Quantitative and qualitative impact of diseases on wildlife populations

In close coordination with ecological and epidemiological studies, a key task is to assess the influence of diseases and reproductive disorders on the viability and dynamics of wildlife populations. Such a task therefore links the health status and fate of the individual to a population perspective that considers the consequences for the dynamics and conservation of wildlife populations.

Pathogenesis of population limiting diseases

The study of the origin and development of a disease is crucial to estimate the influence and threat of the disease for an animal population and to assess the need for management decisions. We investigated the phylogenetic relationship of isolates of bacteria belonging to the species Streptococcus equi ssp. ruminatorum, which caused a strangles-like disease outbreak among spotted hyenas (Crocuta crocuta) in the Serengeti ecosystem in Tanzania.

We sequenced the gene of a major virulence factor of the bacterium, the M-like-protein, in isolates of spotted hyenas and other species. We found that isolates of symptomatic hyenas were closely related to each other and to imported livestock (camels), and less closely related to isolates from non-symptomatic hyenas, other carnivores (wild dogs Lycaon pictus) and prey animals (zebras Equus burchelli and buffaloes Syncerus caffer). This suggests that the strain causing virulent infection among free-ranging spotted hyenas may have originated from livestock.

A rather sinister population decline is the current emergence of white-nose syndrome in North America, a fungal infection of the skin of hibernating bats. Since its first detection in 2006 it resulted in the death of over 6 Mio bats in this region. During our investigations in Europe the same fungus was found on individual hibernating bats of more then 13 countries, but in contrast to North America there is no association with mortality. In cooperation with colleagues from oversea and Europe we are trying to elucidate the reasons for these apparent differences.

Reproductive disorders as a factor relevant to reintroduction programmes

Reintroduction programmes and captive breeding are important aspects of the conservation of threatened species and sustainable and healthy captive breeding is considered a prerequisite for reintroduction success. Some species involved in captive breeding programs, however, reproduce poorly; one prominent example is the cheetah (Acinonyx jubatus). Evaluation of the reproductive status with ultrasonography in free-ranging and captive female cheetahs in Namibia revealed that activity of the inner reproductive organs of cheetah females is determined by their reproductive history and age rather than innate rhythms, captive stress or lack of genetic diversity, as previously suggested. Nulliparous females with an age of 4 years onwards develop with a high probability pathologies on their inner reproductive organs, a phenomenon consistent with the model of asymmetric reproductive aging previously described in elephant and rhinoceros species. The consequence is irreversible low fertility which is unwanted for reintroduction programmes. Cub survival on Namibian farmland, a nearly predator-free ecosystem, was high, thus reproductively healthy cheetahs are likely to raise cubs successfully. Management practices of captive breeding and reintroduction programmes should therefore encourage early reproduction in females to induce long-lasting and healthy reproductive performance. With this practice, reintroduction projects might increase their chances of success.

A more general but frequent cause of fertility disorders in domestic and free-ranging animals are bacteriological infections of the genital tract. Samples from the reproductive tract of clinical healthy and diseased individuals of threatened species from the European Endangered Species Programme (EEP), such as rhinoceroses, are investigated for the occurrence of known bacterial pathogens and species specific differences in the autochthonous flora. As the survival of a threatened species may depend on the fertility and reproduction of a few individuals, proper diagnostic and treatment of bacterial infections of captive individuals of such species are of great importance.

Causes and treatment of sub- and infertility

Sustainability of captive populations and their maintenance for biological conservation has become increasingly important. Restocking of zoo populations with newly captured wild animals is therefore expected to be scaled down. Thus, the success of breeding efforts of wildlife under human care needs to be improved.

Captive populations are often faced with fertility problems which are strongly related to husbandry issues such as the size of enclosures, incompatible pairing or inbreeding. Consequently, wildlife reproductive medicine was established as an important discipline of wildlife medicine. It aims to elucidate the key reproductive parameters of wildlife species which are required to enhance their reproductive success. An important part of this discipline and our research efforts is the identification of the causes and consequences of fertility problems and the development of methods to treat them. These include subfertilities such as teratozoospermia and the ontogenetic development of complete fertility failures such as reproductive ageing, for instance in cases when animals do not have an opportunity to reproduce.

Impact of diseases on the evolution and population dynamics of wildlife

Pathogens and diseases can have a considerable direct or indirect impact on wild animal populations and they are increasingly considered as an ecological factor that may regulate or limit wildlife population size. To this end, statistical methods are used and simulation methods developed to assess the impact of diseases on population trends and host-pathogen co-evolution.

A long-term study on spotted hyenas (Crocuta crocuta) in the Ngorongoro Crater, Tanzania, revealed that an outbreak of a pathogenic bacterium had a substantial impact on the dynamics of this population. The outbreak increased mortality among socially subordinate and young individuals and reduced recruitment of breeding females, causing a short-term decline in population size and a longer-term post-outbreak reduction in population growth. The short-term ‘top-down’ impact of the bacterium during the outbreak was driven by ‘bottom-up’ effects on nutritionally disadvantaged age-sex classes, whereas the longer-term post-outbreak reduction in population growth was caused by poor survival of juveniles during the outbreak and subsequent poor recruitment of breeding females. The results suggest synergistic effects of ‘bottom-up’ and ‘top-down’ processes on the population dynamics of this large carnivore host.

A second issue that has become increasingly important are viral diseases and the population management of wildlife in captivity, particularly in zoological gardens. Zoos may act as sentinels for outbreaks of diseases in urban areas. However, zoos also bring non-sympatric species into close contact with each other which could potentially facilitate the spread of opportunistic pathogens. Ongoing studies monitor the traffic of such opportunists within zoo populations to determine their origin and ability to disperse within the zoo animal community. We can use this information to help zoos monitor and intervene in the case of zoo derived epizootics.

Selected publications

Bouts T, Hermes R, Gasthuys F, Saragusty J, Taylor P, Routh A, Hildebrandt TB (2012) Medetomidine-ketamine-isoflurane anaesthesia in pygmy hippopotami (Choeropsis liberiensis) - a case series. Vet Anaesth Analg 39: 111-118.

Höner OP, Wachter B, Goller KV, Hofer H, Runyoro V, Thierer D, Fyumagwa R, Müller T, East ML (2012) The impact of a pathogenic bacterium on a social carnivore population. J Anim Ecol 81: 36-46.

Lange M, Kramer-Schadt S, Blome S, Beer M, Thulke HH (2012) Disease severity declines over time after a wild boar population has been affected by Classical Swine Fever – Legend or actual epidemiological process? Prev Vet Med 106: 185-195.

Lange M, Kramer-Schadt S, Thulke HH (2012) Efficiency of spatio-temporal vaccination regimes in wildlife populations under different viral constraints. Vet Res 43: 37.

Menzies BR, Renfree MB, Heider T, Mayer F, Hildebrandt TB, Pask AJ (2012) Limited genetic diversity preceded extinction of the Tasmanian tiger. PLoS ONE 7.

Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Wibbelt G, Blehert DS, Willis CK (2012) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci USA 109: 6999-7003.

Drews B, Szentiks CA, Roellig K, Fickel J, Schroeder K, Duff JP, Lavazza A, Hildebrandt TB, Goeritz F (2011) Epidemiology, control and management of an EBHS outbreak in captive hares. Vet Microbiol 154: 37-48.

Schaftenaar W, Fernandes T, Fritsch G, Frey R, Szentiks CA, Wegner RD, Hildebrandt TB, Hermes R (2011) Dystocia and fetotomy associated with cerebral aplasia in a greater one-horned rhinoceros (Rhinoceros unicornis). Reprod Domest Anim 46.

Wachter B, Thalwitzer S, Hofer H, Lonzer J, Hildebrandt TB, Hermes R (2011) Reproductive history and absence of predators are important determinants of reproductive fitness: the cheetah controversy revisited. Conserv Lett 4: 47-54.

Kramer-Schadt S, Holst JC, Skagen D (2010) Analysis of variables associated with the Ichthyophonus hoferi epizootics in Norwegian Spring Spawning Herring 1992-2008. Can J Fish Aquat Sci 67: 1862-1873.

Lueders I, Drews B, Niemuller C, Gray C, Rich P, Fickel J, Wibbelt G, Göritz F, Hildebrandt TB (2010) Ultrasonographically documented early pregnancy loss in an Asian elephant (Elephas maximus). Reprod Fertil Develop 22: 1159-1165.

Portas TJ, Hildebrandt TB, Bryant BR, Göritz F, Hermes R (2010) Seminoma in a southern black rhinoceros (Diceros bicornis minor): diagnosis, surgical management and effect on fertility. Aust Vet J 88: 57-60.

Jewgenow K, Neubauer K, Blottner S, Schon J, Wildt DE, Pukazhenthi BS (2009) Reduced germ cell apoptosis during spermatogenesis in the teratospermic domestic cat. J Androl 30: 460-468.

Saragusty J, Hermes R, Göritz F, Schmitt DL, Hildebrandt TB (2009) Skewed birth sex ratio and premature mortality in elephants. Anim Reprod Sci 115: 247-254.

Aupperle H, Reischauer A, Bach F, Hildebrandt T, Göritz F, Jager K, Scheller R, Klaue HJ, Schoon HA (2008) Chronic endometritis in an Asian elephant (Elephas maximus). J Zoo Wildl Med 39: 107-110.

Hermes R, Saragusty J, Schaftenaar W, Göritz F, Schmitt DL, Hildebrandt TB (2008) Obstetrics in elephants. Theriogenology 70: 131-144.

Speck S, Höner OP, Wachter B, Fickel J. (2008) Characterization of Streptococcus equi subsp. ruminatorum isolated from spotted hyenas (Crocuta crocuta) and plains zebras (Equus burchelli), and identification of a M-like protein (SrM) encoding gene. Vet Microbiol 128: 148-159.

Hermes R, Göritz F, Streich W, Hildebrandt T (2007) Assisted reproduction in female rhinoceros and elephants - current status and future perspective. Reprod Domest Anim 42: 33-44.

Schettler E, Müller K, Fritsch G, Kaiser S, Brunnberg L, Frölich K, Wibbelt G (2007) Progressive ataxia in a captive North American river otter (Lontra canadensis) associated with brain stem spheroid formation. J Zoo Wildl Med 38: 579-582.

Hermes R, Hildebrandt TB, Walzer C, Göritz F, Patton ML, Silinski S, Anderson MJ, Reid CE, Wibbelt G, Tomasova K, Schwarzenberger F (2006) The effect of long non-reproductive periods on the genital health in captive female white rhinoceroses (Ceratotherium simum simum, Ceratotherium simum cottoni). Theriogenology 65: 1492-1515.

Hildebrandt TB, Göritz F, Boardman W, Strike T, Strauss G, Jewgenow K (2006) A non-surgical uterine lavage technique in large cats intended for treatment of uterine infection-induced infertility. Theriogenology 66: 1783-1786.

Portas TJ, Hermes R, Bryant BR, Göritz F, Thorne AR, Hildebrandt TB (2006) Anesthesia and use of a sling system to facilitate transvaginal laparoscopy in a black rhinoceros (Diceros bicornis minor). J Zoo Wildl Med 37: 202-205.

Pukazhenthi B S, Neubauer K, Jewgenow K, Howard J, Wildt DE (2006) The impact and potential etiology of teratospermia in the domestic cat and its wild relatives. Theriogenology 66: 112-121.

Reid CE, Hildebrandt TB, Marx N, Hunt M, Thy N, Reynes JM, Schaftenaar W, Fickel J (2006) Endotheliotropic Elephant Herpes Virus (EEHV) infection - The first PCR-confirmed fatal case in Asia. Vet Quart 28: 61-64.