EPIZOOTIOLOGY OF AVIAN CHOLERA IN WILDFOWL Author(s): Richard G. Botzler Source: Journal of Wildlife Diseases, 27(3):367-395. Published By: Wildlife Disease Association DOI: http://dx.doi.org/10.7589/0090-3558-27.3.367 URL: http://www.bioone.org/doi/full/10.7589/0090-3558-27.3.367

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of Wildlife

Journal

Diseases,

27(3),

© Wildlife

EPIZOOTIOLOGY

OF AVIAN

CHOLERA

1991,

Disease

pp. 367-395

Association

1991

IN WILDFOWL

G. Botzler

Richard Department

of Wildlife,

Humboldt

State University,

Arcata,

California

95521, USA

ABSTRACT: Pasteurella multoctda, the cause of avian cholera, has naturally infected over 100 species of free-living birds. Among wild birds, avian cholera has its greatest impact on North American wildfowl. Epizootics usually are explosive in onset and may involve thousands of birds. The disease has been reported in every month of the year among wildfowl. Disproportionate mortality, with some species suffering proportionately greater mortality than others, has been a common feature of this disease. Presence of animal organic matter plays a significant role in the survival of P. multocida. There are conflicting reports or a lack of information on the role of host

sex, age, body size, other physical features, genetic variation or behavioral differences, as predisposing factors to infection by P. multocida. There also are ambiguities on the relationship between season, precipitation, temperature, nutritional stress, water quality, other microorganisms, and environmental contaminants, and the occurrence of avian cholera in wildfowl. Two competing hypotheses for the year-round reservoir of wildfowl strains of P. multocida are ambient soil or water of enzootic sites, and carrier animals; most current evidence favors the role of carrier animals. Transmission most likely occurs by ingestion of contaminated water, inhalation of bacteriarich aerosols, or both. While many techniques have been proposed to prevent or control avian cholera, none have been rigorously tested to determine their effectiveness. Key words: Avian cholera, Pasteurella multocida, epizootiology, waterfowl, review article,

INTRODUCTION

It

is estimated

that

hunters in North kill approximately each year, waterfowl (Friend,

America 20

and that die from 1981).

about

Stout

fledged

fowl. As our concentrated

and

sociated domestic Rieck,

found

mentally sound avian cholera,

million

amount mortality

Cornwell

American become diminishing

become

(1976)

to stimulate a continued study of avian cholera.

ever

waterfowl

among lations.

North Since

and Bischoff perceptions

multocida

American then, much

INFECTIVE

Pasteurella

greater One such explosive and

agent ported

as-

still

is lacking.

There

(1950) sumabout avian infection)

wildfowl research

are

interest

in

the

AGENT

multocida,

causing from

avian a wide

the bacterial has been reof birds and

cholera, variety

mammals (Blackburn et al., 1975; Brogden and Rhoades, 1983). The genus name of Pasteurella was chosen to honor Louis Pasteur; the species epithet, multocida, reflects the broad Among birds,

Pasteurella earlier

popuhas been

host range of this parasite. this bacterium was called

avicida literature

and

P.

aviseptica

(Rhoades

and

in

Rimler,

1984).

Pasteurella

done (Wilson, 1979; Mulcahy et al., 1988), but critical information about many significant features of avian cholera in wildfowl

effects land

water-

species, upland game birds, and fowl (Rosen, 1971; Wetzel and 1972; Rhoades and Rimler, 1984).

In 1950, Rosen marized current cholera (Pasteurella

for preventing controlling epizo-

use, and management practices on the initiation and course of the disease are not clear. It is my hope in this review paper

of

increasingly habitat,

managers. cholera, an

among

techniques nor for

otics in wildfowl populations. The of ambient environmental conditions,

of Mexico waterfowl

made up about 88% mortality studied

North wildfowl on a

transmissible diseases concerns for waterfowl threat is avian (fowl) disease

north million

an equal nonhunting

estimated that diseases of the total nonhunting among

3.4

ed Gram-negative may vary from bipolar staining

no environ367

multocida

is an

encapsulat-

bacterium whose shape a rod to a coccobacillus. A characteristic is evident This

One

UIIUUIIUI 1111 IIIIUIIUU III11111 IU

LBEL-FKU-8DWW

368

JOURNAL OF

with

methylene

Gram Mutters

Wrights

27, NO. 3, JULY

stain,

stain (Wobeser, et al. (1985)

P. multocida

distinguished by dulcitol, sorbitol, Most

P. multocida

(USA) tocida

wildfowl multocida

multocida

VOL.

Giem-

septica;

these

their differing arabinose and strains are

from

(37%),

gallicida

in

and

P.

The appearing

bird.

mu!by P.

P. multo-

for

tween

occur

biochemical

characteris-

are serotype Mississippi serotypes Atlantic

origin, from

1 in the Pacific, Flyways of North 3 and Flyway

most wildfowl

Central, America,

4 predominating (Brogden and

P.

and with

in the Rhoades,

1983; Windingstad et al., 1983). In the Atlantic Flyway, avian cholera epizootics largely have been caused by serotype 3 P. multocida, until recently when serotype 1 strains rnateria

from eiders (SoWildlife Health

have been isolated spp.) (National

Research 53711,

Center, USA,

Madison,

unpubl.

data).

descriptions of the logical characteristics reported Rimler

Wisconsin More

biochemical and of P. multocida

by Rosen (1984), and

(1971), Adlam

Rhoades and

and Rutter

(1989). HOST

RANGE

over

100

to have

been

naturally

it is evident

that

host

as

range,

wild

avian

species

infected

P. multocida its

species

If one were to include domestic birds from

known

all captive, which P.

all bird cholera

species under

the

multocida

in puffins

provided no Avian cholera a population

sumably posaca),

rosy-billed associated

den

(Fujihara by

in

puffins five

spe-

spp.) are presStill, I found no

in

wild

ducks,

Japan pre-

pochards (Netta with a zoological et

al.,

1986).

the

naturally

pegar-

Although

et a!. (1986) in

occur

arctica),

reported of

originating

pochards

(Fratercula

Fujihara

as wild

U.S.,

rosy-billed

only

in temper-

ate

South America (Johnsgard, 1978). Hinshaw and Emlen (1943) received a personal communication from J. E. Shillinger that bobwhite quail (Colinus virginianus) suffered epizootics of avian and

Rosen

host

avian a!-

puffins that

although

details. was

among

(1971)

reported

a per-

from L. N. Locke of common ravens (Corvus are not available on these

extensions.

zoo, and multocida

are susceptible to right circumstances,

among

evidence

in Chile,

a broad

has been isolated, and the unpublished reports from agency files, the host range would be even greater. Probably most or

(1962) and Rosen Ilazabal (1941) as

cholera

implies.

1),

and

is no

sonal communication mortality among corax), but details

(Table has

epithet

and earspe-

of either puffins or shearwaters in and Ilazabal (1941). Keymer (1958) to an unidentified report of P.

cholera, With

et al.

date species;

(1972)

naturally

birds

seroare

earliest

in that

of shearwater (Puffinus (Johnson, 1965, 1967).

described

detailed

the

Rhoades (1983) reported dates among some bird

avian There

mention Suarez referred but

always observed

McDiarmid cited Suarez

Chile.

that P. multocida species of free-liv-

Heddleston

reporting

cies ent

Table 1 are the first literature for which

is not was

example,

cies. Both (1971)

host species of strains isolated

This

Brogden and lier isolation

septica (80%) of

1981;

California,

dents involving observed on

mortality

Rosen,

Wobeser,

and often

the total wildfowl mortality than one would expect based on their proportion (45 to 55%) in the total live wildfowl populations; in contrast, duck species consistently died

Morse, Most

avian

(Anascrecca),

jamaicensis)

There

as evidenced of sick birds

1949;

teal

paratively less. But Rosen (1969) found that this relative species susceptibility could vary considerably between years.

there was a pronumbers of bac-

teria in the blood up to the time of death; P. multocida was observed in the blood of two chickens for 18 and 47 days, respectively, before they died from avian cholera. Among wildfowl it has been noted that P. multocida

1991

susceptibility

influenced a

other ation, hosts,

by

to a disease such

features

physical characteristics, behavioral differences and

variation

in

immune

as

may sex,

genetic among status

be age, varithe re-

BOTZLER-AVIAN

JAN 1978 AVIAN

CHOLERA

CHOLERA

EPIZOO11OLOGY

375

EPORNITIC

-J

4 I-

0 -J

4

0 30 20 10

I,

0 4

5’

Humboldt

COOlS

(N=901)

-a.---

SWANS

(N=7)

WIGEON

Sequence

County,

sulting agents.

past has

Korschgen

et

mon Maine

10 JANUARY X-

observed

11

12

PINTAIL

exposures

of

been factor al.

to

eiders (USA)

considered to avian

(1978)

observed

SHOVELERS

-0---

MALLARDS

the

(Somateria occurred

to avian

that

is no evidence offshore after (L. Locke, et al. female

cholera

(1979) diving during

Bay, occurred

(1989) found the sex ratios

caerulescens) avian birds.

(N=9)

(N=8)

1978

comin fethat matpers. found ducks an epi-

but specin the live

cholera, Mensik

among

avian

cholera

in avian

cholera and those killed by gunshot. Based on these limited studies, the role of host sex may be significant in some cases, but has no consistent effect.

may affect Hoffman

the

epizootic,

Centervil!e,

susceptibility and Stover

prevalence

of

chickens to be age; P. multocida

30 difference

less mortality mallards dosed ingesting

or receiving no shot. Additional needed to clarify the relationship exposure to lead and susceptibility cholera. There stand the

has been epizootiology

the context land use. vegetation braska diversity, era had Gordon

little

in

P. multocida

in these Wobeser

to birds

ppm

effort of avian

two groups. (1986) also from with steel

avian lead shot

work is between to avian to undercholera in

of habitat characteristics and Brown et al. (1983) found that at an avian cholera site in Ne-

was

characterized by while a site with little high species diversity. (1989)

found

no

apparent

low species avian cholIn contrast, pattern

BOTZLER-AVIAN

between

the

occurrence

and variation Nebraska. In (1989)

in the

found

of

no

relation

cholera mortality and age among wetlands, tions,

and

land

avian

emergent same areas,

cholera

vegetation Smith

et

between

surface wetland

ing in al.

an avian

before,

avian

water drainclassifica-

in OF PASTEURELLA FOR WILDFOWL

RESERVOIRS

The term “reservoir” pendable, nonclinical

MULTOCIDA

is defined source of

(1887) in

noted

sick animals cluded that phytic

had

of

introduced.

He

after They

wildfowl,

of avian Muleshoe

was

the

cholera National

a of

(USA)

and

view was observation

consistent at

P. 120

in northern

be

California

has

that soil reservoir.

that

may

100 days in Bond (1968) to

surat 3 C,

soils held at found that 21

days

in

soils held at 26 C, and 18 days in soils stored at 4 C. Awad et al. (1976) reported survival of P. muUocida in soil for 27 days. Backstrand and Botzler (1986) found that P. mu!tocida survived less than 20 days after inoculation into soil of an enzootic site dur-

assessed al.

P.

of

related about

to the of the

P. mu!tocida.

of

by

(1949) of

high

an

levels

of

Rosen and 0.5 ml of ongoing

ter 3 wk after pond, with no

numerous

reported survived

air

C. On one occasion, that P. mu!tocida

area

240

in these studies. is little evidence that soil can serve

with

P. mu!tocida

the

be

after

epi-

enough virulent P. mu!a mouse in four hours after injection. of P. mu!tocida in water

exclusion

on

could survival

contain

a pond

et

the cholera

not

during epizootics; (1949) observed that

been

Hutyra which the

by Rosen’s cholera may

(1964) found that P. mu!tocida up to 113 days in soils held

up

but

a reservoir

contained tocida to kill intraperitoneal The survival

sites such Refuge

as evidence an important

survived

avian

reservoir of P. mu!tocida. of enzootic avian cholera

waters

from

cholera

mu!tocida days,

speculated

may

Natural

water

Hutyra et al. (1949) referred to a by T. Kitt in which P. mu!tocida three months in garden soil. Di-

P. multocida

avian

from

soils used was presented Taken as a whole, there to support the hypothesis

Bischoff

animal recur-

some Wildlife

strengthened that avian

and from 15 to 20 C. Olson and

an

this site. (1950) buried

in soil was inversely its virulence. Little information physical or chemical characteristics

P. mu!tocida

consapro-

as a density-independent mortality facamong tundra swans of California. The survival and growth of P. multocida in soil has been assessed by several

mov vived

avirulent

sites

no

act tor

authors. study survived

soil;

recovered

dying

as a year-round Water bodies

avian

where

independent

could be interpreted or water might be This (1969)

coots

zootic

association. Among

in Texas

flocks

mu!tocida

organism,

rence as the

cases

bird been

P.

soil or water birds.

many

dometic

as a dea patho-

agent can Two major for avian

cholera in wildfowl: ambient of enzootic sites, and carrier Kitt

of

days.

after

same

recovered to the area

multocida

gen; a place where the infective survive on a year-round basis. reservoirs have been proposed

cholera

soils or

379

In the

were natural

occurring on and Bischoff

hearts

EPIZOO11OLOGY

epizootic.

multocida

during,

epizootic Rosen

use.

cholera

no P. uninoculated

study, from

CHOLERA

for

18

days

at

Rosen (1969) was recovered

100 snow waterfowl in

authors. a study in in water with

the

geese being

5 to

6

observed from wadied on observed

intermittent

a

period.

Bendheim served that

and Even-Shoshan at 18 C, P. multocida

(1975) obsurvived

for

in

12

3 days

distilled

water,

days

in

tapwater, 28 days in deionized water, and 99 days in water contaminated with turkey litter. Titche (1979) found that survival of

P. mu!tocida line”

to 30

ranged from days in marsh

to an opened avian cholera.

carcass

At Centerville, survived

in water

6 days in “sawater adjacent

of a duck California, for

end of one epizootic publ.). In a later study

13 days (R. G. on this

dying

from

P. mu!tocida beyond

the

Botzler, unsite, P. mul-

380

JOURNAL

tocida

was water

pond

OF WILDLIFE

DEASES,

not recovered 4 days before

epizootic, but was isolated after the epizootic started; lated at 17 days or later Botzler, tocida water

and

Except shan base, were

for

Botzler,

natural cholera

and that

at 3 and it was (Backstrand

10 days not isoand

caribou)

and

Even-Sho-

(1975), who used tryptose blood all tests for P. mu!tocida in by mouse inoculation. However,

for establishing tocida. Bredy

the

specific

conditions,

agar water Ro-

medium in some

presence

was cases

found that P. > 1 yr in water including

warm

terperatures (18 to 20 C), the addition of protein, 0.5% NaCl, and the presence of other microorganisms; in contrast, variation in pH, clay content and sucrose level had little effect on survival of the pasteurellae. It is not clear how pertinent these findings are to the year-round survival of

P. mu!tocida habitats. do

not

in water Overall, the

support

the

is an important but the issue Carrier

reservoir is not yet

animals

and

cats

Rosen,

wildfowl of studies

hypothesis

may

reservoir. Pasteure!!a the respiratory tracts variety of mammals. respiratory reyt and way rats

of natural majority

that

be

an

mu!tocida and mouths Examples

important occurs in of a great include the

tracts of domestic sheep (FoJessup, 1982), the mouths of Nor(Schipper, 1947), domestic dogs (Owen

et al.,

1970;

Arnbjerg,

from numerous al., 1968; Rosen, Quan et al., Pasteurellosis

1968;

1986). in both

Hubbert

1978),

wild mammals 1970; Bond mammals

as et

and well

as

(Owen et al., 1972; and

birds

can be mammals. infection

initiated by the bites of infected Human cases of P. mu!tocida commonly have followed bites

of dogs,

cats

and

other

mammals

dation (1980) tocida

reported to birds

found

P. mu!tocida

(Hubbert

Gregg turkeys

cida

to caribou (Rangifer during unsuccessful preSimilarly, Smit et al.

the transmission of P. mu!by cat bite. Korbel (1990)

birds

infections

that

had

in

been

speculated as reservoirs that move

Rhoades

and

wild

P. mu!tocida

isolates

open

sues from carnivores,

P. mu!tocida 3A,

243 P. mu!culturing tis-

period It is of

isolants

the

same

found in wildfowl epizootics. After isolating during an avian braska,

poultry, and mice of avian

wild rodents, lagomorphs, as well as flea pools from

animals, over a 12-yr vatic plague studies. and

rangepointed

originating cattle and

for cats, rats sources

et al. (1986) evaluated isolates collected from

tocida

racoons

(1989) from

sheep were nonpathogenic whereas those from pigs, were considered possible cholera. Quan

domestic

P. mu!to(Proc yon

of onto

Rimler

were

sylthat

serotypes generally

avian

P. multocida cholera

and these

during interest

serotypes during

of

by cats.

that

P. mu!tocida

out that among from mammals,

54%

bitten

et al. (1974) found that could be infected with through the bite of raccoons

!otor) and might serve for turkeys

1A

for P. multocida, resolved.

Bergerud (1971) showed lynx (Fe!is !ynx) trans-

calves attempts.

most

water

1970). infected

P. mu!tocida

mitted

lands.

P. mu!-

of

and Botzler (1989) could survive for

muUocida under

that Das’ inoculation

Rosen, orally

92 wild

1986).

Bendheim

sen (1972) found superior to mouse

1991

from an avian

In the same study, P. mu!less than 6 days in pond with the organisms

1986). survived inoculated

(Backstrand

VOL. 27, NO. 3, JULY

epizootic

cholera serotype in

1 Ne-

Windingstad et al. (1988) isolated from nasal swabs in 35 of 37 cattle. Eighty percent of the P.

P. mu!tocida feedlot

multocida

isolates from cattle were 3 or serotype 3 with cross-reactivity; one weak serotype 1 cross-reactor

type only found. from

No cloacal

P.

mu!tocida or

pharyngeal

serowas

was recovered swabs among

20 domestic ducks and geese on a farm adjacent to the wildfowl epizootic. Thus, there appeared to be little connection between domestic animals and the occurrence ined

of avian cholera during this study.

Pritchett

et al.

(1930a,

in wildfowl b) and

examPritchett

BOTZLER-AVIAN

and

Hughes

(1932)

found

quency

of recovered

riers, avian

and proposed cholera from

that

a high

chickens

became

that birds 1 yr provided

of

fowl.

They

feces from not maintain

established

important

sources

also

fre-

mink

developed

pneumonia,

mice

contracted

a fatal

surviving the res-

concluded

carrier of

that

and

birds could were un-

environmental

con-

P. mu!tocida

P. mu!tocida between variety Serdyuk

from of the

quences.

None

carrying

the

developed

pecially

ervoir

ther

noted

water. that

Iliev

fowl

et al. (1965b)

infected

oral mucous membranes pathogenic P. mu!tocida origin for 50 to 60 days. similarly infected with

fur-

through

of avian origin could become permanent carriers, but the P. mu!tocida never reverted to pathogenic strains in the infected birds. Heddleston (1972) believed that the life bird

duration

of

mestic fowl. and Ollerhead ed carrier with a past

was

only

carrier

state

in

domestic inferred

fowl, that

Curtis infect-

occurred of avian

and

Watko

only in cholera. (1963)

of wildlife, farm animals as potential P. mu!tocida, and as potential

a sheep, response but

P. mu!tocida sages tion. dying bits

do-

flocks

assessed

animals carriers sources

and of of

cholera for domestic birds. They that pigeons, sparrows, mice, and died of acute septicemia after inexposure to a P. mu!tocida strain from a chicken. Rats, ferrets, guin-

ea pigs, noticeable tions,

to the

Among (1981)

a variety laboratory avian found rabbits tranasal isolated

limit

a chronic

birds history

Heddleston

the

when

the

pig and infections tested

After being from avian developed

a pig and a calf after intranasal

34

fed viscera cholera,

a nasal

had no infec-

calf had inapparent in their nasal pasdays

after

inocula-

from chickens one of five rab-

infection,

one

that

their

could shed nonof mammalian In contrast, fowl nonpathogenic P.

mu!tocida

of a carrier

infection,

of two

organisms

et

or

al.

signs

be

checked,

a res-

P. mu!to-

reported of wild

mammals

and

farms experiencing in the preceding

the

of rats

suggested

might

(1988)

premises

somatic were

turkeys

avian two to

serotypes the same

on

only

the

of seven little

avian

P. mu!tocida

of isoas those

two

suggesting

between and

pigeons

infected

They

a variety

affecting

keys

of the

rodents

months. The from wildlife

nection

seand

poultry.

birds on turkey cholera epizootics eight lates

avn

developed 10%

domestic

from

Pasteuchickens

sparrows

pasteurellosis.

Snipes

cida

of the

a

infected

rats with to transmit

infected to healthy chicken-wildlife-chicken

birds

for

and

(1970)

and able

whereas

wild

Thus, readily

wildlife,

Tsimokh

pigeons, and were

cholera in each

11 of 19

to transmit

birds, animals.

and

sparrows, re!!a sp.,

and

381

septicemia.

appeared

domestic of other

tamination; rather, established carriers were significant sources of P. mu!tocida only through oral and nasal discharges, esinto

EPIZOO11OLOGY

car-

ervoir for the next year’s epizootics. Using radio-labelled P. mu!tocida, Iliev et al. (1965a) found that orally ingested pasteurellae were inactivated in the proventriculus

CHOLERA

in

con-

cholera

in tur-

wildlife

in

this

study. Rhoades that

and

wildfowl

P. mu!tocida the

role

Rimler

may

for domestic

of carriers

clearly reported

(1984)

carriers

the

was

authors

among

reported

a snow

suggesting Healthy evaluated

apparently However, and

the

the

exposed

that

carrier

presence

in another (1969)

coots Missouri could

an

but died laboratory,

of

state. have

been

of P. mu!toci-

P. mu!-

et al. (1967) isolated the spleens and livers

Olson

bird (1972)

survived

cholera at his wildfowl

healthy

transwith

caged Rosen

intermittent

appearing for

da. Vaught tocida from

ahue

an

(1946) resis-

P. multocida

goose

apparent case of avian the disease 3 mo later

is not

et al. mallard

to birds

believed

of

However,

wildfowl

P. multocida.

shedding

a source

birds.

established. Quortrup that a wild-caught

tant to challenge with mitted avian cholera it;

suggested

be

in

of three Missouri.

study, not

isolate

Don-

P.

382

JOURNAL

OF WILDLIFE

mu!tocida wild

from

DISEASES,

nasal

waterfowl

VOL. 27, NO. 3, JULY

pharynxes

from

the

of

400

Mississippi

Val-

ley. nasal

There is some question, however, if swabs are a good source of P. mu!tocida in carrier animals (Wobeser, 1981). et al. (1978) isolated P. mu!the tissues in only one of 236

Korschgen from

tocida

apparently healthy from the oropharynx ently healthy nesting

common in one female

(1979) isolated P. multocida of 172 apparently healthy injecting macerated lung birds into white wildfowl carriers

mice, might

than later

believed.

previously isolated

eiders, and of 357 appareiders. Titche

1991

cholera.

Rosen

that

birds

or carriers

from

Grizzly

cholera Klamath

ed this avian

suggesting that be more common

avian

P. multocida

near un-

Morse

National

migration

(1959)

inferred

transmitted

avian

Island

to

Wildlife

as

pathogen. cholera

(Corvus

Titche (1979) type 3 from 3

and

Lower

Refuge,

Ore-

gon, a distance of 275 air-miles (440 km). McDiarmid (1962) reported isolating P. mu!tocida from a swallow (probably Hirundo rustica, no species given) that arrived in England from Africa; he suggest-

from 16(9.3%) wildfowl after tissue from these

of 41 apparently healthy wild ducks a waterfowl facility housing wild birds

sick

a means

of

Novikov among

frugilegus) cholera

in

among

introducing

(1954) migrating the

reported rooks

Soviet

domestic

shortly after the rook mortality. Rosen (1972) speculated that carry P. grounds,

mu!tocida

Wobeser

et al. (1979)

and

north to mortality

sustain

Union;

birds

provided

waterfowl the

nesting there too.

supporting

dergoing an avian cholera epizootic from type 3 P. multocida. Titche (1979) believed the infection may have been intro-

evidence by observing avian cholera snow geese and Ross’ geese during

duced carrier

cholera grounds

to the birds.

Gulls (Rosen al., (1979)

wildfowl

facility

1964; Korschgen et al., isolated P. mu!tocida

he

al., et

1978). from

Titche 15 of 37

gulls (Larus ca!ifornicus), of 23 ring-billed gulls

but

de!awarensis) study,

infected

be reservoirs of P. mu!tocida Bischoff, 1950; Gershman

may and

California from none

by

in noted

(Larus

California. In the same that six of nine California

gulls fed P. mu!tocida-contaminated meat shed the P. mu!tocida in their feces for up to 120 hr; P. mu!tocida also was recovered from three gulls by oral swabs. Sz#{233}cs#{233}nyi (1965) proposed that crows riers of P. multocida.

brachyrhynchos)

and

et al. (1977a) (Corvus spp.) are carAmerican crows (C.

were

Zinkl

observed

dead

spring

dur-

migration

in Saskatchewan.

1964;

Reed

Central followed geese, attempt

from the apparently in this study. It has at the

Sacramento

Valley

follows

the

of

(J.

G. Mensik, life Refuge, Later, C.

1977a).

Sanders

among

101

(Corvus

ossifragus)

rella

infections

in their

and several birds chronic Pasteuposterior

nares.

Overall, most biologists seem to the hypothesis that recovered carriers the most important reservoir for

favor are avian

mu!tocida,

arrival

report,

geese (1984) in the

snow that

geese avian

Complex snow

National

Center not induce

mallards even

cyclophosphamide lins (1984) induced

multocida among of aztreonam. There are still spective

et

1967;

geese

Sacramento National pers. comm.). Brand and P. Whiteley

crows

cleft, with

healthy been noted

usually

et al.,

by the eye and nasal lived up to 66 days

Cousineau,

cholera

Research could

fish

and

and Mississippi Flyways closely the migration patterns of snow starting from Hudson Bay; but no was made to isolate P. mu!tocida

Health Wisconsin)

exposed

Avian

Korschgen et al., 1978) and snow (Brand, 1984). In one intriguing study, Brand found that avian cholera mortality

unpublished

to P. multocida

among their

has been observed on the breeding of common eiders (Gershman

ing an avian cholera epizootic in waterfowl; serotype 1 P. multocida was isolated from both dead crows and waterfowl (Zinkl (1938)

began

contributions

files, Madison, a carrier state

inoculated

by

using on soil

with

P.

them

to Colof P.

low

ambiguities of

(1988 Wildlife

after exposing or dexamethsone. the persistence mice

Wild-

or

doses the

re-

water,

as

BOTZLER-AVIAN

well

as carrier

tocida

was

animals.

Even

isolated

from

or soil and water, not serotyped or

Much

clearly

cholera commonly

these isolates often were inoculated into suscepti-

ble birds to determine cause avian cholera. mu!tocida do not cause fowl.

P. mu!animals

when carrier

whether they could Many strains of P. the disease in wild-

additional

establish

work

the

is needed

reservoir

to

P. mu!-

of

tocida.

CHOLERA

carcasses.

He

were

Once a clinical in susceptible through

mestica) rabbits

which dying

had from

fed

infection animals,

a susceptible

tion. The soft tick, mit P. mu!tocida (Basu, found

possible no direct thropods

is established transmission

population

has

been

of avian

fowl. Rosen

and

P. mu!tocida Argas

persicus,

transbirds

1930; Iovchev, 1967). Petrov that P. mu!tocida survived

(1970) 33 days

among

can

halation

of

fection). turkeys

Morse may bacterial

blood of infec-

Donahue to be very

tocida ferred

that

tocida

mitted readily through Virulent P. multocida

at 4 C in A. persicus.

days

et al. (1978) found that P. mu!survived up to 31 days in A. persicus room temperature. Glukhov and No(1975)

reported

of P. multocida Poultry mites

a 1,000-fold

increase

in A.

persicus. (Dermanyssus

ga!!inae)

from rabbits dying from contained P. mu!tocida Petrov

(1975)

nae

engorging on remained carriers

found

that

birds for 42

on the ambient temet al. (1946) recovered

from

(Derrnanyssus

mites

spp.) collected from ducks dying from an cholera. Derylo (1967, 1970) found virulent

mu!tocida in the gut and aga (Eomenacanthus Menopon ga!!inae) that cholera.

P. mu!tocida

surface 1964).

D. ga!li-

blood of infected of P. mu!tocida

to 64 days, depending perature. Quortrup

mu!tocida

pasteurel(Bigland,

Derylo

P.

of Mallophand on hens with transmitted

stramineus fed (1969)

(1971) found to P. mu!-

the Olson

palatine (1980)

could

be

the air. can occur

and Baker, Blanchard that air interface

1961; and

air intrans-

in high chol1949). water Potter, Syzdek

bubbles breaking remove bacteria

from higher the ing

the bubbles than that

were of the

10 to 1,000 water from

times which

bubbles burst. Thus, waterfowl splashcould create bacteria-rich aerosols. There is limited information available

on the borne served

susceptibility transmission. that 33 (63%)

of wildfowl to airTitche (1979) obof 52 test waterfowl

one

maggots

that

had

through

fed

on

avian

at

concentrated in the surface microlayer and eject them into the atmosphere; the bacterial concentrations in the drops ejected

flesh-fly

P. multocida

of louse im-

wild-

paired skin of the uninfected hens. Kitt (1888) reported that domestic birds contracted pasteurellosis after ingesting

containing

by inoculation

among

coots died from avian cholera when to 1011 P. mu!tocida were inoculated by aerosol over time periods ranging from 15 to 120 mm; but the bacterial inocula and exposure times were far greater than

feces

to hens

feces

avi-

of their

birds, there is time that arrole in the

in water during avian (Rosen and Bischoff, concentrate at the

(Potter Further,

(1970) found an air-water

into and

P. mu!tocida

concentrations era epizootics Bacteria often

transmission Despite

and Olson susceptible

Metwalley

100

flies.

(1959) proposed that be transmitted by inaerosols (droplet in-

by inoculation Simensen

avian

the

cholera

spaces.

P.

maggots susceptible

mu!tocida

role with domestic evidence at this play an important

transmission

ways, inand inges-

domestic

at 30 C and

1954).

on

P.

(1976) reported by tabanid

P. mu!tocida

hypothesized to occur in several cluding arthropods, inhalation

taken losis

that by

tions.

TRANSMISSION

vikov

noted

ingested

383

birds and proposed that fly maggots were an important means of avian cholera transmission (Kitt, 1888). Skidmore (1932) observed that avian cholera was transmitted to turkeys eating house flies (Musca do-

Krinsky

at

EPIZOOTIOLOGY

and 108

would

expect

under

natural

condi-

JOURNAL

384

tions.

Yet,

OF WILDLIFE

Combs

DISEASES,

(1988)

VOL. 27, NO. 3, JULY 1991

observed

that

spe-

cies such as coots, which create aerosols when taking off in large rafts by running across the water, died earlier and in greater numbers during avian cholera epizootics at Centerville, compared to species lifting off singly and vertically tails, shovelers, and mallards). Ingestion is a route by which

tocida tible

may be transmitted wildfowl. Pasteurel!a

readily

passed

(e.g.,

pin-

P. mu!-

among

suscepmu!tocida was

to susceptible

birds

by

the

oral route in the laboratory (Rosen and Bischoff, 1949). Quortrup et al. (1946) found that healthy ducks placed near ducks orally infected with P. mu!tocida died after

28

hr

drinking (1971)

water. found that

infected

after

source keys; water.

if they

with

had

access

Pabs-Garnon susceptible sharing

Other

same

and turkeys

a

was susceptible

Soltys were

common

water tur-

isolated turkeys

to the infected share the same

mained

the

experimentally-infected

P. mu!tocida

proximity did not

to

birds, water

from the in close but which source, re-

mu!tocida

unaffected, suggesting was transmitted more

through

ingestion

of

that P. readily

contaminated

water

than through droplet aerosol. Zinkl et al. (1977a) reported that each of eight coots exposed to drinking water contaminated with 2.3 x 10 P. mu!tocida/ml died from avian In were

cholera within 2 days. the natural environment, observed to concentrate

near

face of water, rather than deeper the water column (Potter and Baker,

bacteria the surwithin 1961;

Potter, 1964). Combs (1988) observed that wildfowl such as American coots and American wigeon, which grazed frequently at the water surface were the first species to die fered

at the

one

avian

greatest

cholera

site,

and

suf-

losses.

While there is some ambiguity on the of water as a year-round reservoir of P. mu!tocida, it appears likely that water plays a significant role in its transmission. and Brand (1984) were the source and noted that

were

stopped when the bacteria detectable in water.

Predation or scavenging imals sometimes may play

no

of infected ana role in trans-

mitting P. mu!tocida. At one avian cholera epizootic, Rosen and Bischoff (1949) reported a dead cat found with the remains of a coot in its stomach; however, it was not

clear

in coots

and

cat. Later, an avian

was

Rosen cholera

was followed by a among meadow montanus). This, in turn,

mu!tocida mice (Microtus followed

by

avian

cholera

(Larus spp.), short-eared (Asio flammeus), and northern (Circus cyaneus). Stomach contents

among

gulls

owls weasel

and

gulls

contained spp.) also

(Muste!a

stomach; P. mu!tocida the spleen of the weasel 1959). It was not stated of

P. mu!tocida

was

an

on fresh

avian

cholera was

mu!tocida

owls harriers

mice. A had mice

isolated

from

study. Zinkl scavenging

waterfowl and in Nebraska. observed flocks

scavenging

deaths

of the dead in its

was isolated from (Rosen and Morse, that the same strain

imals in this interesting (1977a) observed crows fected cholera (1981)

iso-

and Morse epizootic

ducks that epizootic

P.

was

P. mu!tocida

whether

lated from the (1959) reported

dying from Taylor and of common

duck

carcasses

all

an-

et al. on inavian Pence crows during

epizootic in Texas; P. isolated from both mori-

bund and dead crows as well as apparently normal short-eared owls and a cottontail rabbit at this site. Paullin (1987) observed coots cannibalizing other coots dying from avian cholera, but did not izing coots disease. gesting 1950;

determine subsequently

Coots gull Gullion,

also feces

whether cannibalcontracted the

have been observed in(Rosen and Bischoff,

1952),

and

infected

gulls

shed P. mu!tocida (Titche, 1979). Seven of nine California gulls died from avian cholera after being fed contaminated tissues from wildfowl dying from avian can

role

Price casses water,

epizootic longer

observed that carof P. mu!tocida in the avian cholera

cholera (1979) captivity

(Titche,

1979).

However,

Titche

believed the stress of handling and also may have contributed to their

susceptibility.

During

the

1974-1975

epi-

BOTZLER-AVIAN

zootic

at

comm.)

Nebraska,

L.

estimated

(Haliaeetus

leucocepha!us)

an cholera birds. Overall, an cholera

after

by

N.

that eating

bite.

(pers.

pothesis reservoirs

bald eagles died from avi-

carcasses

there is little is transmitted

arthropod

Locke

eight

or

evidence among

inhalation,

ingestion, or both may be important means of transmission. However, the possible role of

fly

maggots

proposed

intriguing,

and

by

deserves

Kitt

(1888)

further

portant wildfowl. is

consid-

eration.

A model

for

MODEL FOR AVIAN EPIZOOTIOLOGY

avian

cholera

epizootiology

in wildfowl should identify creasing the risk of susceptible

P. mu!tocida

fection tors),

by the

means duced

by which to susceptible

reservoir

factors inhosts to in-

(predisposing the disease,

for the

the

disease populations,

facthe

is first the

intromeans

of transmission between susceptible hosts, the events occuring in affected populations during

an epizootic

(disease

dynamics),

the final impact host populations.

of each epizootic The last feature,

mortality, among

best documented Winter habitat

is the wildfowl.

of

fowl generally is well defined wildfowl mortality usually can mined

if the

effort

is made.

vegetation estimated

is thick, total from recovery

carcasses.

There

other aspects of ogy, however. Many potential been and

evaluated, physical

mental

Even

where can be marked

certainty cholera

aspect wild-

and total be deter-

mortality rates of

is less avian

and on the overall

on

the

epizootiol-

predisposing

factors

have

including host age, sex, features, as well as environ-

factors

such

as

rainfall,

ambient

including

1988). The tain.

reservoir Most

studies

of P. mu!tocida do

not

time

support

is uncerthe

hy-

susceptible

can

hosts

duction

of

avian

populations cholera has

may been

the

year.

have 1953,

Rosen,

1969,

Blus

I believe cholera

into may

of avian

small

regularly 1963, et al.,

the

conditions

such

Wo-

R. Botzremain

introduction

of

wildfowl

be common, cholera

epi(Bi1965;

1978;

susceptible and may

one or a few birds and remain However, one of these small flare into an extensive epizootic proper

Avian month of

or

reported Macdonald

1972;

susceptible

Humburg et al., 1983; and others probably

unreported. populations

to

suggestfrom ex-

regularly. in every

mortalities

been 1955;

beser, 1981; ler, unpubl.)

incidents

cholera occur noted

Single

zootics vens,

avian

Wobeser (1981) case resulting

from

of a carrier state among several normal birds might be sufficient an epizootic. is evidence suggesting that intro-

that

involve

most only

undetected. events may under the

as the

high

wild-

fowl densities occurring on wintering and staging grounds. Among eiders, Korschgen et al. (1978) noted that avian cholera epizootics time sities

occurred on the nesting grounds of both severe stress and high of susceptible birds.

ter,

density,

can

acerbation hundred to start There

host

strategy were factors (Combs,

to

birds

animals. one fatal

results.

Centerville,

other pasteurellae

infected ed that

Once ination

land, and feeding as predisposing

and and

transmitted

stress, and chemwith inconclusive

At

waterfowl

P. mu!tocida,

temperature, nutritional ical contaminants, but spent on proposed

reservoir for avian cholera among It is clear that many vertebrates,

carry be

A PROPOSED CHOLERA

385

(Bredy and Botzler, 1989), conditions in this laboratory study were different from those of natural waterfowl habitats. Currently, most biologists favor the hypothesis that carrier birds are the most im-

that aviwildfowl

In contrast,

EPIZOO11OLOGY

that soil or water are important of P. mu!tocida. Although P. can survive >1 yr in water

mu!tocida

sick

CHOLERA

probably

mu!tocida gestion, among greatly between

an epizootic starts, of the environment, among

at a den-

heavy contamespecially wa-

allows transmission dense populations

of P. by in-

inhalation, or both. Mortality infected waterfowl has varied at different enzootic sites, and even years at the same site. An analysis

JOURNAL

386

of

wildfowl

one

site,

any bers tion

OF WILDLIFE

DISEASES,

mortality

VOL. 27, NO. 3, JULY

is summarized

Centerville,

California,

for

al.,

sex, age, body characteristics

based on physical

other

(Oddo

et

1989). terville: swans,

Birds died coots died American

1978;

Mensik

and

Botzler,

in a sequence at Cenfirst, followed by tundra wigeon, northern pin-

tails, northern shovelers, mallards, and respectively (Oddo et al., 1978; Mensik Botzler, 1989), (Fig. 1). Differences wildfowl susceptibility were related to differences ities;

species

dying

commonly face, and

grazed

maintained used land

avian cholera observations verification cability The

to

teal, and in

avian cholera in their activ-

early

in the

epizootics

or fed

at the

water

high density areas together

season (Combs, are of limited (or refutation)

1988). These value without of their appliin

de-

veloping a viable model for avian cholera in wildfowl is not a lack of information, but

rather

a lack

formation. to the among

This

of consistency

in the

inconsistency

is due

in-

in part

variety of species and circumstances the studies cited, and also because

the majority of without adequate

studies controls.

are

descriptive, This inconsis-

tency also may reflect important gaps in our understanding of the disease. Overall, much work still is needed to establish the conditions initiating avian cholera in waterfowl,

and

magnifying

the

disease

This provides prevent high of control

into

epizootics.

efforts

Despite tory

bird

an disease

CONTROL

increasing problems

AND TREATMENT

interest of North

in migraAmer-

ica (Friend, 1981, 1984), there still is much speculation, and little firm fact on strategies to prevent and control avian cholera epizootics. Most recommendations for prevention are oriented to reducing exposure of susceptible birds and lowering contam-

are

relatively

to costs

small

com-

pared to those required for handling an extensive epizootic among wildfowl (Friend, 1987). Marsh surveillance and carcass removal is the strategy followed by the California Department of Game (W. Clark, pers. comm.). A number of recommendations been

made

it starts.

for controlling Carcass

and have once

is almost

Athough

the never

Fish

an epizootic

collection

cass collection has tested, the procedure

always

benefit

been is logical.

of

car-

definitively Carcasses

may serve as decoys and attract ceptible birds to a contaminated

other site.

susWo-

beser et al. (1982) found evidence of seven species of birds and four species of mammals scavenging on avian cholera-killed birds during one epizootic. Wildfowl carcasses commonly have several that

milliliters can be

of fluid discharged

and site.

further Carcasses

add

rich

in P. multocida from their nares,

to the contamination hold a substantial supply

of a of

P. mu!tocida that is constantly added the environment as the birds decompose. Survival of P. mu!tocida is enhanced the lier

presence (Rosen Bond, 1968; 1984). Further, which may

tocida PREVENTION,

the greatest opportunity losses, and the financial

encouraged. sur-

groupings, during the

to other sites. most serious short-coming

of aquatic ecosystems by P. mu!(Friend, 1987). A regular program of monitoring for wildfowl mortality is important to identify an epizootic at the earliest possible stage. ination

tocida

as follows.

Coots suffered greater mortality than other species, both in absolute numand proportion of their live populaaffected. There was no variation in

coot mortality weights, or

1991

to

beser, 1981). that American

of carcasses, and Bischoff, Titche, 1979; carcasses ingest other

scavengers

(Rosen,

1971;

and other days to

P. mu!tocida. the

ability

P. mu!Wo-

Zinkl et al. (1977a) reported crows suffered chronic cases

of P. mu!tocida infection on carcasses of waterfowl an cholera. Friend (1987) crows, several

by

as outlined ear1950; Olson and Price and Brand, attract transmit

and

sites

to

scavengers 2 wk after

This would of scavengers

after scavenging dying from avinoted that gulls, survived infection greatly to spread

from with facilitate the dis-

BOTZLER-AVIAN

ease to new sites, original source. Burning collected to burying them water table occurs son

at

many

the

at the site. It may be ments of bird

available

carcasses is preferred (Friend, 1987). A high during the winter sea-

cation persal methods species

avian

of

beneficial populations, on

to

a site,

sites

for several conditions,

animal

protein

and

to

species,

tified lations

on

will

and

(5)

an

acid

ameri-

an avian

1987).

One extreme recommendation is depopulation of infected birds to reduce the risk that the disease will spread further

to the

site

et al. (1976) of infected

cholera

effective

in

et al.,

halting

an

Chesapeake Bay. While show a decline in avian with

is not possible depopulation

to evaluate in the absence

et

al.

(1979)

poulation also

the

Purs-

on

coot

of coots. questioned

pop-

P.

compound depopulation

it

Montgomery efficacy

of this eradication program. Friend (1987) believed that population reduction of migratory birds infected with avian cholera is justified only under special conditions: (1) the outbreak must be discrete and localized rather than generalized and widespread, (2) techniques must be

of could

icillin.

Zinkl

fected Canada oxytetracycline

these not

Among

different be

domestic

methyl bromide on contaminated

and

Shoshan,

Queen

geese was

and

(1977b) survived given

ly, and also when 500 was given in the feed.

poultry, can

available suffering Quortrup

(1952) successfully of infected ducks et al.

indepenkill litter

1979).

There is little information the treatment of wildfowl cholera.

common

nests; no ad2 wk later,

with

mu!tocida

draw any Following

in conjunction and inciner-

eggs, and was observed

assessed.

and Zuydam several species

the impact of of an untreat-

among

contributions

fumigation

not

mixed avian

off the coast of Maine, (1964) reported the dispuddles and water holes

procedures

dently

avian

the

eradication,

the

control

(Bendheim

presented mortality

the

a cresylic wildfowl

but of an

depoputo be

epizootic the data cholera

concomitant

ed control

1978).

reported the coot populations

copper sulfate during one

epizootic

ation of carcasses, ditional mortality

on some islands off disease later returned

(Korschgen

chol-

bird

cholera epizootic, but could conclusions on its effectiveness.

with with

glove lation

represents of avian

migratory

with

been

in eiders however, the

outbreak

important

be jus-

to other popuis allowed to

extension

eiders on islands Gershman et al. infection of small

epizootic Maine;

the

geographic

infected pond in hydrochloric

from

among susceptible populations. Gershman et al. (1964) reported the eradication remaining eiders, gulls, and terns after

eradi-

must

basis of risk the outbreak

away from an avian cholera epizootic. Use of either aversive devices such as hazing, or attractants such as food have (Friend,

complete

Another suggestion for control is disinfecting small bodies of water. Rosen and Bischoff (1949) treated the water of an

cana)

suggested

allow

(4) eradication

the if

era into ulation.

prevent

(Grus

cranes

target

a new

site. For example, the use of aircraft

whooping

that

387

EPIZOO11OLOGY

without causing widespread disof potentially infected birds, (3) used must be specific for target and pose no significant risk for non-

continue,

control moveboth to contain

populations

onto an infected (1987) reported

move

cholera

1989). Thus, birds burtable may provide consurvival of P. mu!tocida

susceptible

moving Friend

from

survive some

presence

birds

additional

to

the

can under

(Bredy and Botzler, ied in a high water ditions enhancing

infected

distance

enzootic

and P. multocida months in water including

some

CHOLERA

found

on from (1946)

treated with penthat

in-

when 50 mg intramuscular-

g/ton tetracycline However, this pro-

cedure is not yet applicable to free-living populations. Immunization is a potentially important tool of the future. The natural immunity of waterfowl appears to be low. Donahue and Olson (1969) sampled 400 waterfowl in the Mississippi Valley, and found two

388

JOURNAL

OF WILDLIFE

birds

tocida.

with detectable antibodies It is not known if these

were

protective.

Killed vaccines against particular live-attenuated protection

(K.

Turkeys can live-attenuated lins, result era,

DISEASES,

VOL. 27, NO. 3, JULY

to P. mu!antibodies

(bacterins) protect only immunotypes, whereas vaccines provide crossR.

Rhoades,

pers.

be effectively vaccines

1977). While vaccine in signs and symptoms there is no evidence

result from vaccine Rhoades, pers. comm.). Queen and Quortrup

comm.).

immunized given orally

with (Col-

overdoses may of avian cholthat outbreaks

overdoses

(K.

(1946)

R.

showed

potential for an autogenous

immunizing bacterin.

a P. mu!tocida

isolant

goose to develop activated Type

a beta-propiolactone-in1 killed vaccine effective

for

giant

sis

maxima).

Canada This

muscular

from

subcutaneous

Habitat

manipulation

fabric

composing

a broader A major

I believe must behalf

environmental problem

strategy,

is that

1988

ference, sessment procedures that must propriate the value

an

effective tool in the future. Controlled drainage, water diversion and pumping operations potentially can be used to prevent wildfowl use of problem areas and

virtually

Wildlife

years,

the

still

fowl to P. mu!tocida. are based on the results one site on one occasion,

control

operation

with

a flock

of

tive

environment. I advocate avoid major itats. Despite venting the

management of P. mu!tocida

to select in the

management procedures that changes in our waterfowl habour shared concern for preserious losses among our al-

apUntil prolack

the

work is little

done clarity

in

re-

on the

factors as sex, age, physgenetic factors, dension susceptibility of wild-

uninfected on a small

than

managers decisions.

extensive

there

to new, Based

sible to use habitat against the survival

Con-

DIRECTIONS

birds 1987).

drinking water of a site. As the ecological requirements of P. mu!tocida become more clearly defined, it may become pos-

Association

be addressed in planning disease control responses. of these proposed control

roles of such host ical characteristics, ties, and behavior

rather

rec-

have been rigortheir value. At

Disease

susceptible (Friend,

Canada

of the

Gary Wobeser proposed that asof the benefits of disease control is one of the four major issues

FUTURE

cent

control

none

procedures to determine

attract habitat

geese experiencing avian cholera, Zinkl et al. (1977b) proposed adding water to dilute P. muUocida present in contaminated

all

be considered of one favored

impact. assessing

in

cedures is established, bases for making wise

pop-

provide

The

species or group of species. Techniques whose impacts are limited to P. mu!tocida or wildfowl are preferred over those with

Despite may

successful,

of that habitat acting on the

and

wild

systems.

that

were

aspects before

the

for

natural

ulation

snow

injection,

populations, of a complex in our Even if manip-

a lesser

a capwith

wildfowl one part

whole fabric must be considered efforts to manage this one disease. techniques involving major habitat

ommended ously tested

waterfowl during avian cholera The vaccine requires an intraor

troubled are only

with used

one year among geese in contact

an effective delivery system ulations is not available.

ready wildfowl

ducks (1985)

geese (Branta canadenbacterin provided im-

munity for at least tive flock of Canada free-flying epizootics.

wild Price

the

1991

Many past studies for one species at and are descrip-

controlled;

this

may

ac-

count for many of the inconsistencies in past results. There is a need for systematic studies, including repetitions of some past work, to verify (or refute) our current perceptions. A tool

with

important

future

implica-

tions is the use of rRNA probe and restriction endonuclease analysis to fingerprint and distinguish strains of P. mu!tocida (Snipes et al., 1989). Biologists may begin to solve some of our major epizootiological problems once they can trace the origins and

routes

of separate

P. mu!tocida

strains.

BOTZLER-AVIAN

The

apparent

cholera ca, and It

sudden

among indeed

might

onset

of

the manuscript,

avian

avian

wildfowl in North Ameriin the world, is intriguing.

be

no

more

than

began

at this

time.

The

that

less

of

remains.

the

The

historical, birds

are

increased

require disciplines,

study.

practices, and other is a fruitful

Studies

a networking and are

such

teams of experts from diverse Another recommended area the development of techniques nate

certain

high

risk

itat,

of this

avian direction

cholera may

An effective experimental rotype 1 P. mu!tocida

wintering

hold

some

nal

by

promise.

vaccine for seis available

(Price, 1985) and should be in a wide range of wildfowl

tested for use where sero-

type 1 strains are a threat. In concern for endangered species avian cholera justify the additional

particular, at risk to testing,

and

individual

vaccination

of

where

C. in

The

Indian

the

of

AND

A. E.

AND

methyl

1975.

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Sur-

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natural

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C., teurella

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don,

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for

services

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AMERICAN

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EPIZOO11OLOGY

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