Professional Documents
Culture Documents
639659
q Wildlife Disease Association 2004
ABSTRACT: The potential for transport and dissemination of certain pathogenic microorganisms
by migratory birds is of concern. Migratory birds might be involved in dispersal of microorganisms
as their biological carriers, mechanical carriers, or as carriers of infected hematophagous ecto-
parasites (e.g., ixodid ticks). Many species of microorganisms pathogenic to homeothermic ver-
tebrates including humans have been associated with free-living migratory birds. Migratory birds
of diverse species can play significant roles in the ecology and circulation of some arboviruses
(e.g., eastern and western equine encephalomyelitis and Sindbis alphaviruses, West Nile and St.
Louis encephalitis flaviviruses), influenza A virus, Newcastle disease virus, duck plague herpes-
virus, Chlamydophila psittaci, Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato,
Campylobacter jejuni, Salmonella enterica, Pasteurella multocida, Mycobacterium avium, Candida
spp., and avian hematozoans. The efficiency of dispersal of pathogenic microorganisms depends
on a wide variety of biotic and abiotic factors affecting the survival of the agent in, or disap-
pearance from, a habitat or ecosystem in a new geographic area.
Key words: Arboviruses, bacteria, birds, fungi, migration, protozoa, viruses.
639
640 JOURNAL OF WILDLIFE DISEASES, VOL. 40, NO. 4, OCTOBER 2004
fecting survival of the agent in a new en- Carriers of infected hematophagous ectoparasites
vironment. Birds are hosts for many ectoparasites
Migratory birds could be involved in that sometimes serve as vectors of diseas-
carriage of microbial pathogens by three es. Of these, the most important are im-
mechanisms, including 1) as biological car- mature ixodid and argasid ticks that can be
riers, 2) as mechanical carriers, and 3) as transported on their hosts from one site to
hosts and carriers (transporters) of infect- another, even between continents (Ter-
ed ectoparasites. Vartanov et al., 1956; Cerny and Balat,
1957; Hoogstraal et al., 1961, 1963, 1964;
Biological carriers Nuorteva and Hoogstraal, 1963; Brinck et
Birds serve as biological carriers when al., 1965; Kaiser et al., 1974; Nosek and
the pathogen multiplies in the avian body. Folk, 1977; Walter et al., 1979). Many tick-
Infection of birds can be acute (e.g., in borne pathogens can be carried this way:
EEE, WNV, or Usutu virus infections; viruses (tickborne encephalitis viruses
Newcastle disease; duck plague; ornithosis; [TBE], Tyuleniy, Meaban, Bahig, Hughes
mycoplasmal conjunctivitis; avian cholera; group, Sakhalin group, Crimean-Congo
erysipelas), chronic (avian pox, avian tu- hemorrhagic fever [CCHF] virus, Bhanja,
berculosis, aspergillosis, leucocytozoono- Kemerovo, Great Island complex, Chenu-
sis), latent, or asymptomatic (e.g., Sindbis da complex, Thogoto and Dhori viruses),
or St. Louis encephalitis virus infection, bacteria (Rickettsia spp., A. phagocyto-
influenza A, coxiellosis, Lyme borreliosis, philum, B. burdorferi s.l.), and protozoa
campylobacteriosis, cholera, colibacillosis, (Babesia microti). Surprisingly, fleas also
salmonellosis, yersiniosis, listeriosis, can- can be transported over long distances on
didosis, hemoproteosis, toxoplasmosis, sar- migrating birds (Ter-Vartanov et al., 1956;
cosporidiosis, cryptosporidiosis). The in- Schwan et al., 1983).
fected bird often sheds the agent, some- The mode of transport of pathogenic
times for a prolonged period (e.g., orni- agents by migratory birds depends on the
thosis, avian cholera). In some bird species routes of transmission. In insectborne vi-
(e.g., gulls) the shedding of a pathogen is ruses, bacteria, and protozoa, duration and
more intense and clinical signs more ob- concentration of the agent in the blood of
vious in younger birds than in adults (sal- migrating birds is decisive for infection of
monellosis, cryptosporidiosis). competent insect vectors by feeding dur-
ing stopover. In tickborne viruses, bacteria,
Mechanical carriers
and protozoa, the infectious larval or
nymphal tick must remain attached for
Birds act as mechanical carriers when several days and then drop off during mi-
the pathogen does not multiply in or on gration in a new geographic area. In wa-
the bird. This carriage can be either ex- terborne infections, the agent can be shed
ternal, when the agent is located on the by infected migrating birds, resulting in
surface of the birds body (e.g., fungal contamination of water with feces, nasal
spores can survive for at least 12 days discharges, and respiratory exudates (e.g.,
when inoculated on feathers of migratory influenza A virus, Newcastle disease virus
swallows; Warner and French, 1970), or [NDV], duck plague herpesvirus, C. psit-
internal, when the agent passes through taci, Campylobacter, Salmonella, Esche-
the digestive tract and is viable when ex- richia, Vibrio cholerae, Yersinia spp., P.
creted. For instance, it has been speculat- multocida, Enterococcus faecalis, Clostrid-
ed that foot-and-mouth disease virus ium spp.; Candida spp.). Also, pellets of
(FMDV) could be carried mechanically on migratory raptors or corvids are sometimes
free-living birds. infected (e.g., M. avium). In addition, in-
HUBALEKPATHOGENIC MICROORGANISMS OF MIGRATORY BIRDS 641
TABLE 1. Important microbial pathogens of homeothermic vertebrates associated with migratory birds.
Togaviridae: Alphavirus
Eastern equine encephalomyelitis (EEE) Cul PH Am EEE
Western equine encephalomyelitis (WEE) Cul PH Am WEE
Sindbis Cul PH Afr, Eur, As, Aus
Flaviviridae: Flavivirus
St. Louis encephalitis Cul PH Am
West Nile virus (WNV) Cul PH Afr, Eur, As, Am WNV encephalitis
Japanese encephalitis Cul PH As
Tickborne encephalitis (TBE) group Ixo T, OH Eur, As Louping ill, TBE
Bunyaviridae: Nairovirus
Crimean-Congo hemorrhagic fever Ixo T Eur, As, Afr
Reoviridae: Orbivirus
Kemerovo Ixo OH As, Afr
Orthomyxovirdae
Influenzavirus A PH Worldwide Avian influenza
Paramyxoviridae: Paramyxovirus
Newcastle disease virus PH Worldwide Newcastle disease
Adenoviridae
Aviadenovirus galli-1 PH Worldwide Egg-drop syndrome
Poxviridae
Avipoxvirus PH Worldwide Avian pox
Herpesviridae
Herpesvirus anatis PH Am, Eur Duck plague
Rickettsiales
Rickettsia sibirica Ixo OH, T As
Coxiella burnetii (Ixo) OH (T) Worldwide
Anaplasma phagocytophilum Ixo T, OH Holarctic
Chlamydiaceae
Chlamydophila psittaci PH Worldwide Ornithosis
Mycoplasmataceae
Mycoplasma gallisepticum OH Am Mycoplasmosis
Spirochaetaceae
Borrelia burgdorferi s.l. Ixo OH, T Holarctic
Campylobacteraceae
Campylobacter jejuni PH Worldwide Campylobacteriosis
Vibrionaceae
Vibrio cholerae OH Am
Enterobacteriaceae
Escherichia coli (enteropathogenic) OH Worldwide Colibacillosis
Salmonella enterica OH Worldwide Salmonellosis
Yersinia enterocolitica OH Eur, As
Y. pseudotuberculosis OH Worldwide Pseudotuberculosis
Pasteurellaceae
Pasteurella multocida PH Worldwide Avian cholera
Riemerella anatipestifer PH Worldwide New duck disease
HUBALEKPATHOGENIC MICROORGANISMS OF MIGRATORY BIRDS 643
TABLE 1. Continued.
Gram-positive cocci
Staphylococcus aureus OH Worldwide Staphylococcosis
Enterococcus faecalis OH Eur
Endospore-forming gram-positive rods
Clostridium botulinum OH Worldwide Avian botulism
C. perfringens OH Worldwide Necrotic enteritis
Regular nonsporing gram-positive rods
Listeria monocytogenes OH Eur, As Listeriosis
Erysipelothrix rhusiopathiae OH Am, As Erysipelas
Mycobacteriaceae
Mycobacterium avium PH Worldwide Avian tuberculosis
Endomycetes
Candida albicans OH Worldwide Candidosis
C. tropicalis OH Worldwide
Hyphomycetes
Aspergillus fumigatus OH Worldwide Aspergillosis
Piroplasmida
Babesia microti Ixo T Holarctic
Haemosporina
Plasmodium spp. Cul PH Worldwide Avian malaria
Leucocytozoon simondi Sim PH Holarctic Leucocytozoonosis
Haemoproteus spp. Dip PH Worldwide Hemoproteosis
Eimeriina
Toxoplasma gondii OH Worldwide Toxoplasmosis
Eimeria spp. PH Worldwide Coccidiosis
Sarcocystis spp. PH Worldwide Sarcosporidiosis
Cryptosporidium spp. OH Worldwide Cryptosporidiosis
Kinetoplastida
Trypanosoma avium Dip PH Worldwide
a Principal vector of the agent: Cul 5 mosquitoes; Ixo 5 ixodid ticks; Sim 5 simuliids; Dip 5 other biting diptera.
b Association with migratory birds: PH 5 principal biological hosts; OH 5 occasional (or mechanical) hosts; T 5 transport of
infected ectoparasites.
c Am 5 Americas; Afr 5 Africa; Eur 5 Europe; Aus 5 Australia; As 5 Asia.
va, 1980); Acrocephalus scirpaceus, Vanel- migrating (Stamm and Newman, 1963;
lus vanellus, and Sturnus vulgaris in Slo- Lord and Calisher, 1970; Calisher et al.,
vakia (during spring migration; Ernek et 1971). Eastern equine encephalitis virus
al., 1973, 1977); and migrating birds in Es- was also isolated from southward-migrat-
tonia (Uryvaev et al., 1992). It is most ing birds (Colaptes auratus, Icterus gal-
probable that the causative agent of Ock- bula, Zonotrichia albicollis) in eastern
elbo disease (Pogosta, Karelian fever; Long Island (New York, USA); the mi-
i.e., Sindbis virus) was introduced to Fen- grants were thought responsible for initi-
noscandia from subtropical regions by mi- ating a small local EEE epizootic (Bast et
gratory birds (Hubalek, 1994). al., 1973; Morris et al., 1973). Eastern
Eastern and western equine encephalitis equine encephalitis virus was also isolated
viruses (mosquitoborne): Repeatedly iso- from several trans-Gulf migrants (Icterus
lated from North American birds actively spurius, Dendroica striata, Hylocichla
644 JOURNAL OF WILDLIFE DISEASES, VOL. 40, NO. 4, OCTOBER 2004
mustelina). The 1962 epidemic of EEE in ropus, V. vanellus, Larus ridibundus, and
Jamaica probably resulted from the trans- S. turtur just arriving to Slovakia from
port of EEE virus by birds from continen- their winter ranges (Ernek et al., 1977);
tal USA (Work and Lord, 1972). and Sterna albifrons in Tajikistan (Gordee-
Venezuelan equine encephalitis virus va, 1980), as well as from other migratory
(VEE): Suspected of being transported species in Europe or elsewhere, including
from South to Central America. Experi- A. ralloides, Ixobrychus minutus, Botaurus
mental data on migratory birds confirmed stellaris, Plegadis falcinellus, Anas platy-
that they are effective amplifying hosts rhynchos, A. querquedula, Fulica atra, La-
with moderate to high levels of viremia for rus cachinnans, Corvus frugilegus, Corvus
24 days postinoculation, sufficient to in- corone, Pica pica, S. vulgaris, and Turdus
fect vector mosquitoes (Dickerman et al., merula (Hubalek, 1994). A large number
1980). Tonate virus is antigenically related of avian species, many of them migratory
to VEE virus; it was isolated from birds (including, e.g., Corvus brachyrhynchos,
and mosquitoes in French Guiana, and Cyanocitta cristata, Larus spp.), are hosts
then from cimicid bugs (Oeciacus vicarius) of WNV in North America (Bernard et al.,
parasitizing Petrochelidon pyrrhonota and 2001), and the virus was isolated at high
Passer domesticus in the USA (Monath et titers from oral and cloacal swabs of dead
al., 1980). The isolation of this virus in the C. brachyrhynchos, and C. cristata (Ko-
USA might reflect its introduction by mi- mar et al., 2002). A surprisingly high mor-
gratory birds from South America. tality occurs in some WNV-infected North
Mayaro virus (mosquitoborne): Occurs American birds compared with Old World
in South and Central America, but it was avian species, and some bird populations
also isolated from a migrating bird in the could be endangered because of this in-
USA north of the area of virus distribution fection (Anderson et al., 1999; Garmendia
(Calisher et al., 1974). et al., 2000; Male, 2003). Experimental
Semliki Forest virus (mosquitoborne): studies have shown that many North
Isolated from a northward-migrating Mo- American species are competent (i.e., virus
tacilla flava in Kazakhstan (Lvov and Ili- amplifying) hosts for WNV (e.g., C. bra-
chev, 1979). chyrhynchos, C. ossifragus, C. cristata,
Quiscalus quiscula, Carpodacus mexican-
Flaviviridae: genus Flavivirus
us, Larus delawarensis), attaining high vi-
Japanese encephalitis virus (JEV; mos- remias between 1 and 7 days postinocu-
quitoborne): Amplifies well in colonial ar- lation (Komar et al., 2003a). A plausible
deids Nycticorax and Egretta spp. hypothesis supposes dispersal (and reintro-
(Buescher et al., 1959; Scherer et al., 1959; ductions) of WNV by migratory birds be-
Boyle et al., 1983); movements of these tween Africa, southern Asia, and Europe
birds, including migration, provide a (Hannoun et al., 1972; Lvov and Ilichev,
means for dispersal of the mosquitoborne 1979; Hubalek, 1994; Malkinson et al.,
JEV far beyond the area of avian colonies. 2002), as well as recent, rapid long-dis-
West Nile virus: Colonial and other tance dispersal of WNV over the North
birds are significant in the circulation of American continent, Mexico, and the Ca-
this virus. Nestlings could represent ideal ribbean (Rappole et al., 2000; Dupuis et
blood donors for ornithophilic Culex mos- al., 2003; Komar et al., 2003b). Additional
quitoes and might serve as amplifying movements of competent nonmigratory
hosts of the virus. West Nile virus was iso- birds like P. domesticus (Rappole and Hu-
lated from migrating Sylvia nisoria in Cy- balek, 2000) or short-distance migrants (C.
prus (Watson et al., 1972); S. turtur, M. brachyrhynchos, C. cristata, Q. quiscula)
alba, and C. ciconia in Israel (Nir et al., could be responsible for lateral geographic
1967; Malkinson et al., 2002); Tringa och- spread of WNV outside the main migra-
HUBALEKPATHOGENIC MICROORGANISMS OF MIGRATORY BIRDS 645
tory routes of birds in North America. For closely related to Australasian Saumarez
instance, C. brachyrhynchos use regular Reef virus and could have been introduced
communal roosts, and their daily flights to France by Sterna paradisaea terns
from the nocturnal roost to feeding sites (Chastel, 1988).
might range up to 2030 km; the crows
Bunyaviridae: genera Bunyavirus, Nairovirus
feeding on infectious carcasses of birds
might spread WNV through a chain of Simbu group bunyaviruses (mosquito-
neighboring corvid roosts. borne): Ingwavuma virus was isolated from
Usutu virus: Related to WNV and pre- two northward-migrating Muscicapa stri-
viously isolated only in South Africa, ata in Cyprus, and Thimiri virus from Syl-
caused an epornitic among T. merula in via curruca and S. communis migrating
Austria during late summers in 200103 southwards in Egypt (Watson et al., 1972).
(Weissenbock et al., 2002). Tete group bunyaviruses: A total of 41
St. Louis encephalitis virus (SLEV): isolations of Bahig virus and 57 isolations
American mosquitoborne Flavivirus, also of Matruh virus were made from south-
related to WNV, was isolated many times migrating Eurasian birds in Egypt and Cy-
from free-living (including migratory) prus (Watson et al., 1972; Hoogstraal,
birds, which are its principal amplifying 1976); prevailing hosts were Sylviidae,
hosts. These birds have moderate levels of Fringillidae, and Turdidae. Bahig virus was
viremia sufficient to infect vector mosqui- also recovered from larval Hyalomma mar-
toes. Several SLEV isolations were ob- ginatum rufipes ticks (an African subspe-
tained from migratory bird species in the cies) parasitizing a northward-migrating
Caribbean and Amazon basin (Theiler and Oenanthe oenanthe in Egypt (Converse et
Downs, 1973). al., 1974).
Tickborne encephalitis (TBE) complex Hughes group nairoviruses: Hughes,
viruses: Birds can disseminate TBE viruses Punta Salinas, Soldado, and Zirqa occur in
(Central European encephalitis, Russian argasid ticks (Ornithodoros capensis
spring-summer encephalitis, louping ill) by group) living in seabird nests (Varma et al.,
transporting infected ixodid ticks. For in- 1973; Yunker, 1975; Nuttall et al., 1984,
stance, two strains of TBE virus were re- 1986; Chastel, 1988). Marine bird migra-
covered from nymphal Ixodes ricinus col- tions undoubtedly account for the remark-
lected on T. merula in Slovakia (Ernek et ably extensive geographic distribution of
al., 1968). Soldado virus and other arboviruses of this
Omsk hemorrhagic fever (OHF) and serogroup.
Kyasanur Forest disease (KFD): Antigeni- Sakhalin group nairoviruses: Avalon
cally closely related and are also related to (syn. Paramushir) and Clo Mor viruses
TBE viruses. It has been hypothesized that were isolated from I. uriae ticks in colonies
the tickborne KFD virus might be a vari- of marine birds, and all the Sakhalin group
ant of OHF virus after transport to the In- viruses can be transported by seabirds in
dian subcontinent by migratory birds the subpolar regions (Lvov et al., 1975;
(Work, 1958). Some avian sera in Siberia Yunker, 1975; Main et al., 1976).
have been positive for KFD virus antibod- Crimean-Congo hemorrhagic fever nai-
ies (Matukhin and Fedorova, 1969). rovirus: Birds could disseminate the virus
Tyuleniy virus: Occurs in Ixodes uriae long distances by the transport of infected
ticks inhabiting nests of seabirds and it is immature H. marginatum, Haemaphysalis
transported by the birds (Lvov and Ilichev, punctata, or other amblyommine ticks
1979). (Hoogstraal, 1979); antigenic and genomic
Meaban virus: Isolated from Ornithod- identity of the CCHF strains from Africa
oros maritimus ticks collected in nests of and Eurasia is striking.
Larus argentatus in France; the virus is Bhanja virus: As for CCHF virus, mi-
646 JOURNAL OF WILDLIFE DISEASES, VOL. 40, NO. 4, OCTOBER 2004
gratory birds are regarded as carriers of (Hinshaw and Webster, 1982; Webster et
infected immature amblyommine ticks al., 1992). These viruses can adapt to new
(Hubalek et al., 1982). host species (Suarez, 2000). All of the an-
tigenic subtypes of influenza A viruses
Reoviridae: genus Orbivirus (H1H14 and N1N9) are perpetuated in
Kemerovo virus (tickborne): Isolated aquatic birds, particularly in migrating wa-
from a southward-migrating Phoenicurus terfowl (Hinshaw et al., 1980). Isolation
phoenicurus in Egypt (Schmidt and Sho- rate of influenza virus from migratory
pe, 1971), this strain (EgAr 1169-61) was ducks ranges from 0.3% to 30% (Bahl et
indistinguishable from Siberian isolates by al., 1977; Slemons and Easterday, 1977;
antigenic and RNA molecular studies, sug- Hinshaw et al., 1985; Slemons et al.,
gesting the redstart might have acquired 1991). In Europe, approximately 15% of
the virus in Siberia and that migratory migratory geese, mallards, and other dab-
birds are involved in its dispersal over very bling ducks carry and shed the virus even
long distances. in the winter (De Marco et al., 2003).
Other orbiviruses of the Great Island
Paramyxoviridae: genus Rubulavirus
antigenic complex (Bauline, Great Island,
Cape Wrath, Mykines, Tindholmur) have Newcastle disease virus (NDV, avian
been isolated from I. uriae ticks inhabiting parainfluenza virus 1, paramyxovirus-1):
seabird nests (Main et al., 1973; Doherty Isolated from many species of free-living
et al., 1975; Yunker, 1975; Calisher et al., birds (Wobeser, 1997), including a migrat-
1988). These viruses occur in both sub- ing Upupa epops in India (Sharma and
antarctic and subarctic regions and are ob- Baxi, 1980). Infected birds can transport
viously dispersed transoceanically and in- the virus over long distances because re-
troduced by seabirds to new areas and new covered avian hosts and immune carriers
avian hosts. can shed the virus indefinitely (Davis et al.,
Chenuda complex orbiviruses: Baku, 1971).
Chenuda, Mono Lake, etc. have been iso-
Picornaviridae: genus Aphthovirus
lated repeatedly from ticks associated with
migratory gulls (Lvov and Ilichev, 1979; Foot-and-mouth disease virus: Several
Schwan et al., 1988). authors have suggested that FMDV can be
dispersed with birds as mechanical carriers
Orthomyxoviridae: genera Thogotovirus, and even introduced with migrants (S. vul-
Influenzavirus
garis, C. frugilegus, Larus spp.) from con-
Thogoto and Dhori viruses: Suspected tinental Europe to the British Isles (Ec-
of being introduced occasionally by prei- cles, 1939; Hurst, 1968; McDiarmid, 1969;
maginal amblyommine ticks on migratory Kaleta, 2002). However, direct evidence
birds from Africa and/or South Asia to for long-distance mechanical transport of
southern Eurasia (Filipe and Casals, 1979; FMDV by birds is lacking.
Calisher et al., 1987).
Adenoviridae: genus Aviadenovirus
Influenza A virus: Often isolated from
migratory birds, including ducks, geese, Egg drop syndrome virus: Causes high
gulls, terns, shearwaters, guillemots, and, fragility of egg shells and a lower fertility
less often, shorebirds and passerine spe- in fowl and anseriforms. Antibodies against
cies from throughout the world (Stallk- this virus were detected in migratory
necht and Shane, 1988; Alexander, 2000; ducks, coots, and grebes in Europe, Israel,
Fouchier et al., 2003). Wild aquatic birds and USA (Kaleta et al., 1980; Malkinson
are regarded as the principal reservoir of and Weisman, 1980; Gulka et al., 1984).
influenza viruses, and migrating ducks dis- The virus can be disseminated by migra-
seminate influenza viruses worldwide tory anseriform species.
HUBALEKPATHOGENIC MICROORGANISMS OF MIGRATORY BIRDS 647
rate of larval ixodid ticks feeding on cer- F. atra, Gallinula chloropus, and C. frug-
tain bird species (e.g., thrushes, family ilegus in Germany (Glunder, 1989). Less
Turdidae) to be .10% (Humair et al., frequently, Campylobacter species (C. coli
1993; Hubalek et al., 1996; Hanincova et and C. laridis) are isolated from birds
al., 2003); this means that some larval ticks (Glunder and Petermann, 1989; Quessy
were infected either from the spiroche- and Messier, 1992; Sixl et al., 1997). The
temic host or via a so-called cofeeding carrier state of young L. argentatus for C.
mechanism (Gern and Rais, 1996). In one jejuni lasted about 34 wk (Glunder et al.,
study, 22% of 250 preimaginal I. scapularis 1992). Migratory seagulls have been im-
collected from 58 mainly ground-foraging plicated in the spread of campylobacters
birds in Wisconsin (USA) were positive for to domestic animals or humans via feed-
B. burgdorferi, and nearly half of the spi- stuffs or water (Sacks et al., 1986).
rochete-positive ticks were removed from
Vibrionaceae
migrating birds (Weisbrod and Johnson,
1989). Some avian migratory species are Vibrio cholerae: Isolated occasionally
reservoirs of borreliae (B. burgdorferi s.l.; from free-living waterbirds (Lee et al.,
Anderson and Magnarelli, 1984; Olsen et 1982) e.g. from 17% of fecal samples col-
al., 1993). Borrelia garinii repeatedly has lected from 1,131 aquatic birds in Colo-
been isolated from I. uriae collected in rado and Utah (USA; Ogg et al., 1989).
nests of colonial seabirds in the Baltic and The latter study suggests that migratory
North seas and from the birds (Alca torda, waterfowl serve as disseminators of V.
Fratercula arctica) themselves (Olsen et cholerae (three serotype O1 biovar eltor
al., 1993, 1995a; Gylfe et al., 1999). An ex- subtype Ogawa isolates were recovered
perimental study (Burgess, 1989) showed from Ardea herodias and L. delawarensis);
that A. platyrhynchos infected with B. they might have transported the organism
burgdorferi s.s. remained asymptomatic, to Colorado from a focus where O1 sero-
but the spirochete was recoverable from type persists, such as estuaries along the
the blood for 7 days postinoculation and Gulf Coast and Chesapeake Bay. Avian
from the cloaca content for 34 wk post- droppings contaminating a water supply or
inoculation. Migratory birds are therefore inland surface waters with the epidemic
a natural means for distribution of the spi- strain of V. cholerae could thus cause chol-
rochete over long distances (Olsen et al., era outbreaks far from areas where cholera
1995). For instance, the North American is endemic. Non-O1 V. cholerae have also
geographic range of Lyme disease seems been isolated from gulls (Lee et al., 1982;
to parallel known bird migration flyways. West et al., 1983; Buck, 1990).
Campylobacteraceae Enterobacteriaceae
water reservoirs (Hill and Graham, 1961; Branco, 1963; Kawakita and van Uden,
Matveev and Konstantinova, 1974; Hus- 1965; Cragg and Clayton, 1971; Buck,
song et al., 1979), where they can germi- 1983, 1990). A gull experimentally fed fish
nate and cause avian botulism, a major dis- containing C. albicans shed the yeast
ease of wild waterfowl (Hubalek, 1994; heavily in feces over 13 days postinocula-
Wobeser, 1997). tion, and for 40 days postinoculation, it ex-
Clostridium perfringens: Isolated from creted the yeast sporadically, despite being
dead pelicans and marine birds in Florida treated with ketoconazole (Buck, 1986).
(USA; Ankerberg, 1984), other wild birds The gulls might thus serve as carriers, dis-
(waterfowl, shorebirds, raptors, T. migra- seminators, or even reservoirs of C. albi-
torius) with necrotizing enteritis in the cans.
USA, A. cinerea, dead gulls, and U. aalge Candida tropicalis: Isolated repeatedly
in Germany (Petermann et al., 1989; Hu- from excreta of migratory gulls and terns
balek, 1994; Wobeser, 1997). along the coast of Portugal (van Uden and
Castelo-Branco, 1963; Kawakita and van
Regular nonsporing Gram-positive rods
Uden, 1965).
Listeria monocytogenes: Gulls feeding at
Hyphomycetes
Scottish sewage works had a high rate
(15%) of carriage of the agent (Fenlon, Aspergillus fumigatus: The causative
1985) and the bacterium has been isolated agent of avian and mammalian aspergillo-
from C. frugilegus in France (Bouttefroy sis, it was isolated from throat swabs of mi-
et al., 1997). Other migratory birds (Falco gratory waterbirds: 7% of Anser brachyr-
columbarius, S. vulgaris, E. rubecula, An- hynchus, 7% of B. canadensis, and 13% of
thus trivialis) also yielded the agent and L. argentatus (Beer, 1963). Aspergillus fu-
might thus play a role in dispersal of lis- migatus was detected on the feathers of
teriae (Macdonald, 1968; Hubalek, 1994). 11% and 17% of wild birds examined in
Erysipelothrix rhusiopathiae: The agent Britain and Czechland, respectively (Hu-
of erysipelas, it can cause epornitics (Pod- balek, 1994). However, this fungus is a
iceps nigricollis, Jensen and Cotter, 1976) cosmopolitan, ubiquitous species, and the
or sporadic cases in wild, mainly water- role of migratory birds in its dispersal is
birds, including migratory species such as uncertain.
mergansers, ducks, geese, storks, gulls, A number of other pathogenic fungi
cranes, etc. (e.g., Davis et al., 1971; Wob- have been detected on feathers of migra-
eser, 1997). tory birds, including Aspergillus flavus, A.
nidulans, Microsporum gypseum, M. ri-
Mycobacteriaceae
pariae, M. persicolor, and Trichophyton
Mycobacterium avium: Pathogenic to mentagrophytes (Hubalek, 1994).
many wild avian species (tuberculosis is
PROTOZOA
one of the most widespread wild avian in-
fections) can be carried by some migratory Piroplasmida
birds, such as raptors, C. palumbus, or C. Babesia microti: The agent of human
frugilegus (Davis et al., 1971; Smit et al., babesiosis, it might be dispersed by migra-
1987; Hejlcek and Treml, 1993; Hubalek, tory birds via attached, infected nymphal
1994; Wobeser, 1997). and larval Ixodes ticks (Alekseev and Du-
FUNGI
binina, 2003).
Yeasts and yeast-like fungi Haemosporina
pathogenic to ducklings and goslings. In- many birds, including migratory species
terestingly, the protozoan was originally like raptors or seabirds (Petermann et al.,
described in Anas crecca wintering in Vi- 1989). For instance, E. boschadis, E. so-
etnam (Mathis and Leger, 1910), but prob- materiae, and E. truncata are renal coccid-
ably breeding in northern Asia. ia of wild ducks and geese, and infection
Haemoproteus: Currently, total of 128 can occasional result in fatalities. These
species of Haemoproteus include avian he- parasites are distributed by migratory wa-
matozoans that are relatively benign and terfowl (Nation and Wobeser, 1977; Gajad-
not known to cause serious harm to birds har et al., 1983; Wobeser, 1997). Other
in that they coevolved with their avian coccidia, E. aythyae, E. bucephalae, and E.
hosts (Bennett, 1993). Many species of anseris cause severe intestinal coccidiosis
Haemoproteus are transmitted by hema- of diving ducks and geese (Gajadhar et al.,
tophagous ceratopogonid or hippoboscid 1983; Wobeser, 1997).
biting flies. Haemoproteus spp. are quite Sarcocystis, Frenkelia: Sarcosporidiosis
common in migratory species (e.g., Phyl- has been detected in adult avian interme-
loscopus trochilus in Scandinavia [Bensch diate hosts (definitive hosts are carni-
and Akesson, 2003] or anatids in North vores). Migratory ducks (265% adult
America [Bennett et al., 1974, 1975]). ducks) are parasitized by S. rileyi in North
During the autumn migration of Fringilla America (Wobeser, 1997). Other migratory
coelebs along the Baltic Sea, the last wave birds affected are herons, columbids, gulls,
of the migrating birds was observed to be corvids, and swallows (McDiarmid, 1969;
most heavily infected with Haemoproteus Spalding et al., 1994; Wobeser, 1997). De-
fringillae and probably delayed in migra- finitive hosts for Frenkelia microti include
tion because of acute illness (Valkiunas, migratory Buteo buteo in Europe and Bu-
1989, 1991). teo jamaicensis in North America (Upton
Plasmodium relictum, P. circumflexum, and McKown, 1992; Hubalek, 1994).
and P. vaughani: Cause mosquitoborne Cryptosporidium baileyi: An enteric in-
avian malaria, which can result in mortal- tracellular coccidian parasite that can
ity. These protozoa also have been found cause gastrointestinal and respiratory tract
in some migratory species, including pas- disorders or, more often, subclinical and
serines, pigeons, anatids, and raptors asymptomatic infections in birds. Crypto-
(McDiarmid, 1969; Bennett et al., 1974, sporidium oocysts were found in feces and
1975). Plasmodium is quite common in cloacal samples of migratory gulls in Scot-
migratory P. trochilus in Scandinavia land (L. argentatus, L. ridibundus; Smith
(Bensch and Akesson, 2003). Chronically et al., 1993) and Czechland (L. ridibun-
infected migratory birds returning from dus; Pavlasek, 1993). Infectious cryptos-
their winter ranges could initiate summer poridial oocysts were found in feces of mi-
transmission of these parasites. gratory B. canadensis in Maryland (USA;
Graczyk et al., 1998). Waterbirds can thus
Eimeriina
disseminate cryptosporidia in the environ-
Toxoplasma gondii: Was recorded in, or ment.
isolated from, many migratory species, in-
Kinetoplastida
cluding ducks, raptors, L. ridibundus, S.
vulgaris, C. frugilegus, and C. monedula Trypanosoma everetti: Observed in Brit-
(Pak, 1976; Haslett and Schneider, 1978; ain in migratory passerine species that
Lvov and Ilichev, 1979; Literak et al., were obviously infected on their African
1992). Infected birds might be less mobile winter range (Peirce and Mead, 1984).
and more susceptible to predation by fe- Trypanosoma avium and related avian try-
lids (Hubalek, 1994). panosomes are largely nonpathogenic to
Eimeria, Isospora: Coccidia occur in their hosts but can occasionally cause mild
652 JOURNAL OF WILDLIFE DISEASES, VOL. 40, NO. 4, OCTOBER 2004
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289.
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