Avian Cholera and Waterfowl Biology Author(s): G. Wobeser Source: Journal of Wildlife Diseases, 28(4):674-682. Published By: Wildlife Disease Association DOI: http://dx.doi.org/10.7589/0090-3558-28.4.674 URL: http://www.bioone.org/doi/full/10.7589/0090-3558-28.4.674
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Journal
of
Wildlife
28(4), 1992, pp. 674-682 Disease Association 1992
Diseases, © Wildlife
LETTER
TO THE
Avian
Cholera
EDITOR...
and Waterfowl
Biology
In a review of the ecology of Pasteurella multocida infection in waterfowl, Botzlen (1991) indicated that many fundamental
posed individuals laboratory, birds tion of a few
questions
(Hunter and Wobesen, 1980); however, under natural conditions a larger number of organisms is likely required to result infection. The probability of infection
remain virulence
tneme
control waterfowl ca”
one
ease, and
of the management
(Bolen
Botzlen because
unanswered; yet “the of avian cholera makes
et
a!.,
highest
lack
1989).
has
development
wetlands while the
The
particularly a model
of which
of
gies. Research nomena, such
priorities for North Amen-
in
(1991) was it proposed
by
management
strate-
found of the
is increasing
managing habitat tering waterfowl
duced
phe-
to relate
and
habitat
disposing occur. In this
and
in
and winSmith et
disease
bacterium. will
If not
a bird
occur.
The
is not
to the of factors
lated lihood
is con-
on recover
but de-
is influenced
agent, that
as well influence of
enough an in-
bird being exposed, infected, and dying of avian cholera of many separate probabilities
disis the re-
to exposure and of an outbreak
resistance. occurring
long
as by the
The likeintroduces
another range of probabilities. A major unknown in the ecology of avian cholera is the source of P. multocida. I believe that avian cholera is perpetuated by fowl
carriers
of P. multocida
although
evidence
among for
water-
existence
of
carriers in wild waterfowl is inconclusive. Pasteurella multocida has been recovered from clinically healthy waterfowl (Vaught
bird
exposed,
probability
die
by its resistance the presence
dividual eased, product
between P. multocida and a susceptible bird (Fig. 1) as a starting point. Even in the most devastating outbreak not all binds
and
subsequently
ability of a sick bind to survive to recover. Thus, the likelihood
changes
interaction is not all-or-nothing. is the coming together of
cholera
of pro-
on
to avian cholera, with the intent of further stimulating interest in this disease. It is useful to consider the interaction
die, so the Exposure
Avian
consists illness
velop disease following infection is unknown, as is the proportion of diseased binds that recover. The probability that an infected bird will become diseased and
dead, disease
of carcasses letter I hope
management
infection.
Disease signs of
degree and
of
but management to control aviis reactive, consisting primarily
of collecting when outbreaks
by
and organism,
in is
sidered an acute, highly fatal infection the actual proportion of waterfowl that
interest
for migrating (Weller, 1987;
duration of the
the bird’s resistance. physical changes and
research
has centered on local as defining characteristics
There
related to the route, of exposure, virulence
valuable for the dis-
little attention. Waterfowl has, in general, focused of birds, with comparatively to reduction of non-hunting
mortality.
a!., 1989), an cholera
review
hampered
where birds were population ecology
has received management production little attention
exits
become infected. In the can be infected by injecP. multocida organisms
et a!., 1967; Konschgen
of
et al., 1978; Titche,
exposure is related to the density and distribution of bacteria and birds, the amount of time they spend together, and viability of the bacterium in the environment. The
1979) but the virulence lated from these birds
bind’s resistance has no effect on the rate of exposure. Infection involves invasion and growth of bacteria in the bird. Not all ex-
(Hughes and Pnitchett, 1930; Iliev 1964; Curtis and Ollerhead, 1981). riers have been reported in domestic
The ens
674
importance has been
of the bacteria isowas not reported.
of carrier birds in chickknown for many years et
a!., Cargeese
LETTER
and these infection
apparently for chickens
served as a source (Hellen, 1958).
of In-
TO THE EDITOR
675
BSrd
PastoiarUI
vestigators searched unsuccessfully for carriers in domestic turkeys until Carpenten et a!. (1989) demonstrated that they were
common
breaks.
among
Special
survivors
techniques,
of
as used
out-
by Car-
penter et a!. (1989), should be applied the search for carriers among waterfowl and any P. multocida isolated must characterized fully. The most likely routes of transmission
Infoot
to be
among birds are through bird-to-bind contact and via contaminated water. Different routes of transmission may explain different
disease
patterns.
Avian
among northward katchewan each but
1979)
only
a population is confined (Chen rossii),
a few
birds
occurs
are
in Saset a!.,
affected
in
of many thousands. Disease almost entirely to lesser snow
c. caerulescens) although other
lands spread white
cholera
migrating geese spring (Wobesen
and Ross’ geese (C. species share wet-
with these birds, suggesting that occurs within the population of geese through direct contact. Wind-
ingstad pattern
et a!. among
braska
and
(1988) described mallards in
Botzler
of scattered
(1991)
mortality
that
a similar western Ne-
included
reports
“never
develop
to extensive epizootics.” This form of “smouldering” avian cholera may go undetected, unless a special effort is made to search common
for dead than
example, we avian cholera since
1977
dead bers
geese of the
birds, and recognized
is probably currently.
have found in Saskatchewan
geese
but
during
have public
this
been only
more For
but
deaths
cies
migrate
in the
eider
relationship
multocida
continue
Reported
one
between
and
to occur
north.
breaks, with colonial-nesting
as some
spe-
summer
out-
exception, have species such as
(Somateria
mollissima)
been common
(Reed
(Hanson tion was which
and Mutalib, an outbreak >4,900
in
ducks,
1989). The Saskatchewan
primarily
(Aythya
americana)
moulting, 1988).
died (Wobeser common feature
breaks nificant south
period
grounds
by memexplosive
curred terfowl
A
a
and in
(Brand,
1984).
for Leighton, these out-
aggregation. Sigbirds migrating twice. One in-
birds exposed die-off on
in October of at least
in
redheads
concentrated
has been dense mortality among has been recognized involved from
excep-
The
the
to geese rebreeding second
gests
tumn outbreak. When we consider
seasonal, spring when
peaking (Friend, birds
disperse
exposure
to a common
probably outbreaks
contaminatare distinctly
in late winter 1987). Mortality from
the
epizootic
to early declines site,
oc-
1991 when >1,000 waseven species died in
Saskatchewan. Lesser snow geese sandhill cranes (Grus canadensis) from area of an earlier summer outbreak in western arctic were present during the
simultaneous
in and
outbreak, involving hundreds or thousands of birds of many species, is the more generally recognized form of avian cholera. The pattern in many such outbreaks sugsource of infection, ed water. Major
the
a bird.
Cousineau, 1967; Korschgen et a!., 1978; Jorde et a!., 1989), lesser snow and Ross’ geese (Wobeser et a!., 1979), and doublecrested cormonants (Phaicrocorax auritus)
stance turning
14-year
reported once. The
Phases
Pasteurella
dead of spring
each
1.
FIGURE
bacterium
information
from
and the the authe
entire continent it suggests that P. multocida is present in at least some waterfowl populations throughout the year. The prevalence of disease is lowest in autumn,
676
JOURNAL
increasing spring, perse.
OF WILDLIFE
to a peak
in late
VOL. 28, NO. 4, OCTOBER
winter
and then declining Outbreaks occur among
centrated
during
followed grating
by birds.
spring species,
staging while
year
DISEASES,
the
summer
mortality Outbreaks
is restricted
and
discon-
may
be
in southward on wintering
areas often mortality
involve at other
to one
or
changes
to early
as binds species
miand multiple times
a few
of
that
populations reservoirs
of
impact
of less
‘
‘certain
white disease
large geese that
abundant
or other
local
may
have
food important
If R0 is defined
as
this
and
a
serious
ment The
of
problem
and which had resulted in loss of 53% of wetlands in the lower 48 states by the 1980’s 1990).
Stewart
et
“the rates of wintering modification have been last 25 years, and these are affecting the dance of wintering also been a change lands,
with
an
a!.
(1987)
habitat staggering changes
stated loss
and in the certainly
distribution and abunwaterfowl.” There has in the character of wet-
increase
in large
chol-
number
of
to a sininto a sus-
is intuitively
rea-
reservoirs
promote species
popuand
mixing
that
were
of once
mixing of has been the manage-
species (Anonymous, 1991). of carriers of P. multocida
waterfowl
Central lowed which
on sparse Aggregation
Recent large-scale goose populations as a problem for
of these prevalence
among
(Friend, 1981). The most obvious change has been continuation of the loss of wetlands that began at the time of settlement
(Dahl,
average
“it
and
populations
as
cause,
on avian
attributable introduced
in distribution
populations
of
diseases
as the
or dense than in a small lation” (Fine et a!., 1982).
have wild
infectious
effects
population,
changes
pop-
changes affecting as emergence
abunof
of exposure to disease in dense aggregations.
secondary infections gle infectious case
segregated. arctic-nesting recognized
habitat as well
provide
regardless
era. The probability agents is enhanced
ulations” (Anonymous, 1991). Enhanced exposure and/or reduced host resistance could facilitate transition from the enzootic form maintained by bird-to-bind transmission to a water-borne epizootic. During the past several decades there been major waterfowl,
that
but,
sonable to expect that R0 should be a function of population size on density, insofar as any individual is likely to contact more individuals pen unit time in a large
increasing
may serve may adversely
species
in agriculture
dant
ceptible
species.
Colonial-nesting species, such as lesser snow geese, may maintain the bacterium over the summer because of their dense aggregation on breeding areas. There has been speculation
1992
is unknown may
other
but
enhance
agents.
mixing
exchange
Outbreaks
of in
the
and Mississippi flyways have folmixing of populations, some of were known to have been previ-
ously exposed to avian (1984) suggested that the bacterium to new
cholera, carriers areas.
and Brand introduced Pasteurella
multocida is not the only disease agent that may be exchanged. The effect of other agents may not be dramatic but each represents a “cost” to the host (Yuill, 1987) and the aggregate cost of exchanged parasites
may
render
birds
to infection and/on to P. multocida.
more
disease
susceptible
when
exposed
(>200 ha) and a decrease in smaller wetlands (Buller, 1975; Pederson et a!., 1989; Ringelman et al., 1989). Most waterfowl
dividual may be
are gregarious, so that aggregation is normal; however, the dense concentration of binds that now occurs on staging and wintering areas (>1 million binds at some sites
cholera. For example, snow geese on traditional wintering areas along the Gulf coast were “constantly on the move from one location to another, rarely using one
(Strong et al., mal. Concentration
feeding and resting area for more than two or three weeks,” whereas many now spend the entire winter on a water area (Yancey, 1976). Pasteurella multocida persists in
loss of refuges
1991))
is probably may occur
not because
alternate habitat, development on man-made water areas,
norof of
and/or
The
long-term wetlands another
or
continual
use
throughout the change affecting
of
in-
winter avian
LETTER
water
for
days
that bacteria of the disease The
to weeks from will
probability
of
(Botzler,
1991)
carriers accumulate
or birds over
sufficient
bacteria
so
dying time. ac-
cumulating to result in water-borne tnansmission is a function of the number of binds shedding bacteria, the length of time they are present on the wetland, the number of bacteria shed, the survival time of bacteria in water and the amount of water. Bird density should be calculated measure of time, such as use of the area, to account of
accumulation.
culated
Density
in relation
although,
to include a total bird-days for this factor might
to the
if bacteria
be
volume
cal-
of water
accumulate
near
the
surface (Botzler, 1991), area may be more important than volume. Concentration of birds might reduce resistance to infection. “Crowding” is often considered a stressor in relation to disease but and
interactions infectious
predictable resistance increasing
between disease are
social pressure not consistent or
(Esch et a!., 1975). In chickens, to some agents improved with social stress, up to a point, and
then declined; resistance was inversely proportional of stress (Gross, 1984).
other agents to the amount There is little in-
formation
waterfowl.
available
on
to
study, crowded ducks retained administered dose of parasites crowded controls and parasites and caused greaten tissue crowded binds (Ould and Stress,
as a result
a direct
effect
cholera,
as well
enhancing could, in multocida.
other turn,
might effect
parasitic influence
conditions resistance
energy cranes
demands between
supplied 1989).
The
spring;
e.g.,
of mallards October and
by grain situation
many geese. Grains proteins, minerals
have
to
as an indirect
to early
one
in the 1980).
susceptibility
has been a marked to dependence
There waterfowl autumn
damage Welch,
of crowding, on
In
more of an than did lesswere larger
on
avian
through that to P.
shift by grains >90%
some from
of food
and sandhill February are
(Clark and Sugden, i probably similar for are deficient and vitamins
in specific (Baldas-
same natural
et a!., 1983; foods are
TO THE
Jorde required
balanced
diet
(Delnicki
Reinecki
and
Knapu,
et
EDITOR
677
a!., 1983) to maintain
and
and a
Reinecki,
1986;
1986;
Loesch
and
Ka-
minski, 1989). Nutritional deficiencies affect resistance to infectious disease (Watson, 1984; Chandra, 1988) and one nutrient, deficient in many grains, may be of particular consequence. Vitamin A has been called the “anti-infection vitamin” (Sommen, 1990) and effects of deficiency on resistance to disease agents are well-doeumented (Chandra and Newberne, 1977; Gross
and
Sijtsma
Newberne,
et al.,
Deficiency
1980;
1989;
Beisel,
Friedman
interferes
with
Friedman et al., 1991).
A deficiency
have
(Anas
terfowl
is unknown.
to
in black in Masmallards
overwintening
(Wobeser and of deficiency
in
Kost, among
Concentration
terfowl on wetlands riod may exacerbate through quired
reported
wintering 1950) and
platyrhynchos)
Saskatchewan but the extent
of
as barriers to production (Davis and
and Sklan, 1989; Lesions of vitamin
been
ducks (Anas rubripes) sachusetts (Hagar,
1991).
maintenance
epithelial surfaces important infection and with antibody and lymphocyte proliferation Sell, 1989; Friedman
1982;
et a!.,
1992) waof wa-
for an extended penutritional problems
depletion supplement
of
natural foods grain (Jonde et
real.,
1983).
Fungal waterfowl birds
growth might
may
in the
be infected
disease
poisoned Waterfowl
on also
grain affect
consumed disease.
by fungus,
aspergillosis;
others
by toxins produced die of mycotoxicosis
by Some
resulting may
be
by fungi. (Robinson
et al., 1982; Windingstad et a!., 1989) and sublethal exposure to mycotoxins might impair resistance to avian cholera (Smith et a!., 1990). Demand for water has increased, particularly in western North America, so that “wet” lands must compete for a share. Water
available
for
wildlife
is often
of
poor
quality and wetlands have become a method of disposing of effluent-laden water, e.g., the
Kesterson
National
Wildlife
Refuge
in
678
JOURNAL
OF WILDLIFE
California
(Zalm,
novative (Snyder
wastewater and Snyder,
DISEASES,
1986),
VOL. 28, NO. 4, OCTOBER
or a lowcost
treatment 1984). The
“in-
system” most corn-
mon contaminants are associated with agnicultural runoff. Direct toxicity, such as that associated with selenium (Zalm, 1986; Kadlec and Smith, 1989), may be the most obvious problem.
expression Effects
of
of a more sublethal
widespread exposure
to
most chemicals present in runoff water are unknown, as is the interaction between these chemicals and infectious diseases. Some contaminants increase the susceptibility of mallards to P. multocida ley and Yuil!, 1991) but methods ing such complex interactions infancy
(Porter
contaminants tle attention. herbicides duction a grain
of nutrients diet (Cain,
Fertilizers some have
et a!.,
1984).
on wetlands Turbidity, might negatively
(Whitefor studyare in their The
effect
has received insecticides affect the
increase
of litand pro-
nutrients but been implicated
production
and
occurrence
ponds
in the
Rainwater
inorganic fertilizers in the decline of sub-
of avian Basin
cholera
in
ions (Price and Brand, 1984) and protein content, increased salinelevated temperature (Bredy and 1989) enhance survival of the bac-
terium wetlands
in
to a borne
concentration transmission.
Many canadensis)
Cold, are ern
sufficient
mallards, and
winter
north
1975; Bateman
might enhance of P. multocida
Yancey, et a!., inclement
likely binds
of
of and survival in water
for
water-
Canada geese (Branta lesser snow geese now traditional
areas
1976; Jorde 1987; Pederson weather
to be common and might
and
(Buller,
et a!., et a!., food
by wells, or use natural
1984). areas
These birds often of water kept un-
turbulence deep food.
or thermal
1983; 1989).
scarcity
stressons for northreduce resistance to
pol-
reservoirs that Overwintening
provide binds
may
contribute to a decline in water qua!favorable to survival of P. multocida in water; usage of wetlands during winter, ity
as well as during spring migration, increases the potential for accumulation of the bacterium (Smith et a!., 1990). Birds ovenwintering in the north are probably more dependent
on agricultural
crops
and
lards
wintering
in
Nebraska
consumed
If asked to design a set promote frequent occurrence of avian
cholera
include:
a) a large
posed ulations
of a mixture to increase
more
than are For examthat ma!-
diet containing 37% less protein mallards wintering in Louisiana.
a
than
did
of conditions of large
on
a site,
population
I would
of birds
of species and the likelihood and to promote b) restriction
to outcom-
sub-popof in-
exchange of the birds
to a small water area for an extended time to promote accumulation of P. multocida in water, a high rate of contact among binds, a high degree of social stress and depletion
Certain increased ity and Botzler,
thermal pollution and accumulation
frozen lution, little
(Olson, small
cluding carriers of disease agents;
of Nebraska.
water. Thus, contamination with salts, organic matter
on
breaks of
merged aquatic vegetation in Chesapeake Bay (Hindman and Stotts, 1989). Contaminants might also alter survival of P. multocida in water. Windingstad et al. (1984) found a positive correlation between water salinity
infection crowd
prone to nutritional deficiencies birds that winter to the south. ple, Jorde et a!. (1983) reported
needed to supplement 1987; Reid et al., 1989).
might
1992
of
natural
ditions tocida
favorable for (e.g., increased
matter
and
thermal
dence of the in nutritional to mycotoxins; of inclement
foods;
Botzler lead
model
water
pollution);
con-
P. mu!organic d)
depen-
birds on a grain diet to result deficiencies and expose birds and e) frequent weather, food
posure to chemicals in the stnessors. These conditions similar to those experienced terfowl in North America time. The
c)
survival of salinity,
of avian
(1991)
and
to at least
three
ex-
water, and other seem perilously by many waat the present
cholera the
occurrence shortage,
above
hypotheses
proposed
by
discussion that
could
be tested. Hypothesis 1: Pasteurella tocida is maintained by carrier birds in waterfowl populations. Several
mu!withques-
TO THE EDITOR
LETTER
tions
follow
from
this
hypothesis.
Where
However, populations, to reduce
be possible wetlands and exposure of birds
679
to manipulate food resources to P. multocida
it may
is the bacterium carried in the body? What is the prevalence of carriers in different species? How long is the bacterium carried by individual birds? Does the prevalence of carriers change seasonally? What fac-
and to factors that interfere with disease resistance. Avian cholera is a complex disease but, as stated by Leopold (1933) in
tons
regard
promote
shedding
of bacteria
by
car-
riens? of
very
Hypothesis Pasteurella
major
2: Waterborne multocida
outbreaks
is
of avian
transmission involved
cholera.
in
Several
questions also follow this hypothesis. Does P. multocida accumulate in the water of wetlands overwinter? What factors influence
survival
What
of the
is the
multocida various
threshold
Questions include
the
readily raised following.
do
fect resistance prevalent is the by
dian
Wildlife
ada,
14 pp.
and contaminants on resistance to
CITED goose
(1991)
noted
of a model of avian more by a lack of
that
cholera consistency
there may ing various
be a variety combinations
ex-
available
Wildlife
H.
A.,
winter
range.
Weller
(ed).
a single of the
It is unlikely
model disease. that
to the
explain amount
all
occur-
of wetland
area available for wintering birds can increased substantially, so that dispersal birds over a greaten area solution to the problem
is not a practical of avian cholera.
be of
venture.
Venture,
A
Cana-
Alberta,
to
Can-
postbreeding
Society
water-
Bulletin
T.
JOANEN,
1 1 : 25-
History
snow geese In Waterfowl
on
1982.
pp.
their in
D.
status
Gulf
of
Coast
winter,
M.
W.
Press,
Min-
495-515.
Single
Journal
and
of Minnesota
Minnesota,
C.
AND
1987.
University
W. H.
nutrients
of Clinical
and
immunity.
Nutrition
35:
417-
468. E.
BOLEN,
involvrather
used
H. J. WHYTE, E. E. QUINLAN, 1983. Dynamics and quality
corn
American
in
avian cholera of factors are areas. Thus,
of patterns of factors
,
joint
Joint
Edmonton,
in Texas.
neapolis,
hindered in the in-
be
31.
BEISEL,
than by a paucity of data. Many that enhance exposure or reduce to infection could contribute to
the occurrence of epizootic and different combinations likely to apply in different
Goose
Service,
midcontinent
development was
Arctic
STUTZENBAKER.
avian
of at-
day
LITERATURE
BOLEN.
waste
BATEMAN,
af-
does
“this
points
some
1991. Arctic
G. A.
E. G.
fowl
hypowater-
effect
ANONYMOUS.
AND
is
the
grateful to K. F. Higgins, F. A. C. Riddell, and S. V. Tessaro for and suggestions.
G.,
G. A. BALDASSARRE, AND 1989. Playa lakes. In Habitat
GUTHERY.
cholera? Botzler
than rences
I am Leighton, comments
of
in general:
of which may measures.”
BALDASSARRE,
cholera? How of mycotox-
What
posure to mycotoxins wastewater have
deficiencies and contamavian cholera.
deficiencies
to avian consumption
waterfowl?
under
particularly wintering
nutritional
tack, one for control
prospectus.
by this hypothesis How prevalent
deficiency, A, among How
formation factors resistance
transmission
3: Nutritional to mycotoxins resistance to
nutritional vitaminosis
ins
for
of P.
diseases increases
in wetlands?
concentration
required circumstances?
Hypothesis and exposure inants reduce
fowl?
organism
to wildlife complexity
agement
for
in North
America,
and
migrating
H. M. Kaminski
and
wintering
L. M.
Smith,
(eds.).
Texas
F.
S.
man-
waterfowl
H. L. Tech
Pederson, University
Press,
Lubbock, Texas, pp. 341-365. H. G. 1991. Epizootiology of avian cholera in wildfowl. Journal of Wildlife Diseases 27:
BOTZLER,
367-395. BRAND,
C. J.
and
1984.
Mississippi
Journal
of
Avian Flyways
Wildlife
cholera during
Management
in the
Central
1979-80. 48:
The
399-406.
J. P., AND H. G. BOTZLER. 1989. The effects of six environmental variables on Pasteurella multocida populations in water. Journal of Wildlife Diseases 25: 323-339. BULLER, H. J. 1975. Redistribution of waterfowl: Influence of water, protection, and feed. International Waterfowl Symposium 1: 143-154. CAIN, B. W. 1987. Wintering waterfowl habitat in Texas: Shrinking and contaminated. In WaterBREDY,
fowl
in
winter,
of Minnesota 583-596.
M.
Press,
W.
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