Sudden Great Ape Die-Off in the Periphery of the Dja Biosphere Reserve

Great ape die-offs have been occurring throughout Central Africa, with the Ebola filovirus as one of the main causes. We here report the first documented case of such an outbreak for Cameroon, where sympatric gorilla and chimpanzee populations were affected by Anthrax.
In November 2001, the Royal Zoological Society of Antwerp (RZSA-CRC) set up a new great ape research site on the unprotected periphery of the Dja Biosphere Reserve, through the integrated conservation and development project Projet Grands Singes (PGS; Dupain 2001). The site is delimited on the south by the Dja River. Preliminary surveys indicated great ape densities of 2.1 gorillas/km² and 0.9 chimpanzees/km² (Dupain et al. in preparation). Since then, research on great ape socio-ecology has been going on continuously (PGS 2005).
In November 2004, when following the previous day's traces of a group of gorillas, we found the fresh carcass of an adult female gorilla, her 2-week-old son lying alive and whining close by. No injury was apparent. The carcass was situated barely 20 m from the group's nest site (5 nests) in young secondary vegetation. Two of the nests were elevated (height 4 m and 1.5 m) in lianas on saplings; the others were ground nests. We feared a possible Ebola outbreak, contacted the Yaoundé-based PGS office and set up basic quarantine. Nonetheless, the following day, we rescued the infant who had survived the night, taking all possible basic precautions.
The gorilla group was tracked for the next two days, and we noticed some unusual behaviour that we want to describe here. On day 1, they had made their nests (6 ground nests and 1 tree nest, height 7 m) at just 150 m distance from the infant, and had then continued moving south for over 2 km while feeding regularly on several Marantaceae species, Aframomum, Aframomum fruits, Uapaca, Nauclea and mushrooms. During a feeding session (16.10 h), when some of the gorillas were in the Nauclea trees and others on the ground, 20 consecutive "whaa-hoo" calls were heard and some gorillas tapped the soil with their hands or feet. We were at a distance of approximately 50 m and had approached the group quietly, so we had no reason to assume the gorillas had noticed us. Between 16.24 and 16.35 h, still on the same spot, we witnessed several high-pitched vocalisations ("whii-hoo" once, "whiièh-whiièh" 3 times). The experienced trackers confirmed that it was unusual to hear gorillas vocalise that much, and they had also never heard these specific vocalisations before, which were clearly distinct from the "wraagh" alarm call, barks, screams or grunts. At 17.05 h we left the group still at that same spot. On day 2, we followed the tracks again for about 1 km, and found that the gorillas had spent the night in tree nests (n = 6, average height 8 m) and elevated nests (on saplings and lianas, n = 4, average height 2 m); this might be due to the high elephant activity in that area. (These observed fluctuating differences in nest group size often occur in our site and suggests sub-grouping). We finally lost track of the group that same evening as they continued heading south toward the Dja River. We never observed this nesting and travelling behaviour before and never heard such vocalisations; we think that it may be related to the loss of a group member.
A tissue sample was taken from the gorilla body by a Cameroonian Wildlife Aid Foundation (CWAF) vet. We limited personal contact with the infant as much as possible to one caretaker, improvised diapers, and fed him powdered milk. The baby gorilla spent almost 3 weeks in our base camp and regained strength quickly when adequate nutrition was brought in.
By mid-December, during routine research activities, 2 chimpanzees were found dead; they were located by their decay smell. Neither showed signs of injuries. One was lying on its back in a ground nest, as part of a ground nest group of at least 6 individuals in swamp vegetation. The team was evacuated and our baby gorilla was taken to CWAF quarantine. At the request of the Ministry of Forestry and Fauna (Cameroon), a team was organized jointly by the Great Ape Health Monitoring Unit (GAHMU, Max Planck Institute, Germany), Centre International de Recherches Medicales de Franceville (CIRMF, Gabon), Limbe Wildlife Centre (Cameroon), Centre Pasteur (Yaounde), John Hopkins Institute (Yaounde), Wildlife Conservation Society, Institut Recherche Developpement, The Last Great Ape Organization (LAGA) and PGS to collect samples from the three carcasses.
Research was re-activated on 6 January, 2005. On 7 January another dead chimpanzee, again showing no obvious injuries, was discovered. Once again samples were taken. All samples were sent to CIRMF and GAHMU on 17 January for analysis.
After CIRMF had excluded Ebola as the cause of the mortalities, samples from all 4 apes were sent to GAHMU for analysis, and tested positive for Anthrax (Leendertz et al., submitted). Several other animals (incl. forest duiker, pangolin and guenon), but no more apes as yet, have been found dead in the forest in February and March. Since April, no more carcasses have been discovered. The Conservator of the Dja Biosphere Reserve, H. Nlegue, visited the nearby villages to inform them of the possible risks, and provided information on what to do. Based on nest counts on the line transects over the months concerned, we estimate great ape densities to have dropped by approximately 50% (Guislain et al. in preparation).
Anthrax is caused by the presence (in a sufficient amount) of spores of Bacillus anthracis in the body. The spores can stay dormant in the soil for many years. As a result, Anthrax is generally reported in and transmitted by cattle (through faeces, their decomposing bodies or the eating of their meat). At present, it is uncertain how the apes in our research site were infected.
As the Projet Grands Singes is the only research project studying great apes in the northern periphery of the Dja Biosphere Reserve, it is unknown whether the Anthrax die-off occurred in a bigger part of the surrounding forest. Anthrax could be identified as the cause of mortality for all great ape carcasses that were found in our research site (i.e. between the end of November 2004 and the beginning of January 2005).
By the end of February, the baby gorilla was transferred to CWAF's Mefou Sanctuary, close to Yaoundé. He had recovered well and will be joining the social group of gorillas there in the future.

Patrick Guislain and Jef Dupain

We would like to thank MINFoF, MINRESI, the Service de la Con-ser-vation de la Réserve du Dja and the International NGOs for their support and encouragement to keep on monitoring this remarkable great ape population. PGS is currently seeking the necessary funding to continue monitoring large mammals and great apes in this non-protected area.

This is not the first time that great apes were infected with Anthrax; previously, in a series of sudden chimpanzee deaths 2001-2002 in the Taï National Park, Ivory Coast, Anthrax was con-firmed as the cause of death. At least 6 chimpanzees had died from the disease there (Nature 430, 2004, pp. 451-452).

References
Dupain, J. 2001. Conservation of Great Apes on the Periphery of the Dja Reserve. Gorilla Journal 23, 18-20
Dupain, J. et al. (in preparation) Prospection for the set up of a great ape research- and conservation project on the northern periphery of the Dja Faunal Reserve - Cameroon
Guislain, P. et al. (in preparation) Monitoring rapid changes in populations: a case study of Anthrax epidemiological outbreak in gorillas and chimpanzees (Cameroon)
Leendertz, F. H. et al. Anthrax joins Ebola in threatening Central African great apes. Submitted to Emerging Infectious Diseases.
Projet Grands Singes, 2005. Projet Grands Singes 2001-2005. Internal report.

Patrick Guislain studied psychology in Leuven. He has worked in Projet Grands Singes since 2001. He is doing a study on ecological determinants in habitat use of chimpanzees and gorillas. Currently he is linked to the Centre for Research and Conservation of the Zoo of Antwerp.
Jef Dupain works for the African Wildlife Foundation-DRC. He is the coordinator of the Landscape Maringa Lopori Wamba within CARPE-CBFP.

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