German Zoo Research Articles

Genetic characterization of near full length SIVdrl genomes from four captive drills (Mandrillus leucophaeus).

We sequenced near full length SIVdrl genomes from four captive drills (Mandrillus leucophaeus). All four animals were born in captivity in German zoos. Although serologically SIV negative before acquisition in zoo A in 2008 and 2009, during a routine analysis all four animals were determined to be SIV antibody positive in 2011. Comparisons of the four new SIVdrl sequences showed high identity among each other (90.7-97.7% in env) and to the only published full length sequence SIVdrl FAO (90.5-92.8% in env), which is also derived from a captive drill. SIVdrl infections seem to be highly prevalent in captive drills, probably resulting from frequent animal transfers between the zoos in an effort to maintain this highly endangered species and its genetic diversity. This should be kept in mind as SIVdrl may be transmitted to uninfected animals in open groups and potentially also to animal keepers having contact with these nonhuman primates.

Hormonphysiologische und ethologische Untersuchung am Goodfellow-Baumkänguru (Dendrolagus goodfellowi Thomas, 1908)

Currently seven animal species worldwide are managed in Global Species Management Programs (GSMPs). Since 2013 the Goodfellow's tree kangaroo (Dendrolagus goodfellowi) is the first marsupial in this group of species. The primary goal of the GSMP is to enhance the sustainability of the captive population. Reproductive cycles of seven female Goodfellow-tree kangaroo's kept in German zoos were studied during a period of 23 weeks. Faecal samples and behavioural data were collected in order to identify oestrous specific behaviour. Faecal hormone metabolites were analysed using an enzyme-immunoassay for 4-Pregnen-20α-ol-3-one (trivial name: 20α-Progesterone). Faecal hormone metabolites indicated reproductive activity in all females studied, even in a 19 year old individual. The average oestrous cycle was 54.3±1.6 days. During oestrus periods females showed significantly more pouch licking behaviour (p<0,01), while the breeding male had significantly more interest in females (p<0,05) indicated by sniffling and vocalization (sound: clicking/“chitching”). Finally this study demonstrates that the applicability of faecal hormone analysis is an adequate method for reproductive monitoring in Goodfellow's tree kangaroos.

Polycystic kidneys and GM2 gangliosidosis-like disease in neonatal springboks (Antidorcas marsupialis).

Clinical, gross, histopathologic, electron microscopic findings and enzymatic analysis of 4 captive, juvenile springboks (Antidorcas marsupialis) showing both polycystic kidneys and a storage disease are described. Springbok offspring (4 of 34; 12%) were affected by either one or both disorders in a German zoo within a period of 5 years (2008-2013). Macroscopic findings included bilaterally severely enlarged kidneys displaying numerous cysts in 4 animals and superior brachygnathism in 2 animals. Histopathologically, kidneys of 4 animals displayed cystic dilation of the renal tubules. In addition, abundant cytoplasmic vacuoles with a diameter ranging from 2 to 10 μm in neurons of the central and peripheral nervous system, hepatocytes, thyroid follicular epithelial cells, pancreatic islets of Langerhans and renal tubular cells were found in 2 springbok neonates indicative of an additional storage disease. Ultrastructurally, round electron-lucent vacuoles, up to 4 μm in diameter, were present in neurons. Enzymatic analysis of liver and kidney tissue of 1 affected springbok revealed a reduced activity of total hexosaminidase (Hex) with relatively increased HexA activity at the same level of total Hex, suggesting a hexosaminidase defect. Pedigree analysis suggested a monogenic autosomal recessive inheritance for both diseases. In summary, related springboks showed 2 different changes resembling both polycystic kidney and a GM2 gangliosidosis similar to the human Sandhoff disease. Whether the simultaneous occurrence of these 2 entities represents an incidental finding or has a genetic link needs to be investigated in future studies.

Zoopädagogische Aspekte der Papageienhaltung und -präsentation in deutschen Zoos – mit einem Seitenblick auf die private Papageienhaltung

Parrots are among the few animal groups which are kept more in private than in zoo aviaries. Zoos therefore have a central role in presenting their parrots to the public, especially due to a biological based parrot husbandry and suitable exhibit labels. With regard to the main systematic groups of parrots, which are presently kept in zoos and private aviaries, several examples of appropriate and deficient exhibits of parrots in some German zoos are discussed.

Distribution of Mycobacterium avium ssp. paratuberculosis in a German zoological garden determined by IS900 semi-nested and quantitative real-time PCR

Little data concerning the distribution of Mycobacterium avium ssp. paratuberculosis (MAP) in zoological gardens is available. The presence of MAP in captured wildlife might provide further information on non-ruminant hosts and expand the list of animals susceptible to MAP being potential sources of MAP transmission. Therefore, a German zoological garden with recent history of clinical paratuberculosis in Barbary sheep (Ammotragus lervia) and an alpaca (Lama pacos) was selected to estimate the distribution of MAP infections in 21 mammalian and avian species. Pooled faecal samples from individual animals of each species were tested for the presence of MAP. A previously developed IS900 semi-nested PCR (snPCR) assay, amplifying a 587bp and a 278bp fragment, was used for the detection of MAP-DNA. Based on this snPCR, in 14 out of the 21 pooled faecal samples MAP-DNA was detected. MAP positive snPCR results were observed in ruminants and camelids as well as in non-ruminants such as equines, primates, rodents, and birds. Moreover, a quantitative real-time PCR demonstrated that the concentration of MAP-DNA was within the range of 2.2×103–9.6×106 MAP-DNA equivalents per gram faeces. The highest amount was shed by primates such as Black-and-white ruffed lemurs (Varecia variegata) and Cottontop tamarins (Saguinus oedipus).This is the first survey investigating the presence of MAP in a German zoo, which includes non-ruminants. The results of the present study confirm the wide host range of MAP and demonstrate that MAP occurs more frequently in zoo animals than expected. In order to restrict further spread of MAP in European zoos, additional investigations regarding the existing transmission pathways of MAP in zoos are recommended.

Aus der Frühgeschichte des Verbandes Deutscher Zoodirektoren (VDZ) e.V. – Aus den Archiven des Zoologischen Gartens Breslau/Wrocław

The early history of the VDZ is nearly unknown. Surprisingly many historical materials of great value were discovered while reorganizing the library and archives of Wrocław (Breslau) Zoo. One of these discoveries is the nearly full set of the minutes from the meetings of the directors of German zoos starting from the first meeting in 1887 up to the 41st meeting held in 1929. To fill in the gap of the knowlegde about the history of VDZ we give a list of the meetings with some citations of each minutes. The full and complete list of all the meetings from the years 1887 – 1929 is given, with the dates, place and list of the participants. All names, titles and numeration cited here are exactly as printed in the original minutes. Also the citations, randomly derived from the minutes are given here exactly as in the original minutes.

Serosurvey of zoo ungulates in central Europe

In total, 926 individuals representing 69 different species of bovids, cervids and camelids from one Czech and ten German zoos were tested for antibodies against five viral and three bacterial pathogens that can be transmitted across species borders. In addition, the archived veterinary data of all bovids, cervids and camelids, kept at eight of the 11 zoos between 1998 and 2004, were reviewed. The results demonstrate that both malignant catarrhal fever and Chlamydophila psittaci were endemic in zoo ruminants in Germany. Epidemiologic factors are discussed that might have a qualitative implication for cross-species transmission within zoos. The factors included are population size, population density and exhibit type (single species/mixed species).

Development of Feline Microsatellites and SNPs for Evaluating Primary Cataract Candidate Genes as Cause for Cataract in Angolan Lions (Panthera leo bleyenberghi)

Primary cataracts (CAT) are characterized as any form of opacities of the eye lenses and are not accompanied by other diseases. CAT may impair vision depending on their size, location, and their state of progression. In order to investigate the cause of congenital or juvenile CAT in inbred Angolan lions kept in German zoos, we analyzed the genomic sequences of 4 crystalline genes CRYAA, CRYAB, CRYBB2, and CRYBB1. In addition, 10 CAT candidate genes (GJA3, LIM2, CRYGA, CRYGB, CRYGC, CRYGD CRYGS, BFSP2, CRYBA4, and CRYBB1) were analyzed using adjacent microsatellites. We identified 10 single nucleotide polymorphisms in the Angolan lion crystalline genes and 9 segregating microsatellites. Nonparametric and parametric linkage analyses did not reveal any linkage between one of the analyzed markers and CAT. So, we concluded that these genes can be excluded as causative for the familial primary cataract phenotype in these Angolan lions.

Begehbare Freiflugvoliere für Störche, Ibisse und Enten im Opel-Zoo Kronberg: Walk-through aviary for storks, ibisses and ducks at the Opel-Zoo Kronberg

The new “Walk-through aviary” at the Opel-Zoo Kronberg, Germany, which was opened in September 2008 after a ten months construction period, is described. Covering around 1450m 2 and being up to 12.5 m high this aviary is one of the biggest in German zoos. The technical innovation is the first use of a stainless steel mash, which was permanent darkened using a chemical reaction. This method is named: INOX-Spectral ® - technique. The author explains the decision-making for the construction and gives an overview of the first year of keeping the birds in this aviary. The public reaction to this building, which is unlikely for the overall animal keeping attitude at the Opel-Zoo, is also covered by this article.

Presumptive Acute Neural Toxoplasmosis in a Captive Red-Necked Wallaby (Macropus rufogriseus)

A red-necked male wallaby (Macropus rufogriseus) from a German zoo was presented for acute onset of severe neurological signs, including head tremor, lethargy, unresponsiveness, and weakness. Serum biochemical abnormalities included increased LDH- and AST-levels, hyperproteinaemia, and reduced ALT-, ALP-, and creatinine-levels. The wallaby was found serologically positive for Toxoplasma gondii by the indirect haemagglutination test. After initiation of therapy by subcutaneous injections of trimethoprim/sulfadoxin, amelioration of neurological signs was noted and after 10 days the affected wallaby recovered. T. gondii can be confirmed rapidly by serology, and immediate therapy may reduce clinical illness and fatality of the disease within captive macropods.

Transspecies Transmission of the Endogenous Koala Retrovirus

The koala retrovirus (KoRV) is a gammaretrovirus closely related to the gibbon ape leukemia virus and induces leukemias and immune deficiencies associated with opportunistic infections, such as chlamydiosis. Here we characterize a KoRV newly isolated from an animal in a German zoo and show infection of human and rat cell lines in vitro and of rats in vivo, using immunological and PCR methods for virus detection. The KoRV transmembrane envelope protein (p15E) was cloned and expressed, and p15E-specific neutralizing antibodies able to prevent virus infection in vitro were developed. Finally, evidence for immunosuppressive properties of the KoRV was obtained.

GONGYLONEMA PULCHRUM INFECTION AND ESOPHAGEAL SQUAMOUS CELL CARCINOMA IN A VARI (LEMUR MACACO VARIEGATA; KEHR 1792)

This report describes the morphologic and histologic features of a case of esophageal Gongylonema pulchrum infection and esophageal squamous cell carcinoma in a 17-yr-old, female vari (Lemur macaco variegates). The lemur had lived in a German zoo and had a clinical history of dyspnea, vomiting, and anorexia. At necropsy, a whitish, soft, nodular, centrally necrotic mass was found in the caudal third of the esophagus. In addition, numerous intraepithelial nematodes (G. pulchrum) were observed in the entire esophagus. Results suggest a relation between infection with G. pulchrum and development of an esophageal squamous cell carcinoma.

The seroepidemiology of Lyme borreliosis in zoo animals in Germany.

We conducted the first seroepidemiological study to evaluate the exposure of zoo animals to Borrelia burgdorferi s.l. in German zoos and wildlife parks. A total of 1487 individuals representing 148 ungulate and carnivore species belonging to 19 families were examined using a non-species dependent ELISA. Specific antibodies were detected in 154 (10.4%) animals; 168 (11.3%) sera produced borderline results. The percentage of seropositive individuals was related to species and origin (zoo), and increased with age of the animals. Sex and season did not influence seroprevalence. Examination of 600 ticks (Ixodes ricinus; caught from vegetation in the zoos) by darkfield microscopy and indirect immunofluorescence technique revealed infection rates within the range typical for Central Europe. The results substantiate that there is an infection risk for zoo animals. A differential diagnosis of Lyme borreliosis should be taken into account in case of suspicious clinical symptoms and possible contact to ticks.

A new non-species dependent ELISA for detection of antibodies to Borrelia burgdorferi s. l. in zoo animals

Although Lyme borreliosis is regarded as one of the most important zoonotic diseases, in Europe very few research reports have documented examinations on free-ranging wild animal populations and no study on zoo animals has been published. One of the problems regarding the diagnosis of Lyme borreliosis in wild animals is often the lack of species specific secondary antibodies for serological tests. For our study on exposure of zoo animals to Borrelia (B.) burgdorferi s. l. and the occurrence of Lyme borreliosis in various German zoos, a non-species dependent ELISA was developed. Specific IgG antibodies against B. burgdorferi s. l. were detected by peroxidase labeled protein A or protein G conjugates. For this purpose, both conjugates were tested for their binding affinities to 160 different wild animal species representing 25 families and 7 orders. With 2 exceptions, all tested species reacted with either protein A or protein G, and 47 species reacted with both conjugates. In combination with an easy method for the long-term preservation of antigen-coated microtiter plates, the ELISA developed for this study could essentially facilitate serological examinations regarding Lyme borreliosis.in wild animal sera. In summary, the results indicate commercially available protein A and protein G conjugates as useful alternatives to species specific secondary antibodies in various diagnostic assays on sera of a wide range of wild mammals. Therefore, this should be considered more often as versatile diagnostic tools in wildlife studies.

Neospora caninum infection associated with stillbirths in captive antelopes ( Tragelaphus imberbis)

Neosporosis was diagnosed in full-term stillborn twin calves of captive antelopes ( Tragelaphus imberbis) in a German zoo. In both calves a multifocal non-suppurative encephalitis was present and infection with Neospora (N.) caninum was confirmed by foetal serology and PCR. N. caninum-DNA was detected in brain, heart, lung, liver and spleen of a third full-term stillborn calf. Histopathological lesions were absent in this calf and antibodies against N. caninum were not detected in pleural fluid. Immunohistochemistry failed to demonstrate N. caninum antigen in all three calves.

Genetic characterization of feline parvovirus sequences from various carnivores

Infections with viruses of the feline parvovirus subgroup such as feline panleukopenia virus (FPV), mink enteritis virus (MEV) and canine parvovirus (CPV-2) [together with its new antigenic types (CPV-2a, CPV-2b)] have been reported from several wild carnivore species. To examine the susceptibility of different species to the various parvoviruses and their antigenic types, samples from wild carnivores with acute parvovirus infections were collected. Viral DNA was amplified, and subsequently analysed, from faeces or formalin-fixed small intestines from an orphaned bat-eared fox (Otocyon megalotis), a free-ranging honey badger (Mellivora capensis), six captive cheetahs (Acinonyx jubatus), a captive Siberian tiger (Panthera tigris altaica) and a free-ranging African wild cat (Felis lybica). Parvovirus infection in bat-eared fox and honey badger was demonstrated for the first time. FPV-sequences were detected in tissues of the African wild cat and in faeces of one cheetah and the honey badger, whereas CPV-2b sequences were found in five cheetahs and the bat-eared fox. The Siberian tiger (from a German zoo) was infected with a CPV-type 2a virus. This distribution of feline parvovirus antigenic types in captive large cats suggests an interspecies transmission from domestic dogs. CPV-2 sequences were not detected in any of the specimens and no sequences with features intermediate between FPV and CPV were found in any of the animals examined.

Detection of equine herpesvirus types 2 and 5 (EHV-2 and EHV-5) in Przewalski's wild horses.

In blood samples of seven captive equid species from four German zoos EHV-1 specific antibodies were detected in 76% and EHV-4 specific antibodies in 73% of the 55 animals, whereas 93% were tested positive for EHV-2 and EHV-5, respectively. In only one blood sample from a Przewalski's wild horse EHV-4 DNA was amplified by PCR. From seven Przewalski's wild horses EHV-2, and from another one EHV-5 was isolated by cocultivation. The identity of the virus isolates was verified by PCR and restriction enzyme digestion.

On the diagnostics of Sarcocystis in cattle: sarcocysts of a species unusual for Bos taurus in a dwarf zebu

Sarcocysts from the musculature of a dwarf zebu born in a German zoo are described by light and transmission electron microscopy. In addition to the three named bovine Sarcocystis species ( Sarcocystis cruzi, S. hominis, and S. hirsuta) a fourth species was found which was not previously reported from cattle. It mostly resembles Sarcocystis gracilis Rátz, 1909 from roe deer.

A fatal infection in a bengal tiger resembling cytauxzoonosis in domestic cats

A young Bengal tiger born and kept in a German zoo had died of an unknown protozoal infection in 1984. Retrospective histological and electron microscopical examination of the organs showed the changes to be identical with those of cytauxzoonosis in domestic cats. This is the first report of fatal cytauxzoonosis in a tiger.

The Persian Fallow Deer

Discovered less than a hundred years ago, the Persian fallow deer Dama mesopotamica is in serious danger of becoming extinct. Mr. Pepper describes this large deer and the little that is known of its history, and urges the need for establishing a captive herd based on the two females in a German zoo, the only ones in captivity.