Migratory birds and West Nile virus

J.H. Rappole1 and Z. Hubalek2

1Smithsonian Conservation & Research Center, Front Royal, VA 22630, USA, and 2Laboratory of Medical

Zoology, Institute of Vertebrate Biology, Academy of Sciences, Klasternı 2, CZ69142 Valtice, Czech Republic

1. SUMMARY

West Nile virus was first recorded in the New World during

August 1999 in New York City. Aetiology of the disease in

the Old World indicated birds as the likely introductory and

amplifying hosts with ornithophilous mosquitoes, e.g. Culex

pipiens, as the principal vectors. Speculation regarding likely

agents for movement of the virus in its new environment

focused on migratory birds, but evidence to date is

equivocal. While spread of the disease has been fairly rapid,

at a rate of roughly 70 km a month, it has not shown the

kind of long-distance, leap frog movements one might

expect if transient birds were the principal introductory

hosts. Furthermore, movement of the disease has not been

focused southward, but shows a radiating pattern with

detection sites located in all directions from New York

where terrestrial habitat was available. In addition, tests

among potential New World, avian hosts have revealed

prolonged viraemia (up to 5 days) only in the relatively non-

migratory House Sparrow (Passer domesticus). Dispersal

movements by this species could account for the observed

pattern of West Nile virus spread in the Western Hemi-

sphere to date. Regardless of whether avian migration,

dispersal, or some other agent is responsible, West Nile

virus should reach the New World tropics in another

1–2 years, at which time a vast number of new potential

introductory and amplifying avian hosts would be exposed

to the disease and mosquito vectors would be available

throughout most of the year, likely causing serious, long-

term threats to human health and vulnerable avian popu-

lations in the region.

2. INTRODUCTION

On 23 September 1999, West Nile virus was identified using

polymerase chain reaction and DNA sequencing from

materials isolated from the tissues of dead birds collected

in early September 1999 at the Bronx Zoo in New York City

(Centers for Disease Control and Prevention 1999). This

virus had first been identified from the blood of a woman

from the West Nile region of Uganda in 1937 (Smithburn

et al. 1940), but has since been found to be a rather common

pathogen throughout much of the Old World, particularly in

the African tropics, Middle East and temperate Eurasia

(Karabatsos 1985; Peiris and Amerasinghe 1994). An

estimated 40% of the human population of Egypt’s Nile

delta was seropositive for the virus in the 1950s (Smithburn

et al. 1954). Outbreaks in human populations of increasing

frequency and severity in Europe, western Asia and the

Middle East since 1990 indicate possible changes in its

epidemiology (Gariepy et al. 2001). However, until the

outbreak in New York, the occurrence of West Nile virus

had never previously been documented in the Western

Hemisphere.

Mosquitoes of the genus Culex serve as the most common

vector for West Nile virus in both the Old and New World

(Hubalek and Halouzka 1999; Andreadis et al. 2001), and

birds, especially those occurring in large flocks in areas

frequented by these mosquitoes, e.g. wetlands and urban

sites, are the most common amplifying hosts (Hubalek and

1. Summary, 47S

2. Introduction, 47S

3. West Nile Virus in the Old World, 48S

4. Arrival and Movement of West Nile Virus in the New

World: 1999–2002, 49S

5. Mode of Entry of West Nile Virus into the Western

Hemisphere, 52S

6. The ‘Migrant Bird as Introductory Host’ Hypothesis, 52S

6.1 Factors supporting hypothesis, 53S

6.2 Factors not supporting the hypothesis, 53S

7. Alternative Hypotheses for West Nile Movement in the

New World, 53S

8. The Future for West Nile Virus in the New World, 56S

9. Acknowledgements, 56S

10. References, 57S

Correspondence to: John H. Rappole, 1500 Remount Road, Smithsonian

Conservation & Research Center, Front Royal, VA 22630, USA

(e-mail: jrappole@crc.si.edu).

ª 2003 The Society for Applied Microbiology

Journal of Applied Microbiology 2003, 94, 47S–58S

Halouzka 1999). Epidemics appear to be caused by a high

rate of viral infection among avian hosts, which is then

passed by mosquitoes to humans (Hubalek and Halouzka

1999). Most vertebrates are susceptible to West Nile virus

infection, and some, e.g. humans and horses, can suffer

mortality rates of up to 10% of those clinically diagnosed

with the infection (Garmendia et al. 2001). Nevertheless,

there is little evidence to date to indicate that groups other

than birds can serve as significant amplifying hosts. For

instance, viraemia does not appear to be sufficient in

humans, or indeed most vertebrates other than birds, to

allow them to function as sources for transmission of the

virus to other organisms by mosquito vectors or any other

mode (Komar 2000). However, the virus can be passed from

bird to bird in the laboratory without an obvious interme-

diary vector (McLean et al. 2001).

The epidemiology of West Nile virus thus seems well

understood, with infection originating in a large, dense

population of birds, where mosquitoes serve to transfer the

virus from bird to bird, and also from bird to human. Such

episodes are seasonal in temperate areas, with both avian and

human infection rates dropping to near zero as winter

approaches and mosquitoes become dormant (Hubalek and

Halouzka 1999). What has not been clear is how the virus

originates at a particular site. Arboviral persistence at a site

through periods of mosquito dormancy has been documen-

ted for other viruses (Reeves 1974), and new data from both

the field (Miller et al. 2000) and laboratory (Nasci et al.

2001) now indicate that such vertical transmission (viral

infection passed from female mosquito to offspring) could

account for spring reappearance of West Nile at temperate

sites like New York City where high infection rates occurred

in previous years. However, this phenomenon does not

explain how the virus can move from one temperate region

to another, infecting birds, mosquitoes, people and other

organisms at places where no previous infections were

known. Based on information in the Old World literature

(summarized by Hubalek and Halouzka 1999), Rappole et al.

(2000) speculated that migratory birds might serve as the

principal introductory hosts for the virus in the New World.

In the current paper, we examine new data on movement of

West Nile virus in the Western Hemisphere, use this

information to examine the validity of the ‘Migrant Bird as

Introductory Host’ hypothesis, and propose alternative

explanations.

3. WEST NILE VIRUS IN THE OLD WORLD

West Nile virus is enzootic in the African tropics, and has

been for at least 70 years (Garmendia et al. 2001). However,

until recently, outbreaks in Old World temperate regions

appeared to be epizootic and often isolated in both space and

time. For instance, human cases of West Nile viral infection

have been recorded in southern France in 1962, southern

Russia in 1963, Belarus in 1977, western Ukraine in 1985,

Romania in 1996, Czechland in 1997 and southern Russia in

1999, as well as several other sites in southern Europe

(Hubalek and Halouzka 1999). Occurrence of the virus

among humans in Europe has shown other distinctive

characteristics as well: (i) Outbreaks generally occur from

July–September at or near wetlands or urban sites. (ii) The

most common vectors are mosquitoes of the genus Culex,

females of which feed mostly on birds and mammals. (iii)

Birds are the primary vertebrate hosts, several species of

which can produce levels of viraemia sufficient for trans-

mission by vectors to other hosts, including humans

(Hubalek 2000). These characteristics have led researchers

to propose that migratory birds, infected with West Nile

virus on their African wintering grounds, carry the virus

northward on spring migration to stopover sites in Europe

where they can serve as introductory hosts under certain

conditions, i.e. at sites with numerous potential vectors

(mosquitoes) and amplifying hosts (large flocks of birds –

not necessarily the same species as the introductory host)

(Hannoun et al. 1972; Hubalek and Halouzka 1999). This

hypothesis would explain why outbreaks often occur in or

near wetlands and urban areas, where introductory host,

vector, amplifying host and human victim co-occur. It

would provide an explanation for the ability of the virus to

move from site to site, and explain the timing of outbreaks as

well, with migrants carrying the virus northward in April

and May during spring migration and infecting local bird

populations which serve as amplifying hosts, eventually

infecting large portions of the vector population within

2–3 months, and subsequently passing the virus to humans

in the area by July or August. Additional support for the

hypothesis is provided by the fact that individuals of many

species of migratory birds have been found to be carrying

West Nile virus when captured during migration (Nir et al.

1967; Watson et al. 1972; Ernek et al. 1977). Also, a few

laboratory studies have been performed that document

viraemia in some species of migrants of sufficient intensity

and duration to allow an infected bird, in theory at least, to

move the virus in infectious form from one locality to

another (Work et al. 1955; Taylor et al. 1956; Fedorova and

Stavskiy 1972; Chunikhin 1973; Semenov et al. 1973).

The most direct evidence in support of this idea comes

from a recent study in which 13 dead and dying White

Storks (Ciconia ciconia) were taken from a group of ca. 1200

birds that had landed at a site (Eilat) in southern Israel

2 days previously, on 26 August 1998. Laboratory tests

documented high levels of infection with West Nile virus in

this sample. Presumably, these birds had contracted and

transported the virus from stopover sites on their south-

ward migration route across southeastern Europe, an idea

supported by the genetic similarity of the Eilat viral

48S J .H. RAPPOLE AND Z. HUBALEK

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samples with samples from Romania and Volgograd, Russia

(Malkinson et al. 2002).

An interesting aspect of the recent outbreaks of West Nile

virus in Israel is the fact that a number of individuals of

several species (White Stork, Domestic Pigeon Columba

livia, Domestic Goose Anser anser, White-eyed Gull Larus

leucophthalmus) sickened and died as an apparent result of

viral infection (Malkinson et al. 2002). In previous Old

World outbreaks, actual observations of sickness or death

among avian hosts has been rare (Hubalek and Halouzka

1999; Komar 2000), leading Malkinson et al. (2002) to

suggest that the infectious agent might represent a new form

of West Nile virus.

4. ARRIVAL AND MOVEMENT OFWEST NILE VIRUS IN THE NEW WORLD –1999–2002

Significant numbers of sick and dead birds in and around

the Bronx Zoo in New York City, as well as several human

patients suffering from encephalitis of unknown origin from

the borough of Queens in southern New York City during

August 1999, were the first indication of a new epizootic

incident (Centers for Disease Control and Prevention 1999).

The first human testing seropositive for West Nile virus in

the Western Hemisphere was on 5 August 1999 while the

first seropositive bird was found dead on 8 August 1999,

although the pathogen responsible for either case was not

positively identified until 23 September 1999 (Centers for

Disease Control and Prevention 1999; US Department of

Agriculture 2002). Ultimately, 62 human cases were labor-

atory-confirmed during this initial outbreak (August–

October 1999), all from the New York City area, seven of

whom died (Centers for Disease Control and Prevention

2000a). Twenty-five equine cases also were documented in

the region, in addition to large numbers of infected birds

(Steele et al. 2000; Garmendia et al. 2001; US Department

of Agriculture 2002). The date for the last known human

onset for the disease in 1999 was 22 September, while the

last bird to test seropositive for West Nile virus in 1999 was

found dead in New York City on 5 November. A Red-tailed

Hawk, found dead in Bronxville, Westchester County, New

York, 20 km north of Queens, was found on 6 February

2000. Autopsy indicated death resulting from encephalitic

lesions typical of acute infection. Mid-winter is an unlikely

period for a mosquito vector to cause infection, and pathol-

ogists speculated that the hawk may have eaten a bird that

had died in late fall from the virus and contracted the

infection orally (Garmendia et al. 2001), a mode of transmis-

sion documented experimentally in laboratory mice (Odelola

and Oduye 1977) and, possibly, birds (Komar 2000).

Genetic analysis demonstrated that the form of the virus

responsible for the New York outbreak was virtually iden-

tical to that previously recorded from Israel (Lanciotti et al.

1999).

Thousands of birds of as many as 18 species died during

the 1999 outbreak, including an estimated 3000 American

Crows (Corvus brachyrhynchos) from the New York City area

alone (Steele et al. 2000). As noted above, significant avian

mortality has not been characteristic of West Nile virus

outbreaks in the Old World (Hubalek and Halouzka 1999;

Komar 2000). As the epidemic progressed during the late

summer and fall of 1999, reports of dead birds seropositive

for West Nile virus expanded outward from New York City,

eventually reaching many of the counties of New York, New

Jersey and Connecticut located within 250 km of the city

(Fig. 1). The most northerly record came from Columbia

County, New York, about 170 km north from the epicentre

for the outbreak in the New York City Borough of Queens;

the most easterly record was from Suffolk County, New

York on Long Island about 230 km east of Queens; and the

most distant record for a bird testing seropositive for West

Nile virus in 1999 was an American Crow found in

Baltimore, Maryland, on 14 October, roughly 300 km

southwest from Queens (Fig. 1).

VA

MDDE

150 km

NJ

PA

NY

MA

CT

RI

Fig. 1 Counties by state from which dead birds testing positive for

West Nile virus were reported in 1999. Counties from which positive

specimens have been documented are shaded grey

MIGRATORY BIRDS AND WEST NILE VIRUS 49S

ª 2003 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 94, 47S–58S

Speculation regarding the future of West Nile virus in the

New World was intense after the end of the 1999 infection

season. The history of Old World temperate-zone epidemics

of West Nile virus indicated that in order for the virus to

persist in the New World, birds might have to transport the

virus to the New World tropics or subtropics in autumn,

introduce it to a new set of avian, amplifying hosts, and then

bring the virus north from these areas in the spring (Rappole

et al. 2000). Following this scenario, the virus might die out

in the New World unless a suitable migrant bird host carried

the virus southward and introduced it into a tropical or

subtropical environment where it could establish a year-

round base. Given this possibility, efforts were made in

several southern states to find evidence of the virus in dead

birds. Such efforts were futile. No dead birds positive for

West Nile virus were reported from southern states during

the winter of 1999–2000.

However, the virus did reappear. On 22 May, an

American Crow was found dead in Rockland County, New

York, about 50 km north of the 1999 epicentre, and later

confirmed seropositive for West Nile virus to be followed by

many more bird, horse, mosquito and human reports

(Centers for Disease control and Prevention 2000b; Bernard

et al. 2001; Garmendia et al. 2001; Marfin et al. 2001).

Interestingly, all reports were from the northeastern United

States, and in fact, centred on the region of the original 1999

outbreak (Fig. 2). This pattern, plus information docu-

menting the fact that the virus can survive the winter in its

principal mosquito vectors and the absence of evidence of

the virus in New World tropical and subtropical regions,

makes it appear likely that the virus did not depend on

migratory birds to survive in the New World, but rather on

its mosquito vectors.

After reappearing in May 2000 in the New York region,

records confirmed reoccurrence of the virus in many of its

previous localities documented from 1999, but also showed

evidence of continued outward expansion, although not in a

strictly north–south direction, as might have been expected

based on a ‘Migratory Bird as Introductory Host’ scenario,

but rather evenly in all directions (Fig. 2), with the majority

of reports centred in the area where the 1999 epidemic

occurred. The locality furthest from the original New York

epicentre documented in 2000 was an American Crow found

in Chatham County, North Carolina, on 27 September,

about 700 km south of New York City. Assuming a New

World arrival date for West Nile virus of 1 June 1999 and an

infection season lasting from 15 April to 15 November in

Mid-Atlantic states, the virus moved at a rate of roughly

67 km a month (June–October, 1999; 15 April–27 Septem-

ber 2000). The most westerly record in 2000 came from a

mosquito collected in Erie County, Pennsylvania, about

570 km from the New York epicentre for the virus; the most

northerly record came from an Ovenbird (Seiurus aurocap-

illus) collected in August in Clinton County, New York,

about 480 km north of the epicentre; the most easterly

record came from birds collected in Barnstable County,

300 km

NCTN

IN

MI

Canada

PA

WVVA

MD

DE

NY

VTNH

ME

MA

CTRI

NJ

KY

OH

Fig. 2 Counties by state from which dead

birds testing positive for West Nile virus were

reported in 2000. Counties from which pos-

itive specimens have been documented are

shaded grey

50S J .H. RAPPOLE AND Z. HUBALEK

ª 2003 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 94, 47S–58S

Massachusetts, about 370 km east of the epicentre. No

records for birds testing positive for West Nile virus were

reported from Canada during 2000 despite examination of

2288 birds, 185 of which were submitted for laboratory tests,

mostly from regions bordering the northeastern United

States (Canadian Cooperative Wildlife Health Centre 2002).

The pattern of West Nile recurrence in 2001 was similar

to that seen in 2000. The first record for the year was from

an American Crow found dead on 30 April in Upper Saddle

River, Bergen County, New Jersey, about 40 km from the

1999 epicentre (Groves 2001). Subsequently, the majority of

human, avian, equine and mosquito cases came from within

500 km of the 1999 epicentre (Fig. 3). Nevertheless, the

virus continued to expand its distribution outward, reaching

a maximum distance of about 2100 km from the original

1999 New York detection point with report of a horse

positive for antibodies for West Nile virus in Calcasieu

Parish, Louisiana in August (Arbonet 2002). Both human

and avian cases were reported from the Florida Keys in

August, 1900 km from New York, and a possible human

case was reported from even further south on 24 August

from Cayman Brac in the Caribbean, although no avian or

mosquito records have been documented from that site.

Records from El Dorado, Arkansas (1850 km from Queens,

New York), St Louis, Missouri (1450 km), Walcott, Iowa

(1430 km) and Milwaukee,Wisconsin (1200 km), all repre-

sent the western limits of expansion for 2001; while a record

from Sabbatus, Maine (720 km), represents the furthest

northern and eastern expansion of the virus during 2001

(Cornell University Center for the Environment 2002a).

Confirmed records of infected birds also were reported from

Ontario in southern Canada, marking the first time the virus

has been documented outside the United States in the

Western Hemisphere. In moving from its southmost point

500 km

Fig. 3 Counties by state from which dead

birds testing positive for West Nile virus were

reported in 2001. Concentric circles centred

on the New York City borough of Queens are

shown in radius increments of 500 km

MIGRATORY BIRDS AND WEST NILE VIRUS 51S

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of distribution in August 2000 (Chatham County, North

Carolina) to Calcasieu Parish, Lousiana in August 2001, a

distance of about 1400 km, the virus appears to have

increased its rate of range expansion significantly in the New

World from about 70 km a month to as much as 170 km a

month, although the increased rate could be due, at least in

part, to an increase in number of months of vector activity in

the southern United States and/or failure to detect evidence

of further southward range expansion during 2000.

Data for 2002 has provided additional evidence of

continued expansion of the range for the disease, with dead

Blue Jays (Cyanocitta cristata) testing positive for West Nile

virus antibodies reported from Houston, Texas (Brewer and

Hopper 2002), 2700 km from the original 1999 outbreak in

New York City. However, one significant change in the

behaviour of the virus became obvious in 2002, namely that

the quiescent period for vector activity, which appears to

run from November to April in the northeastern states, is

short or non-existent in the Gulf states. Cases of West Nile

were reported from four Florida counties on 18 February

2002 (three horses, two wild birds and a sentinel chicken)

(Florida Department of Health 2002).

5. MODE OF ENTRY FOR WEST NILEVIRUS INTO THE WESTERN HEMISPHERE

Determination of how West Nile virus first crossed the

Atlantic to invade the New World is entirely conjectural.

Hypotheses have ranged from bioterrorism or infected

mosquitoes hitch-hiking in airplanes (Preston 1999) to

imported infected frogs (Zwerdling 2001). We suggested

that the most likely mode of entry was the one apparently

used by the virus in the Old World, namely via an avian

introductory host (Rappole et al. 2000). We proposed

three possible scenarios in which birds could serve as

the introductory host for West Nile virus into the New

World: (i) normal migration, (ii) storm-driven birds or

(iii) importation. Given the levels of viraemia required to

pass the virus from introductory host to vector to amplifying

host, and the generally short duration of such viraemic

states, we believe that importation of an infected bird is the

most likely mode of entry. Also, given that the form of the

virus appears to be quite similar to that found in the Middle

East (Lanciotti et al. 1999), an import from that region

would be the most likely culprit, perhaps for a zoo or private

collection. Although such imports are required to pass

lengthy quarantine periods, it would seem at least possible

for them to be exposed to local, New York mosquitoes at

Kennedy Airport during the period of transport from the

plane to their quarantine site, at which time a vector

mosquito could become infected and transfer the virus to a

local avian host. In addition, it is possible that imported,

West Nile virus infected birds could pass quarantine without

revealing significant clinical symptoms.

6. THE ‘MIGRANT BIRD AS INTRODUCTORYHOST’ HYPOTHESIS

In contrast to mode of entry to the hemisphere for the virus,

there seems to be a consensus regarding how the virus has

been able to move from its apparent arrival point in New York

City across much of eastern North America in the 36 months

since its initial appearance. Migratory birds are considered to

be the most likely introductory host, presumably transporting

the virus to new vectors and hosts at sites hundreds of

kilometres distant from New York (US Geological Survey

1999; Centers for Disease Control and Prevention 2000a;

University of Georgia 2001; American Museum of Natural

History 2002). Old World information on this point, while

mostly circumstantial and correlative, is nevertheless sup-

portive of this hypothesis, as discussed above. Indeed, in a

previous paper (Rappole et al. 2000), we speculated on how

the ‘Migrant Bird as Introductory Host’ hypothesis might be

expected to work in the New World (Fig. 4).

Bird on southwardmigration is infectedwith West Nile virusat a stopover site inthe New York area inSeptember, 1999.

Infected bird migratesnorthward in viremicstate to springstopover site withhigh concentrations ofpotential vectors andamplifying hosts,serving as anintroductory hostat a new, temperatesite.

Bird migrates in viremic stateto subtropical wintering site,serving as introductory hostto large concentrations ofvectors (mosquitoes) andamplifying hosts (other birds).

1

2

3

Fig. 4 ‘Migrant bird as introductory host’

hypothesis for movement of West Nile virus

from region to region

52S J .H. RAPPOLE AND Z. HUBALEK

ª 2003 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 94, 47S–58S

6.1 Factors supporting hypothesis

Two factors lend support to the hypothesis. First, the virus

obviously has moved far and fast in a manner that is not

inconsistent with migratory bird transport; and secondly,

migratory birds have been well documented to be the most

susceptible to, and commonest sufferers from, West Nile

virus infection among all vertebrate groups (Table 1).

6.2 Factors not supporting hypothesis

Nevertheless, there are factors that do not support the

hypothesis:

1) Rate of movement – members of most migratory species

fly at night. Flight speeds range from 30 to 70 km h)1

depending significantly on winds; strong tail winds can

double flight speeds. When conditions are favourable, they

generally depart at dusk, or shortly thereafter, and fly

continuously for as much as 10 h until dawn. Thus, a single

night’s flight for an average migrant might cover 200–

400 km, with considerable variation depending on species,

weather and obstacles (Kerlinger 1995). For example, a

Swainson’s Thrush (Catharus ustulatis), radio-tracked during

migration, flew 1530 km over a 6-day period, flying an

average of 7 h a night for an average nightly distance of

201 km (Cochran 1987), and other radio-tracked thrushes

flew up to 450 km in a single night (Cochran et al. 1967).

These speeds and distances are not unusual for the hundreds

of species of migrants that pass through the New York City

region. Thus, if migrants were, in fact, moving West Nile

virus, it would not be unreasonable to expect the virus to

move hundreds of kilometres in a matter of days. However,

this is not the pattern of movement that has been observed.

Instead, the virus moved a maximum of 300 km during the

3 months of known activity in 1999, and another 400 km

during 7 months of known activity in 2000. This rate of travel

is very slow if migratory birds are involved in transport.

2) Direction of movement – although actual direction can

vary depending on winds and exact destination, migratory

birds generally travel on a north–south axis, i.e. fall migrants

usually travel in a southerly direction on migratory flights,

while spring migrants move in a northerly direction.

However, during 1999, the virus moved nearly as far north

(170 km) and east (230 km) as it did southwest (300 km).

Similarly, while reaching a maximum distance from Queens

of 700 km southwest during 2000, it also reached distances

of 480 km north, 570 km west and 370 km east.

3) Pattern of recurrence in subsequent years – if migratory

birds were responsible for movement of the virus, there

would be no reason to expect an outbreak of West Nile virus

the following year to occur in or near the site of the original

outbreak. Migrants of most bird species in the New World

seldom use the same stopover sites on northward, spring

migration as they do on southward, fall migration because

migration routes are determined by complex interactions of

factors such as direction of prevailing winds, age and sex of

the bird, weather patterns, location of available food

resources and geographical barriers (e.g. large bodies of

water or mountains). These factors seldom combine to

favour the same route in different seasons (Rappole 1994).

Yet the obvious pattern for recurrence of West Nile in 2000,

2001 and 2002 was for it to recur in greatest concentration at

sites where it had occurred previously. This pattern suggests

that the virus probably over-wintered in the vector popu-

lation, and was passed subsequently to local, avian ampli-

fying hosts, rather than being moved south and north by

migrants in transit between breeding and wintering areas.

4) Host competence – the species suggested as the most

likely candidate as ‘Introductory Host’ for West Nile virus

(American Crow) is also the one known to suffer the highest

mortality rate from the virus (Eidson et al. 2001). Obviously,

crows are highly susceptible to infection, in fact apparently

shedding sufficient levels of the virus in faeces to allow bird-

to-bird transmission orally in laboratory situations (McLean

et al. 2001). Nevertheless, it remains unknown whether they

are physically able to move long distances, e.g. undertaking a

migratory flight of 200–300 km, once they have been infected.

5) Duration of viraemia – studies have documented that

levels of West Nile viraemia in several species of New World

birds (including those with migratory populations, e.g.

American Crow and Common Grackle as well as species that

are mostly resident, like the Blue Jay and House Sparrow)

are sufficiently high (105Æ4–1012Æ6 PFU/ml) to allow them to

serve as competent hosts for the virus (Komar et al. 2000;

Bernard and Kramer 2001). However, duration of such high

levels of viraemia has been found to be limited in time for

most species tested (usually <24 h). Interestingly, the House

Sparrow, a resident species, has demonstrated viraemia of

sufficient duration to indicate its ability to serve as a

competent host for West Nile virus (Komar et al. 2000).

7. ALTERNATIVE HYPOTHESES FOR WESTNILE MOVEMENT IN THE NEW WORLD

The considerations listed above raise questions concerning

the validity of the ‘Migrant Bird as Introductory Host’

hypothesis. Until these can be reconciled by field and

laboratory studies, it would seem appropriate to consider

alternative hypotheses, as measures for defence against the

virus are designed based, in part, on our understanding of

how it moves from one point to another. Accordingly, we

suggest below alternatives for West Nile virus movement in

the Western Hemisphere:

1) Sick migrant bird as introductory host – as noted

above, several migrant bird species have been documented

with high levels of viraemia. However, high levels of

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Common name Scientific name Residency status*

Double-crested Cormorant Phalacrocorax auritus Temperate/subtropical

Least Bittern Ixobrychus exilis Subtropical/tropical

Great Blue Heron Ardea herodias Temperate/subtropical/tropical

Green Heron Butorides virescens Temperate/subtropical/tropical

Black-crowned Night-Heron Nycticorax nycticorax Temperate/subtropical/tropical

Black Vulture Coragyps atratus Temperate/subtropical/tropical

Canada Goose Branta canadensis Resident/temperate/subtropical

Mute Swan Cygnus olor Mostly Resident

Mallard Anas platyrhynchos Temperate/subtropical

Bald Eagle Haliaeetus lecocephalus Temperate

Sharp-shinned Hawk Accipiter striatus Temperate/subtropical/tropical

Cooper’s Hawk Accipiter cooperii Temperate/subtropical/tropical

Broad-winged Hawk Buteo platypterus Tropical

Red-tailed Hawk Buteo jamaicensis Temperate/subtropical/tropical

American Kestrel Falco sparverius Temperate/subtropical/tropical

Merlin Falco columbarius Temperate/subtropical/tropical

Ring-necked Pheasant Phasianus colchicus Resident

Ruffed Grouse Bonasa umbellus Resident

Wild Turkey Meleagris gallopavo Resident

Virginia Rail Rallus limicola Temperate/subtropical/tropical

Sandhill Crane Grus canadensis Temperate/subtropical/tropical

Killdeer Charadrius vociferus Temperate/subtropical/tropical

Ruddy Turnstone Arenaria interpres Temperate/subtropical/tropical

Sanderling Calidris alba Temperate/subtropical/tropical

Laughing Gull Larus atricilla Temperate/subtropical/tropical

Ring-billed Gull Larus delawarensis Temperate/subtropical/tropical

Herring Gull Larus argentatus Temperate/subtropical/tropical

Great Black-backed Gull Larus marinus Temperate/subtropical

Black Skimmer Rynchops niger Temperate/subtropical/tropical

Rock Dove Columba livia Resident

Mourning Dove Zenaida macroura Temperate/subtropical/tropical

Great Horned Owl Bubo virginianus Resident

Snowy Owl Nyctea scandica Temperate

Common Nighthawk Chordeiles minor Tropical

Ruby-throated Hummingbird Archilochus colubris Tropical

Belted Kingfisher Ceryle alcyon Temperate/subtropical/tropical

Northern Flicker Colaptes auratus Temperate/subtropical/tropical

Eastern Phoebe Sayornis phoebe Temperate/subtropical/tropical

Blue Jay Cyanocitta cristata Resident

American Magpie Pica hudsonia Resident

American Crow Corvus brachyrhynchos Resident/temperate/subtropical

Fish Crow Corvus ossifragus Resident/temperate/subtropical

Common Raven Corvus corax Resident

Black-capped Chickadee Poecile atricapillus Resident

Tufted Titmouse Baeolophus bicolor Resident

Eastern Bluebird Sialia sialis Resident/temperate/subtropical

Tropical

Veery Catharus fuscescens Tropical

Hermit Thrush Catharus guttatus Temperate/subtropical/tropical

Wood Thrush Hylocichla mustelina Tropical

American Robin Turdus migratorius Temperate/subtropical/tropical

Grey Catbird Dumetella carolinensis Temperate/subtropical/tropical

Northern Mockingbird Mimus polyglottos Resident

European Starling Sturnus vulgaris Resident/temperate/subtropical

Cedar Waxwing Bombycilla cedrorum Temperate/subtropical/tropical

Table 1 Residency status for New World

bird species that have tested positive for West

Nile virus. Taxonomy follows the American

Ornithologists’ Union Check-List (1998,

2000)

54S J .H. RAPPOLE AND Z. HUBALEK

ª 2003 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 94, 47S–58S

viraemia are of short duration in most species that have

been tested and accompanied or followed by illness and

decreasing motor ability in many species. On the other

hand, apathic, less mobile birds (e.g. American Crows) can

attract more vector mosquitoes to feed on them success-

fully. It seems unlikely that such birds could move long

distances in an infectious state, but they might be able to

move 50–100 km before viraemia drops below infectious

levels or they succumb to the illness. However, if sick

migrants were the agents, direction of movement would

more likely be along the typical north–south migration axis,

which would not explain the broad lateral spread of the

virus observed to date.

2) Dispersing sedentary bird as introductory host – Komar

et al. (2001) state, ‘Thus, of the species we evaluated for

seroprevalence, the House Sparrow was an important � � � host

because of its abundance, high seroprevalence, and biological

competence.’ These factors make the House Sparrow a likely

candidate as an important amplifying host for the virus, in

addition to American Crows. The fact that House Sparrows

can move significant distances during dispersal episodes

makes them a plausible candidate as introductory host as well.

Fig. 5 shows distances at which House Sparrows have been

recaptured from original capture point for the 1117 birds

recaptured in the United States during the past 50 years. The

data show that large numbers of this supposedly sedentary

species move significant distances. For instance, 193 of 755

(25Æ6%) recaptured birds banded at <1 year of age moved

>15 km from their original point of capture.

3) Arthropods other than mosquitoes could serve as

vectors – if such arthropods as ticks could serve as vectors,

they could be both infected and transported by migrants,

and serve to introduce the virus to distant sites.

4) Displaced mosquitoes – mosquitoes have been known

to be blown tens of kilometres from sites of origin by strong

prevailing winds or vehicles. Thus mosquitoes themselves

could serve as introductory agents for the virus to new sites

under certain circumstances.

Table 1 (Contd.)Common name Scientific name Residency status*

Black-throated Blue Warbler Dendroica caerulescens Tropical

Yellow-rumped Warbler Dendroica coronata Temperate/subtropical/tropical

Blackpoll Warbler Dendroica striata Tropical

Ovenbird Seiurus aurocapillus Tropical

Canada Warbler Wilsonia canadensis Tropical

Song Sparrow Melospiza melodia Resident/temperate/subtropical

Northern Cardinal Cardinalis cardinalis Resident

Red-winged Blackbird Agelaius phoeniceus Temperate/subtropical/tropical

Common Grackle Quiscalus quiscula Resident/temperate/subtropical

Brown-headed Cowbird Molothrus ater Temperate/subtropical/tropical

House Finch Carpodacus mexicanus Resident

American Goldfinch Carduelis tristis Temperate/subtropical/tropical

House Sparrow Passer domesticus Resident

*Residency status categories: resident – a significant portion (>10%) remain on or near the

breeding region throughout the annual cycle. However, even for populations that appear largely

resident, some birds disperse and some young individuals may undergo short (<500 km)

migratory movements in fall; temperate – a significant portion (>10%) of the breeding population

migrates southward in fall to temperate regions for the winter period; subtropical – a significant

portion (>10%) of the breeding population migrates southward in fall to subtropical regions for

the winter period; tropical – a significant portion (>10%) of the breeding population migrates

southward in fall to tropical regions for the winter period.

Recapture distance

560

133

4 72 7

562

179202

562 3

0

100

200

300

400

500

600

0–14 km 15–45 km 46–90 km >90 km

AdultYoungUnknown

Fig. 5 Dispersal patterns for the House Sparrow in eastern North

America based on recapture data from the US National Bird Banding

Laboratory

MIGRATORY BIRDS AND WEST NILE VIRUS 55S

ª 2003 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 94, 47S–58S

8. THE FUTURE FOR WEST NILE VIRUS INTHE NEW WORLD

The best support for the ‘Migrant Bird as Introductory

Host’ hypothesis is the fact that the virus has reached the

Caribbean island of Cayman Brac, 560 km south of the

Florida Keys, where a single human case was diagnosed in

August 2001 unaccompanied by mosquito or avian evidence

of infection elsewhere on the island (Cornell University

Center for the Environment 2002b). The victim had not

travelled outside the island during 2001.

If migrants can serve as introductory hosts, transporting

the virus across ocean and desert barriers, then it should not

take long before the mainland Neotropics become enzootic

for the virus. In fact, that event already should have

occurred. At present, however, there is no evidence of this.

Nevertheless, it should be remembered that, with the

possible exception of Argentina (Cornell University Center

for the Environment 2001, and the Yucatan Peninsula in

Mexico (National Institute of Allergy and Infectious Dis-

eases 2000), surveillance programmes are scarce and under-

funded in the region.

If House Sparrows or similar ‘sedentary’ species are the

principal agents moving the virus by normal dispersal, then

the virus should continue at its present rate (70 km a

month for 6 or 7 months a year in north temperate regions;

70 km a month for 8–12 months a year in south temperate

and subtropical regions) across the United States and

Canada south perhaps to the latitude of San Antonio and

Corpus Christi in Texas, and the US border in the

southwestern US However, it may take some months or

even years longer for West Nile to invade the mainland

Neotropics because of the existence of significant barriers

to dispersal in the form of the Gulf of Mexico and the

broad belt of arid and semi-arid habitats that separate most

of the New World temperate regions from the tropics

(Dinerstein et al. 1995) (Fig. 6). In fact, 25 avian species,

including Blue Jay, American Crow, Common Grackle

(Quiscalus quiscula) and Fish Crow (Corvus ossifragus), find

the southernmost extreme of their ranges just north of the

latitude of Corpus Christi, Texas (Rappole and Blacklock

1985, 1994). Nevertheless, dispersing House Sparrows or

short-distance migrants (e.g. those cited as ‘subtropical’

migrants in Table 1) eventually will find their way across

these barriers, just as they have in the past. The House

Sparrow, first introduced into North America in New York

City in 1851, is now found almost throughout the

continent from central Canada south to southern Nicaragua

(Lowther and Cink 1995). It spread from its original

release point in New York to south Texas in about

35 years (Barrows 1889).

Whether by natural means, e.g. House Sparrow dispersal,

or artificial means, e.g. importation to zoos or other animal

facilities, West Nile virus eventually will enter the mainland

Neotropics, where it is very likely that it will spread rapidly

throughout the region, given the year-round abundance of

both competent vectors (ornithophilous mosquitoes) and

avian hosts. Human populations will more likely suffer from

this invasion, as will horses, and other domestic and wild

mammals and birds, although the likely results of such an

epidemic are unknown. The prevalence of vast, exposed

garbage disposal sites where high populations of both birds

and mosquitoes occur in proximity to large human popu-

lations pose a very serious threat to public health. Never-

theless, damage may be moderated among indigenous

vertebrates, including humans, by the conferral of some

level of immunity to West Nile virus from prior exposure to

related indigenous flaviviruses, e.g. St Louis Encephalitis

virus or Yellow Fever virus, and/or generations of host

experience with these or other heterologous pathogens

(Tesh et al. 2002).

9. ACKNOWLEDGEMENTS

We thank Stephen C. Guptill, Geography and Spatial Data

Systems, National Mapping Division, US Geological

Survey, for assistance with maps depicting US locations

for birds found seropositive for West Nile virus. Ms

Kathleen Klimkiewicz of the National Bird Banding

Laboratory, Patuxent Environmental Research Center,

US Geological Survey, provided House Sparrow band-

ing-recapture data. Data on avian, human, and mosquito

seropositive records for West Nile virus are derived from

the National Atlas of the United States of America, the

Centers for Disease Control and Prevention, and the US

Geological Survey.Fig. 6 Habitats of Mexico and Central America (light grey ¼ arid and

semi-arid areas) (Dinerstein et al. 1995)

56S J .H. RAPPOLE AND Z. HUBALEK

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