Ebola virus as a zoonotic pathogen
The current Ebola virus outbreak in West Africa is very much on people’s minds as a story of human suffering and death, with nearly 15,000 Ebola cases reported from West Africa as of November. Ebola virus spreads rather slowly but causes a remarkably high fatality rate, with 50% or more of human cases ending in death. The current epidemic dwarfs the cumulative number of cases in previous localized outbreaks, motivating new research into vaccines, treatments, and efforts to slow Ebola spread. Promising signs of slowing transmission have emerged in recent weeks, but many experts predict that widespread vaccination will be needed to fully halt the epidemic. The social, political and economic impacts of the current Ebola virus epidemic will likely linger for years to come.
What many people do not realize is that humans are atypical hosts for Ebola virus, and the origin of this pathogen is far removed from cities, airports and hospitals, and reminds us of the connections between human and animal health. Ebola virus most commonly exists in and around the African rainforests in the Congo Basin, with previous outbreaks extending east to Uganda, north to Sudan and west to Gabon and the Ivory Coast. Other species have died from this virus: most notably, Ebola killed scores of chimpanzees and gorillas in recent decades. Estimates suggest that in one outbreak alone (2002-2003), thousands of gorillas died, and some researchers saw their entire study populations eliminated in a matter of weeks. Given that wild apes are already highly endangered and reproduce slowly, population recovery from Ebola outbreaks could take decades or longer. Other animals, including forest antelopes can also die from the virus. The routes of forest animal infection remain unclear, but wild bats are thought to be the likely natural reservoir for the virus, meaning they could carry and transmit the pathogen with little or no signs of illness. Further Ebola-wildlife connections are underscored by the fact that the butchering and consumption of wild animals, especially apes that had died from Ebola, can provide a clear route for entry into human populations. In David Quammen’s book Spillover, the author noted that wildlife deaths in surrounding forests were harbingers of outbreaks in human villages.
From our own experiences studying wildlife-pathogen interactions, including work on great apes in Africa, we think that animal ecology has much to contribute to efforts to predict the spread of Ebola virus and prevent future outbreaks. Here, we touch on three ways animal ecology can inform our understanding of Ebola virus dynamics, including studies of pathogen spread on great ape social networks, research regarding bats as reservoirs for Ebola and other deadly viruses, and new efforts for wildlife surveillance to predict Ebola outbreak risk in humans. We also note that the ongoing Ebola outbreak has dire consequences for efforts to conserve wildlife by curbing ecotourism and potentially increasing hunting pressure on already-imperiled species.
Social network studies and Ebola transmission in apes
Ebola virus transmits through close contact of body fluids, which means that host sociality can determine transmission dynamics within a population. The precise behaviors that transmit Ebola infections in wildlife are unknown, but the highly social nature of great apes could make them particularly vulnerable to outbreaks of Ebola virus and other socially-transmitted pathogens. During a 2003-2004 Ebola outbreak in the Odzala-Kokoua National Park in the Republic of Congo, one study found that gorillas living in social groups were twice as likely to become infected with Ebola as solitary males. Despite this difference, mortality rates across both solitary and social individuals were staggeringly high (77% – 97%). At the end of the outbreak, only 20 of the roughly 360 gorillas remained, underscoring the catastrophic effects of Ebola virus on wild ape demography. An important question is whether Ebola outbreaks impact ape social structure in ways that delay population recovery. A new study in Journal of Animal Ecology indicates that gorilla social structure is remarkably resilient following Ebola outbreaks. The study’s authors found that birth rates, as well as survival and social dynamics for the affected Odzala-Kokoua National Park population have since returned to their pre-Ebola state. However, there’s still a long road ahead. The population remains small and demographic models suggest that gorillas could require over 100 years to fully rebound from an Ebola outbreak.
Incorporating social behavior into infectious disease models can tell us how contagious pathogens are likely to spread throughout a population. A modeling study by Charlie Nunn and colleagues made the realistic assumption that, after a silverback gorilla dies of Ebola, females and juveniles quickly disperse to new groups. This means that Ebola virus might spread faster through populations of gorillas versus chimpanzees, because chimpanzees, which have multi-male multi-female communities, would be less likely to disperse after the death of a single individual. Additionally, social network analysis has been used to make predictions about which animals are likely to acquire an infection and which intervention methods might be most effective for preventing outbreaks. One recent study simulated the spread and control of Ebola virus (among other pathogens) in wild chimpanzee social networks. By comparing random vs. targeted vaccination strategies, Rushmore and colleagues showed that targeting the most connected individuals in a population for vaccination could prevent large outbreaks and substantially reduce the number of individuals requiring vaccination. Similar types of social network analysis could be applied to human outbreak data to assess the role of “superspreaders” in the current human Ebola outbreak, and to establish initial vaccine distribution strategies following the release of a human vaccine. Notably, network approaches have provided crucial insights towards the control of other human infectious diseases, including influenza, SARS and HIV/AIDS.
Bats as reservoirs for Ebola and other lethal pathogens
Ebola virus is one of many zoonotic pathogens to emerge and spread in human populations. Zoonotic diseases are caused by pathogens typically harbored by animals, and include diseases such as H5N1 and H1N1 influenza (originating in birds and swine), rabies (from carnivores and bats), Lyme disease (from white-footed mice) and West Nile fever (amplified by numerous wild bird species). Zoonotic diseases account for well over half of new and emerging diseases affecting humans. These diseases remind us that human activities such as agriculture, mining, forest clearing and bushmeat hunting are bringing people into closer contact with animal pathogens than ever before. How these pathogens shift from animals to humans, and why this seems to be happening more and more in recent years, is a topic of great concern.
Bats are the source for a disproportionate number of emerging zoonotic human infectious diseases, including SARS, Marburg (another filovirus like Ebola), Nipah, Hendra and rabies. A recent comparison of bats and rodents found that even though rodents as a group harbor more zoonotic pathogens than bats, after controlling for life history and ecological differences among species, bats harbored more zoonotic viruses on a per species basis than rodents. One reason for this could be the high level of spatial overlap among bat species, allowing for cross-species transmission of a diversity of pathogens. Other work suggests that owing to their high metabolic rates during flight, bats have a unique immune physiology that involves daily cycling between high and low temperatures (“flight as fever”), forcing the viruses that infect them to become more tolerant to fever responses. Yet another idea is that the high mobility of bats, combined with dense roosting aggregations leads to small world networks that can maximize pathogen transmission and support high viral diversity in wild bat populations.
Importantly, relatively little is known about the natural ecology of viruses in wild bats. There are practical limitations to studying bats: they are nocturnal, spend a great deal of time in flight, and roost in caves or other hidden areas, making them challenging to capture and observe visually. Overcoming these limitations is important, because understanding the mechanisms of pathogen persistence in bat populations, and effects of seasonality and environmental stressors on bat-pathogen transmission could be crucial for predicting human and livestock exposures. Beyond their role as reservoirs of zoonotic pathogens, bats are critically important in natural ecosystems, offering services in the form of pollination, seed dispersal and insect control. Therefore, efforts to minimize pathogen spread through culling bats are not to be encouraged, and in fact, some recent work indicates that culling bats to prevent disease exposures might do more harm than good.
Consequences of the Ebola epidemic for wildlife conservation
The current Ebola outbreak in West Africa is already having negative impacts on wildlife conservation as fear surrounding Ebola turns travelers away from ecotourism activities across Africa. Sadly, this drop-off is widespread – even affecting countries without any Ebola cases and thousands of miles away from the current outbreak. The drastic reduction in tourism dollars will likely result in decreased funds for wildlife conservation, including funds for park staff and ranger salaries. With less on-the-ground protection, many fear that this chain of events will ultimately increase poaching and weaken wildlife protection in regions most impacted by tourism declines.
Food insecurity in Ebola-hit West African countries could also affect West African wildlife. Quarantines and travel restrictions now limit the labour force leading to substantially reduced annual harvests. Border closings have severely decreased trade, threatening food supply and causing food prices to soar. Vincent Martin from FAO told Reuters reporters in a September 2014 news report “In the three countries severely affected by Ebola, the agriculture and food security situation is really deteriorating. People either cannot afford to buy food or it is not accessible anymore.” If the lack of food options translates into increased hunting, the problem could be two-fold. Additional hunting pressure on wildlife would exacerbate an already dire situation for many endangered wildlife species. Even though bushmeat hunting is common in many West African countries, additional reliance on forest animals for food (e.g., bats, primates) could intensify the chances of another zoonotic spillover event from wildlife into people. Thus, Ebola-linked food insecurity presents a clear risk for both conservation and human health, demonstrating the urgent need for campaigns that provide alternative food solutions and educate hunters about the dangers of bushmeat.
Ways moving forward: Ebola research at the animal interface
Animal ecology has much to contribute to future Ebola research. Increased knowledge about the ecology and behavior of natural reservoir species could be key to understanding the dynamics of Ebola transmission and predicting the risk of future outbreaks. Towards this end, several organizations are actively studying bats and other wildlife host species. FAO recently created a job position for a wildlife expert to examine links between wildlife, bush meat and Ebola. The EcoHealth Alliance is leading studies on bat ecology, physiology and immune defense to understand their role in shedding Ebola and other important emerging pathogens. Beyond the reservoirs, wildlife species (e.g., primates, duikers) infected with Ebola can transmit the virus to humans through close contact. Surveying great ape faeces for Ebola virus antibodies offers a unique way to non-invasively determine previous exposure and monitor great ape prevalence rates over time. While Ebola vaccines are not currently used in wild ape populations, a “conservation-oriented vaccine trial” recently showed a virus-like particle vaccine to be safe and immunogenic against Ebola virus in captive apes. Additionally, the Wildlife Conservation Society is working to develop methods for delivering an oral Ebola vaccine to wild great apes.
The current outbreak in West Africa is far from over, and it is clear that more volunteers and more funds are needed to bring the epidemic to a halt. After the outbreak subsides, it would serve us all – humans and wildlife – to keep the momentum going and to focus our energy on Ebola prevention. Wildlife and human outbreaks are tightly connected: not only do primate die-offs in the forest often precede human outbreaks in villages, but human contact with dying primates could provide a direct link for Ebola entry into human populations. Thus, increasing funding at the federal and global levels for research aimed at understanding the natural ecology of Ebola virus, and other zoonotic infectious diseases, will benefit both conservation and public health efforts.
Associate Editor Journal of Animal Ecology
Julie Rushmore, PhD
* Updated 5/12/14 16:10 GMT