examined………………………………… 159 9.2 Information gathered from radio-collared dams regarding observed reproductive rates, interbirth intervals, litter sizes and cub mortality……………………………………………………... 166 9.3 Life table showing mortality rates for wild cheetahs throughout the study period………………………………………………….. 167 10.1 Results of feeding trials performed on captive Namibian cheetahs………………………………………………………….. 185 vii List of Figures 10.2 Summary of results from the feeding trials for each prey species presented………………………………………………………… 186 10.3 Ratios of prey animals consumed, using the corrected scat analysis, for 100 scats containing prey species………………….. 187 10.4 Contents of wild cheetah scats collected from various locations on the Namibian farmlands………………………………………. 188 10.5 Ratios of prey animals consumed, calculated using the corrected scat analysis……………………………………………………… 189 11.1 Mean age, time tracked, number of fixes, minimum distance moved between fixes, number of fixes to reach first asymptote, and statistical analyses for radio-tracked cheetahs………………. 213 11.2 Radio-collared cheetahs used in lifetime (95% kernel) home range analysis 1993 – 2000………………………………………. 214 11.3 Radio collared cheetahs used in annual (95% kernel) home range analysis 1993 – 2000…………………………………………….. 215 11.4a 95% kernel lifetime yearly home range for different social groups 1993 – 2000……………………………………………… 218 11.4b Mean home range (lifetime 95% kernel) and statistical analysis for social groups and sex by seasons - Seasons 1, 2 and 3 are compared to the dry and wet seasons……………………………. 218 11.5 Minimum density of cheetahs annually – includes all males in coalition group, and cumulative minimum density of cheetahs per 1000km2 using all cheetahs tagged and released in study area 225 11.6 Mean habitat preference by social group and sex………………... 228 11.7 Game densities (animals/km2) and estimated biomass (kg/km2) by habitat type (sparse, medium, thick) using bush canopy……... 229 11.8 Density of cheetahs in this study compared to other studies…….……………………………………………………… 230 11.9 Data on individual leopards and caracals radio-tracked during this study…………………………………………………………. 232 11.10 Mean lifetime home range estimations (95% MCP and 95% kernel for male and female leopards and male caracals. Statistical differences in lifetime home range estimations are shown between 95% MCP and 95% kernel home ranges as well as between sexes and between the wet and dry seasons…………. 233 12.1 Method of calculating the Perception and Tolerance indices……. 251 12.2a Attitudes and removals reported during the baseline 1991-1993 survey…………………………………………………………….. 252 12.2b Attitudes and removals reported during the 1993-1999 survey….. 253 12.2c Statistical analyses of the attitudes and removals between the 1991-1993 and 1993-1999 surveys………………………………. 254 12.3 Comments made by Namibian farmers during the interviews…... 254 12.4a Farmland characteristics reported during the 1991-1993 survey... 256 12.4b Farmland characteristics reported during the 1993-1999 survey... 259 12.4c Statistical analyses of the farmland characteristics between the 1991-1993 and 1993-1999 surveys………………………………. 260 viii List of Figures 12.5a 1991-1993 survey stocking rates and livestock management techniques: relationships with cheetah problems and removals…. 264 12.5b Statistical analyses of the stocking rates and livestock management techniques………………………………………….. 265 12.6a Livestock losses reported during the 1991-1993 survey………… 268 12.6b Livestock losses reported during the 1993-1999 survey………… 269 12.6c Statistical analyses of livestock losses between the 1991-1993 and 1993-1999 surveys…………………………………………... 270 13.1 The sample population of Namibian livestock guarding dogs that the 334 questionnaires were conducted on during the study, separated by farm type, age group and sex………………………. 291 13.2 Relationships between the attentiveness, trustworthiness, protectiveness, farmer satisfaction and care given for the livestock guarding dogs studied on Namibian farms…………….. 294 13.3 Mean scores for attentiveness, trustworthiness, protectiveness, care given and farmer satisfaction, for livestock guarding dogs of different ages on commercial and communal farms……………... 299 13.4 Mean scores for attentiveness, trustworthiness, protectiveness, care given and farmer satisfaction for male and female livestock guarding dogs on Namibian farms……………………………….. 300 13.5 Life table for livestock guarding dogs placed on Namibian farms, using one-yearly intervals………………………………………... 312 A1.1 History of the captive cheetah population……………………….. 353 A1.2 History of the South African captive cheetah population………... 354 A2.1 2000 - 2001 regional groupings of captive cheetahs…………….. 379 A2.2 2000 births by facility……………………………………………. 383 A2.3 2001 births by facility……………………………………………. 389 A2.4 Status of regional populations…………………………………… 396 A3.1 Description of vegetation class by canopy cover………………... 403 A3.2 Comparison of different strip width estimators for large and small ungulates observed in the study area………………………. 405 A3.3 Results from 2-way analysis of variance regarding the seasonal habitat preferences of ungulate species………………………….. 407 ix List of Figures List of Figures 1.1 Distribution of cheetahs throughout Africa and Asia in 1900, 1975, and present…………………………………………………………… 10 1.2 Density distribution of Namibian cheetah population……………….. 13 2.1 Land use map of Namibia, showing National Parks, commercial farms and communal lands…………………………………………... 25 2.2 Namibia rainfall distribution………………………………………… 26 2.3 Vegetation types of Namibia………………………………………… 28 2.4 Map of Namibia, with districts in the North Central Farmlands highlighted where studies for this thesis were conducted.…………… 29 2.5 The Waterberg Conservancy, an area within the north-central farmlands, is the centre of the radio-tracking study area…………….. 32 2.6a Annual rain in Waterberg Conservancy cheetah research study area (1957 – 2000)………………………………………………………... 34 2.6b Mean rainfall per month (averaged from 1957 - 2000) in Waterberg Conservancy research study area……………………………………. 34 2.7a-b Numbers of individuals of seven game species counted 1995-2000... 36 3.1 Design of a typical capture cage used to live-trap cheetahs on the Namibian farmlands…………………………………………………. 52 3.2 Number of days between reported date of capture and date of examination………………………………………………………….. 57 3.3 Reported month of capture for all cheetahs examined………………. 59 3.4 Reported reasons for capture of cheetahs examined………………… 60 3.5 Reported reasons for wild cheetahs entering captivity after examination………………………………………………………….. 64 3.6 Trends in reported captures due to perceived threats towards game and/or livestock……………………………………………………… 65 3.7 Reported causes of death for wild cheetahs…………………………. 66 4.1 Ratios of weight to length for adult cheetahs in excellent, fair and poor physical conditions……………………………………………... 84 4.2 Mean body mass of Namibian cheetahs examined in different age groups, separated by sex……………………………………………... 85 4.3 Growth curves for a) body mass and b) body length of wild Namibian cheetah cubs, separated by sex…………………………… 86 5.1 Map of regions where cheetahs originated…………………………... 99 5.2a-b Distribution of alleles (a) and allele frequencies (b) of selected microsatellites in the 7 regional populations………………………… 105 5.3 Phylogenetic depiction of relationships among 7 subpopulations in Namibia, constructed using proportion of shared alleles distances and the neighbour-joining algorithm………………………………… 105 5.4 Population cluster graph from principal component analysis, showing subpopulation structures……………………………………. 106 5.5 Allele distribution of representative microsatellite loci in the 7 regional groups and the Serengeti population………………………... 107 x