Abstract

In December 1996, a family group of ten western lowland gorillas (Gorilla gorilla gorilla) was transported by air from Apenheul Primate Park, Apeldoorn, The Netherlands to Taronga Zoo, Sydney, Australia. The group was comprised of a 19-yr-old silverback (“Kibabu”), a 24-yr-old female (“Mouila”), its 3-yr-old male (“Haoko”) and 7-wk-old male (“Shabani”) offspring, a 17-yr-old female (“Kriba”), its 3-yr-old female (“Kijivu”) and 3-mo-old female (“Safiri”) offspring, a 15-yr-old female (“Frala”), its 5-yr-old female (“Shinda”) and 2-yr-old female (“Anguka”) offspring. An eleventh animal in the group, the 7-yr-old female daughter of “Kriba” (“Joas”) was crated at the same time as the others, but was transported to Basel Zoo, Switzerland. Although many gorillas have been transported around the world, by sea, air and land, there is no record in the readily available literature of the transportation of ten gorillas by air over such a great distance.

With this in mind, a great deal of planning and preparation was put into the shipment. Planning for the crating procedure focused on a strategy aimed at not using chemical restraint. This involved the construction of a “U” shaped race with an offshoot to which the crate was attached. The order of crating was also significant and was based on hierarchy, personalities and family units within the group. In some cases, manipulation of lighting was used to encourage gorillas to move from one area to another.² Only the last animal, the 3-yr-old female, required immobilization with ketamine at 10 mg/kg for crating.

Five days prior to transport the group was started on a course of the neuroleptic drug, zuclopenthixol (Cisordinol, Lundbeck, Denmark) to reduce anxiety. This was continued throughout the journey and ceased four days after arrival. Dose rates used ranged from 0.10–0.36 mg/kg p.o., b.i.d. and was varied according to individual behavior and stage of the journey (Table 2).

Table 2. Doses of zuclopenthixol used in western lowland gorillas transported from The Netherlands to Australia

Day 7 to day 9=period of crating and transport
*Estimated weights

Zuclopenthixol is a potent neuroleptic of the thioxanthene series with general properties similar to the phenothiazine tranquillizers.³ It is available as an oral formulation in Europe only and an injectable (Clopixol-acuphase, Clopixol depot, Lundbeck) elsewhere.

Apart from some anxiety during the crating procedure, the animals were calm and traveled well, maintaining good appetites, particularly during periods that one would expect to be disturbing for the animals (e.g., loading and unloading the airplane, take-offs and landings).

Careful attention was paid to crate design.² The group traveled in four crates, with the silverback on its own, the females in crates with a division to separate mother with baby from its juvenile offspring. The animals traveled in the cargo section of a Boeing 747-400, 7 pallet. Three keepers and a veterinarian accompanied and attended the animals during the flight.

After arrival in Sydney, the animals were placed in quarantine for 30 days. In order to comply with Australian Quarantine Inspection Service (AQIS) requirements for tuberculosis testing, six animals were anaesthetized 10 days after arrival. Exemption from testing was sought for the two females with babies, as it was considered that the procedure would put the babies at risk during and after the anaesthesia of their mothers. This was granted on the basis that Apenheul Primate Park had never had a case of tuberculosis and that the other six gorillas tested negative for tuberculosis.

The six gorillas were anaesthetized in one morning. This was achieved with two teams of veterinarians working concurrently. Each animal was anaesthetized using 4 mg/kg of tiletamine and zolazepam (Zoletil 100, Virbac, Australia) administered by remote injection (Telinject, Germany). Anaesthesia was maintained using isoflurane (Forthane, Abbott, Australia) in oxygen via an endotracheal tube. Electrocardiogram, heart rate, respiratory rate, blood pressure, and oxygen saturation of hemoglobin were monitored and recorded (Dinamap plus, Critikon, Australia).

A detailed health screen was carried out on each animal and included physical examination, comparative intra-dermal tuberculin test, gamma interferon assay for tuberculosis, thoracic radiographs, hematology, biochemistry, immune testing, viral serology and fecal parasitology and bacterial culture (Tables 1 and 3 through 7). Each animal was vaccinated against tetanus (Tet-Tox, CSL, Australia) and implanted with an identification transponder (Trovan, AEG/Telefunken, Germany).

Table 1. Viral serology for six western lowland gorillas at Taronga Zoo, Australia

EMC: Encephalomyocarditis virus detected by virus neutralization test
HBsAg: Hepatitis B surface antigen detected by EIA/ELISA
HCV: Hepatitis C Virus tested by 3rd generation EIA
HTLV-1: Human T cell leukemic virus, detected by EIA/ELISA
HIV-1/HIV-2: Human immunodeficiency virus 1 and 2 detected by EIA/ELISA
HBc: Hepatitis B core antigen detected by MEIA
HBs: Hepatitis B surface antibody detected by MEIA
CMV: Cytomegalovirus detected by particle agglutination
HAV: Hepatitis A virus detected by MEIA
HIV-1/HIV-2 WB: Human immunodeficiency virus 1 and 2 detected by Western blot
HSV IgG: Herpes simplex virus - complement fixation test for total antibody titre
Rubella IgG: Complement fixation test for total antibody titre
Q fever phase 2 titre: Complement fixation test for total antibody titre

Table 3. Hematology and serum biochemistry of six western lowland gorillas anaesthetized with tiletamine and zolazepam at Taronga Zoo, Australia

Table 4. Immunology testing of six western lowland gorillas at Taronga Zoo, Australia

Table 5. Tuberculosis testing and thoracic radiographs of six western lowland gorillas at Taronga Zoo, Australia

TB test:
Bovine: 0.1 ml bovine PPD (1 mg/ml) (CSL, Australia) intradermally into the left upper eyelid. Read at 72 hr.
Avian: 0.1 ml avian PPD (25 000 U/ml) (CSL, Australia) intradermally into right upper eyelid. Read at 72 hr.

Table 6. Gamma interferon assay (QuantiFERON-TB, CSL, Australia) for tuberculosis in six western lowland gorillas at Taronga Zoo, Australia

HuPPD=Mycobacterium tuberculosis
AvPPD=M. avium
BoPPD=M. bovis
Nil Ag=negative control
Mitogen=positive control

Table 7. Fecal parasitology and culture results for six western lowland gorillas from feces collected at time of anaesthesia

In three subsequent cultures of group fecal samples, neither the Campylobacter nor Shigella were isolated.

Most results fell within or close to published reference ranges for gorillas (where available). The 15-yr-old female and its daughter were mildly anaemic (normocytic, normochromic). The 3-yr-old male, 3-yr-old female, and the 5-yr-old female had elevated serum alkaline phosphatase, most likely due to bone growth in these young animals. The 19-yr-old silverback had slight thrombocytopenia and mildly elevated immunoglobulin. No reference ranges were available for lymphocyte phenotyping in gorillas and most results fell outside those reported for humans.

All six gorillas were positive for cytomegalovirus, which is common in many primate species and always asymptomatic unless the animal is immunosuppressed.¹ Four of the six gorillas were positive for herpes simplex virus. In serological surveys of gorillas, the prevalence of herpesvirus antibodies is over 60%. Clinical disease is rare in gorillas but is similar to humans with facial and oral ulcers and chickenpox. Genital lesions have not been reported.¹

Three gorillas had positive readings to avian PPD after 72 hr. As all were negative to bovine PPD, and showed no immunity to mycobacterial antigens on gamma interferon, it is most likely that this was a non-specific reaction, perhaps to atypical mycobacteria in their gastrointestinal tracts, rather than to tuberculous mycobacteria.

Although the gamma interferon assay used at the time of testing (Quanti FERON-TB, CSL, Australia) had not been validated for use in nonhuman primates, the results in these gorillas were consistent with those seen in people that do not have any form of tuberculosis. The assay has now been validated for use in nonhuman primates and is marketed as Primagam (CSL Veterinary, Australia). None of the gorillas showed evidence of immunity to mycobacterial antigens in vitro, which is strong evidence for freedom from infection with either Mycobacterium tuberculosis, M. avium or M. bovis. The zero reaction to the positive control (mitogen) for “Anguka” merely indicated a poor immune response in vitro, which may be due to the animal’s age (2 yr) and therefore an immature immune system.

Acknowledgments

The author thanks Apenheul Primate Park; Drs. Hulst, Higgins, Woods, Ralph, Keogh; Ms. Libby Kartzoff and Mr. Glenn Smith; the Institute of Laboratory Medicine; St. Vincent’s Hospital; NSW Red Cross Blood Transfusion service; Westmead Institute of Clinical Pathology and Medical Research; and NSW Agriculture Regional Veterinary Laboratory for their assistance with this work, and Vanessa Di Giglio for preparation of this manuscript.

Literature Cited

1.  Janssen DL. 1993. Diseases of great apes. In: Fowler ME, ed. Zoo and Wild Animal Medicine, Current Therapy 3. W.B. Saunders Co., Philadelphia, Pp. 334–338.

2.  Kartzoff L. 1997. The successful transportation of ten western lowland gorillas (Gorilla gorilla gorilla) from Apenheul Primate Park, the Netherlands to Taronga Zoo, Australia. In: Australasian Region of Zoological Parks & Aquaria, Annual Proceedings.

3.  Swan GE. 1993. Drugs used for immobilisation, capture and translocation of wild animals. In: McKenzie AA, ed. Capture and Care Manual: Capture, Care, Accommodation and Transportation of Wild African Animals. Wildlife Decision Support Services CC, South Africa, Pp. 2–64.