Public Health Significance of Urban Pests
Birds
249 248
the song thrush in North America and Europe Anderson et al., 1986; Magnarelli, Stafford Bladen, 1992; H umair et al., 1993; H ubálek, Juˇricová H alouzka, 1995;
Hubálek et al., 1996; Hanincová et al., 2003, Stern et al., 2006. Tick larvae and nymphs have parasitized some species of birds as frequently as they have parasitized the white-
footed mouse Peromyscus leucopus, the principal reservoir host of B. burgdorferi s.s. in North America. Bird-feeding larval and nymphal deer ticks were removed from their
hosts, left to molt, and shown to transmit B. burgdorferi trans-stadially that is, from one stage of the life-cycle to the next into the adult stage Anderson, Magnarelli Stafford,
1990. In Switzerland, 16 of larval and 22 of nymphal castor-bean ticks collected from passerine birds were infected with borreliae; the highest infection rate was observed in
ticks removed from thrushes Turdidae Humair et al., 1993. In the Czech Republic, borreliae were detected in 7 of larval and 12 of nymphal castor-bean ticks collected
from wild birds; positive ticks were collected from synanthropic species: the common blackbird, the European robin Erithacus rubecula and the great tit. Three massively
infected ticks with hundreds of borreliae were collected from robins and blackbirds, and Borrelia garinii
was isolated from a nymphal tick, collected from a young blackbird Hubálek et al., 1996. A high rate of infection with borreliae mainly B. garinii and
Borrelia valaisiana was also found in preimaginal ticks, collected from Turdidae in
Slovakia Hanincová et al., 2003. Moreover, some synanthropic bird species are compe- tent amplifying hosts for B. burgdorferi s.l. – for instance, the common blackbird
Humair et al., 1998 and the American robin Richter et al., 2000; Ginsberg et al., 2005. However, no B. burgdorferi s.l. infections of people have been reported as attributable to,
or directly associated with, urban birds.
8.2.2.5. Campylobacteraceae
Campylobacter jejuni is the most frequently isolated Campylobacter spp. from a wide
variety of aquatic and terrestrial wild birds including synanthropic anatids, gulls, pigeons, corvids, starlings and sparrows, followed by Campylobacter coli and C. laridis
Rosef, 1981; Kapperud Rosef, 1983; Kinjo et al., 1983; Kaneuchi et al., 1987; Mégraud, 1987; Whelan et al., 1988; Glünder Petermann, 1989; Maruyama et al., 1990; Glünder
et al., 1991; Quessy Messier, 1992; Sixl et al., 1997; Odermatt et al., 1998; Gautsch et al., 2000; Haag-Wackernagel Moch, 2004. Campylobacter spp. cause either asymptomatic
carriership in adult birds or signs of anorexia, diarrhoea and occasionally mortality in fledglings. Among birds found in the city of Oslo, very high isolation rates of
Campylobacter
spp. were detected Kapperud Rosef, 1983 in omnivorous and scaven- ging species: carrion crows 90, herring gulls 50 and black-headed gulls 43. C.
jejuni was also recovered from 3 and 14 of feral pigeons in Norway and Croatia,
respectively Lillehaug et al., 2005; Vlahoviˇc et al., 2004. As many as 46 of Japanese crow also known as jungle crow, Corvus levaillantii and carrion crow dropping samples
contained C. jejuni, mostly biovar I serogroup 2, reflecting a close epidemiological asso- ciation between the crow and human isolates Maruyama et al., 1990. Campylobacter spp.
are transmissible to other birds through droppings and aerosols. The carrier state of young black-headed gulls for C. jejuni has been shown to last for about 3–4 weeks
Glünder, Neumann Braune, 1992.
Campylobacter jejuni and C. coli cause human campylobacterosis food-borne enterocoli-
Also, C. psittaci was isolated from synanthropic species such as mallards, herring gulls Larus argentatus, black-headed gulls, feral pigeons, wood pigeons Columba palumbus,
collared doves, common starlings and house sparrows Strauss, Bednáˇr ˇSer´y, 1957; ˇSer´y Strauss, 1960; Illner, 1961; Terskikh, 1964; Davis et al., 1971; Wobeser, 1997; Odermatt
et al., 1998; Gautsch et al., 2000; Dovc et al., 2004; Haag-Wackernagel Moch, 2004; Tanaka et al., 2005. Synanthropic doves, grackles and starlings may transmit C. psittaci
to domestic birds Grimes, Owens Singer, 1979, and wild ducks, gulls and grackles may disperse the infectious agent Page, 1976; Lvov Ilyichev, 1979. The mean world-
wide prevalence of C. psittaci in feral pigeons is 13 by isolation and 30 by serology Davis et al., 1971, but as many as 38 and 56 of pigeons were found to be seroposi-
tive, for instance, in Slovakia and Switzerland, respectively ˇReháˇcek Brezina, 1976; Haag-Wackernagel Moch, 2004. The feral pigeon plays a major role in the epidemio-
logy of human ornithosis Meyer, 1959; Terskikh, 1964; Sixl Sixl, 1971; Sixl, 1975. At least 500 cases have been reported as acquired by people from feral pigeons or other
synanthropic avian species in many parts of the world, often in urban conditions Meyer, 1959; H enry Crossley, 1986; Pospíˇsil et al., 1988; Wobeser Brand, 1982; H aag-
Wackernagel Moch, 2004.
8.2.2.2. Coxiellaceae
Coxiella burnetii , the causative agent of Q fever also known as coxiellosis, was isolated
from more than 40 species of wild birds, including synanthropic barn swallows Hirundo rustica
and white wagtails Motacilla alba in the Czech Republic Raˇska Syr˚uˇcek, 1956, feral pigeons in Italy Babudieri Moscovici, 1952, house sparrows in central Asia and
crows in India Lvov Ilyichev, 1979; ˇReháˇcek Tarasevich, 1988. Pigeons and house sparrows are susceptible to experimental infection: they excrete C. burnetii in faeces, and
the infectious agent is recoverable from the lungs, spleen and kidneys for 48–58 days post inoculation, while the birds do not develop any symptoms of the infection and are sero-
negative Babudieri Moscovici, 1952; Schmatz et al., 1977. Five members of a family living in southern France became ill with acute Q fever in May 1996, and an epidemio-
logical investigation suggested that this outbreak resulted from exposure to contamina- ted pigeon faeces and their argasid ticks Stein Raoult, 1999. Also, the collared dove,
a synanthropic species of dove with an expanding breeding range, has been suggested to be responsible for the introduction of the Q fever to Ireland ˇReháˇcek Tarasevich, 1988.
8.2.2.3. Anaplasmataceae
Anaplasma phagocytophilum, the causative agent of human granulocytic anaplasmosis
previously known as human granulocytic ehrlichiosis, can be carried in immature deer ticks Ixodes scapularis and castor-bean ticks attached to such synanthropic birds as some
turdids, as it was detected in North America Daniels et al., 2002, European parts of the Russian Federation Alekseev et al., 2001 and Sweden Bjoersdorf et al., 2001. However,
no Anaplasma infections of people have been reported as attributable to, or directly asso- ciated with, urban birds.
8.2.2.4. Spirochaetaceae
Borrelia burgdorferi s.l., the causative agent of Lyme borreliosis, was repeatedly detected
in preimaginal deer and castor-bean vector ticks collected from birds, including synan- thropic species of the American robin Turdus migratorius, the common blackbird, and
Public Health Significance of Urban Pests
Birds
251 250
Lévesque et al., 1993; Hubálek, Juˇricová Halouzka, 1995. Gulls could thus play a signi- ficant role in dispersing pathogenic salmonellae, even in urban areas.
Salmonellae Typhimurium, Enteritidis, Paratyphi B serovars have been recovered repeatedly from feral pigeons or synanthropic sparrows Petzelt Steiniger, 1961; Dózsa,
1964; Wobeser Finlayson, 1969; Tizard, Fish Harmerson, 1979; Tanaka et al., 2005. In pigeons, the serovar Typhimurium var. copenhagen is especially common, and its cells
are usually firmly attached to the duodenal epithelium of the birds, causing long-term or persistent infection Grund Stolpe, 1992. A number of house sparrows from 36 sites
in Poland were examined: the prevalence of salmonellae serovars Typhimurium, Dublin and Paratyphi B varied from 0 to 40 Pinowska, Chylinski Gondek, 1976. Certain
Salmonella
serovars can cause lethal enteritis and hepatitis of nestlings, especially gulls and other colonial water birds; the serovars Gallinarum and Typhimurium were encoun-
tered among the causes of death in British sparrows Keymer, 1958; Baker, 1977. Experimental infection of the fledgling house sparrow with the serovar Typhimurium
resulted in a rather severe disease, while some birds remained relatively asymptomatic, but excreted the salmonellae Stepanyan et al., 1964. Epizootic episodes of salmonellosis
with high mortality caused by the serovar Typhimurium have repeatedly been described among sparrows, greenfinches and other urban passerines at bird feeders in Europe and
North America, particularly during the winter and spring Englert et al., 1967; Wilson Macdonald, 1967; Bouvier, 1969; Cornelius, 1969; Schneider Bulling, 1969; Greuel
Arnold, 1971; Locke, Shillinger Jareed, 1973; Nesbitt White, 1974; Macdonald, 1977; Brittingham Temple, 1986; Bowes, 1990; Tizard, 2004. Garden bird feeders can
become heavily contaminated with salmonellae serovar Typhimurium, and the infec- ted birds may transmit the infection to people directly or via cats feeding on them:
Tizard, 2004. Also, an epornitic of salmonellosis occurred in common starlings over- wintering in Israel Reitler, 1955. Osteomyelitic and arthritic salmonellosis was descri-
bed in carrion crows Daoust, 1978 and pigeons, and cutaneous salmonellosis was des- cribed in house sparrows Macdonald, 1977. Human cases of salmonellosis were reported
after the handling of injured gulls Macdonald Brown, 1974 or drinking water conta- minated by gulls Benton et al., 1983, even in urban areas.
8.2.2.6.3. Yersinia Yersinia enterocolitica
infects wild anatids, gulls, pigeons, and some passerines Mair, 1973; Hacking Sileo, 1974; Kapperud Olsvik, 1982; Simitzis-le Flohic et al., 1983; Shayegani
et al., 1986; Kaneuchi et al., 1989; Odermatt et al., 1998; Gautsch et al., 2000. In the United States, 3 of wild avian faecal samples were positive for Y. enterocolitica, but no
serogroup O:8 or O:3 human pathogenic isolates were recovered Shayegani et al., 1986. The isolation rate in Japan for Y. enterocolitica was higher, at 7 Kato et al. 1985. The
avian hosts are usually asymptomatic, but sometimes the clinical signs include anorexia, diarrhoea and weight loss. Unlike Yersinia pseudotuberculosis, Y. enterocolitica is less fre-
quent in birds than in humans, and there is no evidence that birds are significant reser- voirs for it. No Y. enterocolitica infections of people have been reported as attributable
to, or directly associated with, urban birds.
Yersinia pseudotuberculosis can cause mortality in wild birds, including such synanthropic
tis worldwide, but some avian biotypes are distinct from human isolates. In C. jejuni iso- lated from 53 of pigeon faecal samples in the Bordeaux region of France; the main bio-
type was I – that is, the most common biotype in human disease Mégraud, 1987. Seagulls and common grackles Quiscalus quiscula were implicated in the indirect spread
of Campylobacter spp. to domestic animals and people, via feedstuffs and water, respec- tively Sacks et al. 1986. Jackdaws Corvus monedula and European magpies Pica pica
caused a milk-borne Campylobacter epidemic with 59 human cases by pecking milk bottles in England Hudson et al., 1991.
8.2.2.6. Enterobacteriaceae
