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Increased Avian Diseases With Habitat Change


by
Milton Friend
National Biological Service
Changes in disease patterns and trends reflect changing relationships between the affected species (host) and the causes of disease (agent). Host-agent interactions are closely linked to environmental factors that either enhance or reduce the potential for disease to occur. As a result, wildlife disease patterns and trends are, to a substantial extent, indicators of environmental quality and changing host-agent interactions within the environment being evaluated. The types, distribution, and frequency of diseases causing major avian die-offs have changed greatly during the 20th century. Too little is known to assess the changes of most avian diseases that result in chronic attrition rather than major die-offs, or about those that affect reproductive success, reduce body condition, or affect survival in other indirect ways. Nevertheless, the changing patterns and trends in highly visible avian diseases provide notice of problems needing attention.
Information on the status of disease in wild birds was obtained from National Wildlife Health Center (NWHC) evaluations of the cause of death for more than 30,000 carcasses from across the United States during the past two decades, reports of avian mortality received from collaborators, the scientific literature, and NWHC field investigations of bird mortality. Comprehensive assessments of causes of wild bird mortality, magnitude of losses, and geographic distribution of specific diseases are not possible from these data, although we can identify general relationships for waterfowl and some other species.

Changes in Disease Patterns
The occurrence of disease involves three factors: a susceptible host, presence of an agent capable of causing disease, and suitable environmental conditions for contact between the host and agent in a manner that results in disease. Environment is often the dominant factor in this relationship (Fig. 1).

Fig. 1. Common factors required for disease to occur. Environmental factors greatly influence occurrence of disease by changing the amount and type of host-agent interactions.
Avian Botulism
The most dramatic example of geographic expansion of a noninfectious indigenous disease is avian botulism, caused by the bacterium Clostridium botulinum. In 1914 a Bureau of Biological Survey researcher began investigating catastrophic die-offs that had begun in 1910 and in which millions of waterbirds along the Great Salt Lake, Utah, had died. Later studies revealed that avian botulism was responsible for those die-offs. Historically, avian botulism was referred to as "western duck disease" because of its rather limited geographical distribution of occurrence (Kalmbach and Gunderson 1934; Fig. 2).
Avian botulism now occurs all over the United States (Fig. 2) and in many other countries as well. Because of the visibility of massive die-offs, avian botulism is probably the best-documented nonhunting waterfowl mortality (Stout and Cornwell 1976). The continued reporting of avian botulism die-offs since the early 1900's makes researchers suspect that much of the disease's geographic expansion is of recent origin. Also, most (15 of 21) initial outbreaks of avian botulism in countries other than in North America have occurred since 1970.

Fig. 2. Known distribution of "western duck sickness" (avian botulism) in North America, 1934 (Kalmback and Gunderson 1934), and from 1975 to 1993.
Avian Cholera
Avian cholera, caused by the bacterium Pasteurella multocida, has been recognized as an important infectious disease of domestic poultry in the United States since at least 1867 (Rhoades and Rimler 1991). Therefore, it is noteworthy that a 1930 evaluation of the status of waterfowl commented on the lack of documentation of avian cholera in wild waterfowl (Phillips and Lincoln 1930). In 1944, however, the disease was documented in wild waterfowl in the United States (Quortrup et al. 1946). Limited geographical expansion of avian cholera in wild waterfowl occurred during the 1940's and 1950's, and sporadic occurrences were documented at a few new locations during the 1960's (Fig. 3). By the end of the 1960's, though, avian cholera was reported as established in the Central and Pacific flyways. Outbreaks in the Mississippi Flyway were unusual, and only two outbreaks had occurred in the Atlantic Flyway. With the exception of a single instance during the breeding season, outbreaks occurred in winter (Stout and Cornwell 1976). During the 1970's, avian cholera became established as a major cause of waterfowl mortality in all four flyways within the United States and as a recurring cause of waterfowl mortality in Canada (Fig. 3). Geographic expansion of die-off locations continues, and outbreaks now occur during all seasons of the year (Friend 1987).

Fig. 3. Geographic distribution of avian cholera in wild waterfowl within the United States, before 1960 (first outbreak in 1944), during the 1960's, and after 1970, when disease spread (National Wildlife Health Center files).
Duck Plague
Fig. 4. Number of duck plague outbreaks in waterfowl in the United States, by flyway (suspect cases have pathology consistent with duck plague but lack isolation of the virus to confirm the diagnosis), and total number of outbreaks by decade.
Duck plague is another emerging disease of North American waterfowl. This herpesvirus infection first appeared on the North American continent in 1967 when it caused large-scale losses in the domestic duck industry and losses of a small number of wild waterfowl (Leibovitz and Hwang 1968). The first major die-off involving wild waterfowl occurred during January 1973 at the Lake Andes National Wildlife Refuge in South Dakota (Friend and Pearson 1973). Duck plague has expanded throughout North America since the initial outbreak, along with an increasing number of outbreaks in each decade (Fig. 4). Nearly all occurrences of duck plague have involved nonmigratory waterfowl (captive, tame, and resident waterfowl that do not undergo traditional migratory movements). A February 1994 outbreak in the Finger Lakes region of New York State involving mallards (Anas platyrhynchos) and American black ducks (A. rubripes) is the first major outbreak involving migratory waterfowl since the January 1973 Lake Andes outbreak.
Other Diseases
Other diseases affecting wild birds are newly recognized, are occurring with increasing frequency, or have expanded their geographic occurrence during the 20th century. Changes in disease patterns in wild birds are consistent with such changes in other species, including humans, and reflect environmental changes that foster the eruption of disease and the spread of infectious agents (Tables 1 and 2). Table 1. Changes in patterns of diseases affecting wildlife.
Disease Cause Species First occurrence in species
 Major expansion Current status
      Year Location    
Avian botulism Bacteria Waterbirds 1910 UT 1970's Widespread; major problem
Avian cholera Bacteria Waterbirds 1944 TX,CA 1970's Widespread; major problem
Duck plague Virus Waterfowl 1967 NY 1990's Expanding
Avian pox Virus Waterfowl 1978 AK 1990's Expanding
    Bald eagle 1978 AK 1980's Stable
Salmonellosis Bacteria Songbirds Historical MA 1980's Major problem of urban environments (bird feeders)
Canine parvovirus Virus Wild carnivores 1978 TX 1980's Widely distributed
Canine heartworm Parasite Wild carnivores Historical Southeastern U.S. 1960's Continuing spread northward from southeastern U.S.
Fibropapilloma Unknown Marine turtles 1938 FL 1980's Major geographic spread; increased frequency of occurrence

Magnitude of Losses
Changes over time in the frequency of wild bird die-offs and losses from disease cannot be precisely determined because no appropriate data base exists. Also, changes in surveillance and reporting confounds interpretation of existing data. Nevertheless, with the exception of rare catastrophic events, available information suggests that substantially greater numbers of wild birds are dying from diseases now than in earlier periods of the 20th century. The yearly average of 55,066 reported waterfowl deaths from disease during 1930-64 (Friend 1992) has been exceeded or nearly exceeded by single events since 1964. Several disease outbreaks, for example, have killed between 25,000 and 100,000 waterfowl; die-offs of 5,000 to 10,000 waterfowl are common. Table 2. Emerging diseases of wildlife.
Disease Cause Species Occurrence in species
 Ecosystem type
      Year Location  
Inclusion body disease of cranes Virus Exotic cranes 1978 WI Terrestrial (captive-propagation flock)
Eastern equine encephalitis Virus Whooping crane 1984 MD Terrestrial (captive-propagation flock)
Mycotoxicosis (Trichothecenes) Fungus Sandhill crane 1982 TX Agricultural (peanuts)
Coccidioidomycosis Fungus California sea otter 1976 CA Marine
Upper respiratory disease syndrome Bacteria? Desert tortoise 1987 NV Desert
Avian tuberculosis Bacteria Whooping crane 1982 CO Mixed; wetlands and agricultural fields
Neoplasia Unknown Mississippi sandhill crane 1975 MS Mixed; wetlands and agricultural fields
Velogenic Newcastle disease Virus Double-crested cormorants 1990
1992		 Canada
Great Lakes		 Aquatic
Woodcock reovirus Virus American woodcock 1989 NJ Forest
Seal plague Virus Marine mammals 1987
1988
1990		 Russia
Europe
U.S.		 Inland sea
Marine
Marine
Fig. 5. Number of wild bird die-off events listed in the National Wildlife Health Center data base, 1981-93.
The number of avian die-offs in the NWHC data base with reported mortality of 1,000 or more is sufficient to support the contention of increased numbers of birds dying from disease compared with the period before 1965. The annual number of avian die-offs is an additional indicator of the relatively high frequency of avian disease during the late part of the 20th century (Fig. 5).

Habitat and Human Interactions

Causes of major bird die-offs during the past decade and their geographic distribution are shown in Table 3. Composite data indicate a relation between bird concentrations and the occurrences of avian disease. Those states with large concentrations of migratory birds on migrational staging and wintering areas tend to have the most disease outbreaks. Preliminary assessments suggest that habitat quantity and quality are important factors in this relation. Table 3. Geographic distribution of major (>500 birds) die-offs of wild birds by cause, 1983-93.
Disease Cause States (number of events)
    <5 5-9 >9
Aspergillosis Fungus CO(1), VT(1)    
Avian botulism Bacteria AR(1), CO(2), KS(2), LA(2), MD(2) MI(1), MN(1), NM(1), NY(1), OH(2) OK(1), OR(4), WI(3) ID(7) NB(5) NV(5) CA(80), MT(14) ND(25), SD(14) UT(11)
Avian cholera Bacteria CO(3), IA(4), ID(1), ME(1), MN(3) OR(1), NM(4), NV(1), SD(1) MO(5) CA(21), NB(13) TX(18)
Chlamydiosis Bacteria ND(1)    
Erysipelas Bacteria MD(1)    
Mycotoxicosis Fungus TX(3)    
Myocardiopathy Unknown CA(1)    
Necrotic enteritis Bacteria? ND(3), SD(1)    
Newcastle disease Virus MN(1), ND(2), SD(1)    
Salmonellosis Bacteria CA(2), VT(1), WA(1)    
Toxicosis Environmental contaminants AZ(1), CA(2), IL(1), NV(1), VA(1)    
Trichomoniasis Parasite CA(1), NM(1)    
Wetland losses, for example, are well documented and clearly a contributing factor in the spread of avian cholera. California, a focal point for the occurrence and spread of avian cholera in waterfowl, lost 91% of its historical wetland acreage by 1980 (Dahl 1990). A similar situation exists in the Rainwater Basin of Nebraska where avian cholera first appeared in waterfowl in 1975; this area has subsequently become a focal point for spread to other areas. About 90% of historical wetland acreage within the Rainwater Basin has been lost (Farrar 1980). The association between wetland losses and spread of infectious disease is due to the interactive factors that aid disease transmission.
Habitat (environment) loss often results in crowding birds on the remaining habitat, thereby enhancing the potential for transmission of infectious agents. Movement patterns of infected birds can spread the disease to other locations and populations and help establish the disease as a recurring problem.
High concentrations of birds for prolonged periods of time on limited habitat often degrade the quality of habitat through fecal contamination and damage to vegetation. Deposition and survival of pathogenic parasites and microbes are aided by such environmental conditions and can result in enhanced disease maintenance and spread.
Habitat degradation due to human-caused factors is also important. For example, although the bacterium responsible for avian botulism is a common inhabitant of wetland substrates, the production of the botulinum toxin that causes botulism is dependent on specific environmental factors such as ambient temperature, pH, oxygen depletion, and other factors (Locke and Friend 1987). Discharges into wetlands of sewage, agricultural chemicals, and poultry wastes from factories have frequently been associated with eruptions of avian botulism, although cause and effect relationships have not been clearly established.

Prevention of Avian Diseases
Diseases affecting wild birds can be prevented and controlled despite the challenges of dealing with species and populations that are often highly mobile and spend much or all of their lives in remote areas.
Methodical monitoring and surveillance programs are needed to provide early detection of emerging problems so that intervention can begin when problems are most manageable. Accurate diagnostic assessments of the causes of morbidity and mortality are essential for focusing control efforts. Also, greater emphasis is needed on studies of disease ecology to provide enhanced understanding of host-agent-environment relationships for specific diseases. This information serves to identify weak links where disease-control and prevention efforts will be most effective. Molecular biology and the associated field of genetic engineering will greatly assist these efforts.
For further information:
Milton Friend
National Biological Service
National Wildlife Health Center
6006 Schroeder Rd.
Madison, WI 53711
References
Dahl, T.E. 1990. Wetland losses in the United States 1780's to 1980's. U.S. Fish and Wildlife Service, Washington, DC. 13 pp.

Farrar, J. 1980. The Rainwater Basin . . . Nebraska's vanishing wetlands. Nebraska Game and Parks Commission, Lincoln. 15 pp.

Friend, M. 1987. Avian cholera. Pages 69-82 in M. Friend and C.J. Laitman, eds. Field guide to wildlife diseases. Vol. 1. General field procedures and diseases of migratory birds. U.S. Fish and Wildlife Service Resour. Publ. 167.

Friend, M. 1992. Environmental influences on major diseases. Transactions of the North American Wildlife and Natural Resour. Conference 57:517-525.

Friend, M., and G.L. Pearson. 1973. Duck plague: the present situation. Proceedings of the Western Association of State Game and Fish Commissioners 53:315-325.

Kalmbach, E.R., and M.F. Gunderson. 1934. Western duck sickness: a form of botulism. U.S. Department of Agriculture Tech. Bull. 411. 81 pp.

 Leibovitz, L., and J. Hwang. 1968. Duck plague on the American continent. Avian Diseases 12:361-378.

Locke, L.N., and M. Friend. 1987. Avian botulism. Pages 83-93 in M. Friend and C.J. Laitman, eds. Field guide to wildlife diseases. Vol. 1. General field procedures and diseases of migratory birds. U.S. Fish and Wildlife Service Resour. Publ. 167.

Phillips, J.G., and F.C. Lincoln. 1930. American waterfowl. Houghton Mifflin Company, Cambridge, MA. 312 pp.

Quortrup, E.R., F.B. Queen, and L.T. Merovka. 1946. An outbreak of pasteurellosis in wild ducks. Journal of the American Veterinary Medical Association 108:94-100.

Rhoades, K.R., and R.B. Rimler. 1991. Pasteurellosis. Pages 145-162 in B.W. Calnek, H.J. Barnes, C.W. Beard, W.H. Reid, and H.W. Yoder, Jr., eds. Diseases of poultry. 9th ed. Iowa State University Press, Ames.

Stout, I. J., and G.W. Cornwell. 1976. Nonhunting mortality of fledged North American waterfowl. Journal of Wildlife Management 40:681-693.


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