By Peter Daszak

This article was first posted on The Scientist: The News Journal for the Life Scientist.

 

Sometime in the 1980s, the emerging infectious disease (EID) movement began. The "emerging" label had been used earlier, but a series of high-profile disease outbreaks in the 1980s, combined with perceived funding gaps, began to galvanize the field. A book by Richard Krause of the National Institutes of Health (Krause 1981) formed part of the initial thrust. Published in the same year as the recognition of AIDS, it commented on the alarming phenomenon of antibiotic-resistant microbes. Further threats surfaced: Legionnaire's disease, toxic shock syndrome, multiple-drug resistance in a host of important pathogens, Lyme disease, and others.

The year 1992 saw the publication of an Institute of Medicine treatise on emerging infections (Lederberg 1992), and a special section in Science talked about a "post-antimicrobial era," tuberculosis as a "reemergent killer," and the "crisis in antibiotic resistance." This was rapidly followed by Emerging Viruses by Stephen S. Morse of Rockefeller University (1993), and another Science section included a high-profile plea to close the surveillance gap for these EIDs (Berkelman 1994).

By the mid-1990s, a new Centers for Disease Control and Prevention (CDC) journal, Emerging Infectious Diseases (edited by Joseph E. McDade), a rash of popular books, and the continual flow of newly discovered pathogens and globally reemerging diseases firmly established the field.

The message reached Congress, which appropriated funds for public health surveillance, infrastructure to combat bioterrorism threats, and new approaches to outbreak investigation.

Now Wildlife

Now, some 20 years after the first rumblings of the EID threat, a growing interest in emerging diseases of wildlife is repeating the pattern. Wildlife EIDs are "one of the most significant, yet underestimated and underfunded, anthropogenic threats to biodiversity conservation," says Andrew A. Cunningham, a veterinarian pathologist at the Zoological Society of London. Cunningham, coauthor on a recent Science review that defines this group of diseases (Daszak 2000), has spent the last 15 years working on the role of diseases in conservation programs for captive and wild animals.

Cunningham is part of a group that recently described a fungal disease of amphibians, chytridiomycosis, which is causing die-offs in Australia and Central America (Berger 1998). Dramatic amphibian declines in these areas have included the extinction of the golden toad of Costa Rica and two species of gastric brooding frog (Rheobatrachus spp.) in Australia. While habitat loss and other factors are involved in amphibian declines elsewhere, the discovery of chytridiomycosis helps to explain the so-called "pristine rainforest declines" that have puzzled herpetologists. In a rare example of a conservation body (Environment Australia) funding disease investigations, veterinarian Lee Berger, working in virologist Alex D. Hyatt's lab at the Australian Animal Health Laboratory of the Commonwealth Scientific and Industrial Research Organization, first discovered the disease in 1997.

"One of our group's key roles is to identify the new and unusual," says Hyatt, codiscoverer of equine morbillivirus (Hendra virus) and other emerging Australian viruses. "We originally began characterizing iridoviruses from amphibians as part of a biocontrol program for the cane toad, and it's this work that put in place the infrastructure to look at diseases of amphibians."

But this previously unknown pathogen is simply the latest in a string of disease outbreaks that are changing the way conservationists view disease. This extensive EID list includes marine mammal morbillivirus diseases, mycoplasmal conjunctivitis in house finches, coral diseases, African wild dog rabies, and kangaroo blindness. An early wake-up call for the impact of wildlife EID came in 1985, with an epizootic of canine distemper in Park County, Wyoming. This viral disease of domestic dogs is unusual in its wide range of susceptible hosts, including -- dramatically in this case -- the black-footed ferret (Mustela nigripes). The black-footed ferret, once common on the prairies and badlands of the United States, is ideally suited to its habitat and solely dependent on prairie dogs as prey.

The gradual conversion of prairie to agriculture and destruction of prairie dog towns led to a unique situation in the 1970s: With only one small population of ferrets known in the wild and a handful in captivity, both of which rapidly died out, the species was considered extinct. Its rediscovery in 1981 led to a series of crucial events that culminated in the near actual extinction of the species. The first threat was an outbreak of sylvatic plague in 1985 in the prairie dog towns that supported the ferret populations. To maintain the prey base for the ferret, the largest non-public health, nonurban sylvatic plague control effort was conducted and the disease managed. As the planned development of a captive breeding program progressed, population surveys of the ferret revealed a drastic decline, and wild ferrets captured for breeding began to die of canine distemper.

The small population that survived the outbreak in the wild was considered insufficient to preserve the species, and the radical strategy to capture the whole remaining population for captive breeding began. The strategy of making a species temporarily extinct in the wild won through, with the first babies being born in 1987.

But the critics were harsh, according to Tom Thorne of the Wyoming Game and Fish Department and team leader of the management effort. "In my professional career I have never experienced pressure like that. We came extremely close to extinction in '85-'86, and criticism came from a multitude of angles. The discussion on whether to capture the remaining ferrets after we'd diagnosed canine distemper was particularly heated. Some groups had even argued that we should let the species become extinct."

Endangering Endangered Species

The lesson learned was that infectious diseases are a significant threat to the management of endangered species. Ongoing developments in host-parasite population biology bolstered this. Andy Dobson of Princeton University, working with models of host-parasite dynamics, has emphasized the importance of disease in conservation for the last 15 years. Building on developments in the epidemiology of human diseases, Dobson and others have shown that parasites are crucial in moderating animal populations and, in some circumstances, can have a devastating impact on small or fragmented populations.

"Parasites and infectious diseases are the forgotten half of biodiversity and have a significant impact on the way communities are structured and function," says Dobson. In the past, this impact has been underestimated or misjudged. "Despite a greater appreciation of the role parasites play in natural populations, there remains a confusion over how to manage for disease threats. For example, conservation biologists remain confused and overanxious that the potential benefits of corridors that link populations might act to aid in disease transmission," says Dobson.

Management may be crucial: Dobson has shown that one of the most significant disease threats to conservation is the emergence of "spill-over" pathogens (pathogens that move from domestic animals to wildlife populations). Here, the continued presence of domestic animals can maintain disease transmission even when the endangered species is driven to extinction. Furthermore, the role of spill-over and cointroduction of disease with translocations of domestic and wild animals ("pathogen pollution" -- Daszak 2000) implicates humans as the major drivers of wildlife disease emergence.

But if these diseases were emerging in parallel with the same environmental changes that drive EIDs of humans, why the delay in labeling them emerging? Perhaps the time lag between the human EID and wildlife EID movements reflects natural anthropocentric concerns? Cunningham thinks this is short sighted. "Consider the major emerging disease threats to humans: AIDS, Hantavirus, Lyme disease, Influenza, Ebola virus--they're all either zoonotic or have resulted from pathogens switching hosts from wild animal reservoirs."

Domestic animals also play a role here. The emergence of Nipah virus in pig farmers and abattoir workers of Malaysia and Singapore in 1999 is just such a case. The virus is thought to originate from fruitbat hosts that infected pigs, where it is amplified in the respiratory tract and transmitted to humans as an aerosol during coughing. Changes in Malaysian pig farming practices may have driven this event, in the same way that domestic pigs play a role in emergence of new strains of influenza virus. This may be the rub with wildlife EIDs, that anthropogenic environmental changes affecting wildlife disease ecology may increase the threat of emerging zoonoses.

Funding Gap

Despite this dual threat to conservation and public health, wildlife diseases have in the past fallen between the cracks between the funding agencies. Bob McLean, director of the U.S. Geological Survey National Wildlife Health Center (essentially the CDC equivalent for wildlife diseases), cites a "funding gap between wildlife and human emerging diseases that needs to be closed." In the past, the National Science Foundation has been reluctant to support disease studies, NIH to support nonhuman disease work, and other government agencies to deal with nondomestic animal issues.

However, the massive interest in the global crisis of amphibian declines may be changing the horizon for wildlife disease funding. As part of the fallout from the discovery of chytridiomycosis, James P. Collins of Arizona State University, working with Berger, Hyatt, and a group of co-principal investigators, was recently awarded a $2.9 million National Science Foundation grant to study the host-pathogen biology of amphibian diseases (NSF: Integrated Research Challenges in Environmental Biology). The next step is to convince conservation biologists of the importance of wildlife EIDs, which still receive short shrift in the planning of captive breeding programs (Daszak 2000).

According to Dobson, "In terms of population regulation, parasites are probably much more powerful than predators, so assuming we can manage biodiversity and ignore pathogens is simply naïve."

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Peter Daszak (Daszak@uga.edu) is a research scientist at the Institute of Ecology and Department of Botany, University of Georgia, working on amphibian chytridiomycosis and other emerging wildlife diseases.

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References

R.M. Krause, "The restless tide: the persistent challenge of the microbial world," Washington, D.C., National Foundation for Infectious Diseases, 1981.

J. Lederberg et al., "Emerging infections. microbial threats to health in the United States," Institute of Medicine, Washington, D.C., National Academy Press, 1992.

S.S. Morse, Emerging Viruses, New York, Oxford University Press, 1993.

R.L. Berkelman et al., "Infectious disease surveillance: a crumbling foundation," Science, 264: 368-70, Apr. 15, 1994.

P. Daszak et al., "Emerging infectious diseases of wildlife--threats to biodiversity and human health," Science, 287, 443-9, Jan. 21, 2000.

L. Berger et al., "Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America," Proceedings of the National Academy of Sciences, 95:9031-6, 1998.

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