The paper by Hartup et al. (2001) on House Finch (Carpodacus mexicanus) conjunctivitis is an example of the rapid geographic spread that can result from disease emergence in naïve populations. That event was neither novel nor transient relative to its occurrence or effects. Disease emergence and reemergence are hallmarks of the latter part of the twentieth century (Center for Disease Control 1994, Levins et al. 1994, DaSilva and Laccarino 1999, Gratz 1999). Current examples involving domestic animals include the problems in Europe with bovine spongiform encephalopathy (BSE, or “mad cow disease”) (Brown 2001) and foot-and-mouth disease (FMD) (Kitching 1999). Human health has been affected by diseases caused by an array of viruses (Morse 1993, Nichol et al. 1993, Murphy and Nathanson 1994), bacteria (Dennis 1998, DaSilva and Laccarino 1999), rickettsia (Walker and Dumier 1996, Azad et al. 1997), protozoans (Tuerrant 1997, Saini et al. 2000), and metazoan parasites (Hildreth et al. 1991, Gubler 1998), as well as other causes. Acquired immune deficiency syndrome (AIDS) has received the most notoriety of those diseases (Hahn et al. 2000, Schwartlander et al. 2000). A similar pattern exists on a global scale for free-ranging wildlife populations (Table 1) (Friend 1994, 1995; Epstein et al. 1998, Daszak et al. 2000). However, in comparison to disease emergence affecting humans and domestic animals, response to emerging diseases of wildlife is generally superficial. We present concepts and data to support our contention that failure to adequately address disease emergence in free-ranging wildlife is resulting in a diminished capability to achieve and sustain desired geographic distributions and population abundance for species of wild birds, including some threatened and endangered avifauna.

For clarity, we define disease and disease emergence in the context of our use of those terms because they are the focus of our comments. Disease is any departure from health (Guralnik 1982); that is, dysfunction contributing to physiological, physical, reproductive, behavioral, or other impairment that reduces the probability of survival of individuals. If enough individuals are affected, the collective effects can reduce the sustainability of the population. Although disease can result from exposure to a wide variety of physical, chemical, and biological agents and other conditions, we focus this paper on microbes and parasites and to overt mortality caused by them. Thus, disease effects presented only represent the proverbial “tip of the iceberg” relative to the challenges wild avifauna face from disease. Our perspective of disease emergence expands the earlier definitions of emerging diseases by others (Centers for Disease Control and Prevention 1994, Morse 1995) to include all species. Our comments are defined by the context of disease occurrences that have increased within the past three decades, or threaten to increase in the near future relative to populations affected, geographic distribution, or magnitude of effects.

Disease Effects

Haldane (1949) cited by May (1988) stated “…infectious diseases have undoubtedly been the main agents of morbidity and mortality (and thus the dominant selective factors) in human populations at least for the past 10,000 years.” Support for the continued dominance of microbes and protozoan and metazoan parasites over humankind can be found in the writings of such notable scholars as McNeill (1976) and Lederberg (1988, 1993, 1997).

It is folly to think that wild birds and other wildlife are less susceptible to the influences of disease than humans and domestic animals. Nevertheless, “…ecologists and evolutionary biologists virtually ignored parasites [including microbes] until recently, even as a source of mortality for host species [wildlife] of primary interest” (Toft 1991). This is inconsistent with the viewpoints of Price (1980) that “…parasites affect the life and death of practically every other living organism;” and that

 More recent evaluations have clearly demonstrated that the emergence of avian malaria (Plasmodium relictum) and avian pox in Hawaii has regulated the geographic distribution and abundance of native Hawaiian forest birds on the Island of Hawaii (Warner 1968, van Riper et al. 1986, Atkinson et al. 1995). Others (Hudson 1986, Hudson and Dobson 1991) have shown that the parasite Trichostrongylus tenuis regulates population numbers of Red Grouse (Lagopus lagopus scoticus).

The biological significance of Mycoplasma gallisepticum infections in House Finches is equivocal. The Hartup et al. (2001) study did not detect gross differences in survival for diseased and normal finches. However, others have concluded that mycoplasmal conjunctivitis is a significant mortality factor for eastern populations of House Finches and is capable of causing population declines (Luttrell et al. 1998, Nolan et al. 1998, Hochachka and Dhondt 2000). Our purpose is not to debate the merits of different evaluations involving House Finch conjunctivitis. Instead, we note that this new disease for wild birds is a recent addition to the continuum of emerging diseases that are challenging the integrity of avian communities (Table 2).

It is noteworthy that disease challenges for avian communities are occurring in some of the more pristine ecosystems on Earth. For example, it has recently been stated that

Avian disease has also become an issue in Antarctic penguins. An infectious agent is suspected as the cause for mass mortality in Adelie Penguin (Pygoscelis adelaiae) chicks during the 1990s (Gardner et al. 1997a, b). More recently, antibodies to infectious bursal disease virus (IBDV), a pathogen of domestic chickens (Gallus domesticus), have been found in sera collected from wild Emperor (Aptenodytes forsteri) and Adelie penguins (Gardner et al. 1997a, b). Antibodies to IBDV have also been found in sera of Spectacled Eiders (Somateria fischeri) nesting in a remote area of western Alaska and in nesting Common Eiders (S. mollissima) and Herring Gulls (Larus argentatus) in the Baltic Sea (Hollmén et al. 2000).

Discussion

The importance of disease emergence for human society is of international scope and has stimulated the development of a wide variety of projects, collaborative efforts, scientific publications, and reports and other actions focused on combating that problem on behalf of human health. The economic effects of emerging diseases such as BSE and FMD are enormous and demand aggressive efforts to combat the emergence of not only those diseases, but also other emerging diseases that threaten the products of agriculture needed to provide food and fiber for a continually expanding human population and global economy.

We have provided testimony of the biological effects for avifauna of emerging disease, a situation that also extends to other species and groups of free-ranging wildlife. Our testimony deals only with the tip of the iceberg rather than the full effect of disease emergence. The true cost from disease is associated with the chronic attrition that occurs from the broad spectrum of diseases present, rather than from the high-visibility events that generate media attention and transient crisis responses from the conservation community. In addition, the magnitude of losses from some disease events can be of sufficient severity to challenge the ability of already diminished avian populations to overcome those single-event losses.

If disease emergence is not aggressively addressed on behalf of avifauna, the resulting effects will extend beyond the biological to social and economic losses as well. Consider for example the potential effects of significant reductions of scavenger species such as vultures in India and crows in the United States on the removal of carcasses; revenue lost from ecotourism and sport hunting due to declines in bird populations; and the influence on cultural relations and social needs of native peoples.

The primary causes for the emergence of diseases affecting humans are generally agreed upon and provide a focus for corrective actions (Centers for Disease Control and Prevention 1994, Morse 1995, Wilson 1995, DaSilva and Laccarino 1999). Many of the same factors are involved for disease emergence in free-ranging wildlife. However, neither the avian nor greater conservation communities are responding to disease emergence in a manner consistent with the biological significance of that threat, or with the ecological understanding of how to approach that problem. Successful disease prevention and control for free-ranging wildlife requires that the approaches used are based on the fact that disease is an outcome, rather than a cause. Environmental conditions are often a basic cause associated with disease emergence, persistence, and spread, and must be addressed to successfully combat disease. Thus, two of the barriers inhibiting adequate response to disease emergence in avian and other wildlife species are (1) the persistence of perspectives that disease is not a significant factor relative to the population dynamics of wild species; and (2) a tendency to focus on the affected species or the causative organism rather than on the affected environment.

Aldo Leopold (1933) spoke to the issue of disease control in his classic treatise Game Management by stating that treatment of afflicted animals was a recessive approach. He further noted that “…the real determinants of disease mortality are the environment and the population,” both of which are being “doctored daily, for better or for worse, by gun and axe, and by fire and plow.” The wisdom of Leopold (1933) regarding disease has even greater relevance today. Continued landscape changes due to demands for human living space and other basic needs will continue to alter the geographic distribution and aggregation of avifauna in a manner likely to facilitate disease emergence and spread among wild birds. Reductions in the habitat base for avian species due to landscape changes challenges the ability to sustain population levels that can withstand major effects from disease and still provide the collective values human society seeks from wild birds.

Human behavior is additionally an important barrier inhibiting adequate response to disease emergence in wild birds. This factor is complex and is beyond the scope of this paper, other than to note that major differences afforded disease-control efforts for humans and domestic animals are personal ownership and economic influences. Wildlife in the United States and in many other countries is held in trust by government agencies with stewardship responsibilities for various species. Therefore, the public does not have the same incentives that have resulted in the development of major programs and industries to address disease in humans and domestic animals. The common ownership of wildlife by others (government) contributes to a detached perspective and approach to disease that is, in part, a variation on The Tragedy of the Commons (Hardin 1968) and, in part, laissez-faire, except for transient crisis responses.

We have provided a perspective towards disease that may challenge personal viewpoints of others involved in the conservation of wild birds. Our intent is to stimulate reexamination of the importance of disease on behalf of our avian resources. We strongly believe that due to landscape changes that have already occurred, and those certain to occur in the near future, a proactive, rather than a reactive, approach towards disease is required to discharge our stewardship obligations. Approximately 40 to 50% of land on the Earth has been irreversibly transformed or degraded by human actions. An additional one-third of global land cover will be transformed over the next 100 years (Ayensu et al. 2000). Human-induced changes in biotic diversity and alterations in the structure and function of ecosystems are the two most dramatic ecological trends of the past century (Vitousek et al. 1997). The consequences of these changes are that society must now discharge a role of perpetual stewardship to maintain components and functions that once constituted the natural processes at the time Lack (1954, 1966) and others were making their judgments about the role of disease. Combating emerging disease has now become one of the adjustments that must be made to repair ecological integrity in a manner that sustains avian biodiversity and desired levels of avian populations.