A
case study in evolution: West Nile
Virus and its impact on North American bird populations
David Joseph Horn
Assistant
Professor of Biology, Aurora University, Aurora, Illinois 60506
A presentation to the State Microscopical Society of Illinois
October 17, 2003
Introduction
Since its arrival to North America in 1999, West Nile Virus (WNV) has had a major impact on human, horse, and bird populations.
- According to the Centers for Disease Control and Prevention (CDC) as of October 1, for the year 2003, 5,861 human cases of WNV infection have been reported in 42 states. 115 of these human cases were fatal.
- In addition, WNV infections have been reported in 2,449
horses and 8,955 dead birds.
In Illinois, as of October 1, for the year 2003, there were
26 human cases of WNV infection with 1 human case being fatal.
In addition, WNV infections have been reported in 25 horses and 213 birds
in 66 of the state's 102 counties.
In this presentation, I will: 1) provide an overview of WNV
including a discussion of the spread of virus through North America and its
transmission cycle, 2) address the continent-wide and local impacts of the virus
on bird populations, and 3) give predictions of future consequences of WNV on
bird populations, all within an evolutionary context.
Overview of WNV and its transmission cycle
The spread of WNV
West Nile Virus is a Flavivirus in the family Flaviviridae.
- Members of this complex include St. Louis encephalitis
and are transmissible via mosquitoes
In 1999, an Israeli strain of WNV arrived in Queens, NY where it was mostly confined to a 50-mile radius around New York City
- There were at least 55 human cases, and 7 human deaths.
1000's of crows also died.
By the end of 2002, WNV was reported across the U.S. and Canada
- It had affected 44 states and 5 Canadian provinces.
* WNV caused 3, 400 human cases, 9,100 equine cases, and >14,100 wild bird deaths.
WNV virus first arrived in Illinois in September 2001,
where dead crows were found in the Chicago Metropolitan Area.
One year later, in 2002, Illinois, led the nation with 884 human cases with 66 deaths, and WNV was detected in 100 of the state's 102 counties.
- Cook County had the most human cases with 565 of which 32
resulted in death.
The global distribution of WNV and outbreak history
OVERHEAD – Global distribution of WNV
While WNV first arrived in the Western Hemisphere in 1999.
The distribution of the WNV is global and encompasses parts of Africa,
Europe, the Middle East, west and central Asia, Australia, North America, Latin
America (Mexico), and the Caribbean (Dominican Republic and Jamaica)
WNV was first isolated in an adult woman in the West Nile
district of northern Uganda in 1937.
Since its isolation notable human outbreaks occurred in Israel (1951-1954) and South Africa (1974)
From 1975-1993, no major epidemics of WNV were reported
Since 1994, however, human outbreaks have occurred in Romania, Morocco, Tunisia, Italy, Russia, Israel, France and the U.S.
- The outbreak of Romania in 1996 was the first in an urban
area of the industrialized world (~400 cases of encephalitis and ~40 deaths)
These recent outbreaks have shown an increase in severity of disease, and a high loss of birds accompanied with the human outbreaks.
- Reported deaths of birds in natural populations by WNV were few until 1998
* The increased severity of the outbreaks could be a result
of there being two lineages of WNV, and the lineage present in the U.S. and
Europe is the more virulent of the two.
(Lineage 1 is found in Africa, Middle East, Europe, Australia, and North America, while Lineage 2 is found in Africa)
* The increased severity of the outbreaks could also be due
to the previous history of WNV in the area and the subsequent level of
background immunity in the populations (Campbell et al. 2002)
(Studies conducted in the 1950's in Egypt found that WNV
circulates in most years, and West Nile fever is a mild and common childhood
disease, and background immunity is high - 40% of the human population in
Egypt's Nile Delta were seropositive for WNV)
How did WNV arrive in the U.S, and why has it spread so
quickly?
There are several proposed pathways by which birds may have brought WNV to North America (Rappole et al. 2001)
1) interhemispheric migration - several bird species migrate regularly in August and September from breeding grounds in the Old World to wintering grounds along the eastern seaboard of North America (i.e., Eurasian Wigeon)
2) tropical storm - a few birds are carried by tropical storms across the Atlantic each summer from the coast of West Africa to the New World (i.e., Cattle Egret)
3) legal and illegal importations - In 1999 alone, over
16,000 birds passed through J.F.K.International Airport legally.
There are other pathways by which WNV could have arrived in
North America such as an infectious mosquito on a jetliner.
The rapid spread of the virus is most likely due to migratory birds
- This is due to the pattern of spread, and the fact that the virus has been isolated from birds during the migratory period.
* In the late spring/early summer of 2000, spread of the virus occurred northward from New York City, while southward spread of the virus occurred in late summer and fall
*In a laboratory study by Jennifer Owen et al. of the University of Southern Mississippi captive wood thrush, swainson's thrush, and catbird were infected with WNV. The virus slowed migratory activity, but birds still displayed considerable levels of migratory activity.
* Malkinson et al. (2002) isolated WNV in a flock of 1,200 juvenile white stork in Israel during their migration from Europe in 1998.
(Because they did not fly over Israel, rather they were blown in a storm from Jordan, it was presumed that the storks acquired the virus on their migratory route.)
How is WNV transmitted?
WNV is transmitted mainly by mosquitoes, and primarily Culex species.
- However, 43 mosquito species have been found to be WNV positive in the U.S.
- Ticks and parasitic flies are also known to be vectors
The primary hosts of WNV are birds
- The virus stays within the host's blood for 1-6 days and are typically infectious for 3-4 days.
- The host develops antibodies after approximately 5 days
* The virus, however, can persist in the organs of
inoculated species for up to at least 100 days
Numerous mammal, reptile, and amphibian species are also
susceptible to the virus including humans, other primates (rhesus monkeys,
pigtail macaques, baboons, lemurs), horses, wolves, dogs, cats, sheep, goats,
bats, squirrels, chipmunks, skunk, seal, alligators, crocodiles, and the lake
frog
*Transmission of the virus is primarily through the salivary glands of mosquitoes to hosts during blood feeding meal
*Laboratory studies also indicate that WNV can be transmitted orally by saliva, via fecal matter, through unknown contact, and via predators eating prey (i.e., ingestion of mosquitoes or ingestion of mice infected with WNV)
(In humans, WNV may also be transmitted via blood
transfusion and organ transplantation)
What factors determine if an outbreak will occur?
The presence of WNV in an area does not mean an outbreak
will occur, loss can be minimal to severe depending upon the factors associated
with the virus, vector, host, and environment.
1) Virus factors – (i.e., genomic type, molecular
structure, phylogenetic relationship, virulence to host cells, and presence of
viral proteins that induce immunity)
2) Vector ecology – mosquito life history (i.e., susceptibility to the virus, competence to transmit, density and survival rate, feeding habits, and ecological association with the host)
3) Host ecology – bird life history (i.e., susceptibility
to virus, reservoir competence, attractiveness to vectors, daily activity
patterns, residence status of bird)
4) Environmental factors – climatic conditions (i.e.,
temperature, rainfall, seasonal weather patterns, surface water, and water
quality)
Continent wide-impacts of the virus on bird populations
What is the
magnitude of the impact of WNV on bird populations?
The magnitude of the impact caused by WNV is unknown
We do know that a large proportion of individuals tested have WNV infections
- In 2002, Of 31,514 birds tested, 50% were reported to be infected.
* However, we do not know the percentage of individuals
that show symptoms, die, or the extent to which viral infection may influence
lifetime survival or reproduction)
Since the arrival of WNV in 1999, there has been an
approximate doubling in the number of dead birds reported each year that are WNV
positive.
- However, the number of reported dead birds is most certainly an underestimate of the true number of birds that have died from WNV
* Larger bodied species are more likely to be found
* Bird testing usually takes place in larger-bodied species such as American crow and blue jay
* In many communities once the presence of WNV is reported
in 1 or 2 birds no further testing is conducted.
WNV infection in birds begins in May, peak infection occurs
in mid-August and goes through to the end of October.
The number of species that can be infected is extremely large
- Over 130 bird species are now known to be infected with West Nile Virus in the U.S.
* These species occur in a wide variety of ecosystems, and
include endangered species, game and non-game species, and domestic species.
Has WNV caused population declines in birds?
WNV virus has continental impacts that are most apparent at the local level
- infections are patchy at all spatial scales, and an outbreak may be ~ 1 km in diameter
* Christmas Bird Counts indicate a 90% decline in American
Crow population in western Long Island, but no change in population in central
and eastern Long Island.
Declines in American crows, black-capped chickadees, and
tufted titmice have been reported in the upper Midwest
Bonter and Hochachka (2003) used data from Project Feeder Watch, a continent-wide feeder survey, to examine population changes between the winter of 2001-2002 with the winter of 2002-2003.
- Observed greater than expected drops in counts of Black-capped/Carolina Chickadees at 74% of 203 sites, and the number of Chickadees counted was down 19% in the upper Midwest.
- American Crows declined at 70% of 173 sites, and the number of crows counted was down 61% in the upper Midwest.
- Tufted Titmice declined at 63% of 234 sites, and the
number of titmice counted was down 29% in the upper Midwest.
Not all species, however, had significant drops in counts. Blue jay, house sparrow, and northern cardinal were all seen at levels comparable with levels observed in the previous winter.
- Blue Jays increased at 52% of 301 sites.
- House Sparrow increased at 56% of 253 sites
- Northern Cardinals increased at 64% of 327 sites.
[Again, impacts of WNV are patchy. For example, blue jays increased at 52% of 301 sites but
displayed a 6% decrease in the upper Midwest, while increasing 15% elsewhere.]
West Nile Virus does not affect all species equally
In a study by Komar et al. (2003), 87 individuals of 25
species were exposed to WNV by infectious mosquito bite.
The scientists then examined viremia levels in birds and survival.
The most competent order of birds were the Passeriformes
(songbirds)
The least competent orders of birds included the
Galliformes (chickens) and Anseriformes (waterfowl)
The five most competent species for viral transmission were
blue jay, common grackle, house finch, American crow, and house sparrow (all
passerines)
Five of the least competent species for viral transmission
were Canada goose, American coot, rock dove, northern bobwhite, and ring-necked
pheasant
The majority of birds infected with WNV did not show signs of illness
- Of the 87 infected individuals, 28 birds showed signs of illness.
- However, in the majority of birds, death followed within
24 hours of signs of illness.
Individuals of eight species exposed to WNV died:
ring-billed gull, blue jay, black-billed magpie, American crow, fish crow,
common grackle, house finch, and house sparrow.
What are the symptoms of a bird infected with WNV – a
case study with raptors?
Raptors, such as Red-tailed Hawk, Cooper's Hawk, and Great Horned Owl, are highly susceptible to WNV
- Between August and October 2002, the Raptor Center at the University of Minnesota, College of Veterinary Medicine admitted 70 birds suspected of being infected with WNV. Approximately 60 of these birds died.
- At a long-term study site in Crawford County, Ohio, Thomas Grubb of Ohio State University observed a disappearance of 61 of 61 Eastern Screech Owls from the study area in 2002
Clinical symptoms of West Nile Virus in raptors include:
- thin to emaciated; dehydrated
- unaware of surroundings
- star gazing
- blindness
- head tremors
- head tilt and other postural disorders
- bobble head
- ataxia and unable to fly
- internal swelling of spleen, kidneys, and brain
- fly infestations
(other symptoms of WNV found in non-raptors include lethargy, ruffled feathers, and external hemorrhaging at the mouth and cloaca)
(WNV has been detected in brain, eye, kidney, heart, spleen, liver, lung, intestines, gonads, esophagus, and skin)
Different species, however, have different symptoms
- Great Horned Owls have bobble head, while Red-tailed Hawks do not
*most likely based on location of swelling (i.e., swelling
in Great Horned Owl brain may be greater than that in the Red-tailed Hawk)
A closer look at the effects of WNV using micrographs
The mechanisms and sites of WNV replication are unknown.
- Once inside the host, WNV envelope protein facilitates cell attachment and may be a primary virulence factor.
- In severe cases, pathological changes in the central nervous system may be a result of (Campbell et al. 2002)
1) viral proliferation within nerve and glial cells,
2) cytotoxic immune response to infected cells,
3) diffuse perivascular inflammation
4) microglial nodule formation
Local impacts of the virus on bird populations
First appeared in 2001
Widespread in 2002, with only 2 of >100 counties in Illinois not reporting an infected pool or bird
- Results of state studies are similar to those observed
nationally
In a study by Sarah Yaremych et al. of the University of
Illinois, from May – October 2002, 28 crows in the Champaign/Urbana region
were given radiotransmitters, and 19 died of WNV
In a study by Moskoff of Lake Forest College, a comparison
of the abundances of eight common species of birds during Christmas Bird Counts
(CBCs) in the Chicago Region during Dec. 2002 - Jan. 2003 was compared with
historical averages from the same count areas during 1982-2001.
- Moskoff found that the abundances of Blue Jay, American Crow, and Black-capped Chickadee declined significantly, and were below 95% confidence levels.
- Mourning Dove, Downy Woodpecker, White-breasted Nuthatch,
Northern Cardinal, and American Goldfinch populations showed no significant
change, and abundances were within expected values.
Bonter and Hochachka (2003), using Project Feeder Watch
data, found that the average number of crows counted in Illinois was down 91%,
and the average number of chickadees and blue jays counted was both down by 26%
Future predictions
WNV is here to stay and will spread throughout the rest of Western Hemisphere's tropical and temperate climates
- In the near future, major epidemics will be reported as immunologically naive populations become exposed. However, several years from now epidemics will be fewer occurring only when conditions are appropriate.
* In most years, the impact of WNV will be low to moderate
The long-term impact of WNV on North American species will be small
- Populations of immunologically naive individuals will be replaced via natural selection
(A study of Hooded Crows found few deaths in Egypt and a high seroprevalence rate in natural crow populations; suggesting a high rate of survival of infection)
- The virulence of WNV will decrease
Greatest impact will be in tropical species whose population sizes are small and distributions are local.
- Small populations are more susceptible to changes in population size or reproductive success
* Dominican Republic's White-necked Crow or Hispaniolan
Palm Crow are already diminishing in population size, and corvids have
been found to be competent reservoir species
West Nile Virus is the prelude to other new parasitic infections in North America
- assuming there are efficient vectors, suitable amplifying
vertebrate hosts, and reliable overwintering mechanisms we will continue to see
the introduction of additional diseases in this era of global commerce and
travel
Acknowledgements
Robert G. McLean, National Wildlife Research Center, Fort
Collins, Colorado provided several of the data slides
Many of the case studies described above were presented at
the American Ornithologists' Union 121st State Meeting at the
Symposium “West-Nile Virus and Birds”
Answers to other questions:
How does the virus survive in winter?
Studies in Africa found that it is through adult mosquitoes hibernating, and
trans-ovarial transmission (egg of mosquitoes have virus).
It is also possible that the migration of birds from tropical to
temperate regions allows the virus to survive in winter.
Does age affect survival of WNV infection?
Because juvenile birds may have a less developed immune
system and more exposed skin, they may be more susceptible to WNV infection.
Two studies indicate that there is no effect of age.
- Mary Garvin et al. of Oberlin College found 51% of 950 Blue Jays tested for WNV in Ohio were positive in 2002
*However, there was no effect of age
(Infections also occurred in nests; of 5 nests sampled, 4
had nestlings that were WNV positive)
- Kevin McGowan et al. of Cornell University found that only 3.2% of American Crows sampled had antibodies (suggests if crow gets virus it dies).
* However, found no difference in susceptibility between
age classes and between sexes
What else do we need to know about West Nile Virus and
its impact on bird populations?
There is a need to develop predictive models for outbreaks of West Nile Virus
- Need to determine what virus, vector, host, and
environmental factors are most important factors causing an outbreak.
We do not have a system in place to adequately measure localized changes in bird populations, or determine their causes
- Continent-wide surveys such as Breeding Bird Survey, Christmas Bird Count, and Project Feeder Watch do not always show the same trend
- In many communities once the presence of WNV is reported in 1 or 2 birds no further testing is conducted.
* Furthermore, there are many factors that influence whether a dead bird will be reported. (There are factors influencing if a dead crow is found (human density, crow density, scavenger density), if a dead crow is reported (discoverer's motivation, institutional motivation), and how reports are generated (does the report give the exact location, city, county, state, etc.)
- Birds may be infected by WNV, but it may not be the sole
cause of mortality
We do not know the extent that bird to bird contact, and oral and cloacal transmission play on the spread of WNV
- Bird feeders attract large numbers of individuals within a small area, however, we don't know whether the high congregation of birds influences the spread of WNV through transmission of feces, saliva, or other contact
What is probably the least known consequence of WNV?
- In 2002, over 15,000 equine cases were reported in 40 states.
- WNV causes stumbling and incoordination, depression or apprehension, weakness of limbs, muscle twitching, and partial paralysis.
* Around 33% of infected horses die.
- A WNV vaccine license for horses was approved in November 2002
What is the risk of humans to WNV?
- The majority of mosquito bites will not lead to WNV infection
- The majority of people infected with WNV will not show any symptoms
- Approximately 20% of infected individuals will develop West Nile fever (fever, headache, and body ache)
- Approximately 0.67% of infected individuals have central nervous system infections (i.e., encephalitis and meningitis)
* Symptoms usually occur 3-14 days after bite of infected mosquito.
* Older individuals (i.e., >50) are more likely to suffer from more severe consequences
What precautions can I take to reduce my chances of
acquiring WNV?
WNV can be deadly (hundreds of people died of WNV in 2002), however, it is not as deadly as other diseases such as influenza, which averaged over 30,000 deaths per year during the 1990's.
To lower your risk of contracting the disease avoid being bitten by mosquitoes, and reduce the probability of mosquitoes breeding in your neighborhood
- Limit outdoor activity when mosquitoes are most active (i.e., dawn, dusk, nighttime)
- Wear long clothing
- Use insect repellants, including those that contain DEET
* a product containing 20 deet may provide nearly 4 hours of protection
Prevent mosquitoes from breeding by reducing sources of standing water (mosquitoes can breed in temporary areas that last more than 4 days)
- drill holes in bottom of containers
- clean clogged roof gutters regularly
- change water in birdbath
- aerate ornamental pools
- turn over wading pools and wheelbarrows
- clean and chlorinate swimming pools or let water stands on pool covers
- where standing water cannot be eliminated, consider using commercial larvicide such as BTI to prevent mosquito reproduction
At the community level, surveillance and control programs need to be put in place
- Programs may include passive surveillance of dead birds such as crows and active surveillance using sentinels such as chickens