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Felicia Keesing, Richard S. Ostfeld, and Valerie T. Eviner
PATHOGENS ARE UBIQUITOUS. We are all familiar with the cold viruses that give us sniffles, coughs, and aches, and with the more frightening pathogens that cause diseases such as AIDS, malaria, and tuberculosis, which kill millions of people each year. But pathogens affect much more than our own health. Farmers struggle with fungi that attack their crops, managers of endangered species worry about the potential impact of an epidemic on the fragile populations under their stewardship, and tourists find their favorite snorkeling destinations devastated by coral bleaching diseases. Because of concerns like these, enormous quantities of energy and resources are deployed each year in the diagnosis and treatment of infectious diseases of humans, nonhuman animals, and plants. Yet annihilation of harmful pathogens is an unrealistic goal in most cases, and many other pathogens play critical positive roles in ecosystems, from recycling nutrients to increasing biological diversity. We are just beginning to recognize the degree to which pathogens, and the diseases they cause, are embedded within ecological systems.
Infectious diseases necessarily involve interactions among at least two species, the pathogen and the host species it infects. For many pathogens, such as the virus that causes avian flu, the fungus that causes soybean rust, and the protist that causes African sleeping sickness, more than one species can serve as a host. And many pathogens are transmitted from host to host by at least one species of vector, such as a mosquito, an aphid, or a tick. Understanding the dynamics of any partic u lar disease system, then, involves understanding at best a simple but more often a complex system of interactions among the organisms most directly involved in disease transmission. Ecologists would seem to be natural allies of a suite of health specialists, including epidemiologists, physicians, veterinarians, and agricultural scientists.
With notable exceptions, however, ecologists have not traditionally studied infectious diseases or have considered disease outbreaks as disturbances rather than inherent parts of the ecosystem. Similarly, most biomedical scientists have not considered the broader ecological contexts of disease. But the need to integrate these disciplines has become increasingly apparent in the past several years as we face a surge of emerging or reemerging infections, including West Nile virus encephalitis, sudden oak death, severe acute respiratory syndrome (SARS), monkeypox, and new types of avian infl uenza. Typically, a newly emerging infectious disease is recognized from a cluster of mysterious disease cases arising in a host population, followed by the elimination of well-known pathogens as potential causes, and fi nally the identifi cation of a new pathogen, or perhaps of an old one outside its known range. Remedial action is then undertaken to prevent further spread of the disease. When the pathogen is specialized—that is, largely restricted to one host species—and is transmitted directly between individuals, the standard public health arsenal to battle disease—quarantine, vaccination, emergency public education—is usually effective. SARS is a recent example. However, when the pathogen is more generalized, infecting multiple host species, including asymptomatic reservoirs, or when it is transmitted indirectly, such as by vectors or through environmental contact, then remedial action is much more problematic, and outbreaks may be followed by poorly contained spread, often with devastating consequences. Recent examples of poorly contained outbreaks include West Nile virus in humans, horses, and wild birds; sudden oak death in live oaks and tanoaks; Ebola virus in humans and apes; Lyme disease in humans; hantavirus pulmonary syndrome in humans; and various transmissible spongiform encephalopathies in livestock, wildlife, and humans. Failure of the standard biomedical arsenal in the cases of some human, nonhuman animal, and plant diseases may be largely a consequence of the ecological complexity involved in the evolution, transmission, and maintenance of these pathogens in nature.
Other lines of evidence also suggest that a more ecological perspective would greatly enhance our understanding and management of diseases. For example, more than 75% of emerging human pathogens are zoonotic (Taylor et al. 2001), that is, they are transmitted to humans from other animals. This observation suggests that a focus on the ecological interactions between wildlife hosts and zoonotic pathogens would be fruitful. Climate change has been associated with an increase in the frequency, distribution, and severity of many infectious diseases worldwide (Harvell et al. 2002), demonstrating ecological impacts on pathogen dynamics. And the rapid spread throughout Eurasia and Africa of the H5N1 strain of avian flu virus highlights just how much we need to know about bird migration patterns to develop appropriate management strategies for a potential human pandemic (Olsen et al. 2006). Some recent studies attest to the ability of ecological approaches to inform disease prevention and management. For example, the number of Lyme disease cases can be predicted almost two years in advance simply by monitoring annual acorn production (Ostfeld et al. 2006), allowing early, targeted public warnings. As another example, planting a diversity of rice strains rather than a monoculture has been shown to increase yields and reduce rates of infection with fungal rice blast in China (Zhu et al. 2000). More and more case studies like these are being published every year.
There are, in our view, two pressing needs if we are to improve our ability to predict the occurrence, dynamics, and consequences of infectious diseases. The first and most obvious need is to forge stronger alliances between ecologists and the traditional infectious disease specialists. Biomedical, veterinary, and agricultural scientists are well equipped to track infectious disease in populations and to treat and attempt to prevent disease in individual patients or populations. The power of these disciplines to improve the quality of life for people and other animals is enormous. Nevertheless, these disciplines often are not well equipped to anticipate disease outbreaks or to track the consequences of diseases beyond direct effects on victim populations. We see a strong role for ecologists in both these endeavors. Assembling the conceptual expertise is only part of the challenge, however: disease biologists from all disciplines need to work together more effectively to integrate knowledge of the functioning of ecological systems with knowledge of pathogens, cells, tissues, and immune systems and to develop effective management strategies based on this integration.
The second need is to identify the general ecological principles that underlie the dynamics of disease systems. Case studies now exist in sufficient number to allow the vigorous pursuit of conceptual syntheses. Such syntheses would provide a crucial unification of many disparate diseases and provide guidance for researchers attacking new disease systems. We know, for example, that some hosts are more efficient at transmitting partic u lar pathogens than others, but what generalities, if any, can be made about the role of host diversity in disease transmission? Habitat fragmentation has been shown to affect the transmission of malaria in Brazil (Vittor et al. 2006), Lyme disease in New York and New England (Allan et al. 2003; Brownstein et al. 2005), and hantavirus in Panama, but do we know enough to be able to predict the impact of habitat fragmentation—and perhaps other forms of habitat alteration— on other diseases? Are some types of pathogens more likely than others to affect ecosystem functioning, and similarly, are some ecosystems more vulnerable to the impacts of pathogens? Under what conditions do infectious diseases alter the functioning of ecological systems in desirable ways, by, for example, increasing the cycling rates of nutrients or increasing biological diversity?
This book attempts both to develop conceptual frameworks and to more fully integrate ecology with traditional disease biology. We have invited outstanding scientists and educators to provide conceptual syntheses of their areas of expertise. We have organized these efforts into three main sections. The first focuses on the effects of ecosystems, in the broadest sense, on infectious diseases, the second on the effects of infectious diseases on ecosystems, and the third on management and applications using these ideas. In an effort to foster the developing dialogue among scientific specialties, we have included contributions from ecologists, biomedical scientists, agricultural scientists, and veterinarians.
The contributions in this book exhibit a three-pronged conceptual approach. They articulate the generalities emerging from the increasing number of case studies appearing in the scientific literature, raise specific questions to guide future studies, and demonstrate both the challenge and the potential for ecologists and other disease biologists to work together. Owing to increased interest, particularly on the part of young scientists, and to rising levels of funding, opportunities to study the ecol ogy of infectious disease are increasing. From higher agricultural yields to more diverse animal communities to reduced human suffering and mortality, we have much to gain from the marriage of ecology and disease biology.
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