Buffalo, cow, man, and mycobacterium – inside the microbial exchange in Tanzania

-David Wolking

“For a time, all was bountiful in the land, but then drought came. No rain fell for months, and it became drier and drier, hotter and hotter. The stream stopped flowing. The water hole turned first to mud and then to dry, cracked earth.  One by one, the animals slowly left or starved until no one was left…”  - Lion, Chameleon and Chicken, A Gogo Bantu Folktale from Tanzania

Change is coming.  It was first recognized in the landscape, when the Great Ruaha River in Tanzania, the lifeblood of a land where miombo woodlands of Southern Africa blend into the Sudanian Acacia-Commiphora zone of East Africa, slowly dried up.  That seasonal drying, along with other changes in the landscape, agricultural intensification, deforestation, extension of grazing lands into protected areas, may be the source of other less noticeable changes, microscopic changes. 

In the Ruaha ecosystem, home to Tanzania’s largest national park and protected area, researchers with the Health for Animals and Livelihood Improvement (HALI) project are investigating how these changes at both the landscape and microscopic level affect the health of wildlife, domestic animal and human communities.  In a new publication released in June, HALI researchers report the detection of Mycobacterium bovis, a bacterium that can cause tuberculosis in animals and humans, in 8 species of wildlife, including the first detection of M. bovisin 3 new species: Kirk’s Dik Dik, vervet monkeys, and yellow baboons.  In addition, the team detected M. bovis in African buffalo inside Ruaha National Park, the first confirmed buffalo infection in Tanzania. 

“Although we anticipated we might find bovine tuberculosis in species closely related to cattle, like buffalo, the documentation of infection in 8 different species occupying different ecological niches both within and outside wildlife protected areas was unexpected and suggests the existence of a complex wildlife-livestock transmission cycle.”   - Dr. Deana Clifford, founding HALI project coordinator and wildlife veterinarian for the California Department of Fish and Wildlife

The microbial market place

In Ruaha, M. bovis is not a stranger, at least to domestic animals and their caretakers.  There is wide spread bovine tuberculosis (bTB) in cattle in the area, and as a zoonotic pathogen, tuberculosis may also affect human communities.  The HALI team looked at bTB in livestock, and observing the land-use changes in the Ruaha area, hypothesized that tuberculosis was also infecting wildlife populations. Livestock herds frequently share grazing lands, foraging areas, and water holes with wildlife, and as a result may swap microbes and parasites with other species through environmental contamination, or in the case of M. bovis, even through aerosols, through a cough or a sneeze.   

From 2006-2010, HALI worked with game scouts employed by the Community Wildlife Management Areas bordering Ruaha National Park, hunting companies, Park staff, and village networks to obtain tissue samples from hunter-killed, depredated animals (animals killed for causing crop damage in fields), and carcasses.  Two HALI game scouts, Coaster and Shukuru, social network nodes for news of animal deaths, would hear about a kill or a carcass and bicycle out into the bush to collect tissue samples and GPS the location.  Samples were then sent to the project laboratory at the Sokoine University of Agriculture, a center of excellence for molecular diagnostics and tuberculosis detection. 

The team collected tissues from 149 animals of 30 different species, the majority (69%) collected outside protected areas in village lands.  Sokoine University cultured the samples for mycobacterium and used PCR assays to detect M. bovis.  Positive samples were spoligotyped (a technique used to delineate mycobacterium species and distinguish unique strains), and they found that M. bovis isolates from infected wildlife were identical to the strains of M. bovis found in livestock herds.  In an area where human settlements, activities and livestock grazing areas are pushing further and further into wildlife habitat, the animals are trading.  They just don’t know it, and it is possible that this microbial trade could be making them sick.

Although the team’s findings suggest that livestock herds and wildlife are sharing M. bovis, it is not clear who started it.  With M. bovis-infected African buffalo herd inside Ruaha National Park, a herd that encounters livestock rarely, and little to no bovine tuberculosis control among livestock in the area, it is possible M. bovis is maintained in the ecosystem by both wildlife and livestock.  Because the team found M. bovis in wildlife species occupying very different ecological niches, from buffalo to other ungulates like dik diks and impala all the way up the evolutionary chain to our primate cousins vervet monkey and yellow baboon, it appears that M. bovis is settled down and is planning to stay.  Buffalo in particular are a major maintenance host for bovine tuberculosis in Africa, once bTB is established in a free-ranging herd, that herd can sustain infection without repeated trade of M. bovis with other animals like livestock.  In other words, M. bovis becomes a resident, and since buffalo are often preyed on or scavenged by carnivores and other wildlife, the microbe can spillover to other species in the ecosystem, even humans like hunters.  In Tanzania wild meat is usually smoked or roasted, nyama choma, but before you have meat you must have a butcher, and field dressing a carcass without appropriate hygiene and sanitation measures can be a risk for exposure to bTB.

Regulating the exchange?

Now that M. bovis seems to be a microbial resident in both livestock and wildlife in the area, how do you control its spread?  The HALI team identify several management options in the article, but for a pathogen intrinsically linked to multiple species in different ecological niches, these management options require an ecosystem-based approach linking livestock and human health interventions with conservation and development goals. 

  1. The Ruaha River is drying, and if that continues, the health of the entire ecosystem will suffer.  The good news is that continuing and enhancing current conservation efforts to improve hydrologic flow, prevent bank erosion and improve water quality will increase water abundance, allowing more spaces for animals to drink and limiting interspecies contact. 
  2. Ecological restoration and conservation efforts should be expanded to preserve remaining wildlife habitat and help address wildlife forays into village land, farms, and grazing areas.  
  3. The veterinary community can target test of cattle and wildlife for bTB and a range of other diseases in shared grazing lands to identify areas or sites with increased spillover risk, and work to better understand livestock grazing strategies, locations, and sites to improve planning for pasture access and livestock production.  
  4. Finally, and perhaps most critical is improving livelihoods.  Increasing income to rural residents through poverty reduction programs, increased market access, training and education can reduce reliance on natural resources for survival, the driving force behind land use change that may be undermining ecological health and driving M.bovis and other zoonotic disease transmission dynamics.

In this approach, conservation is linked to development – with more water from a flowing river, better grazing opportunities, healthier livestock, and improved livelihoods, the pressure for livestock and wildlife to share resources, interact, and exchange microbes can be reduced, and the animals, along with their caretakers, will not have to slowly leave the water holes until no one is left.

 Read the full article “Tuberculosis infection from wildlife in the Ruaha ecosystem Tanzania: implications for wildlife, domestic animals, and human health” at Epidemiology & Infections, or contact the author, Dr. Deana Clifford (dlclifford@ucdavis.edu)