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Introduction
Bacterial diseases are among the foremost causes of single and multiple cases of morbidity and mortality in wild bird populations. In waterfowl, it is estimated that approximately 20 million birds die from non-hunting mortality every year and that diseases make up about 88% of the total non-hunting mortality studied among fledged North American waterfowl (1). Bacterial diseases may be of particular significance where a population represents an endangered or threatened species. Disease may either act as a direct cause of mortality, or an indirect cause whereby the host is immunocompromised, and thus fitness and survival are decreased, ultimately threatening the population (2). Additionally, wild birds may act as reservoirs for the infection of humans, domestic animals including livestock, and other species of wildlife. In the past, most of our knowledge of avian disease has stemmed from studies on poultry; however, relevant data on infection and disease in wild birds is becoming increasingly available (2). This paper will attempt to overview the most significant known bacterial infectious agents of free-living birds around the world, notably those of special significance to veterinary medicine and human health. These agents include Salmonella species, Clostridium botulinum, Mycoplasma species, Pasteurella multocida, and Mycobacterium species. Other important bacteria that will be briefly discussed include Escherichia coli, Chlamydia psittaci, Yersinia species, Erysipelothrix rhusiopathiae, Reimerella anatipestifer, Clostridium perfringens, Clostridium colinum, Francisella tularensis, and Staphylococcus aureus. In addition, bacteria such as Campylobacter jejuni may be carried by healthy birds which could contribute to water supply contamination, and subsequent human disease (3,4)
Salmonella
Species of the genus Salmonella are the causative organisms of the economically important poultry diseases Pullorum disease (S. pullorum) and fowl typhoid (S. gallinarum), both of which may also inflict wild birds, although wild birds are not known reservoirs for the organisms (5). However, wild birds are commonly infected by paratyphoid forms of Salmonella, notably S. typhimurium, which is becoming an increasingly common agent of illness and death in wild birds (5). Paratyphoid salmonellosis may vary from a mild enteritis to a systemic disease, and is a common cause of disease and death in recently imported and transported birds (6).
Salmonella infections are most often contracted by wild birds via food and water that may be contaminated with feces, as well as through direct contact with infected birds, animals, and insects (5). Salmonella is an environmentally persistent pathogen, and individually infected birds may harbour it commensally and thus act as reservoirs for the organism, shedding it into their environment for up to months (5,7,8).
Salmonella species are widely distributed in the environment and thus their prevalence often reflects the degree of environmental contamination (9). For example, Monaghan et al. (10) isolated 23 serotypes of Salmonella from gulls, with S. virchow and S. typhimurium being the most common. These species are often isolated from environmental sources. In addition, Quessy and Messier (9) found 10 Salmonella serotypes in the feces of 8.5% of sampled gulls, with birds that fed at refuse sites having the greatest levels of the bacterium. In a study by White and Forrester (11), antibiotic resistant Salmonella were found in double-crested cormorants and common loons in the Tampa Bay area of Florida. Isolates in the cormorants included S. agona, S. typhimurium, and S. infantis, all of which the birds likely acquired from contaminated feeding areas.
Salmonella infection and mortality has been found in a wide variety of avian species including gulls, terns, and passerines which congregate at bird feeders; waterfowl such as herons, egrets, geese, cormorants, swans, coots, and cranes; and raptorial species such as owls, eagles, falcons, and hawks (5). Salmonellosis due to paratyphoid serotypes is becoming increasingly prevalent among wild birds in a variety of habitats worldwide, and has the potential to reach all levels of the food web. Salmonellosis has even been introduced into remote bird populations such as Antarctic penguins and skua (5). This disease is rapidly emerging among songbirds in both urban and suburban environments, and thus potentially poses a great risk to human health. Salmonellosis is one of the most common causes of food-borne disease, notably acute enteritis, in humans (5). Birds such as gulls, which commonly feed in contaminated waterways, are a significant threat to human health through pollution of water storage reservoirs (12,13) or through infection of farm animals (14,15). Monaghan et al. (10) found similar Salmonella serotypes in gulls and humans, with S. typhimurium and S. virchow being amongst the most common in both groups; incidentally, these serotypes are most commonly isolated from environmental sources. Zoonotic infection in humans often occurs through maintenance of contaminated bird feeders (16,17) or through infection of domestic animals which may consequently pass on the infection to their owners or other animals (17,18). In 1999, an outbreak of S. typhimurium infection in cats and humans occurred, and was specifically associated with the wild finch species, Carduelis flammea and C. spinus, which spread the disease at feeders in gardens (18).
Clostridium botulinum
Botulism, also known as Western duck sickness, is one of the main natural causes of mortality in waterfowl, particularly in North America. Millions of waterfowl die each year from Clostridium botulinum infection, while many other species of wild birds, as well as domestic fowl, can also be affected (19). Botulinum type C is most commonly associated with disease in waterfowl and other avian species. Spores of Clostridium are hardy and may survive many years in the environment, provided conditions suitable for germination are present (20). Various species of birds are suspected of disseminating C. botulinum in their body excretions, with the toxin taken into exposed animals via the oral route (21). Kalmbach and Gunderson (22) suggested that birds may carry C. botulinum type C from an epizootic area into a previously uncontaminated one. Carcasses of infected birds may also present a hazard to predators and scavengers (23), and live and dead invertebrates may additionally provide a medium for pathogen growth, as well as dispersal (23,24). Poultry farms and operations experiencing botulism may contaminate soils, water sources, and feeds by discharging waste in an economic but unsanitary manner (25).
Feeding habits tend to be the most important factor in the susceptibility of an avian species to botulism, with carnivorous, omnivorous, and carrion-eating birds being most often affected (25). Kalmbach and Gunderson (22) provided an almost complete list of species of susceptible birds, with the pintail duck being the most frequently involved species among the 69 noted. By the end of 1984, 117 species of birds in 22 families were believed to have been affected by type C botulism (23). Only 3 endangered species of birds: the peregrine falcon, the brown pelican and the bald eagle are known to have developed botulism in the wild (National Wildlife Health Laboratory, U.S.A., unpublished observations). Type C botulism can occur in humans, although fully substantiated reports are lacking (24).
Mycoplasma
In recent years, an important emerging disease of wild birds is mycoplasmosis, notably caused by the bacterium Mycoplasma gallisepticum. Mycoplasmosis first occurred extensively in the late winter of 1994, causing severe conjunctivitis in house finches in the Washington D.C. area (26,27). Since then, the disease has spread rapidly throughout the eastern range of the house finch (27), and other wild bird species such as the American goldfinch, purple finch and pine grosbeaks have been found to be susceptible (28,29). The disease continues to spread westward into new areas where it has not been established (30). House finches are highly gregarious species, and their use of backyard feeders facilitates transmission of the pathogen between individuals (27). Infected finches are then thought to be responsible for spreading this disease over a wide geographic area since they move between local bird feeders and to distant locations during their migration. In poultry, mycoplasmas such as M. gallisepticum and M. synoviae can cause severe clinical disease and result in significant commercial losses (31). With the 1994 outbreak of mycoplasmosis in the house finch, concern has arisen that wild birds may act as reservoirs for infection in poultry, and thus contribute significantly to the epidemiology of this disease. Molecular studies, however, indicate that the strain of M. gallisepticum that infects wild birds such as the house finch differs from the strain implicated in disease in domestic poultry (32). However, the strain in finches may still infect and cause a mild infection in poultry (33). Poultry farms provide an ideal location for the feeding and nesting activities of house finches and other free-living passerines. This may prove to be a problem in the future control of this pathogen, and bird feeders which attract seed-eating passerines should be located away from poultry houses (32).
In addition, M. gallisepticum has a high host range in other species of wild birds. For example, studies of mycoplasmosis in Spain have resulted in isolation of M. gallisepticum from species such as free-ranging peregrine falcons, and a yellow-naped Amazon parrot (5). Falconiformes (34), Passeriformes, and Psittaciformes (35) have all been found susceptible to M. gallisepticum. Furthermore, the mycoplasmal species M. anatis has been found in major groups of wild birds: Falconiformes, Gruiformes, Anseriformes, Ciconiiformes, and Charadriiformes (36), thus demonstrating the ability of a single pathogenic strain to infect different avian groups and facilitate interspecies transmission. Mycoplasmas are generally considered host-specific and wild birds are not considered to have any involvement in human disease.
Pasteurella multocida
Avian cholera is a contagious disease which is caused by infection with the bacterium Pasteurella multocida. Several subspecies of P. multocida have been proposed, as well as at least 16 different serotypes, which are then further differentiated. Infection may be acute or chronic, with the agent probably entering the tissues of birds through the mucous membranes of the pharynx, upper air passages, membranes of the eye, or cuts and abrasions in the skin. A primary source of infection is environmental contamination from diseased birds. A variety of species of animals may carry P. multocida; however, types of P. multocida that are found in most mammals do not generally cause disease in birds (37).
Over 100 species of wild birds are known to be naturally infected with this pathogen, with waterbirds most often involved in major outbreaks of avian cholera due to their gregarious nature and the long-term environmental persistence of this pathogen (5). It is proposed that migratory birds such as snow geese (38,39,40) may act as chronic disease carriers, thereby continuing the chain of infection in waterfowl as well as other species; for example, to raptors that prey on waterfowl or scavenger species such as crows and gulls (5). A gyrfalcon (Falco rusticolus) was reported to have died from P. multocida of somatic serotype 1 after eating avian cholera infected ducks (38,39,41). A study by Samuel et al. (42) found that avian cholera has become endemic in Banks Island (Northwest Territories, Canada) snow geese, and this population may play an important role in transmitting this disease to other waterbirds, especially in wintering areas where many species are concentrated.
Wild birds living in or around farms could be a reservoir for P. multocida infection, and migratory birds have previously been reported as a source of fowl cholera (38,43,44). In a study by Peterson et al. (45), an isolate recovered from an outbreak of fowl cholera in wild birds including eiders, cormorants, oyster-catchers, and gulls was found to be highly virulent for turkeys, partridges, and pheasants, while chickens were found to be much more resistant. Avian cholera may represent an important threat to endangered avian species, particularly due to the increasing number of avian cholera outbreaks, and the expanding geographical distribution of this disease, notably in the United States of America and Canada. Avian cholera is not considered high risk for humans because of differences in species susceptibility to different strains of the bacterium; however, isolated infections may occur (5).
Mycobacterium avium
Tuberculosis, caused by Mycobacterium avium or other species of myco- bacteria, has been implicated as a cause of disease in individual birds of many species, most often waterfowl and seabirds which may become infected through contaminated sewage effluent (46). M. avium is generally transmitted by direct contact with infected birds, ingestion of contaminated feed and water, or contact with a contaminated environment (5). At least 20 different types of M. avium exist; however, only 3 are known to cause disease in birds. Tuberculosis has been known to affect waterfowl in the Western USA as early as 1941 (40). MacNeill and Barnard (47) reported the disease in 0.6% of 636 free-flying birds in British Columbia. Smit et al. (48) diagnosed tuberculosis in 2.4% of 288 waterfowl found dead in the Netherlands. In Kenya, an epizootic of tuberculosis in free-ranging lesser flamingos occurred due to contamination of their feeding algae by large numbers of the bacterium (49). M. avium is also existent in species including house sparrows and starlings that live in close association with livestock, and in scavenging and raptorial species (5). Prevalence of tuberculosis among whooping cranes is the highest among any wild birds species; for example, approximately 39% of the Western United States of America populations of free-ranging whooping cranes necropsied at the National Wildlife Health Centre had been infected with avian tuberculosis. This high prevalence in whooping cranes may be due to the fact that M. avium that is shed by disease carriers may survive in the environment for a long time and whooping cranes may repeatedly use infected sites, and that this species may just have a high susceptibility to avian tuberculosis (5).
In domestic poultry, tuberculosis is prevalent, being worldwide in distribution, and stemming mainly from fecal contamination of the environment. Interchange of tuberculosis between poultry and free-living birds is likely, and wild birds are often implicated as a potential source of infection for domestic flocks (50). Recent molecular studies have also shown that M. avium can potentially be transmitted between birds and pigs. Humans, though quite resistant, may become infected by M. avium (5). In addition, cattle may develop M. avium subspecies paratuberculosis infection, otherwise known as “Johne’s Disease”, and birds such as crows and rooks, and possibly, wood pigeons (Columbus palumbus) may act as carriers (51,52). Parrots, macaws, and other large perching birds are also susceptible to human and bovine types of tuberculosis bacilli (5,52).
Escherichia coli
Colibacilliosis is an infection caused by Escherichia coli, and is occasionally implicated in the illness and death of wild birds. The presence of E. coli in the environment is an indicator of fecal contamination and potential transmission (53). E. coli is a normal component of intestinal tract flora, but may infect the respiratory tract of birds causing chronic respiratory disease, particularly when in conjunction with infection by other pathogens (5). Among wild birds, E. coli has been found to cause infection in Anseriformes, Galliformes, Falconiformes, Passeriformes, Psittaciformes, and Sphenisciformes (54). Furthermore, a study by Morishita et al. (53) found that free-living passerines such as the European starling, house sparrow, and house finch can serve as a source of E. coli infection to other birds and mammals. However, avian strains from waterfowl and pigeons may serve as possible sources of genes for antimicrobial drug resistance, and Shiga toxin variants, respectively (55,56). Shiga toxin producing E. coli can cause a broad spectrum of diseases ranging from diarrhoea to haemorrhagic colitis, and sometimes haemolytic uremic syndrome in humans (56).
Chlamydia psittaci
Chlamydia psittaci is the causative organism of chlamydiosis (psittacosis, ornithosis), and has been reported from at least 159 species of wild birds in 20 orders, but most isolations have been made from 6 groups of birds (5). Psittacines are most commonly identified with this disease, particularly caged birds, and waterfowl, herons, and pigeons are the most commonly infected in North America. Chlamydia also occasionally infects gulls and terns, shorebirds, songbirds, and upland gamebirds (5). The organism is shed in nasal secretions and feces, and transmission probably occurs from inhalation of infected dust (57). Certain species of healthy birds may shed Chlamydia, such as tits (58). Large scale mortalities of birds have occurred due to this pathogen; for example, in white-winged doves in Texas (59), and in several hundred wild California gulls and ring-billed gulls (60). Chlamydiosis can be a serious human health problem, particularly infecting those who work with birds (5).
Erysipelothrix rhusiopathiae
Erysipelothrix rhusiopathiae is the causative agent of erysipelas, a disease best-known in domestic animals, particularly turkeys and swine. However, erysipelas has been documented in wild birds, including waterfowl, which may acquire the causative organism through ingestion or breaks in the skin, particularly during periods of susceptibility such as environmental stress and food shortages (61). Erysipelothrix may be present in the slime bodies of fish and crustaceans, with infection in waterbirds occurring through ingestion of a fish meal. Infection may also occur through a wound. Jensen and Cotter (62) reported an epizootic among waterbirds on Great Salt Lake, Utah, with eared grebes accounting for at least 99% of the mortality. Erysipelas has also been diagnosed in waterfowl, herring gulls, and brown pelicans in North America. Other susceptible free-ranging birds include hawks, crows, raven, wood pigeon, starling, doves, finches, and European black bird. Humans may be infected with E. rhusiopathiae via cuts and abrasions (5).
Yersinia
Yersiniosis is caused by Yersinia pseudotuberculosis and Y. enterocolitica. It is thought that infection occurs through consumption of food contaminated by the feces of carrier animals, and that stress such as inclement weather or food deprivation is necessary before disease occurs (40). Susceptible orders of birds include Coraciformes, Falconiformes, Musophagiformes, Passeriformes, Pisciformes, and Psittaciformes (63). Both Y. pseudotuberculosis and Y. enterocolitica can infect man (40).
Clostridium perfringens
Clostridium perfringens is the causative agent of necrotic enteritis. This disease is found throughout much of the world where poultry are produced, and sporadic cases have been diagnosed in wild mallards, black ducks, and Canada geese. C. perfringens was responsible for a die-off that occurred in Florida involving mallards and other wild ducks along with several species of shore-birds and wading birds. Wild ducks are also reported to have died of this disease in Germany. In addition, in recent years increased numbers of small die-offs have been detected in snow geese, Canada geese, and white-fronted geese in both Canada and the United States. An abrupt change in diet associated with seasons and bird migrations are thought to disrupt the intestinal microflora and allow C. perfringens to proliferate in the intestine (5). Enteritis due to C. perfringens was a cause of death in numerous free-living lorikeets (Trichoglossus spp.) in Australia (64).
Riemerella anatipestifer
Riemerella (Reimerella/Pasteurella) anatipestifer is the cause of a septicemic disease known as New Duck Disease (duck septicemia, anatipestifer syndrome, infectious serositis) of domestic ducklings that occurs in many areas of the world. However, it has been diagnosed as the cause of mortality in small numbers of free-ranging birds including ducks and lesser snow geese. Outbreaks with large mortalities have occurred in black swans in Tasmania, and in tundra swans in Canada (40). This organism can be transmitted by mosquitoes (40), but there is no report of human infection due to this bacterium. Riemerella columbina, a bacterium related to R. anatipestifer can cause respiratory disease in pigeons (65).
Francisella tularensis
Tularemia, caused by Francisella tularensis, is primarily a disease of mammals, but may affect wild avian species. For example, major die-offs have occurred in the ruffed grouse and other grouse species. The primary source of disease transmission in natural cases of tularemia in gamebirds such as grouse and pheasants is ticks, while in raptors, gulls, and other scavenger species, infection generally occurs through ingestion of diseased prey species. Strains of F. tularensis are not highly infectious to humans, and little is known concerning transmissibility to domestic animals and livestock (5).
Clostridium colinum
Clostridium colinum is the causative agent of “quail disease” or ulcerative enteritis. Outbreaks of this disease in free-ranging wild birds are rare but outbreaks have been reported in California quail in Washington state. Outbreaks have also been reported in pigeons and robins, and occur worldwide where gamebirds are raised in captivity under crowded conditions(5)
Staphylococcus aureus
Staphylococcus aureus is the causative agent of staphylococcosis. S. aureus is also commonly associated with chronic arthritis-synovitis or “bumblefoot” in a variety of captive birds and domestic poultry. Staphylococci are normally found in the skin and mucous membranes, and only tend to cause infection where a break in these protective layers has occurred (40). A great variety of wild bird species are susceptible to S. aureus infection including members of the Anseriformes (66), Columbiformes (67), Falconiformes (68), Galliformes, Passeriformes, and Pisciformes (69).
Conclusions
Many bacteria can cause morbidity and mortality in free-living birds. Domestic poultry may acquire infection from several agents. Free-living birds can get clinical salmonellosis, and may serve as reservoirs of salmonellae pathogenic to animals and humans. Crows and rooks have recently been found to be carriers of the agent of Johne’s disease of cattle. For the preservation of free-living birds, and to protect domestic species and humans, mortalities should be investigated, and where bacteria are involved efforts should be made towards their identification.
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