Social Structure of Spotted Hyena (Crocuta crocuta) Populations around Mekelle city in Tigray, Ethiopia

Elien
Schramme

OPGELET: HYENA’S IN DE STAD!

16 september 2014

Met bijna honderd waren ze. Grommend en huilend omringden ze de open jeep in het donker. Deze dieren waren duidelijk gewend aan elkaars nabijheid. Ongelooflijk dat zoiets in zulk een dichtbevolkte regio kon ontwikkelen.

Gevlekte hyena’s. Iedereen kent ze wel, de vraatzuchtige beesten met hun gebochelde rug en griezelige lach uit “De Leeuwenkoning”. Ze worden verafschuwd wegens hun reputatie als aaseter en hun vreemde verschijning. Maar wie ze ooit in het wild heeft bestudeerd, weet wel beter. Hyena’s zijn zeer sociale dieren. In tegenstelling tot wat de meeste mensen denken, eten ze niet alleen aas maar jagen ze regelmatig in teamverband hun eigen prooien. Ze leven in groepen of clans van vier tot 95 individuen, waarbinnen elk dier zijn eigen rang heeft in de hiërarchie. Vrouwtjes en hun jongen komen hier op de eerste plaats, zoals voor toegang tot voedsel. Mannetjes blijven niet in de clan waar ze geboren zijn, maar zoeken een nieuwe groep hyena’s op wanneer ze volwassen worden. Zo wordt inteelt op een natuurlijke wijze voorkomen.

Maar deze schijnbaar rigide structuur blijkt verrassend anders in Noord-Ethiopië. Rondom de stad Mekelle leeft een populatie gevlekte hyena’s die bijna volledig overgeschakeld is van hoofdzakelijk jagen op het eten van menselijk afval. De dieren verlaten ’s nachts hun schuilplaatsen om zich in de straten en op de vuilnisbelten tegoed te doen aan slachtresten.

Aangezien de hyena’s op deze manier niet meer van elkaar afhankelijk zijn voor het verkrijgen van voedsel, rees de vraag of dit een invloed zou hebben op de kenmerkende sociale structuur van deze grote roofdieren. Dit is waar ik me met mijn thesis op heb gefocust.

Hyenastront en weerbarstig DNA
In september 2014 vertrok ik naar Ethiopië voor veldwerk. Om de aantallen en structuur van de populatie in te schatten zonder de hyena’s daarbij te storen, baseerde ik me op hun uitwerpselen. Deze verzamelde ik zowel op plekken waar de dieren overdag schuilen als op de vuilnisbelten. Begeleid door zes gewapende mannen bezocht ik daarnaast ook een nationaal park 325 km ten westen van Mekelle. De gelijkaardige ligging maar de beperkte menselijke activiteit maakte deze stalen geschikt als referentie.

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Uitwerpselen bestaan niet alleen uit voedselresten, maar ook uit cellen van de darmwand van het dier. Terug in België trachtte ik uit deze cellen het DNA te isoleren en genetische informatie af te leiden. Dit was echter niet vanzelfsprekend. Uitwerpselen van vleeseters bevatten namelijk ook DNA van hun prooidieren. Bovendien is het DNA in uitwerpselen vaak beschadigd. In mijn zoektocht naar geschikte methodes bouwde ik echter interessante contacten op, zoals met onderzoekers van de KMDA (Koninklijke Maatschappij voor Dierkunde Antwerpen) en hyena-specialisten aan het IZW (Leibniz Institute for Zoo and Wildlife Research) in Berlijn. Deze laatste waren zo geïnteresseerd in mijn onderzoek dat ze me een samenwerking aanboden. In februari 2015 trok ik dus voor drie weken naar Duitsland om hun technieken te leren en mijn stalen te verwerken in hun labo.

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Mannetjes maken de massa
De resultaten waren verbazingwekkend. Ten eerste werd de populatiegrootte geschat op ruwweg 900 individuen, wat overeenkomt met een dichtheid van 1.84 hyena’s per km². Dit is beduidend hoger dan wat ooit geobserveerd werd elders in Afrika.

Bovendien bleek dat de groepering van de uitwerpselen op basis van hun vindplaatsen niet terug te vinden was in de genetische structuur. Dit kan erop wijzen dat al de individuen van Mekelle tot dezelfde clan behoren. Als dit zo zou zijn, zouden we hier te maken hebben met de grootste clan gevlekte hyena’s die ooit werd beschreven. Zelfs indien deze clan minder dan 900 dieren zou bevatten, is hij nog steeds vele malen groter dan de clan met de meeste individuen, 95, geobserveerd in Tanzania.

Toch was er ook een aanwijzing voor het bestaan van twee clans in de genetische structuur terug te vinden. Ook dit zou een boeiend resultaat zijn, aangezien de kans groot is dat leden van beide groepen elkaar ’s nachts tegenkomen in de stad en daar dezelfde voedselbron delen. Dit is niet het geval voor de meeste andere populaties gevlekte hyena’s, waar voedsel enkel gedeeld wordt met clanleden en territoria zelfs fel verdedigd worden.

Tenslotte gaf ook het delen van het aantal vrouwtjes door het aantal mannetjes een opmerkelijk resultaat. Deze totale “sex ratio” was 0.87, wat aangeeft dat er rond Mekelle meer mannelijke hyena’s leven dan vrouwtjes. Dit in tegenstelling tot elders in Afrika, waar de gemiddelde sex ratio veel hoger ligt. Het grote aantal dieren en mannetjes in het bijzonder zou een aanwijzing kunnen zijn dat in Mekelle de mannetjes niet langer een nieuwe clan opzoeken wanneer ze volwassen worden.

Mekelle: stad van mens en hyena
Met deze thesis heb ik aangetoond dat uitwerpselen succesvol gebruikt kunnen worden om de populatiestructuur van grote maar moeilijk te volgen dieren te bestuderen. Daarnaast geven al de bevindingen aan dat we hier te maken hebben met een uitzonderlijke populatie gevlekte hyena’s. De dieren tonen bijzondere aanpassingen in hun sociale structuur, wat hen toestaat dicht bij mensen te leven in een gebied waar haast geen wilde prooidieren meer te vinden zijn. Dit blijkt zelfs zo succesvol dat ze rond Mekelle in grotere aantallen kunnen voorkomen dan in “natuurlijke” omstandigheden. De vermoedelijke aanleiding is de overvloedige aanwezigheid van slachtafval.

Opmerkelijk is ook het feit dat er haast geen conflicten plaatsvinden met de inwoners van Mekelle. Jammer genoeg is het omgekeerde vaker waar in regio’s waar grotere steden zich ontwikkelen. Leeuwen, luipaarden, beren en wolven bijvoorbeeld, slagen er meestal niet in stand te houden. De wederzijdse tolerantie in Noord-Ethiopië is een fraai voorbeeld van hoe mensen en grote roofdieren kunnen samenleven zonder dat een van beide partijen een bedreiging vormt voor de andere.

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Bibliografie

REFERENCES

 

Aasen, E., & Medrano, J. F. (1990). Amplification of the ZFY and ZFX genes for sex identification in humans, cattle, sheep and goats. Biotechnology 8: 1279-1281.

 

Abay, G. Y., Bauer, H., Gebrihiwot, K. & Deckers, J. (2011). Peri-urban spotted hyena (Crocuta crocuta) in Northern Ethiopia: diet, economic impact, and abundance. European Journal of Wildlife Research 57: 759-765.

 

Aerts, R., Negussie, A., Maes, W., November, E., Hermy, M., & Muys, B. (2007). Restoration of dry Afromontane forest using pioneer shrubs as nurse plants for Olea europaea ssp. Euspidata. Restoration Ecology 15: 129-138.

 

Albert, R. (2002). Gene structure and gene flow in selected populations of spotted hyaena (Crocuta crocuta). (Unpublished thesis dissertation). Freie Universitaet Berlin, Berlin.

 

Albert, R., Hofer, H., East, M., & Pitra, C. (2000). Genetische Identifizierung der geographischen Herkunft vond Tüpfelhyänen. Der Zoologische Garten 70: 1-10.

 

Alemayehu, W. E. (2007). Ethiopian Church Forests: opportunities and challenges for restoration (Doctoral dissertation). Wageningen Univeristy, Wageningen, The Netherlands. ISBN: 978-90-8504-768-1

 

Boom, R., Sol, C. J. A., Salimans, M. M. M., Jansen, C. L., Wertheim-Van Dillen, P. M. E., & Van Der Noordaa, J. (1990). Rapid and Simple Method for Purification of Nucleic Acids. Journal of Clinical Microbiology 28: 495-503. BMC Research Notes 5: 257-265.

 

Bowcock, A. M., Ruiz-Linares, A., Tomfohrde, J., Minch, E., Kidd, J. R., & Cavalli-Sforza, L. L. (1994). High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368: 455-457.

 

Boydston, E. E., Kapheim, K. M., Van Horn, R. C., Smale, L., & Holekamp, K. E. (2005). Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyena (Crocuta crocuta). The Zoological Society of London 267: 271-281.

 

Boydston, E. E., Morelli, T. L., & Holekamp, K. E. (2001). Sex differences in territorial behavior exhibited by the spotted hyena (Hyaenidae, Crocuta crocuta). Ethology 107: 369-385.

 

Broquet, T. & Petit, E. (2004). Quantifying genotyping errors in noninvasive population genetics. Mol. Ecol. 13: 3601-3608.

 

Carbone, C., & Gittleman, J. L., (2002). A common rule for the scaling of carnivore density. Science 295: 2273-2276.

 

Castilho, C. S., Marins-Sa, L. G., Benedet, R. C. & Freitas, T. R. O. (2012). Genetic structure and conservation of Mountain Lions in the South-Brazilian Atlantic Rain Forest. Genetics and molecular Biology 35: 65-73.

 

Chaves, P. B., Paes, M. F., Mendes, S. L., Strier, K. B., Louro, I. D., & Fagundes, V. (2006). Noninvasive genetic sampling of endangered muriqui (Primates, Atelidae): Efficiency of fecal DNA extraction. Genetics and Molecular Biology 29: 750-754.

 

Conover, W. J., Johnson, M. E. & Johnson, M. M. (1981). A comparative study of tests for homogeneity of variances, with applications to the outer continental shelf bidding data. Technometrics 23: 351-361.

 

Cooper, S. M. (1989). Clan Sizes of Spotted Hyaenas in the Savuti Region of the Chobe National Park. Botswana Notes and Records 21: 121-133.

 

Cooper, S. M. (1990). The hunting behaviour of spotted hyaenas (Crocuta crocuta) in a region containing both sedentary and migratory populations of herbivores. African Journal of Ecology 28: 131-141.

 

Cooper, S.M., Holekamp, K.E., & Smale, L. (1999). A seasonal feast: long-term analysis of feeding behavior in the spotted hyaena, Crocuta crocuta (Erxleben). African Journal of Ecology 37: 149-160.

 

Cracraft, J., Feinstein, J., Vaughn, J., & Helm-Bychowski, K. (1998). Sorting out tigers (Panthera tigris): mitochondrial sequences, nuclear inserts, systematics, and conservation genetics. Animal Conservation 1: 139-150.

 

Crnokrak, P., Roff, D. A. (1999). Inbreeding depression in the wild. Heredity 83: 260-270.

 

Croes, B. M., Funston, P. J., Rasmussen, G., Buij, R., Saleh, A., Tumenta, P. N., & De Iongh, H. H. (2011). The impact of trophy hunting on lions (Panthera leo) and other large carnivores in the Bénoué Complex, northern Cameroon. Biological Conservation 144: 3064-3072.

 

Cunha, G. R., Wang, Y. Z., Place, N. J., Liu, W. H., Baskin, L., & Glickman, S.E. (2003). Urogenital system of the spotted hyena (Crocuta crocuta Erxleben): A functional histological study. Journal of Morphology 256: 205-218.

 

Czech, B., Krausman P. R., & Devers P. K. (2000). Economic associations among causes of species endangerment in the United States. Bioscience 50: 593-601.

 

den Tex, R.-J., Thorington, R., Maldonado, J. E., & Leonard, J. A. (2010). Speciation dynamics in the SE Asian tropics: Putting a time perspective on the phylogeny and biogeography of Sundaland tree squirrels, Sundasciurus. Molecular Phylogenetics and Evolution 55: 711-720.

 

Earl, Dent A. & vonHoldt, Bridgett M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359-361.

 

East, M. L., Burke, T., Wilhelm, K., Greig, C., & Hofer, H. (2003). Sexual conflicts in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure. Proceedings of the Royal Society of London B 270: 1247-1254.

 

East, M. L. & Hofer, H. (1991). Loud calling in a female-dominated mammalian society: II. Behavioural contexts and functions of whooping of spotted hyaenas, Crocuta crocuta. Animal Behaviour 41: 651-669.

 

East, M. L., & Hofer, H. (1997). The peniform clitoris of female spotted hyaenas. Trends in Ecology & Evolution 12: 40-402.

 

East, M. L. & Hofer, H. (2001). Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behavioural Ecology 12: 558-568.

 

East, M. L., Hofer, H., & Wickler, W. (1993). The erect ‘penis’ as a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behavioral Ecology and Sociobiology 33: 355-370.

 

East, M. L., Höner, o. P., Wachter, B., Wilhelm, K., Burke, T., & Hofer, H. (2009). Maternal effects on offspring social status in spotted hyenas. Behavioural Ecology 20: 478-483.

 

Eloff, F. C. (1964). On the predatory habits of lions and hyaenas. Koedoe : African Protected Area Conservation and Science 7: 105-112.

 

Engh, A. L., Esch, K., Smale, L., & Holekamp, K. E. (2000). Mechanisms of maternal rank ‘inheritance’ in the spotted hyaena, Crocuta crocuta. Animal Behaviour 60: 323-332.

 

Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620

 

Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.

 

Excoffier, L., & Slatkin, M. (1998). Incorporating genotypes of relatives into a test of linkage disequilibrium. The American Journal of Human Genetics 62: 171-180.

 

Falush, D., Stephens, M., & Pritchard, J. K. (2003). Inference of population structure: Extensions to linked loci and correlated allele frequencies. Genetics 164: 1567-1587.

 

Farell, E. M., & Alexandre, G. (2012). Bovine serum albumin further enhances the effects of organic solvents on increased yield of polymerase chain reaction of GC-rich templates.

 

Forester, D. J., & Machlis G. E. (1996). Modeling human factors that affect the loss of biodiversity. Conservation Biology 10: 1253-1263.

 

Frank, L. G. (1986a). Social organization of the spotted hyaena ( Crocuta crocuta). I. Demography. Animal Behaviour 34: 1500-1509.

 

Frank, L. G. (1986b). Social organization of the spotted hyaena ( Crocuta crocuta). II. Dominance and reproduction. Animal Behaviour 34: 1510-1527.

 

Frank, L. G. (1997). Evolution of genital masculinization: why do female hyaenas have such a large ‘penis’? Trends in Ecology & Evolution 12: 58-62.

 

Frank, L. G., Glickman, S. E., & Powch, I. (1990). Sexual dimorphism in the spotted hyaena (Crocuta crocuta). Journal of Zoology, London 221: 308-313.

 

Frantzen, M., Silk, J., Ferguson, J., Wayne, R., & Kohn, M. (1998). Empirical evaluation of the preservation methods for fecal DNA. Molecular Ecology 7: 1423-1428.

 

Gade, D.W. (2006). Hyenas and humans in the Horn of Africa. Geographical Review 96: 609-632.

 

Gersick, A. S., Cheney, D. L., Schneider, J. M., Seyfarth, R. M., & Holekamp, K. E. (2015). Long-distance communication facilitates cooperation among wild spotted hyaenas, Crocuta crocuta. Animal Behaviour 103: 107-116.

 

Goldstein, D. B., Linares, A. R., Cavallisforza, L. L., & Feldman, M. W. (1995). An Evaluation of Genetic Distances For Use With Microsatellite Loci. Genetics 139: 463-471.

 

Graf, J. A., Somers, M. J., Szykman Gunther, M., & Slotow, R. (2009). Heterogeneity in the density of spotted hyaenas in Hluhluwe-iMfolozi Park, South Africa. Acta Theriologica 54, 333-343.

 

Hardy, G. H. (1908). Mendelian Proportions in a Mixed Population. Science 28: 49-50.

Hartl, D. L., & Clark, A. G. (1988). Principles of Population Genetics. Sinauer Associates, Sunderland, Massachusetts.

 

Hayward, M.W. (2006). Prey preferences of the spotted hyena (Crocuta crocuta) and degree of dietary overlap with the lion (Pantera leo). Journal of Zoology 270: 606-614.

 

Hayward, M. W., & Hayward, G. J. (2006). Activity patterns of reintroduced lions Panthera leo and spotted hyaena Crocuta crocuta in the Addo Elephant National Park, South Africa. African Journal of Ecology 45: 135-141.

 

Hayward, M. W., O’Brien, J., & Kerley, G. I. H. (2007). Carrying capacity of large African predators: predictions and tests. Biological Conservation 139: 219-229.

 

Hedrick, P. W. (2000). Inbreeding depression in conservation biology. Annual Review of Ecology, Evolution, and Systematics 31: 139-162.

 

Henschel, J. R. (1986). The socio-ecology of a spotted hyaena Crocuta crocuta clan in the Kruger National Park. (Unpublished doctoral dissertation). University of Pretoria, Pretoria, South Africa.

 

Henschel, J. R., & Skinner, J. D. (1991). Territorial behavior by a clan of spotted hyaenas Crocuta crocuta. Ethology 88: 223-235.

 

Hofer, H., & East, M. L. (1993a). The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey I. Social organization. Animal Behaviour 46: 547-557.

 

Hofer, H., & East, M. L. (1993b). The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. II. Intrusion pressure and commuters’ space use. Animal Behaviour 46: 559-574.

 

Hofreiter, M., Serre, D., Rohland, N., Rabeder, G., Nagel, D., Conard, N., Münzel, S., & Pääbo, S. (2004). Lack of phylogeography in European mammals before the last glaciation. PNAS 101: 12963-12968.

 

Holekamp, K. E., & Dloniak, S. M. (2010). Intraspecific variation in the behavioral ecology of a tropical carnivore, the spotted hyena. Advances in the Study of Behavior 42: 189-229.

 

Holekamp, K. E., Ogutu, J. O., Frank, L. G., Dublin, H. T., & Smale, L. (1993). Fission of a spotted hyena clan: Consequences of female absenteeism and causes of female emigration. Ethology 93: 285-299.

 

Holekamp, K. E., Sakai, S. T., & Lundrigan, B. L. (2007). Social intelligence in the spotted hyena (Crocuta crocuta). Philosophical Transactions of the Royal Society B 362: 523-538.

 

Holekamp, K. E., & Smale, L. (1991). Dominance acquisition during mammalian social development: the ‘inheritance’ of maternal rank. American Zoologist 31: 306-317.

 

Holekamp, K. E., & Smale, L. (1993). Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with other immature individuals. Animal Behaviour 46: 451-466.

 

Holekamp, K. E., Smale, L., Berg, R., & Cooper, S. M. (1997). Hunting rates and hunting success in the spotted hyena (Crocuta crocuta). Journal of Zoology 242: 1-15.

 

Holekamp, K. E., Smith, J. E., Strelioff, C. C., Van Horn, R. C., & Watts, H. E. (2012). Society, demography and genetic structure in the spotted hyena. Molecular Ecology 21: 613-632.

 

Holmern, T., Nyahongo, J., & Røskaft, E. (2007).Livestock loss caused by predators outside the Serengeti National Park, Tanzania. Biological Conservation 135: 518-526.

 

Höner, O. P., Wachter, B., East, M. L., Runyoro, V. A. & Hofer, H. (2005). The effect of prey abundance and foraging tactics on the population dynamics of a social, territorial carnivore, the spotted hyena. Oikos 108: 544-554.

 

Höner, O. P., Wachter, B., East, M. L., Streich, W. J., Wilhelm, K., Burke, T., & Hofer, H. (2007). Female mate-choice drives the evolution of male-biased dispersal in a social mammal. Nature 448: 798-801.

 

Höner, O. P., Wachter, B., Hofer, H., Wilhelm, K., Thierer, D., Trillmich, F., Burke, T., & East, M. L. (2010). The fitness of dispersing spotted hyaena sons is influenced by maternal social status. Nature Communications 1: 1-7.

 

Irwin, D. M., Kocher, T. D., & Wilson, A. C. (1991). Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution 32: 128-144.

 

Jarne, P., & Lagoda, P. J. L. (1995). Microsatellites, from molecules to populations and back. Tree 11: 424-429.

 

Kamler, J. F., & Ballard, W. B. (2002). A review of native and nonnative red foxes in North America. Wildlife society bulletin 30: 370-379.

 

Kendall, M. et Stewart, A. (1977). The advanced Theory of statistics, volume 1. Macmillan, New York.

 

Kerr, J. T., & Currie D. J. (1995). Effects of human activity on global extinction risk. Conservation Biology 9: 1528-1538.

 

Khorozyan, I. G., Malkhasyan, A. G., & Abramov, A. V. (2008). Presence–absence surveys of prey and their use in predicting leopard (Panthera pardus) densities: a case study from Armenia. Integrative Zoology 3: 322-332.

 

Kissui, B. M. (2008). Livestock predation by lions, leopards, spotted hyenas, and their vulnerability to retaliatory killing in the Maasai steppe, Tanzania. Animal Conservation 11: 422-432.

 

Koepfli, K.-P., Jenks, S. M., Eizirik, E., Zahirpour, T., Van Valkenburgh, B., & Wayne, R. K. (2006). Molecular systematics of the Hyaenidae: Relationships of a relictual lineage resolved by a molecular supermatrix. Molecular Phylogenetics and Evolution 38: 603-620.

 

Koepfli, K.-P., & Wayne, R. K., (1998). Phylogenetic relationships of otters (Carnivora: Mustelidae) based on mitochondrial cytochrome b sequences. Journal of Zoology 246: 401-416.

 

Kolowski, J. M., & Holekamp, K. E. (2006). Spatial, temporal, and physical characteristics of livestock depredations by large carnivores along a Kenyan reserve border. Biological Conservation 128: 529-541.

 

Kolowski, J. M., Katan, D., Theis, K. R., & Holekamp, K. E. (2007). Daily patterns of activity in the spotted hyena. Journal of Mammalogy 88: 1017-1028.

 

Krebs, C. J. (1994). Ecology: The Experimental Analysis of Distribution and Abundance. Harper Collins, New York.

 

Kruuk, H. (1972). The Spotted Hyena. A Study of Predation and Social Behavior. University of Chicago Press, Chicago.

 

Lewontin, R. C., & Kojima, K. (1960). The evolutionary dynamics of complex polymorphisms. Evolution 14, 458-472.

 

Libants, S., Olle, E., Oswald, K., & Scribner, K. T. (2000). Microsatellite loci in the spotted hyena Crocuta crocuta. Molecular Ecology 9: 1433-1449.

 

Løe, J., & Røskaft, E., (2004). Large carnivores and human safety: a review. Ambio 33: 283-288.

 

Lyons, A. J. (2005). Activity patterns of urban American black bears in the San Gabriel Mountains of southern California. Ursus 16:255-262.

 

Mamo, D., Bauer, H., & Tesfay, Y. (2013). Crop damage by African elephants assessment in Kafta Sheraro National Park, Ethiopia. African Journal of Ecology 52: 138-143.

 

Marshall, T. C., Slate, J., Kruuk, L. E. B., & Pemberton, J. M. (1998). Statistical confidence for likelihood based paternity inference in natural populations. Molecular Ecology 7: 639-655.

 

McManus, J. S., Dalton, D. L., Kotzé, A., Smuts, B., Dickman, A., Marshal, J. P., & Keith, M. (2015). Gene flow and population structure of a solitary top carnivore in a human-dominated landscape. Ecology and Evolution 5: 335-344.

 

Merkle, J. A., Krausman, P. R., Decesare, N. J., & Jonkel, J. J. (2011). Predicting spatial distribution of human-black bear interactions in urban areas. Journal of Wildlife Management 75: 1121-1127.

 

Mills, M. G. L. (1985). Related spotted hyaenas forage together but do not cooperate in rearing young. Nature 316: 61-62.

 

Mills, M. G. L. (1990). Kalahari Hyaenas: The Behavioural Ecology of Two Species. Unwin Hyman, London.

 

Mills, M. G. L., & Hofer, H. (compilers) (1998). Hyaenas. Status Survey and Conservation Action Plan. IUCN/SSC Hyaena Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK.

 

Mullis, K. & Faloona, F. (1987). Specific synthesis of DNA in vitro via a polymerase catalyzed chain reaction. Methods in Enzymology 155: 335-350.

 

Navidi, W., Arnheim, N., & Waterman, M. S. (1992). A Multiple-Tubes Approach for Accurate Genotyping of Very Small DNA Samples by Using PCR: Statistical Considerations. The American Journal of Human Genetics 50: 347-359.

 

Ogada, M. O., Woodroffe, R., Oguge, N. O., & Frank, L. G. (2003). Limiting depredation by African carnivores: the role of livestock husbandry. Conservation Biology 17: 1521-1530.

 

Ogutu, J. O., & Dublin, H. T. (1998). The response of lions and spotted hyenas to sound playbacks as a technique for estimating population size. African Journal of Ecololy 36: 83-95.

 

Otis, D., Burnham, K., White, G., & Anderson, D. (1978). Statistical inference from capture data on closed animal populations. Wildlife Monographs 62: 3-135.

 

Panasci, M., Ballarda, W. B., Breck, S., Rodriguez, D., Densmore, L. D., Wester, D. B., & Baker, R. J. (2011). Evaluation of Fecal DNA Preservation Techniques and Effects of Sample Age and Diet on Genotyping Success. Journal of Wildlife Management 75: 1616-1624.

 

Peterson, M. N., Birckhead, J. L., Leong, K., Perterson, M. J., & Peterson, T. R. (2010). Rearticulating the myth of human–wildlife conflict. Conservation Letters 3: 74-82.

 

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155: 945-959.

 

Ralls, K. (1976). Mammals in which females are larger than males. Quarterly Review of Biology 51: 245-276.

 

Reddy, P. A., Bhavanishankar, M., Bhagavatula, J., Harika, K., Mahla, R. S., & Shivaji, S. (2012). Improved Methods of Carnivore Faecal Sample Preservation, DNA Extraction and Quantification for Accurate Genotyping of Wild Tigers. PLoS ONE 7: 1-7.

 

Roeder, A. D., Archer, F. I., Poinar, H. N., & Morin, P. A. (2004). A novel method for collection and preservation of faeces for genetic studies. Molecular Ecology Notes 4: 761-764.

 

Rohland, N., Siedel, H., & Hofreiter, M. (2004). Nondestructive DNA extraction method for mitochondrial DNA analyses of museum specimens. BioTechniques 36: 2-6.

 

Rojas, M. Gonzalez, I., Fajardo, V., Martin, I., Hernandez, P. E., Garcia, T., & Martin, R. (2008). Polymerase Chain Reaction-Restriction Fragment Length Polymorphism Authentication of Raw Meats from Game Birds. Journal of AOAC International 91: 1416-1422.

 

Roughgarden, J., May, R. M., & Levin, S. A., eds. (1989). Perspectives in Ecological Theory. Princeton University Press, Princeton, New Jersey.

 

Santini, A., Lucchini, V., Fabbri, E., & Randi, E. (2007). Ageing and environmental factors affect PCR success in wolf (Canis lupus) excremental DNA samples. Molecular Ecology Notes 7: 955-961.

 

Savolainen, O., Lascoux, M. & Merilä, J. (2013). Ecological genomics of local adaptation. Nature Reviews Genetics 14: 807-820.

 

Schmider, E., Ziegler, M., Danay, E., Beyer, L. & Bühner, M. (2010). Is it really robust? Methodology 6: 147-151.

 

Schwerin, M., & Pitra, C. (1994). Sex determination in Spotted Hyena (Crocuta crocuta) by Restriction Fragment Length Polymorphism of amplified ZFX/ZFY loci. Theriogenology 41: 553-559.

 

Shehzad, W., Riaz, T., Nawaz, M. A., Miquel, C., Poillot, C., Shah, S. A., Pompanon, F., Coissac, E., & Taberlet, P. (2012). Carnivore diet analysis based on next-generation sequencing: application to the leopard cat (Prionailurus bengalensis) in Pakistan. Molecular Ecology 21: 1951-1965.

 

Skinner, J. D., & van Aarde, R. J. (1991). The distribution and ecology of the brown hyaena Hyaena brunnea and spotted hyaena Crocuta crocuta in the central Namib desert. Madoqua 12: 231-239.

 

Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462.

 

Smale, L. Frank, L. G., & Holekamp, K. E. (1993). Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with adult females and immigrant males. Animal Behaviour 46: 467-477.

 

Smith, J.E., & Holekamp, K.E. (2010). Spotted Hyenas. Michigan State University, East Lansing, MI, USA.

 

Smith, J. E., Kolowski, J. M., Graham, K. E., Dawes, S. E., & Holekamp, K. E. (2008). Social and ecological determinants of fission-fusion dynamics in the spotted hyaena. Animal Behaviour 76: 619- 636.

 

Sugimoto, T., Aramilev, V. V., Kerley, L. L., Nagata, J., Miquelle, D. G., & McCullough, D. R. (2014). Noninvasive genetic analyses for estimating population size and genetic diversity of the remaining Far Eastern leopard (Panthera pardus orientalis) population. Conservation Genetics 15:521-532.

 

Sunnucks, P. (2000). Efficient genetic markers for population biology. Tree 15: 199-203.

 

Sunquist, M. E., & F. Sunquist. (2002). Wild cats of the world. University of Chicago Press, Chicago, USA.

 

Taberlet, P., Griffin, S., Goossens, B., Questiau, S., Manceau, V., Escaravage, N., Waits, L. P. & Bouvet, J. (1996). Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research 24: 3189-3194.

 

Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725-2729.

 

Tende, T., Hansson, B., Ottosson, U., & Bensch, S. (2014). Evaluating preservation medium for the storage of DNA in African lion Panthera leo faecal samples. Current Zoology 60: 351-358.

 

Thermo Fisher Scientific (2013). T009‐TECHNICAL BULLETIN NanoDrop 1000 & 8000. Accessed December 16, 2014 via http://www.nanodrop.com/Library/T009-NanoDrop%201000-&-NanoDrop%208000-….

 

Tilson, R. L., & Hamilton, W. J. (1984). Social dominance and feeding patterns in spotted hyenas. Animal Behaviour 32: 715-724.

 

Tilson, R. L., & Henschel, R. (1986). Spatial arrangement of spotted hyaena groups in a desert environment, Namibia. African Journal of Ecology 24: 173-180.

 

Tilson, R. L., von Blottnitz, F., & Henschel, J. R. (1980). Prey Selection by spotted hyaena (Crocuta crocuta) in the Namib Desert. Madoqua 12: 41-49.

 

Treves, A., Naughton-Treves, L., Harper, E. K., Mladenoff, D. J., Rose, R. A., Sickley, T. A., & Wydeven, A. P. (2004). Predicting human-carnivore conflict: a spatial model derived from 25 years of data on wolf predation on livestock. Conservation Biology 18: 114-125.

 

Trinkel, M., Fleishmann, P. H., Steindorfer, A. F., & Kastberger, G. (2004). Spotted hyenas (Crocuta crocuta) follow migratory prey. Seasonal expansion of a clan territory in Etosha, Namibia. Journal of Zoology 264: 125-133.

 

Valière, N. (2002). GIMLET: a computer program for analysing genetic individual identification data. Molecular Ecology Notes 2: 377-379.

 

Van Horn, R. C., Engh, A. L., Scribner, K. T., Funk, S. M., & Holekamp, K. E. (2004). Behavioral structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation. Molecular Ecology 13: 449-458.

 

Vynne, C., M. R. Baker, Z. K. Breuer, & S. K. Wasser (2011). Factors influencing degradation of DNA and hormones in maned wolf scat. Animal Conservation 15: 184-194.

 

Wang, X.-M., Cao, L.-R., Liu, Z.-S., & Fang, S.-G. (2006). Mitochondrial DNA variation and matrilineal structure in blue sheep populations of Helan Mountain, China. Canadian Journal of Zoology 84: 1431-1439.

 

Waples, R. S., & Gaggliotti, O. (2006). What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology 15: 1419-1439.

 

Wasser, S. K., Houston, C. S., Koehiler, G. M., & Cadd, G. G. (1997). Techniques for applications of faecal DNA methods to field studies of Ursids. Molecular Ecology 6: 1091-1097.

 

Watts, H.E. (2007). Social and ecological influences on survival and reproduction in the spotted hyena, Crocuta crocuta (Unpublished doctoral dissertation). Michigan State University, East Lansing, MI.

 

Watts, H. E., & Holekamp, K. E. (2008). Interspecific competition influences reproduction in spotted hyenas. Journal of Zoology, London 276: 402-410.

 

Watts, H.E., & Holekamp, K.E. (2009). Ecological determinants of survival and reproduction in the spotted hyena. Journal of Mammalogy 90: 461-471.

 

Watts, H .E., Scribner, K. T., Garcia, H. A., & Holekamp, K. E. (2011). Genetic diversity and structure in two spotted hyena populations reflects social organization and male dispersal. Journal of Zoology 285: 281-291.

 

Whateley, A. (1981). Density and home range of spotted hyaenas in Umfolozi Game Reserve, Natal. Lammergeyer 31: 15-20.

 

Whateley, A., & Brooks, P. M. (1978). Numbers and movements of spotted hyaenas in Hluhluwe Game Reserve. Lammergeyer 26: 44-52.

 

White, P.A. (2006). Costs and strategies of communal den use vary by rank for spotted hyaenas, Crocuta crocuta. Animal Behaviour 73: 149–156.

 

Wilhelm, K., Dawson, D. A., Gentle, L. K., Greig, C., Horsefield, G., Schlötterer, C., Burke, T., East, M. L., Hofer, H., & Tautz, D. (2003) Characterisation of spotted hyena Crocuta crocuta microsatellite loci. Molecular Ecology Notes 3: 360-362.

 

Woodroffe, R., & Ginsberg, J. R. (1998). Edge effects and the extinction of populations inside protected areas. Science 280: 2126-2128.

 

Wright, S. (1931). Evolution in Mendelian populations. Genetics 16: 97-159.

 

Wright, S. (1969). Evolution and the Genetics of Populations, Vol. 2. University of Chicago Press, Chicago.

 

Wright, S. (1978). Evolution and the Genetics of Populations. Vol. 4. Variability Within and Among Natural Populations. University of Chicago Press, Chicago.

 

Wydeven, A. P. (2004). Predicting human-carnivore conflict: a spatial model derived from 25 years of data on wolf predation on livestock. Conservation Biology 18: 114-125.

 

Yirga, G. (2013). Ecology and Conservation of Spotted Hyena (Crocuta crocuta Erxleben 1777) in Human Dominated Landscapes in Northern Ethiopia. 1. General introduction (Unpublished doctoral dissertation). Leiden University, Leiden, The Netherlands.

 

Yirga, G. & Bauer, H. (2010a). Diet of the spotted hyena (Crocuta crocuta) in southern Tigray, northern Ethiopia. World Journal of Science, Technology and Sustainable Development 7: 391-397.

 

Yirga, G. & Bauer, H. (2010b). Livestock Depredation of the Spotted Hyena (Crocuta crocuta) in Southern Tigray, Northern Ethiopia. International Journal of Ecology and Environmental Sciences 36: 67-73.

 

Yirga, G. & Bauer, H. (2010c). Prey of Peri-urban Spotted Hyena (Crocuta crocuta) in Southeastern Tigray, Northern Ethiopia. Asian Journal of Agricultural Sciences 2: 124-127.

 

Yirga, G., De Iongh, H. H., Leirs, H., Gebrehiwot, K., Deckers, J., & Bauer, H. (2012). Adaptability of large carnivores to changing anthropogenic food sources: diet change of spotted hyena (Crocuta crocuta) during Christian fasting period in Northern Ethiopia. Journal of Animal Ecology 81: 1052-1055.

 

Yirga, G., De Iongh, H. H., Leirs, H., Gebrehiwot, K., Deckers, J., Asfaw, T., Acha, A., & Bauer, H. (2013a). Hyenas (Crocuta crocuta) depend on anthropogenic food across Ethiopia (Unpublished doctoral dissertation). Leiden University, Leiden, The Netherlands.

 

Yirga, G., De Iongh, H.H., Leirs, H., Gebrihiwot, K., Deckers, J. & Bauer, H. (2013b). Spotted hyena (Crocuta crocuta) concentrate around urban garbage dumps in northern Ethiopia. (Unpublished doctoral dissertation). Leiden University, Leiden, The Netherlands.

 

Yirga, G., Ersino, W., De Iongh, H. H., Leirs, H., Gebrehiwot, K., Deckers, J., & Bauer, H. (2013c). Spotted hyena (Crocuta crocuta) coexisting at high density with people in Wukro district, northern Ethiopia. Mammalian Biology 78: 193-197.

 

Yirga, G., Imam, E., De Iongh, H.H., Leirs, H., Kiros, S., Yohannes, T., Teferi, M., & Bauer, H. (2014). Local spotted hyena abundance and community tolerance of depredation in human-dominated landscapes in Northern Ethiopia. Mammalian Biology, DOI: http://dx.doi.org/10.1016/j.mambio.2014.05.002

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Universiteit of Hogeschool
Universiteit Antwerpen
Thesis jaar
2015