Prepared by the USGS National Wildlife Health Center 

in cooperation with the U.S. Fish and Wildlife Service

Tularemia

U.S. Department of the Interior

U.S. Geological Survey

Circular 1297

Tularemia

By Milton Friend

Prepared by the USGS National Wildlife Health Center in cooperation with the 

U.S. Fish and Wildlife Service

Circular 1297

U.S. Department of the Interior

U.S. Geological Survey
U.S. Department of the Interior

DIRK KEMPTHORNE, Secretary

U.S. Geological Survey

P. Patrick Leahy, Acting Director

U.S. Geological Survey, Reston, Virginia: 2006

Major funding support was provided by the U.S. Fish and Wildlife Service, 

Division of Federal Assistance, Administrative Grant No. AP95-017.

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Suggested citation:

Friend, Milton, 2006, Tularemia: Reston, Va., U.S. Geological Survey, Circular 1297, 68 p.

Library of Congress Cataloging-in-Publication Data

Friend, Milton.

Tularemia / by Milton Friend

 p. cm. – (Circular ; 1297)

Includes bibliographic references.

ISBN 1-4113-1045-4

1. Tularemia. I. Title. 

RC186.T85F84 2006

616.9’239–dc22 2006020762
Field Manual of

Wildlife Diseases

General Field Procedures and Diseases of Birds

U.S. Department of the Interior

U.S. Geological Survey

Prepared by the USGS National Wildlife Health Center 

in cooperation with the U.S. Fish and Wildlife Service

Disease Emergence and Resurgence: 

The Wildlife-Human Connection

U.S. Department of the Interior

U.S. Geological Survey

Circular 1285

Disease Emergence and Resurgence:

The Wildlife-Human Connection

Prepared by the USGS National Wildlife Health Center

in cooperation with the U.S. Fish and Wildlife Service

Circular 1285

U.S. Department of the Interior

U.S. Geological Survey

iii

Related USGS Publications

Disease Emergence and Resurgence­—The 

Wildlife-Human Connection, by Milton Friend, 

USGS Circular 1285 (also available on CD-ROM)

Field Manual of Wildlife Diseases—General 

Field Procedures and Diseases of Birds, 

edited by Milton Friend and J. Christian 

Franson, USGS Information and Technology 

Report 1999–001

Preface

“It was the best of times, it was the worst of times...”

Charles Dickens, 1859

The continually emerging story of the bacterial disease tularemia (Francisella tularensis) is akin 

to a major theme of the Charles Dickens classic, “A Tale of Two Cities.”1 That theme is “the 

possibility of resurrection and transformation, both on a personal level and on a social level.”2

Within the USA, tularemia is primarily a disease of times past; in 1994, it was removed from 

the notifiable list of diseases because of the low number of human cases.3 However, tularemia 

has recently re-emerged as a threat for contemporary society in the USA and elsewhere. Global 

social unrest and political issues have elevated concerns over the use of F. tularensis as a biological weapon,4

 causing its reinstatement as a notifiable disease in the USA in 2000.5

Like the differences in life within the cities of London and Paris at the time of Dickens’ novel, 

the consequences from infection by F. tularensis are associated with different characteristics of 

the organism. One form of this bacterium typically results in inconsequential negative impacts 

on human health while the other commonly results in serious illness, and even death. The latter 

outcome, the broad spectrum of species infected, and because F. tularensis is one of the most 

infectious organisms known for humans and animals6, 7 have resulted in a history of development, and some use of this organism as a biological weapon.5, 8

F. tularensis has been classified as a Category A select agent because of its potential as a biological weapon.4

 This classification highly regulates scientific investigations and other possession and/or use of this agent as a way of protecting society from its nefarious use. Beyond concerns of intentional introduction of tularemia is the presence of this disease among the global 

plethora of emerging infectious diseases impacting humans and animals.9 Tularemia clearly is 

an emerging and resurging disease4 and one likely to gain increased prominence as a disease to 

be anticipated. Wildlife are an important component of the ecology of tularemia, including the 

maintenance of F. tularensis in nature and in disease transmission. This publication emphasizes 

the wildlife component of tularemia and is presented in a non-technical format to be useful for 

a broad audience with varying levels of biological knowledge. Technical terms are defined in a 

glossary. The citations serve as the foundation for the information presented and as a gateway 

to the scientific literature for those seeking greater detail. This publication is one of a series of 

publications on selected emerging diseases to supplement Disease Emergence and Resurgence: 

The Wildlife-Human Connection.9

Milton Friend

vii

Acknowledgments

I gratefully acknowledge the numerous individuals that provided their expertise and time in 

contributing to the completion of this publication. Especially noteworthy is the outstanding 

assistance provided by Ms. Katherine Wesenberg, librarian, and her USGS National Wildlife 

Health Center (NWHC) library staff. Countless documents needed for review, including obscure 

historic reports and journal articles, were obtained in a timely manner and always delivered with 

a smile. The editorial support by Ms. Gail Moede Rogall (NWHC) and layout, design, and associated editorial assistance by Ms. Elizabeth Ciganovich of the USGS Cartography and Publication 

Program (CAPP) significantly enhanced the information provided here and is greatly appreciated. 

The major illustrations by Mr. John Evans of the USGS Colorado Water Science Center greatly 

aided and enhanced the presentation of material in this circular, as well as the illustration 

and graphics provided by NWHC project assistant Ms. Jennifer Rodriguez, and Ms. Rosemary 

Stenback and Ms. Erin Dornaus of CAPP. NWHC staff, Ms. Kelly Conrad, Ms. Melissa Lund and 

Ms. Rochele Streb also provided invaluable assistance by compiling data, checking information, 

typing manuscript drafts, and providing other logistical support. Dr. Robert L. Rausch provided an 

early technical review and encouragement, and Drs. David Blehert, Louis Locke, Jeffrey Ryan, 

and Suzanne Medwell provided technical reviews for the final draft. I sincerely appreciate the 

contributions of those noted above and apologize for any oversight that may have occurred due 

to the extended period of time in completing this project.

ix

Contents

Preface ............................................................................................................................................................v

Acknowledgments.......................................................................................................................................vii

Overview..........................................................................................................................................................1

Background.....................................................................................................................................................2

Causative Agent.............................................................................................................................................3

Geographic Distribution................................................................................................................................9

Patterns and Trends ....................................................................................................................................11

Species Susceptibility.................................................................................................................................13

Human Infections................................................................................................................................18

Animal Infections................................................................................................................................18

Obtaining a Diagnosis .................................................................................................................................19

Wildlife..................................................................................................................................................19

Humans.................................................................................................................................................19

Disease Ecology...........................................................................................................................................22

Lagomorphs ........................................................................................................................................24

Rodents.................................................................................................................................................36

Carnivores............................................................................................................................................36

Birds......................................................................................................................................................37

Invertebrates .......................................................................................................................................38

Domestic Animals...............................................................................................................................46

Companion Animals............................................................................................................................46

Environmental Persistence ...............................................................................................................46

Points to Ponder...........................................................................................................................................48

Disease Prevention and Control................................................................................................................49

Treatment .............................................................................................................................................53

Literature Cited.............................................................................................................................................53

Glossary.........................................................................................................................................................63

Topic Highlight Boxes

Box 1. The Journey of Bacterium tularense to Francisella tularensis..................................................6

Box 2. Birds and Tularemia.........................................................................................................................17

Box 3. Tularemia and You: Forms of Infection .........................................................................................20

Box 4. Human Movement of Tularemia ....................................................................................................22

Box 5. “Keep the Bare Hands Out of a Wild Rabbit” .............................................................................26

Box 6. Rodents and Tularemia ...................................................................................................................32

Box 7. Cats, Dogs, and Tularemia..............................................................................................................47

Box 8. Tularemia—Who Is At Risk? ..........................................................................................................50
Illustrations

1. General distribution by biogeographic region of type A and type B strains of 

Francisella tularensis and their primary wildlife vectors.......................................................5

2. Reported occurrence of tularemia by country.........................................................................8

3. Geographic distribution of tularemia in Norway, Sweden, Japan, and the 

former Soviet Union......................................................................................................................9

4. Reported human cases of tularemia in the USA, 1924–2000 ..............................................11

5. Geographic distribution of human cases of tularemia within the USA .............................12

6. Seasonal occurrence by decade of human cases of tularemia within the USA.............12

7. Gross lesions of tularemia.........................................................................................................19

8. Relative frequency within North America of tularemia cases diagnosed in 

humans caused by different strains of Francisella tularensis ............................................24

9. Noncontributor, reservoir, donor, and recipient species in the ecology

 of tularemia.................................................................................................................................25

10. Pathways, hosts, and primary vector associations for lagomorphs and tularemia 

in North America.........................................................................................................................31

11. Rodents and tularemia in North America: general pathways for infection. .....................36

12. Generalized life cycle for three-host Ixodid ticks that commonly vector tularemia,

and pathways for the transfer of Francisella tularensis between ticks, animals, 

and humans .................................................................................................................................44

13. General geographic ranges for the primary tick vectors of tularemia in 

North America; A, species commonly feeding on humans, B, species that 

rarely feed on humans but do feed on birds and small mammals......................................45

14. An endangered Delmarva fox squirrel that was a postrelease casualty 

of tularemia..................................................................................................................................49

15. Humans can acquire tularemia by many routes and from numerous sources ................52
xi

Tables

1 Tularemia, a disease of many names ........................................................................................1

2 Diversity of host species for Francisella tularensis................................................................2

3. Examples of historic diseases of humans now believed to be occurrences 

of tularemia....................................................................................................................................2

4. First documentation of tularemia in selected countries ........................................................3

5. Recent examples of tularemia in nontraditional geographic locations.............................10

6. Examples of reported human cases of tularemia by country..............................................10

7. A synopsis of North American mammals known to be susceptible to infection 

by Francisella tularensis and probability of human infection .............................................13

8. Domestic animals naturally infected with Francisella tularensis ......................................14

9. General importance of invertebrates in the natural history of tularemia..........................15

10. Incidental species susceptible to Francisella tularensis.....................................................18

11. Upland game birds reported to be naturally infected with Francisella tularensis ..........37

12. Response of upland game birds to laboratory exposure to Francisella tularensis .........38

13. Reported susceptibility of waterbirds to Francisella tularensis .........................................39

14. Birds of prey reported to be naturally infected with Francisella tularensis .....................40

15. Response of birds of prey to laboratory exposure to Francisella tularensis ...................40

16. Reported susceptibiltity of Corvidae, Laniidae, and Alaudidae to infection 

by Francisella tularensis ...........................................................................................................41

17. Reported susceptibiltity of domestic bird species to infection 

by Francisella tularensis ...........................................................................................................41

18. Arthropod species of primary importance in transmission of 

Francisella tularensis.................................................................................................................42

19. Examples of environmental persistence of Francisella tularensis ....................................48

Words in bold type in the text, the topic highlight boxes, and the tables are defined in the 

Glossary.

“I know of no other infection of animals communicable to man that can be acquired 

from sources so numerous and so diverse” (Parker10).

“The causative agent of tularemia, Francisella tularensis, is one of the most 

infectious pathogenic bacteria known...” (Dennis et al.4

).

are not contagious and most often result from contact with 

infected wildlife, ingestion of or contact with contaminated 

water, or bites from ticks and other arthropods that have 

fed on infected wildlife. Aerosol transmission is another 

way humans can become infected. Disease is expressed in 

different clinical forms, and varies in severity depending on 

the virulence of the organism, dose, and site of inoculum.4

Tularemia has a broad geographic distribution in the Northern Hemisphere and is more restricted elsewhere.11 A wide 

variety of species have been naturally infected by F. tularensis;

11–13 the number of species reported to be susceptible to 

infection exceeds 300, according to a recent report, which 

does not include some of the cold-blooded species such as 

fish and snakes (Table 2) reported by others.14

By Milton Friend

Table 1. Tularemia, a disease of many names.

Country Synonyms Primary animal hosts

USA13,15–18 Plague-like disease of rodents, plague-like lymphadenitis, 

conjunctivitis tularensis, Francis’ disease, deerfly fever, rabbit 

fever, rabbit disease, cattle-fly fever, Pahvant Valley fever or 

plague, glandular-type tick fever, Bacterium tularense

Beavers, water voles, rabbits

Japan19,20 Yato-byo (hare disease), hare meat poisoning Japanese hares

Former Soviet Union19,21 Sibirskaia iazva (Siberian ulcer), epidemic polyadenitis, water-rat 

trappers’ illness, epidemic lymphadenitis, khvar (“the ailment”)

Water voles

Norway22,23 Leemands soet (lemming fever), hare plague Lemmings, hares

Sweden Hare plague Hares

Tularemia

Synonyms

Colloquial terms for tularemia have their origins in 

several countries. Those synonyms include clinical 

manifestations of the disease, sources of disease, 

recognition of early investigators associated with this 

malady and geographic areas of occurrence (Table 1).

Overview

Tularemia is a highly infectious disease caused by the 

bacterium Francisella tularensis. Infections in humans 
Table 2. Diversity of host species for Francisella tularensis.

Representative species Number of speciesa

Mammals

190

Invertebrates

88

Birds

23

Amphibians

3

Reptiles

Very few

Fish

Very few

a

Data presented for mammals, invertebrates, birds, and amphibians are 

from a recent scientific review of tularemia.14 These data represent relative 

numbers of species in each of the groups that have been found to be susceptible to infection by F. tularensis, but are less than the cumulative total 

of all reports. For example, approximately twice the species of birds shown 

are documented within this chapter as being susceptible to infection by 

F. tularensis. Also, only limited investigations have been undertaken with 

amphibians, reptiles, and fish.

Background

The history of tularemia is both that of a disease of two 

ages and a “tale of two diseases.” Tularemia is thought to 

have evolved as a disease of wild animals in both the New 

World and the Old World about 11 million years ago during 

the end of the Miocene or early Pliocene.

24,25 The transition 

between those epochs was a time of rapid evolution for land 

mammals and the evolution of Francisella spp. is thought 

by some to be associated with that of rabbits and hares. 

The present forms of F. tularensis have different levels of 

virulence for humans in the Old World than those in the New 

World.25

Tularemia was first described as a disease of humans prior 

to the discovery of the causative agent (Table 3) and probably 

occurred in Japan as early as 1818 and in Norway since at 

least 1890 26 and perhaps as early as 1653.27 The first verified 

human cases occurred early in the 20th century (Table 4). 

Within North America, the first case supported by laboratory diagnosis occurred in 1914 in an Ohio meat cutter.28,29

However, retrospective evaluations indicate that the first 

two human cases occurred in 1904 in California and in 1907 

in Arizona.15 Six additional cases in Utah during 1908 and 

1910 of what is now known to be tularemia were diagnosed 

as deerfly fever.30 Dr. Edward Francis provided the linkages 

between disease syndromes in the United States, Japan, and 

the former Soviet Union (Table 1) as being caused by bacteria 

of the genus that now bears his name.19,31

Table 3. Examples of historic diseases of humans now believed to be occurrences of tularemia.

Disease Year Location

Lemming fever 1653 Norway27

Siberian ulcer 1741 Western Siberia21

Hare meat poisoning 1818, 1837 Japan26

Steinkrankheit 1825 Siberia32

Pestis minor 1877–79 Astrakhan, former Soviet Union32

Typhus associated with buboes 1877–78 Astrakhan, former Soviet Union32

Deerfly fever 1908–10 Utah, USA30

Plague-lilke disease of rodents 1908–11 California, USA17

Epidemic polyadenitis 1921 Irtysh River, former Soviet Union21

Epidemic lymphadenitis 1925 Voronezh Oblast, former Soviet Union21

  Tularemia
The first North American case of tularemia in wild 

animals supported by a laboratory diagnosis occurred in 

1912 during plague studies in California ground squirrels.

16 Francis proposed the name tularaemia to differentiate 

this disease from rodent plague because of the characteristic septicemia seen.24 Other investigations established the 

presence of tularemia in meat market cottontail rabbits in 

Washington, D.C.33

Reported human cases of tularemia within the USA were 

greatest during the 1930s and 1940s, averaging over 1,000 

cases per year. Since then, the yearly average has fallen 

below 200; however, the past importance of tularemia as a 

human disease, considerations of tularemia as a biological 

weapon,4 and several recent major epidemics have caused 

renewed interest in this disease.5

Causative Agent

Tularemia is caused by infection with a small, aerobic, 

pleomorphic, nonspore-forming, Gram-negative coccobacillus now classified as F. tularensis,34 following the 

original name of Bacterium tularense16 and other designations.11,35 Combinations of biochemical, epidemiological, 

virulence,and pathogenesis data have been used to subdivide 

F. tularensis into two major biovars (subspecies). Biochemical and molecular studies of isolates have identified different varieties of those subspecies (Box 1), raised a number of 

questions about the taxonomy of Francisella spp., and have 

also provided some enhanced insights regarding the ecology 

of tularemia. 

Despite taxonomic questions and strain differences, a basic 

understanding of tularemia in humans and wildlife can be 

gained by viewing tularemia as being caused by type A and 

type B subspecies,36 which distinguishes the highly virulent strains of the bacterium (type A) for humans from less 

virulent strains (type B). In North America, these different 

strains of F. tularensis have typically been associated with 

infections of different species of wildlife (Fig. 1). Only type 

A forms (F. tularensis tularensis) are moderately to highly 

virulent for humans and animals. Type A strains can cause 

illness in humans from an inoculum containing as few as 10 

organisms.37 Type B strains (e.g., F. tularensis holarctica) can 

also cause high mortality in wildlife but are generally of low 

virulence for humans. These strains usually require an inoculum of 10,000 organisms or more to cause illness in humans.37

Type A, once thought to be present only in North America, 

has recently been found in arthropods in Europe.38

Table 4. First documentation of tularemia in selected countries.

Continent Countrya Yearb Case

North America USA 1911 Animal17

Canada 1929 Animal39

Mexico 1944 Human40

South America Colombia 1948 Human41

Venezuela 1948 Human42

Argentina 1953 Human42

Ecuador 1958 Human43

Europe Austria 1917/1935c Human44.45

Former Soviet Union 1926 Human25

Norway 1926/1929d Human46

Germany 1928 Human45

Italy 1931 Animal40

Sweden 1931 Human50

Czechoslovakia 1936 Human45

Greece 1938 Human32

Finland 1938 Human47

France 1938 Animal41

Poland 1942 Animal32

Yugoslavia 1944 Human32

Causative Agent  
  Tularemia

Continent Countrya Yearb Case

Europe Netherlands 1961 Animal48

Romania 1997 Human49

Belgium 1947e Human41

Switzerland 1948 Human41

Denmark 1949 Animal41

Bulgaria 1951 Animal51

Spain 1952 Animal13

Croatia 1952h Human52

Kosovo 1999 Human53,54

Middle East Turkey 1913/1936f Human55

Iran 1970 Animal48

Africa West Africa 1936 Human56

Tunisia 1938 Animal56

Ruanda-Urundi 1951 Human41

French Cameroons 1952 Human41

Austro-Asia Japan 1924 Human57

Thailand 1954 Human41

Chinag 1980 Human58

Australiai 2003 Human59

a

For several countries (i.e., Ecuador, Colombia, Thailand), reports could only be found of a 

single case of tularemia and in others (i.e., Argentina, French Cameroons), a small number of 

cases were reported for a single year. Those data do not establish tularemia as being enzootic 

in those countries as it cannot be determined if the human cases reported were acquired within 

country or elsewhere (see Fig. 2).

b

The variability in reporting by different countries is such that earlier occurrences of laboratory-confirmed cases of tularemia likely exist for some countries. Also, retrospective analyses 

of disease reports from times prior to the isolation and identification of F. tularensis as the cause 

of tularemia clearly indicate the appearance of this disease in some countries in the 1800s; 

examples include Japan, the former Soviet Union, and Norway.50

c

Designated as the first documented human case in Europe based on serology and clinical signs; 

first major human epidemic did not occur until 1936;56 the first human cases associated with that 

epidemic occurred the previous year (1935).

d

Report includes two human cases from 1926 diagnosed in 1929 based on serology taken in 

1929 and clinical signs from 1926; the first human cases with isolation of F. tularensis are from 

1929.46

e

Most reports for the first appearance of tularemia in the Netherlands (Holland) are for 1953 

rather than the 1947 date given by a few authors.

f

An early case from 1913 diagnosed on basis of serology and clinical signs is reported; the first 

isolations of F. tularensis are from cases in 1936.56

g

Report exists suggesting that tularemia may have affected soldiers in China and Burma during 

World War II.56

h

First year for compulsory reporting of human cases.52

i

First report of tularemia in the Southern Hemisphere.59

Table 4. First documentation of tularemia in selected countries—Continued.
Nearctic

Palearctic

Neotropical

Ethiopian

Oriental

Australian

Holarctic

EXPLANATION Rabbit Hare Rodent Japanese hare Unknown

?

?

Figure 1. General distribution by biogeographic region of type A and type B strains of Francisella tularensis and their primary 

wildlife vectors.

Pathogen Type of 

organisima

Primary area

of occurrence

Principal 

wildlife vectors

Francisella tularensis tularensis

A North America Rabbitsb

F. tularensis holarcticae

B

Throughout Nearctic and 

Palearctic region 

(Holarctic)

Hares, rodentsd

F. tularensis mediasiatica

B Central Asia Rodentse

, hares

F. tularensis novicida

B North America, Australia Unknownf

a

Type A organisms typically cause moderate to severe disease in humans while type B organisms cause mild disease unless complications develop.

b

Cottontail rabbit in Central and Eastern USA, Mexico, and Latin America; black-tailed jackrabbits in West; and snowshoe hare in Northern areas.

c

Includes Japanese strains previously designated F. tularensis subsp. holarctica, biovar japonica Rodionova.5,7.59

d

Beaver, muskrat, and voles in North America and Eurasia; varying hare, European brown hare, and Japanese hare in Eurasia along with voles (especially 

water vole) and muskrat.

e

Voles, gerbils, and other small rodents.

f

Closely linked to waterborne transmission.

Causative Agent 
The Journey of Bacterium tularense to Francisella tularensis

 Tularemia

A Home at Last

1947–1959

Francisella tularensis

Agreement is reached among leading microbial taxonomists that the 

bacterium causing tularemia should be placed in an independent 

genus. That genus is designated Francisella in honor of the investigations of Dr. Francis.34,60

Discovery

1912

Bacterium tularense

McCoy and Chapin name the bacteria they isolated from California ground 

squirrels with a “plague-like” disease; the species name is drawn from 

Tulare County, California, the location for their investigations.

The nomenclature for the various subspecies of the bacterium causing tularemia 

has changed many times. As scientists developed a greater understanding of 

the genetic, biochemical, and molecular properties of the different strains of this 

organism, its geographic distribution, and the differences in the severity of disease 

in humans infected by these different forms of the bacterium, the nomenclature 

evolved. Highlights associated with these changes in nomenclature are provided 

here to document the transition that has occurred, the relations between nomenclature and enhanced knowledge of the epidemiology of tularemia, and to provide 

a basic understanding of the different nomenclature that is encountered within the 

literature.

Transitions

1920s–1946

Bacterium tularensis

Dr. Edward Francis determines that 

the disease reported by McCoy and Chapin and several other disease syndromes from North America, 

Asia, and Europe are all the same disease and suggests the name tularaemia to reflect the bacteremia 

often found in association with this disease.26,33 The 

species name is later changed from from tularense to 

tularensis.

Bacterium tularensis

Bacillus tularensis

Brucella tularensis

Pasteurella tularensis

Over time, the causative bacterium is placed in different genera by different investigators based on the 

properties of this bacterium relative to other bacteria. 

No general acceptance exists for any of the classifications.11

Box 1 The Journey of Bacterium tularense to Francisella tularensis
Unique isolations of organisms associated with human cases of tularemia63-65, aided 

by molecular technology, are continuing to refine the nomenclature for organisms 

within the genus Francisella. That technology indicates that F. novicida and F. tularensis are indistinguishable and has resulted in support for F. novicida being considered a subspecies of F. tularensis.

7

 Also, an additional species not involved with 

tularemia, F. philomiragia, has been added to the genus Francisella.

11,66,77 Further 

changes in the nomenclature for Francisella are likely.

Family Ties

1970

Francisella tularensis nearctica 

Francisella tularensis holarctica (syn. palaearctica)

Francisella tularensis mediaasiatica

Francisella tularensis holarctica a. japonica

Francisella novicida

Based on biochemical and pathogenic properties, the bacterium causing tularemia 

was divided into four geographic subspecies associated with North America 

(F. t. nearctica), throughout the Holarctic Region (F. t. holarctica), central Asia 

(F. t. mediaasiatica), and Japan (F. t. japonica). The placement of F. novicida, an 

organism found only in Utah, was a significant question as only rodents at that 

time were known to be affected.62

A Family Divided

1959–1961

Francisella tularensis tularensis

Francisella tularensis palearctica

Increasing notice is given to the marked differences in the severity of 

tularemia in humans in North America in comparison to other parts of 

the world. This difference is attributed to there being two major varieties of the bacterium: one occurring in the Nearctic Region (tularensis 

tularensis) and the other in the Palearctic Region. 60 (See figure 1.)

The Present

Francisella tularensis biovar (subspecies) tularensis 

(syn. nearctica; also known as type A)

Francisella tularensis biovar palaearctica (syn. holarctica, type B) 

Francisella tularensis palaearctica mediaasiatica

Francisella tularensis palaearctica japonica

More recent evaluations classify F. tularensis into four distinct subspecies:5,7

Francisella tularensis tularensis

Francisellla tularensis holarctica

Francisella tularensis mediasiatica

Francisella tularensis novicida

Kinship

1961–1970

Francisella tularensis, type A

Francisella tularensis, type B

It is shown that the geographic separation for 

different variants of the causative bacterium is 

not valid; tularemia cases of low severity caused 

by similar bacteria occur in the Nearctic and 

Palearctic Regions. Also, severe human cases 

of tularemia in North America are associated 

with different wildlife vectors than milder human 

cases. 

It is proposed that two distinct types of tularemia exist in North America and that they can be 

defined as tick-borne tularemia of rabbits (type A) 

and waterborne tularemia of rodents (type B). It is 

also noted that type B is comparable to tularemia 

in Europe and Asia.61

The Journey of Bacterium Tularense to Francisella Tularensis  

1 2 3 4 5 6
Common

Disease clearly enzootic and active.

PeriodicDisease clearly enzootic but extended periods may occur between new cases.

SporadicInfrequent occurrences suggest low level of disease in nature.

UncommonIsolated reports of low numbers of cases suggest transient presence rather thanenzootic status.

 Tularemia

Figure 2. Reported occurrence of tularemia by country.
Former Soviet Union

Norway

Sweden

Japan

in Scandinavia, the former Soviet Union, and in Japan is well 

documented (Fig. 3). Far less is known about the geographic 

distribution and the prevalence of tularemia in many other 

countries. Conflicting reports about the presence or absence 

of tularemia in some countries is partly due to questionable 

documentation for some areas and sporadic occurrences in 

new areas (Table 5). It is generally accepted that tularemia 

is absent from New Zealand and Central America. However, 

until 2003, tularemia had not been reported from Australia.59

Geographic Distribution

Tularemia occurs throughout much of North America and 

Eurasia (Fig. 2) but has a patchy distribution in the Northern 

Hemisphere (Holartic Region). In the USA, tularemia has 

been reported from every state except Hawaii.12 It has also 

been reported in every province of Canada.68 Although documentation is poor for the remainder of North America, tularemia is known to occur as far south in North America as Guadalajara, Mexico.11,36 The geographic distribution of tularemia 

Figure 3. Geographic distribution of tularemia in Norway,22 Sweden,69,70 Japan,71 and the former Soviet Union.25,66

Geographic Distribution  
10 Tularemia

Table 5. Recent examples of tularemia in nontraditional geographic locations.

Location Year Human 

cases

Cause Comments

Tuscany, Italy 1982 49 Contaminated village water 

system; infected hare 

suspected source

Only two cases previously reported in Italy; 

thought to be associated with importation of 

hares for hunting purposes.72

Western Bosnia 1985 ? Infected hares Poswar outcome.53

Central Spain 1997 585 Infected hares Only one case previously documented in Spain; 

outbreak associated with hare hunting.49

Central Spain 1998 19 Contaminated water and 

crayfish

Site far removed from 1997 epidemic; sewage 

plant suspected as contamination source; 

exposure of humans associated with crayfish 

fishing and cleaning.49

Kosovo 1999–2000 327 Rodent-contaminated food 

and water

First outbreak of tularemia in Kosovo; associated 

with postwar environmental conditions.53, 54

Southern Sweden 2000 270 Primarily mosquito bites Widespread outbreak in a geographic area where 

tularemia was previously rare. One of the factors 

correlated with human cases was owning a cat.70

Northern Territory,

Australia

2003 1 Waterborne infection First report from Australia and from the Southern 

Hemisphere. Suggestion that infections by 

F. tularensis novicida may be more common and 

widespread than previously thought.59

Table 6. Examples of reported human cases of tularemia by country.

Country Year of first report Reporting period Number of cases Average per year

USA 1911 1924–1960

1990–2000a

30,851

1,368

857.0

136.8

Japan 1924 1924–1994 1,372 19.6

Former Soviet Union 1926 1926–1942 73,300 4,581.3

Canada 1929 1930–1950

1946–1958

79

73

4.0

6.1

Sweden 1931 1931–1996 5,963 91.7

France 1938 1946–1947 404 36.7

a

Not a reportable disease from 1985 through 1999. Therefore, the number of cases may be somewhat less than occurred, even though cases generally still were 

reported.
1930 1940 1970 1990 2000

0

500

1000

1500

2000

2500

NUMBER OF HUMAN TULAREMIA CASES

1950 1960

DECADES

1980

Patterns and Trends

In general, reported human tularemia cases have substantially declined during the past half-century within endemic 

areas of the world;11, 73, 74 however, human cases have been 

reported during the past few years in areas where tularemia 

had not previously been found (Table 5). Fewer outbreaks of 

this disease are also being reported for wildlife, but, because 

wildlife disease surveillance is passive in most of the world, 

disease activity is most likely underreported. In humans, 

tularemia, especially the milder forms, is also undoubtedly 

underrecognized and underreported.4 Nevertheless, reported 

human cases provide sufficient information for evaluating patterns and trends for this disease. Although tularemia is widely 

endemic in Eurasia, it is typically a disease of Northern and 

Central Europe; Scandinavia and countries of the former 

Soviet Union report the most human cases. In Asia, tularemia 

is most prevalent in Japan (Table 6). 

In the USA, 15 human cases of tularemia with 2 deaths 

were recorded prior to 192436 and a total of 30,851 human 

cases were reported between 1924 and the end of 1960. 

However, a steady decline in the number of cases began in 

the 1940s75 after the high of 2,291 cases in 1939.76 Less than 

200 cases were reported during the 1990s (Fig. 4). In addition 

to reduced case numbers, geographic prevalence of tularemia within the USA has changed (Fig. 5). In contrast to the 

more eastern occurrence of tularemia cases during the first 

half of the 20th century, most human cases currently occur in 

the South, Central, and Western States, especially Missouri, 

Arkansas, Oklahoma, South Dakota, and Montana.4 Educating 

the public about tularemia and sources of infection has helped 

to reduce the number of cases.24 Changes in the pattern of 

disease may also reflect local and regional changes in wildlife 

and insect vector populations due to changes in the landscape 

and in human activities, such as trapping and hunting that 

have altered human interactions with wildlife reservoir hosts. 

The general pattern of tularemia within the USA is 

sporadic, small clusters of human cases. Tularemia is more 

likely to occur in males than females, in children younger 

than 10, and adults aged 50 or older,4 and may reflect activity 

patterns that enhance opportunities for exposure. Most cases 

now result from arthropod bites during the summer months 

(Fig. 6). Cases during winter are most common in hunters and 

trappers who handle infected animal carcasses.77, 78 The largest reported epidemic in the USA involved 50 tick-associated 

cases among military personnel on maneuvers in Tennessee.79

The largest reported wildlife associated epizootic resulted 

in a similar number of cases among muskrat trappers in 

Vermont.78 Despite the low number of human cases associated with individual events, the persistence of F. tularensis in 

nature has resulted in substantial numbers of humans contracting tularemia over the years. Also, the potential for this 

disease to be “explosive” was vividly demonstrated in Europe 

during World War II when thousands of Soviet and German 

soldiers on the Eastern European front contracted tularemia.4

Recent outbreaks, 585 confirmed human cases in Spain49 and 

327 confirmed cases in Kosovo,53 attest to the continuous 

potential for tularemia to jeopardize human health.

Figure 4. Reported human cases of tularemia in the USA, 1924–2000. Tularemia was not a reportable disease 

during the period of 1995 through 1999, but was reinstated to that status at the start of 2000.80–83

Patterns and Trends 11
Over 50

21–50

11–20

6–10

0–5

NN Not notifiable 2000

4

23

NN

1

1

1 5

3 28

11

2

2

2

11

1

3

1 2

2

2

2

13

1

2

NN

NN

AK 0

HI 0

0

0

0

0

0

0

0 0

0

0

0

0

0

0 VT NN

0

Over 500

201–500

101–200

51–100

0–50

1976–94

61

854

147

37

141

42

13 10

629 44

352

90

39

30

35

14

14

105

96

7

8

15

3

8

49 14

17

50

117

23

83

53

35

2 1

1

52

134

4

24

26

46 AK 17

HI 0

Over 1,000

501–1,000

101–500

51–100

0–50

1950–75

736

1640

581

489

712

538

60

234

295 573

547

177

283

234

189

28

158

422

328

90

124

83

29

30

49

136

90

38

45

10

122

58

20

1

VT 64 0

33

44

11

22

45

336 AK 3

HI 0

 MA 25

 RI 3

 CT 3

 NJ 11

 DE 2

 MD 119

DC 19

 MA 25

 RI 4

 CT 5

 NJ 51

 DE 9

 MD 442

DC 139

 MA 56

 RI 2

 CT 5

 NJ 12

 DE 5

 MD 38

DC 3

 MA 0

 RI 0

 CT 0

 NJ 0

 DE 0

 MD 17

DC 0

Over 1,000

501–1,000

101–500

51–100

0–50

NN Not notifiable 1924–49

3044

1613

790

1310

1100

1401

1500

863

1484 1315

698

383

542

607

496

500

451

24

637

161

302

391

114

336

95 240

436

84

94

189

346

96

34

1 0

2

43

17

49

33

65

787

AK NN

HI NN

0

10

20

30

40

50

60

PERCENTAGE OF CASES

1930–39 1940–49 1950–59 1960–69 1970–79 1980–89 1990–94 2000

DECADE

Oct–Dec

July–Sept

Apr–June

Jan–Mar

12 Tularemia

Figure 5. Geographic distribution of human cases of tularemia within the USA (not a reportable disease from 1995–1999). 80–82

Figure 6. Seasonal occurrence by 

decade of human cases of tularemia within 

the USA. The major decline of the 1930s 

and 1940s in the percentage of cases 

during October to December is likely due 

to reduced hunting activities associated 

with males being involved with World War 

II. Similarly, the decline since the 1950s 

in the percentage of human cases during 

January to March is likely associated with 

reduced trapping of muskrat and beaver 

due to the declining fur market. Major 

increases over time in the percentage of 

cases during other periods of the year 

reflects both the decreases in cases previously associated with hunting and trapping 

and increased outdoor recreation by the 

general public that facilitates tick-borne 

cases of tularemia. 80–82
Species Susceptibility

“Few, if any, zoonotic disease agents have a broader host distribution 

than F. tularensis.” (Hopla and Hopla11) 

Wild mammals are the primary hosts of F. tularensis, 

especially species within the orders Lagomorpha, Rodentia, 

and Sciuromorpha (Table 7). Sheep are the domestic mammal most commonly associated with tularemia (Table 8), but 

within recent years domestic cats have become an increasing 

source for human cases of this disease.84–89 Birds are fairly 

resistant,11 but a variety of species have acquired natural 

infections (Box 2) and mortality has been reported in some 

instances. Invertebrates, primarily ticks, have substantial 

roles both in the maintenance of F. tularensis in nature and in 

disease transmission (Table 9). A variety of other species has 

also been infected naturally or experimentally (Table 10). 

Table 7. A synopsis of North American mammals known to be susceptible to infection by Francisella tularensis and probability of 

human infection.a

Family Species Source for

human infectionb

Cervidae Mule deer, white-tailed deer Common

Antilocapridae Pronghorn Rare

Ursidae Black bear Rare

Canidae Coyote, red fox, gray fox, kit fox Occasional

Felidae Bobcat Rare

Mustelidae Mink, badger, spotted skunk, striped skunk, weasel, black-footed ferret Occasional

Procyonidae Raccoon Occasional

Erethizontidae Porcupine Rare

Soricidae Wandering shrew Occasional

Leporidae Snowshoe or varying hare, black-tailed jackrabbit, white-tailed jackrabbit, cottontail rabbit (eastern, desert, brush, pygmy, mountain) Very common

Dipelphidae Opossum Rare

Castoridae Beaver Very common

Muridae

(formerly Cricetidae)

Mouse (deer, canyon, piñon, western harvest, and house); white-footed mouse 

(redwood, Sonoran, Osgood); rat; muskrat; woodrat (white-throated, dusky-footed, 

bushy-tail, desert); Norway rat; meadow vole (Sawatch, Drummond’s, Tule); vole 

(California, montane)

Very common

Heteromyidae Pocket mouse (Great Basin, long-tailed); kangaroo rat (Ord’s, chisel-toothed, Great 

Basin) Rare

Sciuridae Chipmunk (eastern, least, cliff); woodchuck; yellow-bellied marmot; ground 

squirrel (antelope, Townsend’s, Piute, Richardson’s, Wyoming, Columbian, Uinta, 

California); white-tailed prairie dog, black-tailed prairie dog; squirrel (gray, red, 

fox, Wind River pine)

Very common

Zapodidae Jumping mice Rare

a

Adapted and modified from Reilly13 with some additions.

b

Relative importance varies for species identified within family groups.

Species Susceptibility 13
14 Tularemia

Table 8. Domestic animals naturally infected with Francisella tularensis.

Species Probabillity

for diseasea Comments

Sheep High Humans in the USA, Canada, and Russia have become infected from 

shearing, skinning, and slaughtering infected sheep and from infected ticks 

previously attached to sheep.90–92

Goats Low Rarely have clinical disease.

Swine Intermediateb Infections are primarily in young animals, due to bites from infected ticks 

and from eating infected rodents.27

Cattle Moderatec Bites of infected insects and contaminated pasture and water may result in 

fatal infections;27 57–91 percent of cattle tested in a tularemia enzootic area 

of the former Soviet Union had antibody to F. tularensis.

93

Water buffalo Low Chronically infected experimentally and shed F. tularensis in urine for as 

long as 37 days.19

Camel Moderate Isolation of F. tularensis in Kazakhstan region of former Soviet Union;25

camels are highly susceptible and are commonly infected in the desert areas 

of that country. Transmission to camels is thought to be by biting midges

that have fed on infected gerbils.

94

Horse Intermediate More resistant than cattle, but foals heavily infested with infected ticks 

have died.95

Catd Moderate Reported to be highly resistant by early investigators in the former Soviet 

Union. However, tularemia has been diagnosed in domestic cats within that 

region and also in Europe, Asia,27 and North America96–99; cats can directly 

(bites and scratches) and indirectly (transfer of infected ticks) transmit 

tularemia to humans.84,100

Dog Intermediate More resistant than cats, but numerous cases have occurred in Europe, the 

former Soviet Union, and in the USA; most involve hunting dogs and dogs 

associated with sheep ranching.27,101 Transmission to humans is mechanical, from contaminated mouth parts following the killing and sometimes 

consumption of infected rabbits, and from infected ticks.

a

With the exception of sheep and cats, tularemia in domestic animals is uncommon in North America.

b

Infection relatively common but clinical disease seldom reported.

c

Clinical disease is relatively common in this species.

d

Recent studies indicate that cats are mildly to highly susceptible to infection by F. tularensis and may die from tularemia. However, this disease is 

infrequently recognized in cats because clinical signs often mimic other infectious diseases.84,85,96–100
Table 9. General importance of invertebrates in the natural history of tularemia.

[a designates the role of the species in maintaining foci of Francisella tularensis; b designates role of the species in infecting humans]

Transmission role

Species type Comments Naturea Humansb

TICKS “It is generally accepted that ticks are of major importance in maintaining the enzootic foci of tularemia.”11

• Ticks are biological vetors, some species of which serve as both hosts and reservoirs for F. tularensis.

• Ticks may harbor F. tularensis in their saliva/gut for as long as 2 decades.31

• Tularemia in North America is primarily a tick-borne disease.45

Hard ticks Those of the genera Ambylomma and Dermacentor are usually resposnsible for human 

cases, while those of the genera Ixodes and Haemophysallis, because they seldom feed 

on humans, are of greater importance for maintaining enzootic foci among wildlife.11,19

Primary vectors of type A strains of tularemia.

High High

Soft ticks Although experimental infection can occur, not important in the ecology of tularemia.11,19

Viability of F. tularensis following laboratory infection was at least 674 days in one 

species and 701 days in another.19,36

Localized—

low

Not

important

MITES

Natural infections demonstrated but, in general, do not support prolonged development 

with the mite; primarily mechanical vectors.102 General belief that mites are unimportant may be based on inadequate evidence, as gamisid mites are reported to be principal 

vectors in some associations.19 Persistence of F. tularensis for 47 days in infected mites 

and transmission via bite has been documented in the former Soviet Union. Mites of the 

genus Hirstionyssus are thought to transmit infection in water voles during winter and 

in other rodents during spring and summer.41 Because these mites feed repeatedly, they 

may continuously maintain infections in the host population for long periods. Also, 

experimental studies in the USA with the rat mite resulted in transovarial and transphasic transmission of F. tularensis within the mite and infection of mice by eating the 

infected mites.94

Localized—

low

Not

important

BITING FLIES

Deerflies, 

stable flies, 

and 

horseflies

Efficient vectors in specific areas such as Utah103 and the former Soviet Union;19 most 

transmission occurs between June and September in the western USA.41

Mechanical vectors that acquire F. tularensis by feeding on infected host or substrate 

and transmit agent when a blood meal is taken within a few days.

Hares, water voles, and contaminated water are primary sources for horseflies to 

acquire F. tularensis in the former Soviet Union; they remain infective for 2–3 days;94,102

deerflies in Utah acquire F. tularensis primarily by feeding on infected jackrabbits and 

transmit the organisim when they bite humans.103

Localized—

high

Localized—

high

Mosquitoes Not important in the transmission of F. tularensis in North America but are historic 

vectors in Russia and Sweden.11 Serve as mechanical vectors. Species of the genus 

Aedes commonly feed on tularemic water voles in the former Soviet Union where they 

transmit F. tularensis between voles and from voles to humans. F. tularensis can 

maintain itself in mosquitoes for up to 43–50 days and can be transmitted by the bite of 

the mosquito for up to 22–35 days.94

Localized—

high

Localized—

high

Species Susceptibility 15
16 Tularemia

Table 9. General importance of invertebrates in the natural history of tularemia—Continued.

[a designates the role of the species in maintaining foci of Francisella tularensis; b designates role of the species in infecting humans]

Transmission role

Species type Comments Naturea Humansb

BITING FLIES—Continued

Gnats and 

midges

Culicoides are occasional vectors of infection from hares to humans and between hares; 

gnats attack hairy parts of head and neck.19 In desert regions of Western Siberia, these 

smallest of all biting flies may also vector tularemia between gerbils, gerbils and camels, and camels and humans.94

Localized—

high

Localized—

low

Blackflies Too little information to know the significance, if any, for these species.102 Unknown Unknown

OTHERS

Fleas Can be infected experimentally, are infected in nature, and can retain infection for long 

periods of time.19 Although not considered important as a vector of F. tularensis to 

humans, they may have a greater role than is currently recognized in the transmission 

of F. tularensis between rodents.11,102 The squirrel flea has the distinction of having been 

the first ectoparasite found infected with F. tularensis.

41 Experimentally infected fleas 

have maintained viable F. tularensis for 355 days and some species shed F. tularensis in 

their feces for up to 30 days.94

Localized—

low

Not

important

Lice Sucking lice may have a more important role than thought in the transmission of

F. tularensis within a species.19 Experimental studies have shown infection to persist 

for as long as 35 days and that lice are capable of transmitting F. tularensis among 

rodents.41 However, the high degree of host specificity precludes transmission between 

species. There is no evidence that lice of humans are an important source of human 

infection.

Low Not

important

Bedbugs Capable vectors with infection being transmitted by ingestion of contaminated feces;19

laboratory infections have resulted in feces remaining infective from 36–88 days in one 

evaluation12 and for as long as 250 days in another.41

Not

important

Not

important

Caddis flies Become infected through water contaminated with F. tularensis and infect species that 

feed on them.102

Not

important

Not

important

Snails Same as caddis flies. Not

important

Not

important

 
In general, the role of birds in the ecology of tularemia is poorly understood. Because early investigations 

showed most birds to be relatively resistant to clinical disease even though they could be infected104,105 and 

because most human cases of tularemia are associated with lagomorphs and rodents, few investigations have 

focused on birds and tularemia. Nevertheless, within the USA, human cases of tularemia have been associated 

with preparing game birds, such as pheasant, grouse, and quail, for consumption.106–109 Pheasants, partridges 

(ruffed grouse), and prairie chickens are reportedly the sources of 11 human cases of tularemia in an early summary of this disease in Wisconsin.106 These cases, along with other human cases reported from upland game 

birds, contrast with expectations based on experimental studies.

The role of birds in the ecology of tularemia appears to be associated more with the persistence of this disease 

in nature than with direct transmission of F. tularensis to humans. In some areas, North American grouse share 

ticks with hares and cottontail rabbits, which helps maintain the natural foci of disease that is then transferred 

to humans from rabbits and hares (Fig. 13). Transmission occurs by contact with infected lagomorphs or arthropods, such as biting flies and other ticks that feed on humans and lagomorphs.36 Also, infected birds may be a 

source for fecal contamination of surface waters with F. tularensis. This was postulated for the first outbreak of 

tularemia in Vermont when nearly 50 people involved with trapping and handling muskrats contracted tularemia 

within a 4-week period.78 Migrating birds have also been considered a potential factor in the spread of tularemia throughout Central Europe,56 primarily by transporting infected ticks into new areas where they then infect 

small rodents or hares. For example, in 1983 on the island of Stora Karlsö in Southern Sweden, tularemia was 

established as a tick-borne disease of mountain hare, probably from migrating birds carrying infected ticks. This 

is the only area of Sweden where ticks are primary vectors of tularemia, whereas mosquitoes are the primary 

vector elsewhere.116,117

Available information from most bird-associated human cases of tularemia suggests entry of the organism 

through punctures or abrasions in the skin while preparing birds for consumption (i.e., skinning and dressing). 

Wearing protective gloves can protect against this type of exposure. Regardless, the potential for contracting 

tularemia from contact with birds is low and should not be a major concern, even in areas where tularemia is 

enzootic. However, the potential for translocation of ticks infected with tularemia should be considered when 

moving birds for conservation and other purposes to new locations.

Early experimental studies stimulated by the 

1925–1926 precipitous 

decline of rabbit and 

grouse populations in 

Minnesota show that 

ruffed grouse and blue 

grouse are susceptible 

to infection.89 Ringnecked pheasants110

produced antibody 

against Francisella tularensis when inoculated 

with this organism but 

did not exhibit clinical 

disease.111

Tularemia is established as a natural 

disease of wild birds 

by the isolation of 

Pasteurella 

(= Francisella) tularensis from a quail 

dying in the wild112

and from dead and 

dying sage grouse.109

Infected ticks are collected from healthy 

sharp-tailed grouse 

and ruffed grouse.110

Evidence emerges that F. tularensis isolated from grouse is of lower virulence 

than organisms isolated from rabbits. 

In addition, isolates from bird ticks are 

also of lower virulence.113 The organism 

involved may be a type B strain rather 

than the type A strain commonly seen 

in rabbits and hares in North America. 

Isolates of F. tularensis are also obtained 

from naturally infected gulls and the 

great horned owl. Waterfowl are 

infected experimentally.102 Pheasants in 

experimental studies in Japan are resistant to clinical disease but researchers 

conclude that pheasants could become 

carriers of F. tularensis.

114

An experimental study 

demonstrating high 

susceptibility of several 

species of oceanic birds 

to F. tularensis also discloses large numbers 

of viable bacteria in the 

cloacal contents of 

infected birds.115 That 

finding poses questions 

relative to the potential 

for migrating water 

birds to contaminate 

surface waters via their 

body discharges.

1925–1928 1929–1935 1935–1945 1968–

Birds and Tularemia Box 2

Birds and Tularemia 17
18 Tularemia

been reported in muskrat trappers78 and others experiencing 

multiple exposures.11 However, typically only a single ulcer 

is present at the site of entry for parenteral inoculation of F. 

tularensis by insect vectors, bone splinters, knife wounds, or 

pre-existing lesions when skinning or dressing infected wild 

animals.19 Enlargement of lymph nodes is another common 

clinical sign of this form of tularemia in humans (Box 3).

Animal Infections

Clinical cases of tularemia are infrequently observed in 

free-ranging wildlife as infected animals are often severely 

moribund or dead when found. Also, the clinical appearance 

of tularemia in afflicted wildlife commonly is not diagnostic. 

Among the clinical signs reported for hares and cottontail rabbits afflicted with tularemia12,14,24,19 are depression in behavior, 

easy capture, exhaustion, tameness, stupor, rubbing their nose 

and forefeet into the ground, not rearing their head or carrying their front feet well, recurrent spasms, and stagger.

Human Infections

Tularemia (type A infections) in humans is a moderately 

severe disease that follows a well-described course (Box 3) 

leading to the development of one of several clinical syndromes dependent on the route of exposure, dose, and virulence of the infecting organism.4,12 Prior to the use of antibiotics for the treatment of tularemia, infection resulted in death 

in 5 to 15 percent of the cases within North America; this has 

fallen to 1 to 3 percent during recent years12 and now averages 

less than 2 percent. However, untreated cases of tularemia that 

progress to systemic infections may result in severe disease 

with high rates of fatality. Outside of the USA, human deaths 

rarely exceed 1 percent because of the less virulent forms of 

F. tularensis present.49 Immunity following clinical disease is 

usually lifelong.11

The ulceroglandular form of tularemia is the primary 

clinical syndrome seen in humans, accounting for 70 to 85 

percent of North American cases.11,31 The classical ulcerated 

skin lesion associated with this form of disease is generally 

found on the fingers or hands of those that acquire infection 

from wildlife (Box 3). Multiple cutaneous ulcerations have 

Table 10. Incidental species susceptible to Francisella tularensis.

Species type Comments

Frogs and toads Spontaneous infections of lake frogs and green toads in Russia. Conflicting information relative to 

susceptibility level. Studies in Turkey showed that experimentally infected frogs contaminated water that then 

infected other frogs placed in that water. Some of the newly infected frogs established latent infections and 

excreted virulent F. tularensis back into the water.

Turtles The snapping turtle has been infected by F. tularensis.

Fish Naturally acquired F. tularensis documented for a loach in Kazakhstan. Human infections in the USA have 

been associated with handling catfish but most likely involved mechanical transfer of bacteria from 

contaminated waters on the external surfaces of the fish being handled.118,119 Experimental studies have failed 

to result in infection of six species of fish.120

Crustaceans Two species of Gammarus and freshwater crab with naturally acquired F. tularensis in the former Soviet 

Union. Fairy shrimp were sources of F. tularensis in the Western USA.

Mollusks Francisella tularensis isolated from six different species within the former Soviet Union. Snails were sources 

of F. tularensis in the Western USA.

Annelids Francisella tularensis isolated from leeches in the Ukraine.

Snakes Human infection associated with the skinning of a bull snake.44

Spiders A human case of tularemia in Oklahoma is attributed to the bite of a spider, presumably the brown spider.121
Death from tularemia following infection of sensitive species such as rabbits and hares is usually about 2–10 days.14 

Some cottontail rabbits that became affected with tularemia 

following their placement within a large enclosure were dead 

within 7 days. In two instances, apparently healthy rabbits 

trapped within that enclosure were found dead of tularemia 3 

days later.122

Nonspecific field signs for tularemia-infected domestic 

sheep include lagging behind the flock, labored breathing, 

rigid gait, diarrhea and frequent urination.73 Often, large numbers of the ticks that transmit tularemia to sheep are found at 

the base of the sheep’s ear and on the neck,73 a condition that 

affords a high index for suspicion of tularemia.19 Tularemia 

in domestic cats can range from mild to fatal disease and 

result in a broad spectrum of clinical signs, such as marked 

behavioral depression, enlarged lymph nodes, spleen, and 

liver, along with acute oral ulcerations and changes in blood 

chemistry.100,123

The extent and appearance of gross lesions of tularemia 

differ somewhat for different species of wild mammals, and, 

in some instances, may resemble those of bubonic plague

and tuberculosis.

104 In rodents, the lesions resemble that of 

paratuberculosis.

13 Lesions are more pronounced in less 

sensitive species, such as squirrels, because of the prolonged 

course of disease.14 Typical lesions visible on the surface of 

the liver, spleen, and lymph nodes are pale white to gray, 

often slightly raised necrotic foci, ranging in size from pinpoint to a few millimeters in diameter (Fig. 7). Similar lesions 

may also occur on the lungs and in the bone marrow; the 

spleen and liver may have a dark bluish-red coloration and be 

enlarged.13,24

Obtaining a Diagnosis

Wildlife

When one is determining causes of wildlife mortality, 

describing the field conditions associated with the dead 

animals is often as important as the carcasses. Fully record 

field observations and include observation notes along with 

any carcasses submitted for laboratory evaluations. Field 

examination of carcasses is not recommended when tularemia 

is suspected because of the potential for human exposure, 

the need for laboratory evaluations to confirm tularemia, and 

the potential for further contaminating the environment. Take 

appropriate precautions when collecting field specimens, 

keeping in mind the various routes for exposure to F. tularensis, such as skin contact, aerosol exposure, and ticks. 

Double bag carcasses in a manner that protects the integrity of the outer bag and avoids contamination of the exterior 

surfaces of that bag. The diagnostic laboratory processing the 

specimens will provide guidance on preservation and shipping methods. In general, diagnosis is based on the combined 

results of necropsy findings and isolation of F. tularensis 

from the carcass. When only tissues, ticks, or environmental 

samples are available for testing, a combination of laboratory assays, including animal inoculations, are used to isolate 

and identify the presence of F. tularensis in those specimens. 

Serology can also be used to identify specific antibodies present in blood.

Humans

The diagnosis of tularemia in humans is supported by a 

variety of assays and clinical evaluations readily interpreted 

by physicians. However, in a small number of the cases, diagnosing tularemia during early stages of the disease may be 

difficult because of the multiple clinical syndromes presented 

(Box 3).4,11 In addition, the current low number of tularemia 

cases in humans within the USA has resulted in a low index 

of diagnostic suspicion among clinicians and laboratory 

workers.4 In many other parts of the world, the number of 

human cases of tularemia is also declining and may be creating similar situations. Nevertheless, early treatment is often 

needed, especially in North America because of the presence 

of the more virulent type A strains, to prevent the progression 

of infection to the more serious clinical syndromes. Those 

seeking medical assistance can aid their health professionals by providing information about their activities prior to 

becoming ill (i.e., outdoor recreation, contact with animals, 

and similar information) that might reflect the potential for 

exposure to tularemia and other zoonoses.

Figure 7. Gross lesions of tularemia. The “spots” within the liver 

of this beaver are focal necrosis and are typical lesions of tularemia seen in infected lagomorphs and rodents.

Photo by James Runningen

Obtaining a Diagnosis 19
20 Tularemia

Humans are highly susceptible to Francisella tularensis and infection can range from mild, unapparent cases to 

severe illness that may progress to death. Under some circumstances, untreated mild infections can progress 

to severe disease. Susceptibility to infection, multiple sources and routes for exposure, and the consequences 

from infection are among the reasons why F. tularensis is considered a potential biological weapon. Recent events 

involving bioterrorism have resulted in the Working Group on Civil Biodefense developing consensus-based 

recommendations for response by medical and public health professionals if tularemia is used domestically as a 

biological weapon.4

The virulence of the organism, dose, and route of exposure are important factors influencing the clinical form 

and severity of disease. In general, the course of clinical disease is abrupt and includes sudden onset of fever 

(38–40oC), shaking chills, generalized body aches that often are prominent in the low back, headache, sore throat, 

and thick nasal discharge (coryza). Nausea, vomiting, sweats, fever and chills, progressive weakness, general discomfort (malaise), loss of appetite (anorexia), and weight loss may also occur as the disease progresses.4

 Several 

primary clinical forms of tularemia have been described to categorize human infections. Those highlighted below 

are described in greater detail by Cunha,31 Dennis et al.,4 and others.

3 Oculoglandular Tularemia

In 1914, Dr. Derrick Vail presented a paper titled “A Case of 

‘Squirrel Plague’ Conjunctivitis in Man” before the Ophthalmatic Section of the Michigan State Medical Society. 

He contended there was no precedent for this case in the 

written ophthalmic literature and believed it to be the first 

report of infection of the human eye by the agent causing 

a plague-like disease among rodents, notably the California 

ground squirrel.28 The patient was a Cincinnati meat cutter in 

an inexpensive restaurant and was thought to have become 

infected by handling wild rabbits purchased by the restaurant. About 1 to 5 percent of tularemia cases within the 

United States are of this form. Exposure generally involves 

direct contamination of the eye by fingers, water spray, and 

aerosol transmission. For example, handling of a wild baby 

rabbit brought into the home likely contaminated the fingers 

of one individual who acquired oculoglandular tularemia.127

This form of tularemia can be quite painful and in extreme 

cases may result in a loss of vision. Clinical signs may 

include ulceration of the conjunctiva and the development 

of abnormally large amounts of fluids (edema) within the 

eye. Tearing, pussy discharge from the area of infection, 

sensitivity to light, and ocular pain are also associated with 

the infection. Enlargement of regional lymph nodes also 

occurs.

4 Oropharyngeal Tularemia

This form of tularemia is acquired by drinking contaminated water, ingesting contaminated food, and, in some 

instances, by inhaling contaminated droplets or aerosols. 

Contaminated wells that serve as public water supply have 

been a source for numerous human cases of tularemia in 

Europe.53,55,72 Contamination generally results from infected 

animals contaminating water that feeds the well, or by 

those animals entering the well itself. War, civil strife, and 

other conditions that may negatively impact the quality 

of public water supplies in tularemia endemic areas can 

contribute to the occurrence of this disease. The ingestion 

1 Ulceroglandular Tularemia

Most North American cases of tularemia (70 to 85 percent) 

are of this type and generally arise from handling contaminated carcasses or following a tick or other infective 

arthropod bite. Hunters and trappers are especially prone 

to exposure from contaminated carcasses during tularemia 

outbreaks within the species being pursued because gloves 

are seldom worn when handling animals. Hikers, campers, 

and others may be exposed to arthropods such as ticks and 

biting flies that have previously fed on infected animals. 

For example, deerfly bites were the source of two July 

2001 cases of tularemia in Wyoming.124 During that same 

time, one of two cases among rabbit hunters in Utah was 

attributed to a deerfly bite while camping and the other 

to handling a rabbit that may have been ill.125 During the 

summer of 2000, there was a cluster of 10 cases, including 

one death, on Martha’s Vineyard, Massachusetts; these 10 

men were all involved in outdoor activities.126 Ulceroglandular tularemia typically involves a painful, hard, discolored 

skin lesion that appears in 3–5 days at the site of exposure. 

Two days later, a firm, punched-out tender ulcer with raised 

edges is formed. Disease progression involves the spread 

of the organism from the skin lesion to the lymphatics, 

producing painful enlargement of the lymphatic glands. 

Further spread of the organism through the bloodstream 

may follow with associated impacts on major organs and 

other body systems.

2 Glandular Tularemia

Similar to the ulceroglandular form, but no skin lesions are 

evident to indicate the site and cause of exposure. About 5 

to 10 percent of human cases are of this type.

Box 3 Tularemia and You: Forms of Infection
3

1

5

4

2

7

6

of inadequately cooked meat from infected game animals, 

including birds, is another source for infection.36 This form 

of tularemia may result in a painful sore throat accompanied 

by inflammation of the mouth, tonsillitis, and swelling of the 

throat that is accompanied by fluid discharge. Lymph nodes 

can also become enlarged. 

The number of human cases of tularemia in the USA has decreased significantly from more than 1,000 per 

year prior to 1950 to less than 200 per year in the 1990s.130 Nevertheless, tularemia remains a global disease 

worthy of consideration as outdoor activities are pursued in areas where this disease is known to exist. 

5 Tularemia Pneumonia

This can result from inhaling contaminated aerosols or, as 

a secondary outcome, from spread of the organism from 

infection at other infected sites within the body. Cases of 

tularemia with primary lung involvement are most common 

in persons in high-risk occupations, such as laboratory workers. Outside of the laboratory, large outbreaks associated 

with handling F. tularensis-contaminated hay have occurred 

in rural communities of Scandinavia and in other countries.128 Francisella tularensis-laden aerosols are developed 

by handling infected dead animals, examining pets with 

respiratory infections, and from handling agar plates on 

which the organism has been isolated.129 Clinical symptoms 

are highly variable, as is the course and severity of disease. 

There is an absence of skin ulcers and enlarged lymph 

nodes with this form of disease. The significance of infection is reflected in this form of tularemia rapidly progressing 

to severe pneumonia, respiratory failure, and death in some 

instances. About 10 percent of cutaneous cases (ulceroglandular) and 50 percent of septicemias are complicated by 

pneumonia.129 Prior to the use of modern antibiotics to treat 

these infections, pleuropneumonic cases had a fatality rate 

of 30 to 60 percent.26

6 Typhoidal Tularemia

The diagnosis for this systemic form of tularemia is 

complicated by the absence of signs that identify either a 

site of entry by the organism, location of infection within 

the body, and a variety of symptoms also associated with 

other diseases. About 5 to 15 percent of human cases of 

tularemia are of this type.11 A personal history of sudden 

onset of acute illness associated with outdoor activity or 

contact with animals provides reason for consideration of 

this disease in tularemia endemic areas. The high casefatality rate (30 to 60 percent) associated with this form of 

tularemia underlines the importance of providing physicians 

with a good personal history of recent activities associated 

with the outdoors and animal contacts, including companion 

animals that are allowed to roam outdoors.

7 Tularemia Sepsis

This form of tularemia, like typhoidal tularemia, lacks 

specific clinical signs for guiding a rapid diagnosis. The 

consequences of tularemia sepsis are often grave, unless 

treated promptly, as septic shock (circulatory failure due to 

the release of endotoxins by high levels of bacteria within 

the blood) and other complications lead to severe illness and 

often to death.

Photos courtesy of the Centers for 

Disease Control and Prevention.

Tularemia and You: Forms of Infection 21
Because tularemia is not normally spread from person to person, efforts to prevent this 

disease may sometimes be less than rigorous. There also appears to be a willingness 

to accept risks that may facilitate outbreaks of tularemia that ultimately result in human 

cases. For example, moving infected animals and/or arthropod vectors of tularemia to new 

locations has established new geographic foci for this disease.

 1 The Massachusetts Experience

Prior to 1937, only three cases of tularemia had been documented in humans within the State of Massachusetts, all 

of which involved infections acquired outdoors. From 1937, 

the first year that releases of wild rabbits were reported, 

through 1940, nearly 26,300 Western rabbits were released 

into Massachusetts. During 1946, about 3,000 more wild 

rabbits were imported, primarily from Arkansas and Kansas. 

The Cape Cod area saw the first locally acquired human 

case of tularemia in 1937. Tularemia has persisted in this 

tick-infested area since then.126 Other early human cases of 

tularemia following rabbit releases include a 1941 case near 

Lawrence (northeastern Massachusetts) and cases during 

1946 from Martha’s Vineyard and Boston.131 These imported 

rabbits were certified at the shipping points by accredited 

health authorities who stated there had been no outbreaks 

of tularemia in the counties in which the rabbits were 

trapped and that these counties were free from contagious

and infectious rabbit diseases. Nevertheless, 2 of 136 rabbits that were examined during 1940 following their death 

during transit or shortly after arrival at game clubs were 

found to have tularemia. Those rabbits were found in shipments from Missouri and Arkansas, states with a combined 

total of more than 900 human cases of tularemia during the 

period of 1937–1940.131

Between 2000 and the end of summer 2005, nearly 40 

human tularemia cases were diagnosed on Martha’s Vineyard. Most of the cases are associated with landscaping, 

grounds caretaking, and gardening. Landscapers in this area 

are at greatest risk of contracting tularemia.132–134

2 Italy

During 1971, several thousand black-tailed jackrabbits 

trapped in an enzootic area for tularemia in southern Idaho 

were shipped (along with their Dermacentor parumpertus

ticks) to Italy for release on private hunting preserves. At 

that time, tularemia had not been isolated from wildlife or 

ticks from that country.24 Up to one million hares (jackrabbits) were imported to Italy for hunting in 1982 from several 

countries, including some from countries in which tularemia 

is present. The first reported major outbreak of tularemia 

in Italy occurred in Tuscany during 1982 in an area where 

hares are regularly imported for sporting purposes and was 

thought to be caused by an infected hare falling into and 

contaminating a public water supply. A total of 49 human 

cases occurred during a 3-week period from consumption 

of the contaminated water.72 A total of 223 cases were 

recorded by the end of August 1984.135

3 Prairie Dogs

Investigations of a 2002 outbreak of tularemia involving 

wild-caught, black-tailed prairie dogs at a commercial facility 

in the United States disclosed that in the 2 months prior to 

diagnosis of the problem, hundreds of potentially infected 

animals were shipped to several states and other nations.136 

The first reported prairie dog-to-human tularemia transmission was associated with this epizootic.137 These animals 

are primarily sold as pets and, in addition to markets within 

the United States, were also shipped to Japan, the Czech 

Republic, the Netherlands, Belgium, Spain, Italy, and ThaiDisease Ecology

Tularemia remains a persistent disease of humans because 

of the well-adapted relations that exist between F. tularensis 

and its small mammal and arthropod hosts. Those relations 

result in the ecology of this disease being as diversified as 

the morphology of F. tularensis.

19 What is representative for 

tularemia in one geographic area or set of environmental conditions may deviate greatly from that of another location and 

other environmental conditions. Thus, tularemia is a disease 

of many faces, a chameleon that adapts to various environmental conditions.

Occurrences of tularemia within geographic areas vary 

over time due to changing environmental conditions and 

because of human actions and behavior patterns. For example, 

the occurrence of tularemia in the former Soviet Union as a 

significant disease of humans is closely associated with the 

Box 4 Human Movement of Tularemia

22 Tularemia
1 2

3

3

3

land. As a result, international surveillance and investigations were mobilized in an attempt to minimize the potential 

for disease occurrence.138,139

Wild-captured prairie dogs from Texas for use as laboratory 

animals for study of an unrelated human disease introduced 

tularemia into a Missouri laboratory animal facility.140 In 

unrelated events, research institutions in Boston, Massachusetts, and Houston, Texas, also received wild-caught 

prairie dogs infected with tularemia.136

Decades ago it was noted that:

“...we are in an era of emerging zoonoses, which will involve 

extension of old problems into new areas and the evolvement of 

entirely new problems in zoonoses” (Hess).141

development of water vole trapping as a major activity. This 

activity was stimulated by the economic returns from water 

vole pelts and the great abundance of this species.142

Landscape changes affect plant, insect, and animal communities that are important components of the ecology of 

tularemia and many other diseases. Human activities within 

those landscapes influence the potential for exposure to 

F. tularensis. In addition, the great mobility of modern society 

has created a global community with expanded opportunities 

to encounter tularemia within different types of landscapes. 

Therefore, it is prudent to consider tularemia from a global 

ecology perspective rather than from just a local perspective. 

This broader perspective is also useful for evaluating disease 

risk that may be associated with wildlife translocations for 

conservation, zoological collections, sporting purposes, or 

other reasons (Box 4). 

Tularemia is a classic old problem that continues to be extended into new areas by human 

actions. Greater steps, including more rigid control of wildlife translocations and better 

wildlife disease surveillance, need to be taken so that human actions do not spread this 

disease any further.24

Disease Ecology 23
0

20

40

60

80

100

PERCENTAGE OF CASES

STRAIN

Type B

Type A

24 Tularemia

The ideal vertebrate reservoir host is highly susceptible 

to infection, is not killed by the infection, and remains as 

an infective source for other species for prolonged periods 

of time. Typically, only a minimal number of organisms are 

required for invasion of the host by the pathogen. Multiplication of the disease agent within the reservoir host results in 

infective levels of F. tularensis either circulating in the blood 

or being excreted through body discharges such as feces and 

urine over time. In some instances, F. tularensis may follow a 

recurring pattern of presence and absence throughout the life 

of the host. 

Lagomorphs 

The Lagomorphs (hares, rabbits, and pikas) and Rodentia 

(rodents) are the most important vertebrates in the ecology 

of tularemia. Hares and rabbits, but not pikas, are globally 

important natural foci of tularemia and as sources for infection of humans (Box 5).11 The rabbit and hare tularemia cycle 

of North America is tick-borne and involves type A strains 

of F. tularensis. Human infections generally result from 

contact with infected rabbits, bites from ticks that have fed 

on infected rabbits, and to a lesser extent from other means, 

including the consumption of inadequately cooked contaminated meat (Fig. 10). The Old World rabbit, known to many 

as the domestic rabbit, is relatively resistant to the indigenous 

strains of F. tularensis within its native geographic area and 

is not an important source of infection for humans or other 

mammals.11 However, fatal infection has resulted from experimental exposure to a virulent type A organism.104,143

The concept of type A and type B tularemia as distinct 

diseases is useful for understanding the ecology of the disease 

in North America. Type A tularemia is a tick-borne disease 

of rabbits and is generally of moderate to high virulence for 

humans and other species. Arthropods, other than ticks, can 

vector this form of disease. Transmission can also occur by 

other means such as by direct contact with infected animals. 

In North America, 90 percent of tularemia cases in humans 

are caused by type A strains (Fig. 8), whereas tularemia 

involving rabbits elsewhere is comparable to type B tularemia, a disease of low virulence for humans.61

Type B tularemia is typically a waterborne disease generally vectored by true rodents (i.e., species with only two 

incisor teeth above and below for gnawing, such as beaver 

and mice). About 5 to 10 percent of human tularemia cases 

within North America are attributed to this form of disease.61

Prairie dog-associated cases have been of this type.136,139 The 

low virulence of type B results in many undiagnosed cases 

because infected individuals may not seek medical assistance. 

Also, when medical assistance is sought, the general nature of 

an uncomplicated course of disease may result in a misdiagnosis. 

A wide variety of species can become infected by type A 

and type B forms of F. tularensis and both can cause severe 

disease resulting in mass mortalities of wildlife. Species contributing to the ecology of tularemia may be reservoir hosts 

important for the maintenance or perpetration of tularemia in 

nature (e.g., ticks) or simply be sources of infection for other 

species and are not directly involved in the maintenance of F. 

tularensis during periods of disease quiescence.24 Reservoir 

hosts are the species of ecological importance and are also the 

species of primary importance for the occurrence of tularemia 

in humans (Fig. 9). 

Figure 8. Relative frequency within North 

America of tularemia cases diagnosed in 

humans caused by different strains of 

Francisella tularensis.
Noncontributors

Non-contributors=Dead-end hosts that do not contribute to the continuous 

 maintenance of F. tularensis in nature.

Reservoirs

Donors

Recipients

May be susceptible to infection but generally do not develop

high enough levels of bacteria to infect vectors with sufficient

levels of F. tularensis to cause disease in other animals.

Recipients=Species required for circulation of F. tularensis as amplification hosts for

maintaining the epizootic; they are often the same species as the donors.

Provide for the maintenance of F. tularensis in nature during interepidemic/

epizootic periods.

Provide for the circulation of F. tularensis among species within enzootic foci.

Persistently infected throughout adult life and may pass infection to 

progeny in some instances.

Donors=Species that are the primary source for infection of reservoir hosts that 

 maintain F. tularensis in nature; in some instances they may develop 

 chronic infections and serve as reservoir hosts.

Reservoirs= Primarily ticks; species that continually maintain F. tularensis

in nature.

Highly susceptible to infection by F. tularensis.

Develop high levels of bacteria in blood, other tissues, and organs.

Maintain sufficient levels of F. tularensis for infection of vectors that feed on

the animal, for contamination of environments with infective levels in feces

or urine, and for direct contact transmission.

Figure 9. Non-contributor, reservoir, donor, and recipient species in the ecology of tularemia. The persistence of tularemia as an 

enzootic disease is to a large extent dependent upon the composition and interactions of animal and vector populations present within a 

specific habitat. The roles for these different species can be thought of as reservoir, donor, recipient, and non-contributing hosts.142 The 

composition and numbers of these various species and their interactions are often greatly influenced by human actions and by environmental factors.

Illustration by John M. Evans

Disease Ecology 25
26 Tularemia

Rabbits and hares are globally important in the ecology of tularemia. Within the New 

World, the cottontail rabbit, black-tailed jackrabbit, and snowshoe hare are the lagomorphs associated with tularemia.44 Several other species are involved in the Old 

World.14,45,56 A significant difference between tularemia in New World and Old World 

lagomorphs is that the strains of Francisella tularensis isolated from New World lagomorphs are of much greater virulence for humans (Jellison type A strains). However, 

large-scale epizootics from tularemia occur both in New World and Old World lagomorphs.

The collective importance of rabbits and hares as a source for human cases of tularemia is great because of human contacts from hunting,144 the large numbers of these 

animals utilized as food,33,145 and the role of these species as hosts for ticks that can 

transmit tularemia.36 Some perspective on the magnitude of human contacts with wild 

rabbits and hares in the USA is provided by an evaluation made decades ago. In 1932 it 

was reported that an estimated 25 million wild rabbits and hares are killed annually in 

the USA for food and fur.36 During recent years, fur harvests of wildlife have declined 

greatly within the USA, but many millions of rabbits and hares are still harvested by 

sport hunting and for other purposes.

The large number of human cases of tularemia associated with direct contact with 

rabbits and hares in the USA caused a leading tularemia investigator to state, “Keep 

the bare hands out of a wild rabbit.”44 He concluded that about 1 percent of wild rabbits and hares in the USA are naturally infected with F. tularensis, thereby providing a 

continuous risk for humans, even when epizootics are not occurring.

Wild lagomorphs are also a significant indirect source of human cases of tularemia. 

A number of reports, mostly from Old World countries, suggest that public water 

supplies have become contaminated with F. tularensis by tularemic rabbits falling into 

those water sources. Substantial numbers of human cases have resulted from such 

events.72

NEW WORLD

Cottontail rabbit 

distribution in 

North America149

cottontails.144 Ecological studies disclosed that weather in 

Illinois is an interactive factor with cottontail populations 

and tularemia. When cottontail populations are higher than 

average and warm weather precedes opening day of the 

hunting season, the risk of contracting tularemia is substantially higher. When cottontail populations are average, 

the risk of infection closely follows a curve of the mean 

Box 5 “Keep the Bare Hands Out of a Wild Rabbit”

Cottontail rabbit

(Sylvilagus spp.)

There are 2 subgenera and 14 species of cottontail rabbits. 

These species occupy ranges that extend from Southwestern Canada (mountain cottontail) and southern Manitoba 

to as far south as Venezuela (eastern cottontail) and 

Argentina (forest rabbit).146 The cottontail rabbit is the most 

important vertebrate in the ecology of tularemia within the 

USA.36,44,147 The eastern cottontail and the desert cottontail 

are the most important of these species in the transmission of tularemia to humans102 though hares are more 

important in some western and southern areas.148

More than 10,000 human cases and over 500 deaths from 

tularemia within the USA were attributed to cottontail 

rabbits by the early 1970s. Many of those cases occurred 

in Illinois. From 1926 to 1948 there were more than 3,000 

human cases of tularemia in Illinois, approximately twice 

the number for that time period of any other state. The 

great majority of these cases were due to contact with 
Black-tailed jackrabbit

(Lepus californicus)

Globally, there are 22 species of hares and jackrabbits, 

several of which are important hosts in the ecology of 

tularemia. In North America, the black-tailed jackrabbit 

is the most important of these species and occupies a general range that extends across much of the Western and 

Central conterminous USA and south to Northern Mexico 

and Baja California.146 Historic evaluations indicate that 

jackrabbits are the source of about 30 percent of human 

cases of tularemia caused by lagomorphs.12 Human cases 

of tularemia acquired from jackrabbits are more typically 

contracted during spring and summer than autumn,148 or 

historically, from market rabbits during winter.33 In general, 

the taking of jackrabbits has been loosely regulated relative to bag limits and time of year for harvest. They are 

Cottontail rabbit

Black-tailed 

jackrabbit distribution 

in North America149

date of the first 10 freezing autumn nights. That is, the 

earlier the mean date for frosts, the lower the risk. When 

cottontail populations are well below average, human 

tularemia cases are low even during warm autumns.144

The opening of the rabbit season after several frosts have 

occurred results in most ticks having left their rabbit hosts 

and also decreases the likelihood of tularemic rabbits still 

being alive.150 A number of state wildlife conservation 

agencies have considered these regulations when setting 

the hunting season for cottontail rabbits.144,150,151

Illinois is no longer one of the leading states in the number 

of human cases of tularemia. From 1976 to 1994, 61 

human cases were reported from Illinois; however, 11 

states reported many more cases than that.152,153 The reasons for this change in status are in part related to reduced 

human contacts with cottontails in Illinois. The Illinois 

harvest for this species from 1956 to 1977 declined by 58 

percent and the number of hunters declined by 33 percent 

in association with a 33 percent reduction in farms and 

changes in agriculture that reduced habitat and opportunities for rabbit hunting.154

Cottontail rabbits have also been associated with pneumonic forms of tularemia in urban and other areas. This 

form of tularemia can be very severe with a mortality rate 

of 30 percent155 and generally involves exposure through 

inhalation. For example, in the late 1970s in the Washington, D.C. area, three men training their dogs during the 

summer in an undeveloped wooded area adjacent to a 

housing complex handled a rabbit caught and killed by one 

of their dogs. The handling activities involved familiarizing 

their dogs with the rabbit’s scent. All three men contracted 

tularemia pneumonia and the dog that captured the rabbit 

died of unknown causes (no examination done) shortly 

after the owner became ill.156

In the early 1970s, five children were diagnosed with 

tularemia pneumonia. The source for infection was attributed to their poking a dead, partially opened rabbit with a 

stick.155 The rabbit was caught and killed by their dog while 

the children were in a wooded area of a neighborhood park 

in urban Baltimore, Maryland. A dead cottontail that was 

mowed over in a lawn was probably the source of infection 

in one of the human cases during a pneumonia tularemia 

outbreak on Martha’s Vineyard, Massachusetts in 2000.132

A cluster of seven tularemia cases, five of which were 

pneumonic, previously occurred on Martha’s Vineyard 

among a group of people sharing a cottage for a week. 

Their dogs killed several rabbits in the vicinity of the cabin 

and they most likely became exposed when the wet dogs 

shook rainwater from their fur when entering the cabin 

after their “rabbit hunting” forays.157 These examples illustrate that neither tularemia nor cottontails are restricted to 

rural and natural environments. The cottontail is common 

in urban and suburban areas where it is often found in 

yards and in vegetated areas adjacent to walkways.

Because of the popularity of the cottontail rabbit as a 

game animal, like the jackrabbit, large numbers have been 

translocated to restock depleted habitat and establish new 

populations.147,154 Kansas, Missouri, Texas, Maryland, New 

Jersey, and Pennsylvania are among the states that have 

received cottontails for stocking wildlife areas. Typically, 

disease has received little consideration in carrying out 

this activity.154

considered a pest species by many and in the past have 

commonly been harvested as feed for domestic animals 

raised for their fur. That practice has resulted in cases 

of tularemia in cats, dogs, and chickens148 as well as in 

ranched mink and foxes.158–160 Historically, jackrabbits were Photo by Milton Friend

“Keep the Bare Hands Out of the Wild Rabbit” 27
28 Tularemia

Black-tailed jackrabbit

Snowshoe hare

distribution in 

North America149

rounded up and large numbers of them killed to reduce 

depredation on crops and to reduce competition with 

livestock for forage on open range. The largest rabbit drive 

on record took place in California in 1892, involved about 

8,000 people, and resulted in the harvest of about 20,000 

to 30,000 rabbits.161

Despite being considered a pest species by some segments of society, jackrabbits are a desired species for 

others. To establish populations for hunting, jackrabbits 

have been translocated, including large-scale releases in 

Florida, Virginia, New Jersey, Massachusetts, Maryland, 

and in Italy.161

The primary role of jackrabbits in the ecology of tularemia 

may be the maintenance of this disease in nature through 

its principal ectoparasite, the tick Dermacentor parumapertus.

102 This tick rarely feeds on humans but can transmit 

tularemia among jackrabbits and perhaps other small 

rodents. The enzootic jackrabbit foci for tularemia is transferred to humans through direct contact with infected jackrabbits and by the bite of deerflies and other tabanids that 

have fed on an infected jackrabbit prior to biting a human.24

Jackrabbits may also be a component of tularemia epizootics among range sheep in the western United States. Tularemia in sheep kept on rangelands is associated with infesSnowshoe hare

(Lepus americanus)

The snowshoe hare is also called the snowshoe rabbit and 

the varying hare. Like other species of Lepus that live in a 

snowy winter climate, they molt into a white winter pelage. The snowshoe hare is generally found in coniferous 

forests—rather than in the open type of habitat occupied 

by jackrabbit—and in the great diversity of habitats including fields, farms, woodlands, deserts, swamps, prairies, 

and hardwood, rain and boreal forests occupied by various species of cottontail rabbits.146 The snowshoe hare is 

the most important small game animal in Canada because 

in remote areas it is often a mainstay winter food for Indians, homesteaders, and trappers.163 It is also the main food 

source for several carnivores.

147

The first isolation of F. tularensis from wildlife in Canada 

was made from a snowshoe hare in British Columbia, but 

anecdotal information suggests a much earlier presence of 

tularemia in Canada and in snowshoe hares.164,165 However, 

despite early reports that snowshoe hares are as important 

a source of tularemia for humans as cottontail rabbits and 

jackrabbits, that evaluation is no longer considered to be 

valid.36,147,150 More recent information indicates that while 

snowshoe hares maintain tularemia in nature, and can 

transmit F. tularensis to humans, they account for less than 

1 percent of the total source of human infection.12

Unlike other species of North American lagomorphs, 

the snowshoe hare appears to be relatively resistant to 

clinical disease and mortality from tularemia despite the 

tations by the tick D. andersoni;

102 human cases follow as 

a result of processing wool, meat, and other products from 

the infected sheep.162 In some situations tularemia may be 

a secondary outcome of tularemia cycling between ticks 

and jackrabbits.61,91 Sheep and jackrabbits share sagebrush 

areas where D. andersoni is abundant.102 The immature 

stages of this tick (larvae and nymphs) feed on a great 

variety of small mammals including jackrabbits and rodents 

while the adults feed on larger mammals including sheep, 

in addition to feeding on humans.36

Snowshoe hare (winter pelage)

Photo by Milton Friend

Photo by Charles Krebs
findings of antibody to F. tularensis that provide evidence 

of susceptibility to infection.147 The low-grade infection that commonly occurs is likely a factor in the small 

number of human cases of tularemia associated with 

this species,44,147 despite the large numbers of snowshoe 

hares that are harvested. For example, a historical report 

states that “about 2,000,000 varying hares are caught 

each winter in Maine.”166 More recent data indicates that 

OLD WORLD

hunters in Michigan harvest about 200,000 to 400,000 

snowshoe hares annually.167 However, in some situations 

the snowshoe hare may be an important source for human 

cases of tularemia. Over a 5-year period, Douglas County, 

Wisconsin, ranked fourth in number of snowshoe hares 

harvested in the State and second in the number of human 

cases of tularemia.106

Brown hare 

distribution in 

Europe168

Brown hare

Mountain hare (blue hare)

(Lepus timidus)

The mountain hare inhabits the tundra and coniferous forest zones from Scandinavia to Eastern Siberia, the Alps of 

Europe, and is also found in Scotland, Sakhalin, and Hokkaido.146 It is also referred to as the varying hare because 

of changes in coloration during the year due to pelage 

changes. The mountain hare serves as both a reservoir 

of tularemia in nature and as a source for infection of 

humans.19 In the former Soviet Union, it is important in the 

European part of the RSFSR, in West Siberia, and Yakuts- Distribution of 

mountain hare 

in Europe168 Photo by Laurie Campbell

European brown hare/Cape hare

(Lepus europaeus/capensis)

Debate exists whether or not the Cape hare is a separate 

species or only a race (variant) of the brown hare.168 The 

4th Edition of Walker’s Mammals of the World recognizes 

Lepus capensis as the brown hare and gives its distribution as the entire Palearctic region south of the coniferous 

forest zone except Northwestern China and Japan and all 

nonforested parts of Africa.146 Others identify Lepus europaeus as the European brown hare and note the densest 

populations are found in open country, preferably that with 

lush brushy vegetation. L. europaeus prefers pastureland 

to hayfields,168 while L. capensis is found occasionally in 

coniferous forests in addition to its usual habitat of open 

country.169

The European brown hare is reported to be the most 

common reservoir and vector for tularemia in Central 

Europe, along with rodents; tularemia causes 3 percent of 

the annual mortality in this species in France.14 Although 

rodents are the primary hosts and vectors of tularemia 

in the former Soviet Union, brown hares are important in 

the Northern Caucasus, the Ukraine, and in the Central 

and Western Provinces (Oblasts) of the Russia Soviet 

Federative Socialist Republic (RSFSR). Cape hare are commonly found infected by F. tularensis throughout much of 

southern Kazakhstan, especially in the spring.102 Tularemia 

is reported to cause mortality of up to 80–90 percent in 

cape hare populations in some areas.168

“Keep the Bare Hands Out of the Wild Rabbit” 29
30 Tularemia

Clearly, rabbits and hares are important hosts and vectors for tularemia, yet the European 

wild rabbit, more commonly known in North America as the domestic rabbit, is relatively 

resistant to infection by the indigenous type B strains of its natural geographic range and 

is not a common source of human disease.19

Distribution of 

Japanese hare71

Japanese hare 

(winter pelage)

Japanese hare

(Lepus brachyurus)

The Japanese hare and a subspecies, the Etigo hare, are 

the primary sources of tularemia in Japan. The geographic 

distribution of these hares coincides with that of human 

tularemia cases.57, 102 More than 90 percent of those cases 

are contracted from hares74, 170 and nearly all of those from 

the Japanese hare.57,71,171

kaya.102 Mountain hare are also an important species in the 

ecology of tularemia in Scandinavia.14,117 Tularemia in Sweden is correlated with population peaks of field vole and 

mountain hare.69 In Norway, mountain hare also are closely 

associated with human tularemia cases and have caused 

tularemia when carcasses are fed to ranched foxes.102

Mountain hare in its winter pelage

Photo by Jonathan Jordan, Sheffield, UK
Disease maintenance

Figure 10. Pathways, hosts, and primary vector associations for lagomorphs and tularemia in North America.

Illustration by John M. Evans

Disease Ecology 31
32 Tularemia

“Rodents are the chief source of infection of tularemia and 

the reservoir of its virus [bacteria] in the external world.” 

(Karpoff and Antonoff 172)

Mouse-like and other small rodents of varying sizes from voles and 

lemmings to muskrat and beaver are important hosts in the ecology 

of tularemia. Most, if not all, rodent species are highly susceptible 

to infection. They are hosts for the immature stages of a variety of 

ticks that can transmit tularemia, and they contribute to the ecology 

of tularemia in other ways, including contamination of freshwater 

used by humans and at times through the contamination of agriculture products such as hay and cereal grains. Worldwide, rodents are 

responsible for more human cases of tularemia than rabbits and hares, 

despite the prominence of lagomorphs as a source for human infection. Fortunately, the virulence for humans of F. tularensis from rodents 

is far less than that from North American rabbits and hares. Nearly all 

field isolates evaluated from rodents are of the Jellison type B variety. 

The following species, from among the many species of rodents 

known to be susceptible to tularemia, are worthy of note because of 

their prominence in epizootics and epidemics of this disease.

Ground squirrels

(Spermophilus spp.)

California ground squirrel

that farmers attempted to obtain sick squirrels during the 

“squirrel plagues” at the start of the 20th century and 

release them as a form of “biological warfare” against 

the ground squirrel hordes of that time.28 The human risks 

associated with such actions are high as it is likely that F. 

tularensis type A strains were involved36 rather than the 

lower virulence type B strains found in aquatic and semiaquatic rodents. Photo by Milton Friend

Box 6 Rodents and Tularemia

The first North American recognition of tularemia as a disease in wild animals involved California ground squirrels.17

At least nine North American species of ground squirrels 

have now been found to be infected with F. tularensis in 

nature.12 Recognition that McCoy’s “plague-like disease of 

rodents” was tularemia raised questions about how many 

other mortality events of ground squirrels, prairie dogs, 

and other small terrestrial rodents thought to be plague 

(Yersinia pestis) may also involve tularemia. 

Ground squirrels are important hosts for several species of 

ticks that are vectors of tularemia36 and contribute to the 

natural history of this disease. They also serve as a potential source for direct contact transmission to humans.28

However, ground squirrels have not been a prominent 

species in outbreaks of tularemia since the initial investigations of McCoy and Chapin,16,173 and there have been few 

human cases of tularemia directly attributed to ground 

squirrels.75 Nevertheless, ground squirrels are commonly 

infected by F. tularensis. At high population levels, these 

usually herbivorous animals are known to feed on the flesh 

of carcasses and even prey upon other warm-blooded animals. This behavior facilitates disease transmission within 

those species.174

Historically, population levels for some species of ground 

squirrels reached such high levels that they were considered major pests. The level of depredation was such 
Tree squirrels

(Sciurus spp.)

Gray squirrel

Red squirrel

Distribution of European 

beaver168

Beaver

(Castor spp.)

Distribution of beaver in North America149

North American beaver

Photo by Julia Gregory, Texas Parks & Wildlife Dept.

Photo by Phil Myers

Photo by Milton Friend

Tree squirrels are widely distributed in the Americas and 

are found in deciduous, coniferous, and tropical forests, 

both humid and arid. Although they spend most of their 

time in the trees, they come to the ground to forage for 

food and to bury nuts and acorns.146 The gray squirrel 

and fox squirrel, which are hunted, are the squirrel species most commonly involved in the direct transmission 

of tularemia to humans. Infected squirrels have caused 

human cases of tularemia as a result of contact transmission in the preparation of the animal for cooking10,175 and by 

arthropod vectors that transfer from squirrels to humans. 

Improper cooking of diseased animals is another pathway 

for human infection. Bites from squirrels handled in the 

outdoors and from squirrels kept within the home as pets 

have also resulted in human cases of tularemia.10,176 Natural 

infections of squirrels by F. tularensis have also been 

documented for the European red squirrel in Sweden and 

in North America for the red squirrel and Wind River pine 

squirrel.12

Beaver are the largest rodent native to North America and 

Europe. Both the European beaver and the North American 

beaver were among the most widely distributed mammalian species prior to their exploitation by humans. The 

North American beaver has been successfully introduced 

into Finland146 and the European beaver (Castor fiber) has 

been restored to many areas from which it had been extirpated.177 Beaver are highly susceptible to tularemia10,178–180

and have been the source for numerous human cases 

of this disease.180 The first documentation of tularemia 

epizootics in beaver is from 1939–40,181–183 but retrospective evaluations of large-scale mortality events like those 

described by Seton164 suggest that tularemia has caused 

mortalities in this species since at least the 1920s.

Heavy contamination by F. tularensis of surface waters 

has been a consistent finding associated with tularemia 

epizootics in beaver and is likely the source for infection of 

those animals.180,181 Because of their high susceptibility to 

tularemia, beaver are not an important reservoir host but 

instead serve primarily as a source for infection of humans 

who may handle these animals or their pelts during trapping and fur-trade operations. Beaver that die from tularemia also can contaminate the waters they inhabit.

A closer association between humans and beaver was 

present in North America in earlier times than exists today. 

This species probably contributed to the development of 

the USA and Canada more than any other animal because 

of the value of its pelts. Settlers moved westward following the quest by trappers for the financial rewards from the 

fur trade.146 Human exposure to tularemia from beaver in 

the USA today is more likely to be associated with removing beaver from an area because their impacts conflict with 

human use of the area and also from recreational uses of 

water inhabited by beaver.

Rodents and Tularemia 33
34 Tularemia

Muskrat

(Ondatra zibethicus)

Voles (“Meadow mice”)

(Microtus spp.)

The genus Microtus consists of 6 subgenera and more 

than 60 species distributed throughout much of the globe 

except for South America, southern areas of Eurasia 

continent, and further south in the Old World.146 “Boom 

and bust” populations are a common dynamic both in the 

New World and the Old World for many of these species, 

several of which are considered to be important in the 

ecology of tularemia.186 Tularemia has often been associated with major die-offs of voles during population highs. 

In North America, tularemia epizootics frequently result in 

the death of beaver, muskrat, and voles during the same 

event because of the intimate contacts that occur between 

these species (Figs. 9 and 11). Beaver and muskrat commonly share aquatic habitat and interface with voles at the 

bank areas of that habitat.36

Voles are thought to be involved in maintaining long-term 

contamination of waterbodies. For example, voles are 

suspected as being the source for continual contamination 

in Montana by F. tularensis of two small streams for 16 

months beyond the end of a tularemia epizootic involving 

mented human cases (47) in North America associated 

with a single outbreak of tularemia in muskrat occurred in 

Vermont. That event was also the first time tularemia was 

documented in that state.78

Distribution of muskrat

in North America149

Distribution of 

muskrat in Europe168

Muskrat

Meadow vole

Photo by Phil Myers Photo by R. Town, U.S. Fish 

and Wildlife Service

The muskrat is a New World species that has been introduced into the Old World. It was first introduced in the 

former Soviet Union in 1927 and cases of tularemia in this 

species within that geographic area were first documented 

in the Novisbirsk region in 1939. However, muskrat have 

not attained the abundance or geographic distribution of 

the water vole and are regarded to be of lesser importance 

in the ecology of tularemia than that species.180

Muskrat occur widely over a geographic area that extends 

from Alaska and Labrador in the North to parts of Texas 

and California in the South.146 Like the beaver, this species 

is trapped for its fur. It has been reported that muskrat 

pelts are 40 percent more durable than other pelts and at 

one time were the greatest source of revenue from trapping in North America.169 As recently as the trapping season of 1976–77, the value of the North American harvest 

of muskrat pelts was approximately $45 million.146 In some 

areas, the meat is also eaten. Muskrat meat is commonly 

referred to as “marsh-rabbit,” an appropriate term since 

muskrat, like rabbit, are an important source of human 

cases of tularemia.

Like beaver, muskrat-trapping activities are the primary 

source for human cases of tularemia. Muskrat are also 

highly susceptible to tularemia and suffer large-scale 

epizootics that may then contribute to the contamination 

by F. tularensis of the waters in which they die.181 The 

first North American human cases of tularemia associated with muskrat were described in 1929184 and for some 

time were thought to be anomalies.36 However, it was 

later recognized that tularemia acquired from muskrat and 

beaver is more common than apparent. This is because of 

the nonspecific febrile illness that generally results from 

uncomplicated infections.185 The largest number of documuskrat and beaver.180 Like beaver and muskrat, voles are 

highly susceptible to tularemia; unlike beaver and muskrat, 

voles may also become chronically infected and serve as a 

source for contamination of surface waters by F. tularensis

through their body discharges.187 Contamination of waters 

by voles could then initiate epizootics in species such as 

muskrat and beaver whose carcasses would then further 

contaminate those waters.180,181 Laboratory studies have 

resulted in some voles developing chronic infections of the 

kidneys and shedding F. tularensis in their urine.174,188,189 If 

this occurs in nature it would be an important mechanism 

for maintaining F. tularensis-infected waters over long 
Few animals Excessive population

Stress

Salt hunger

Adrenal exhaustion

Cannibalism Epizootic spread

Water vole

(Arvicola terrestris)

periods of time and for initiating tularemia outbreaks in 

wildlife11 that then serve as a bridge for human cases.11,19

Small rodents are probably the species most often infected 

with F. tularensis and are also the most common source 

for human infection in Europe.19 Species commonly 

involved include water voles, lemmings, red-backed voles, 

and Microtus spp.11 The water vole is the most important 

of these species because of its broad geographic distribution, abundance, and contact with humans.19,21,25 The 

shedding of F. tularensis into water by voles is thought 

to be the underlying cause for much of the tularemia 

reported in Eurasia.11 For example, the water supply is 

considered to be the most important source of F. tularensis in Turkey, with infected rodents being the source of 

contamination.55

A leading North American investigator has theorized that the evolution and spread of tularemia organisms has occurred with Rodentia, in contrast to the viewpoint of an equally 

prominent Russian investigator who theorizes that the evolution of Francisella was mainly 

within Lagomorpha and less within Rodentia.

102 In either case, the long association of 

Francisella with these two major groups of animals has afforded eons of time for adaptive 

host-parasite relations to be formed. Within this context, the population dynamics and 

associated behavioral characteristics of high population levels of voles and other small 

rodents results in a theory that cannibalism is a major factor for epizootic spread of 

type B infection in terrestrial rodents.174

Distribution of water 

vole in Europe168

Water vole

The water vole is one of three species in the genus 

Arvicola and is the largest microtine rodent in the Old 

World, having a body size about two-thirds the length of 

the muskrat. It is distributed throughout most of Europe 

and Siberia, and in parts of Southwestern Asia.146 It is the 

most common animal source of human cases of tularemia 

in Eurasia, partly because of direct contacts, including 

harvest of its pelt.19 Millions of these animals are trapped 

annually for their fur.142 The magnitude of human cases of 

tularemia attributed to this species in the former Soviet 

Union alone far exceeds that reported for any other species anywhere else in the World. During 1928, four and a 

half million water vole pelts from the Ural area were sold 

in the fur market. At that time the first epidemic wave of 

tularemia was occurring in the former Soviet Union and 

water voles were essentially the sole source of human 

infection.32 About 1,000 tularemia cases occurred in Russia 

in 1928 in persons skinning these animals for their pelts.44

Previously described disease syndromes known as waterrat-trapper’s illness and Siberian ulcer, now known to be 

tularemia, are historically associated with trapping these 

animals19 and support the presence of tularemia in the 

former Soviet Union long before the 1926 initial diagnosis 

of tularemia in Russia.

In addition to being highly susceptible to tularemia, water 

voles may become chronically infected, thereby serving as 

disease reservoirs during periods between epizootics.24,180

High population levels “trigger” widespread epizootics of 

tularemia among rodents,25 perhaps by stimulating shedding of F. tularensis organisms, thereby resulting in waterborne transmission as a means for initiating the epizootic. 

In addition, stress-related aggression and cannibalism 

could also serve as a means for initial disease transmission.174 Regardless of the mechanisms involved, the water 

vole is an important species in the Old World ecology of 

tularemia.

Rodents and Tularemia 35
36 Tularemia

Rodents

Rodents are of greater importance than rabbits and hares 

for maintaining enzootic foci for tularemia in many areas 

of the Old World. They are also of major importance generally because they are highly susceptible to infection and are 

hosts for immature stages of several important tick vectors of 

the genera Dermocentor, Ixodes and Amblyomma.

11,190,239 The 

primary North American rodent hosts for F. tularensis type B 

are species of the genera Microtus (meadow mice and voles), 

along with muskrat and beaver. Rodents within the family 

Sciuridae (primarily tree and ground squirrels) can also be 

locally important hosts for tularemia (e.g., California ground 

squirrel) (Box 6). In contrast with earlier times, tularemia 

has become a more prominent disease of prairie dogs since 

the 1990s.136–139 Direct contact with infected rodents, their 

ectoparasites, and ingestion and inhalation of water and other 

materials contaminated by them are the typical ways in which 

tularemia is transmitted to humans (Fig. 11). 

In Eurasia, voles, especially those of the genus Microtus, 

also contribute to human infections of tularemia by their contamination of terrestrial and aquatic environments. Examples 

include occasional large epidemics of tularemia among 

agriculturists as a result of processing grain or stacked hay 

contaminated by voles and other rodents,32,128,191 contamination 

of public-water supplies,25 and infection of workers in a sugar 

beet processing plant from water spray contaminated with

F. tularensis.

26,174

Carnivores

Clinical cases of tularemia in wild carnivores are rare. 

Canids are not believed to have a major role in the maintenance of tularemia in nature, and they are not important as a 

source for human infections,11,19 although human cases have 

been attributed to handling red foxes.

44,106 The first documented outbreak of tularemia in wild canids involved gray 

foxes in Minnesota.192 Other documentation of tularemia in 

carnivores is limited to incidental cases. 

High percentages of carnivore and scavenger species 

with antibody titers from serological surveys indicate past 

exposure to F. tularensis,

193,194 thereby illustrating the susceptibility of carnivores to natural infections and their ability 

to survive those infections. Coyotes infected experimentally 

have developed clinical disease in some studies but not others. In some instances carnivores may indirectly contribute to 

tularemia cycles by being a host for adult ticks that are part of 

the disease transmission cycle. However, because carnivores 

generally do not develop a bacteremia following exposure to 

F. tularensis24 they are unable to infect the ticks but may serve 

to help maintain tick vector populations.

Figure 11. Rodents and tularemia in North America: general pathways for infection.

Illustration by John M. Evans
Table 11. Upland game birds reported to be naturally infected with Francisella tularensis.

Species Geographic

area

Bird

mortality

Human

cases

Comments

Dove

(species not specified)

Former 

Soviet Union

Insufficient 

information

No cases 

reported

F. tularensis isolated from tissues.25,107

Ring-necked pheasant USA No cases 

reported

One or more 

cases of bird 

origin reported

Human cases of tularemia reported in association with preparing harvested birds for consumption.107.108,175,195

Cooper (coppera)

pheasant

Japan No cases 

reported

One or more 

cases of bird 

origin reported

Human cases associated with preparing pheasants for 

consumption.57

Pheasant

(species not specified)

Japan No cases 

reported

One or more 

cases of bird 

origin reported

Human cases associated with preparing pheasants for 

consumption.57

Bobwhite quail USA Death attributed 

to tularemia

One or more 

cases of bird 

origin reported

Bacterium isolated from dead birds;111 human cases 

associated with hunter-killed birds also 

reported.15,109,196

Japanese quail Former 

Soviet Union

Insufficient 

information

No cases 

reported

F. tularensis isolated from tissues of bird from 

Western Siberia.25

Blue grouse

(Columbian grouse)

USA No cases 

reported

One or more 

cases of bird 

origin reported

109

Ruffed grouse USA Death attributed 

to tularemia

One or more 

cases of bird 

origin reported

Tularemia was initially thought to be widespread and 

involved in population declines of this species,110,197

but is no longer considered a cause of population 

declines; human cases have been associated with 

hunter-killed birds.175

Sage hen

(Sage grouse)

USA Death attributed 

to tularemia

One or more 

cases of bird 

origin reported

A grouse-rabbit-tick cycle suggested by early investigators.109

Sharp-tailed grouse USA Death attributed 

to tularemia

No cases 

reported

110

Willow grouse USA No cases 

reported

No cases 

reported

Moderate virulence strain of F. tularensis isolated 

from ticks removed from grouse, suggesting grouse 

were source of infection for ticks.102

Capercaillie Former 

Soviet Union

No cases 

reported

No cases 

reported

Bacterium isolated from tissues of bird from 

Byelorussia.25

a

Spelling inconsistencies in the literature.

Birds

Numerous species of birds of several families have been 

naturally infected with F. tularensis (Tables 11–17). Also, 

there are close associations between the species of birds most 

commonly infected and the environment where tularemia 

occurs. Upland game birds (Tables 11 and 12) share habitats 

with hares and rabbits and in some instances share tick-vectors of tularemia. Various waterbirds (Table 13) frequent 

areas possibly contaminated with F. tularensis by rodents, 

and birds may become exposed through ingestion of contaminated water, sediment, and invertebrates; by aerosols created 

as they land, take-off, and splash around in those waters; or 

by infected insects feeding on the birds. Preying upon sick 

and dead rodents and lagomorphs afflicted by tularemia is the 

likely primary route for exposure of predatory and scavenger 

species of birds (Tables 14–16). Environmental associations 

also extend to poultry (Table 17) that have died from tularemia after being fed wild rabbit meat and viscera.36 Nevertheless, few epizootics of tularemia in wild birds have been 

documented and, in general, birds are not considered to be an 

important component of the ecology of tularemia.11,19 Perhaps 

the most significant roles of birds in the ecology of tularemia 

are their potential to transport infected arthropod vectors to 

Disease Ecology 37
38 Tularemia

new areas,19 the use of serology from predatory and scavenger 

species to monitor tularemia activity in their prey species,194

and the potential for infected birds to contaminate surface 

waters through body discharges (Box 2).

Invertebrates

Ticks are the most important arthropods in the ecology of 

tularemia (Table 18). Persistently infected with F. tularensis, 

some Ixodidae ticks pass the infection through their eggs to 

the next generation. In addition to being a major reservoir 

host, they have a persistent role in the transmission of F. tularensis to humans (Fig. 12). Following infection, ticks amplify 

the number of bacteria for retransmission of F. tularensis

(biological vectors). Therefore, ticks are true reservoir hosts 

that may perpetuate specific endemic/enzootic foci for tularemia during interepidemic/enzootic periods.11,24,102,240 Hard 

ticks (Ixodidae) are major vectors of F. tularensis to humans 

and they maintain tularemia in the Northern Hemisphere (Fig. 

13).

A variety of factors influence the role of particular species 

of ticks in the ecology of tularemia. Feeding patterns and host 

range are of primary importance.11 For example, within the 

USA, Dermacentor andersoni is a direct source for human 

infection, but D. parumapertus is not because they rarely 

attach to humans.24 D. parumapertus is a vector among wild 

mammals; larval and nymphoidal stages feed on rodents, 

and the adult feeds on jackrabbits. Its role in the ecology of 

tularemia is maintaining infections in mammals as sources 

for infection of other arthropods, such as deerflies. Infected 

mammals also serve as potential sources for environmental 

contamination and for contact disease transmission with, or 

by ingestion of those mammals. In contrast, subadult stages 

of D. andersoni feed on small rodents and lagomorphs and 

the adult ticks feed on large wild mammals, livestock and 

humans. The broad host range of D. andersoni results in this 

tick being a source for infection of humans as well as maintaining endemic foci of tularemia in nature.24

Transmission of F. tularensis by ticks is not limited to tick 

bites. Coxal fluid and feces of infected ticks contain viable 

F. tularensis, and may contaminate the bite wound and other 

broken surfaces of the skin. Although most of the consideration of tick-borne tularemia in North America is focused 

on type A strains involving a tick-lagomorph cycle, ticks 

also vector type B strains of F. tularensis in Eurasia, North 

America,11 and Japan.170 Much of that vectoring involves 

infection of rodents by immature stages of ticks. No arthropod-borne human cases of tularemia were reported in Japan 

prior to 1951; however, there has been a steady increase 

in the percentage of cases transmitted by this means since 

1960, peaking at about 10 percent of tularemia cases during 

the period of 1980–1989. Most of these cases have been tick 

transmitted.170

Other blood-sucking arthropods also contribute to the 

transmission of tularemia (Table 18). Rather than being 

infected by F. tularensis, as are ticks, these other arthropods 

transmit tularemia mechanically. In essence, the insect’s 

mouthparts and surface areas become contaminated while 

they feed on infected animals or in contaminated environments, then they feed on a susceptible host and infect them. 

The importance of different types of arthropods varies with 

Table 12. Response of upland game birds to laboratory exposure to Francisella tularensis.

Species Response Comments

Mortality Antibody Agent isolation

Mourning 

dove

Occurrence Occurrence Occurrence Aerosol exposure at high dosage resulted in 

infection but low susceptibility to disease.198

Ring-necked 

pheasant

Occurrence Occurrence Occurrence Species not very susceptible and reported to be 

immune to infection under field conditions.199

Bobwhite 

quail

Occurrence Not determined Occurrence Fatal infections in quail fed infective material.111,196

Hungarian 

partridge

Occurrence Information not 

given

Information not 

given

Highly susceptible; fatal infection resulted from 

inoculation of a skin abrasion.199

Blue grouse Occurrence Not determined Occurrence Highly susceptible.148,196

Ruffed 

grouse

Occurrence Not determined Occurrence Mortality paralleled that for highly susceptible 

guinea pigs and rabbits;199 tularemia also 

transmitted to grouse by infected ticks in the

laboratory.197
Table 13. Reported susceptibility of waterbirds to Francisella tularensis.

Species Geographic

area

Type of

exposure

Bird

mortality

Human

Cases Comments

WATERFOWL

Canada goose USA Natural No cases 

reported

One or more 

cases of bird 

origin reported

200

Green-winged teal USA Experimental,

natural

Death 

attributed to 

tularemia

Not applicable Single bird infected died and 

F. tularensis recovered from its tissues.10

Mallard duck USA Experimental,

natural

Death 

attributed to 

tularemia

Not applicable Birds infected orally and by injection; 

pure cultures of F. tularensis recovered 

from tissues of birds that died;10

seropositive birds found in nature.194

GALLINULES AND RAILS

Gray moorhen Former Soviet 

Union

Natural Insufficient 

information

No cases 

reported

Bacterium isolated from tissues of birds 

in Byelorussia.25

Corncrake Former Soviet 

Union

Natural Insufficient 

information

No cases 

reported

Bacterium isolated from tissues of birds 

from Western Siberia.25

GULLS AND TERNS

Black-headed gull Former Soviet 

Union

Natural Insufficient 

information

No cases 

reported

Bacterium isolated from tissues of bird 

from Moscow region.25

California gull USA Natural No cases 

reported

No cases 

reported

Multiple seropositive birds.194

Franklin gull Canada, USA Natural Insufficient 

information

No cases 

reported

Tissues from a carcass collected during 

routine surveillance were positive for 

F. tularensis in Canada;201 isolations 

were also made in the USA from gull 

tissues.200

Common tern Former Soviet 

Union

Natural Insufficient 

information

No cases 

reported

Bacterium isolated from tissues of birds 

from Western Siberia.25

Sooty tern USA Experimental Death 

attributed to 

tularemia

Not applicable Bird died 5 days following respiratory 

exposure and had high levels of 

F. tularensis in cloacal contents.115

White tern USA Experimental Death 

attributed to 

tularemia

Not applicable Results inconclusive due to intolerance 

of birds to captivity; dose as few as 250 

organisms may have been lethal.115

Common noddy USA Experimental Death 

attributed to 

tularemia

Not applicable Lethal infections induced by respiratory 

route.115

White-cap noddy USA Experimental Death 

attributed to 

tularemia

Not applicable Highly susceptible; large numbers of 

organisms found in cloaca; high level of 

bacteremia.

Disease Ecology 39
40 Tularemia

Table 14. Birds of prey reported to be naturally infected with Francisella tularensis.

Species Geographic

area

Bird

mortality

Human

cases

Comments

HAWKS

Red-tailed hawk USA No cases reported No cases reported Isolation of bacterium from tissues of a bird 

collected by shooting.202

“Chicken hawk” USA No cases reported One or more cases 

of bird origin 

reported

Species not identified.108

Kite Russia Insufficient 

information

No cases reported Isolation of bacterium from tissues of a bird found 

in nature.25

Prairie falcon USA No cases reported No cases reported Based on serology.194

OWLS

Great horned owl USA Death attributed 

to tularemia

One or more cases 

of bird origin 

reported

Reported as a source of a human case of 

tularemia;108 bacterium isolated from tissues of a 

dead nestling.203

Great Basin

screech owl

USA No cases reported No cases reported Based on serology.194

Ural owl Sweden Death attributed 

to tularemia

No cases reported Bird observed sick in nature prior to death; 

F. tularensis isolated from tissues at necropsy.204

BUZZARDS

Rough legged 

buzzard

Sweden Death attributed 

to tularemia

No cases reported Bird found dead in nature; F. tularensis identified in tissues at necropsy by fluorescent antibody 

technique.204

Table 15. Response of birds of prey to laboratory exposure to Francisella tularensis.

[IM, intramuscular; IP, intraperitoneal; SC, subcutaneous]

Species Geographic

area

Response

Comments

Mortality Antibody Agent 

isolation

HAWKS

Red-shouldered

hawk

USA Occurrence Inconclusive 

finding

Occurrence Six-week-old birds fed viscera of guinea 

pigs dying of tularemia.205

Eastern redtailed hawkUSA Occurrence Occurrence Occurrence Adult bird fed viscera of guinea pigs dying 

of tularemia.205

Goshawk Sweden No occurrence Occurrence Occurrence Fed mice that died of tularemia or were 

incoculated via IM, SP, or SC routes; 

antibody persisted for the 77 days of the 

experiment and reached 1:1,280 in one 

bird.206

Sparrow hawk Sweden No occurrence Not

 determined

No

occurrence

No evidence of infection following IM 

inoculation.206

OWLS

Tawny owl Sweden No occurrence Not 

determined

Not

determined

Two birds exposed via IM route survived 

and failed to exhibit clinical signs of 

diseases.206

Great-horned 

owl

USA No occurrence No 

occurrence

No

occurrence

Unable to infect adult birds and mature 

birds not considered to be susceptible.203

BUZZARDS

Rough-legged

buzzard

Sweden No occurrence Not

 determined

No

occurrence

206

Common

buzzard

USA No occurrence Occurrence No

occurrence

206,207
Table 16. Reported susceptibility of Corvidae, Laniidae, and Alaudidae to infection by Francisella tularensis.

Species Geographic

area

Type of 

exposure

Bird

mortality

Human

cases

Comments

Raven Sweden,

USA

Natural No cases 

reported

No cases

reported

Several apparently healthy birds were shot; 

some exhibited tissue lesions suggestive of 

tularemia and were fluorescent antibody

positive.208 Seropositive birds also found in 

western USA.194

Crow Insufficient

information

Natural Insufficient

information

Insufficient

information

209

Crow Austria, 

former Soviet 

Union, Japan

Natural Insufficient

information

Insufficient

information

Species not identified.27,57,210

Hooded

crow

Sweden Experimental No cases 

reported

Not

applicable

Birds were exposed by being fed mice that 

died of tularemia or by intramuscular injection; 

short term antibody response but not clinical 

disease.206

Azure-winged

magpie

Former Soviet 

Union

Natural Insufficient

information

Insufficient

information

209

Common 

magpie

Former Soviet 

Union

Natural Insufficient

information

Insufficient

information

209

Loggerhead

shrike

USA Natural No cases 

reported

No cases

reported

Antibody detected in sera.194,211

Horned

lark

USA Natural No cases 

reported

No cases

reported

Antibody detected in sera.194

Table 17. Reported susceptibility of domestic bird species to infection by Francisella tularensis.

Species Geographic

area

Type of 

exposure

Bird

mortality

Human

cases

Comments

Pigeon Japan,

USA

Experimental No cases 

reported

Not

applicable

Highly resistant17 but may carry the bacterium 

for a period of time after exposure.57,209

Intramuscular inoculation resulted in 

septicemia in some birds.212

Europe Natural No cases 

reported

No cases 

reported

Highly resistant but may spread infection via 

excretions.101

Chicken USA Experimental Death 

attributed to 

tularemia

Not

applicable

Highly resistant but may harbor F. tularensis 

for as long as 27 days.209 Baby chicks are 

susceptible and F. tularensis grows readily 

in chick embryo tissue culture;101 high titer 

antiserum produced by roosters inoculated 

intravenously with F. tularensis.

213

Intramuscular inoculation resulted in death of 

one bird.212

USA,

Japan

Natural Death 

attributed to 

tularemia

One or more 

cases of 

bird origin 

reported

Mortality of “backyard chickens” from 

tularemia after being fed wild rabbit meat and 

viscera;36 human case in Japan associated with 

preparing chicken for food.57

Domestic

turkey

USA Experimental No cases 

reported

Not

applicable

Highly resistant to laboratory infection;209

seropositive birds found during testing of 

flocks.194

Disease Ecology 41
42 Tularemia

Table 18. Arthropod species of primary importance in transmission of Francisella tularensis.

Speciesa Area of importance Comments

TICKS

Amblyomma americanum

(Lone Star tick)

North America One of three primary vectors of human cases within the USA;31 accounts for 

about 60 percent of cases during recent decades.11 A host and a vector.27

Dermacentor albipictus

(Winter, elk, or moose tick)

North America Reported as a vector.102

D. andersoni

(Rocky Mountain wood tick)

North America One of three primary vectors of human cases within the USA; 31 “Second only 

to direct contact with rabbits as a source of human infection.”10

D. occidentalis

(Pacific Coast tick)

North America Reported as a vector;14 F. tularensis isolated from ticks removed from cattle.215

D. parumapertus

(Rabbit dermacentor)

North America Important vector in transmitting F. tularensis from jackrabbit to jackrabbit but 

seldom feeds on humans.103

D. pictus

(Meadow tick)

Eurasia Vector for human cases.24 One of three principal tick vectors in the former 

Soviet Union.26 Vectors tularemia in France.27

D. marginatus Eurasia One of three principal tick vectors in the former Soviet Union.26 Vectors 

tularemia in France.11

D. reticulatus Europe Important for initiation and acceleration of epizootics involving natural foci in 

Slovakia.216

D. variabilis

(American dog tick)

North America One of three primary vectors of human cases within the USA.31 A host and a 

vector.27

Haemaphysalis chordeilis

(Bird tick)

North America Reported as a vector.102

H. concinna Europe Supports maintenance of F. tularensis in nature in Slovakia.216

H. flava Japan One of three important tick vectors in Japan.71

H. leporis-palustris

(Rabbit tick)

North America Important for maintenance of tularemia in nature as infections of lagomorphs 

and birds.19 Rarely vectors tularemia to humans.14

Ixodes angustus North America Infected ticks removed from tundra vole in Alaska.102

I. apronophorus Eurasia Principal vector in some areas of the former Soviet Union;27 primarily a vector 

among rodents.41

Ixodes dentatus North America Same as H. leporis-palustris.

14

I. trianguliceps Eurasia Involved in forest foci of tularemia in the former Soviet Union.66

I. japonensis Japan One of three important tick vectors in Japan.71

I. nipponensis Japan Same as I. japonensis.

102

the geographic area but most, except for ticks, appear to have 

little biological significance in either maintaining tularemia 

in nature or in directly transmitting F. tularensis to humans. 

Tabanids in North America and in the former Soviet Union 

and mosquitoes in Scandinavia and the former Soviet Union 

are exceptions.

Deerflies have been responsible for the transmission of 

numerous cases of tularemia in Utah.19,103 Chrysops discalis

is a primary vector of deerfly fever (tularemia), but other 

species, including C. fulvaster and C. aestavans, have also 

been found infected and were the first spontaneously infected 

tabanids to be reported in North America.11 Several species of 

tabanids have also been found infected in the former Soviet 

Union.142,214

In general, the source of infection for biting flies is 

thought to be sick mammals, especially hares. Tabanids 

have also been observed to feed on carcasses of animals 

dead as long as 48 hours, and under experimental conditions 

have transmitted F. tularensis from such feedings to normal 

animals.19 However, infection can also occur by other means. 

Hares, water voles, and contaminated water are the primary 

routes for infection of tabanids in the former Soviet Union. 

The tabanids remain infective for 2–3 days.142,214
Table 18. Arthropod species of primary importance in transmission of Francisella. tularensis—Continued.

Speciesa Area of importance Comments

TICKS­—CONTINUED

I. pacificus

(Western black-legged tick)

North America Reported as a vector.102

I. persuleatus

(Taiga tick)

Europe Reported as a vector.27

I. Scapularis

(Deer or black-legged tick)

North America Reported as a vector.102

I. ricinus

(European castor bean tick)

Eurasia Vector for human cases.24 Supports maintenance of F. tularensis in nature in 

Slovakia.216 Frequently found infected throughout much of its Palearctic 

distribution.102

Rhipicephalus rossica Eurasia Vector for human cases.24 One of three principal tick vectors in the former 

Soviet Union.142

R. pumilio Eurasia Involved in “Tungai” foci of tularemia.66

BITING FLIES

Chrysops discalis

(Deerfly)

North America First presumed important vector of F. tularensis in the USA;102 the most 

significant vector of the 97 North American species of deerflies.174

C. fulvaster North America First naturally infected biting flies reported in North America.102

C. aestuans North America Same as C. fulvaster.

C. relictus Eurasia One of the two most important vectors in the former Soviet Union.102

First infections found in Rostov region.25

Chrysozona pluvialus Eurasia Same as C. relictus; large-scale 1957 outbreak of tularemia involved 

transmission of infections by this species to humans and rodents.209

Tabanus autumnalis

(Horsefly)

Eurasia First infections found in Astrakhan region of the former Soviet Union.25

T. flavoguttatus Eurasia Same as T. autumnalis.

T. bromius Eurasia First infections found in Perm region of the former Soviet Union.25

MOSQUITOES

Aedes cinereus Sweden, former 

Soviet Union

Particularly adapted to feeding on small mammals, especially water voles.102,217

A. excrucians Sweden, former 

Soviet Union

Same as A. cinereus but also feeds on other animals.102

a

 The species identified in this table are those most frequently mentioned in the literature in a manner that suggests they have an important role in the ecology 

of tularemia. Many additional species are cited in various review papers as being vectors of F. tularensis.

11,12,15,16,30,33,35,36

Disease Ecology 43

Mosquitoes of the genera Aedes, Mansonia, Theobaldia, 

and Anopheles have been shown to be capable of mechanical 

transmission of F. tularensis. Therefore, in theory, mosquitoes that feed on infected hosts should be able to retransmit 

the bacteria during their next blood meal.19 Nevertheless, 

despite the abundance of mosquitoes in tularemia enzootic 

areas of North America, they have not been important in the 

transmission of F. tularensis11 Only one sample of mosquitoes 

from North America has tested positive for F. tularensis. In 

contrast, mosquitoes are important vectors of tularemia in the 

former Soviet Union and in Sweden.11,217,221

Sucking lice, in addition to ticks, biting flies, and mosquitoes, can also transmit F. tularensis. However, their high 

degree of host specificity precludes a major role as interspecies vectors of tularemia.11 Other types of arthropods have 

also been identified as being capable of mechanically transmitting F. tularensis (Table 9).
Female deposits eggs on 

ground and dies

Six-legged larvae hatch and 

generally attach to small 

rodents; larva takes blood 

meal, usually drops from 

host, and digests blood meal, 

then molting into 

eight-legged nymph Adult attaches to a third host, 

usually a larger animal species 

(or human) and takes a blood 

meal

Ticks drop from host, 

female digests blood meal, 

and develops her eggs

Male generally mates with 

female on the host

ENZOOTIC HOSTS

DEAD-END HOSTS

Large mammals Small wild animals

Small wild animals

and ground birds

Nymph attaches to 

second host, generally 

another small animal, 

takes blood meal, 

generally drops off host, 

digests blood meal, and 

molts to adult stage

DISEASE

TRANSMISSION

TICK

LIFE CYCLE

Pathways for infection:

With transovarian 

 transmission

Without transovarian 

 transmission

 Non-tick transmission

44 Tularemia

Figure 12. Generalized life cycle for three-host Ixodid ticks that commonly vector tularemia, and pathways for the transfer of 

Francisella tularensis between ticks, animals, and humans. Dermacentor albipictus is a notable exception by completing its entire 

life cycle on a single host. [Tick photographs by Jim Lalisch and Wayne Kramer, University of Nebraska-Lincoln, Department of 

Entomology.]
A

B

American dog tick

Dermacentor variabilis218,220

Winter tick

Dermacentor albipictus220

Lone Star tick

Amblyomma americanum219,220

Rocky Mountain wood tick

Dermacentor andersoni218,220

Pacific Coast tick

Dermacentor occidentalis220

Rabbit dermacentor

Dermacentor parumapertus220

Rabbit tick

Haemaphysalis leporis-palustris220

Ioxides dentatus220,247

Figure 13. General geographic ranges for the primary tick vectors of tularemia in North America; A, species commonly feeding on 

humans, B, species that rarely feed on humans but do feed on birds and small mammals.

Disease Ecology 45
46 Tularemia

Domestic Animals

Sheep are associated with tularemia to a greater degree 

than any other species of domestic animal (Table 8). Individual epizootics of tularemia have killed more than 1,000 

sheep,90 and associated economic losses due to residual 

effects have also resulted from animals that survive infection.11,19 However, in laboratory tests sheep are reasonably 

resistant to tularemia. It is thought that weather, body condition and perhaps heavy infestations of ticks, that in some 

instances result in tick paralysis, are confounding factors 

associated with tularemia on rangeland. Outbreaks generally 

occur in the spring, especially during the lambing season 

when sheep are in a somewhat weakened condition due to 

physiological stress. The tick, Dermacentor andersoni, is 

the primary source for infection of sheep in North America. 

Contaminated water has not been associated with tularemia 

outbreaks in sheep.102 In some instances, tularemia epizootics 

in sheep have been preceded by epizootics in jackrabbits or 

other species.158

Human cases of tularemia have been associated with the 

sheep industries of North America162 and the former Soviet 

Union.91 Cases in the latter situation have been associated 

with workers in the meat packing industry rather than with 

rangeland conditions. Serologic evidence from North America 

indicates that contact with infected sheep has resulted in cases 

of tularemia occurring in sheep shearers.174 Other livestock 

species have far less involvement with tularemia (Table 8) and 

are not considered to have an important role in the ecology or 

transmission of this disease. 

Companion Animals

The role of companion animals (primarily cats and dogs) 

is unclear but appears to be increasing in importance (Box 7) 

and is predicted to be of greater importance in the future.11

Companion animals such as dogs and cats are exposed to a 

variety of habitats where they become infected as they travel 

with people or as they roam outside. In Massachusetts, a 

10-year-old girl became infected by saliva from her dog that 

presumably acquired F. tularensis from feeding on cottontail 

rabbits.36

Raising wildlife in captivity is another way that humans 

may contract tularemia. In one incident, a 16-month-old child 

contracted tularemia after being bitten by a pet gray squirrel 

allowed to be outside the home during much of the day.176 In 

another situation, after bringing a wild baby rabbit home, an 

18-year-old contracted oculoglandular tularemia.127 Additional 

human cases of tularemia have been acquired from other species and circumstances involving wild species brought into 

the home.

Environmental Persistence

An important early discovery in the ecology of tularemia 

was that surface waters and mud in stream bottoms and ponds 

can become contaminated with F. tularensis and that the 

organism can survive at infective levels in those substrates 

for more than a month.181 Survival of F. tularensis in nature 

is dependent upon a variety of factors such as temperature, 

direct exposure to sunlight, and other physical factors that 

generally affect the survival of microbes (Table 19). The 

source for contamination of surface waters is primarily urine 

and feces from infected animals (primarily voles) and the 

carcasses of animals dying from tularemia. Experimental 

studies have shown that one infected water vole, lemming, 

or mouse can contaminate up to 500,000 liters of water with 

F. tularensis.

142 Once contaminated, water may become an 

important vehicle for contamination or infection of biting 

insects, vertebrate animals, and humans. About 50 percent of 

mice became infected when the concentration of F. tularensis

in water reached 100 to 1,000 organisms per liter and about 

90 percent when the concentration reached 10,000 organisms 

per liter.142 These high infection rates from low concentrations 

of organisms are due to the high susceptibility of some species of rodents (lethal dose for a mouse can be as low as one 

organism222) and results in water being an important medium 

for disease transmission. Direct contact, ingestion, and 

aerosols containing F. tularensis are all routes for exposure, 

depending on the species involved. 

Well water and tap water from urban water systems have 

also been contaminated by F. tularensis.

24 During 1998, a 

waterborne outbreak of tularemia occurred among individuals 

fishing for crayfish in Spain.49 Infective dusts from contaminated hay, litter, and other substrates associated with agriculture are occasional sources for infection of humans, and 

perhaps other species, but are less important than infective 

surface waters.
Companion animals have been an important component of human culture throughout recorded history. 

Dogs and cats are, by far, the primary species kept as companion animals and tularemia is a disease that 

can take advantage of the close and frequent contacts that occur between humans and these species. 

Cats and dogs may become indirectly involved in the transmission of tularemia by harboring ticks infected 

with Francisella tularensis that detach themselves within the household and then reattach themselves to 

humans. In addition, humans can become infected by crushing ticks between their fingers when removing them from companion animals. A highly unusual form of indirect transmission occurred as an aerosol 

exposure when dogs shook off rainwater within a cabin after killing tularemia infected rabbits.225 Direct 

transmission by bite and scratch wounds inflicted by cats has occurred on numerous occasions.84,226 In 

addition, there has been at least one case of tularemia resulting from a dog licking the face of a child.225

The results of natural and experimental infections of dogs and cats by F. tularensis can range from an 

absence of clinical disease to death. As for other species, the severity of disease is mediated by a number 

of factors including age of the animal and route of exposure. In general, very young animals are more 

susceptible than young adults. Dogs are moderately resistant to tularemia but serious disease leading to 

mortality can result following subcutaneous or intramuscular inoculation of F. tularensis. Cats are more 

susceptible to tularemia than dogs (see Table 8).225

The transmission of F. tularensis from cats and dogs to humans has involved healthy animals as well as 

animals with clinical cases of tularemia. However, it is unlikely that dogs and cats with clinical cases of 

tularemia are a source for direct infection of humans. Instead, mechanical transfer of bacteria occurs from 

the contaminated mouths and claws of pets that have recently fed on diseased small rodents and rabbits. 

The relatively prolonged survival of F. tularensis within the environment (see section on Environmental 

Persistence) and low infective dose for humans of as few as 10 organisms5,227 facilitates mechanical transmission. Veterinarians and others who might contact infected tissues and body fluids during postmortem 

examinations of animals that die of tularemia or, less likely, during procedures involving the evaluation and 

treatment of clinical cases are at greater risk than the general population.228

Nearly all of the documented cases of tularemia in domestic cats and those involving transmission of 

this disease from cats to humans have two common denominators. First, these cats are allowed to roam 

outside of the home in rural or near rural areas. Second, these cats hunt, kill, and consume infected small 

rodents and rabbits.84,229 City dwellers are not immune to this means for exposure to tularemia, because 

domestic cats often accompany their owners to such areas during excursions to the “family cabin” and on 

vacations.

“Cats...make it possible for the stay-at-home to acquire tularemia.“ 

(Evans et al.224)

Cats, Dogs, and Tularemia Box 7

Cats, Dogs, and Tularemia 47

Photos by Milton Friend
48 Tularemia

Points to Ponder

Tularemia has implications for wildlife managers and those 

who are involved with wildlife in other ways. Mink and fox 

ranchers have used jackrabbit carcasses as feed that caused 

tularemia outbreaks among their animals.158,159 Tularemia 

has also erupted in beaver farms from contaminated water,178

illustrating the need for considering the relative “purity” and 

sources of food and water when rearing susceptible wildlife 

in captivity. Propagation of wildlife for sporting purposes, 

reintroduction, and enhancement of existing populations is 

currently more popular than fur farming. Regardless of the 

purpose for raising animals, the same principals for disease 

prevention exist. Tularemia can negate wildlife propagation 

efforts by killing animals after they are released (Fig. 14). 

Further, translocating hares, rabbits, and prairie dogs has 

introduced tularemia into new areas (Box 4).24,31,72,223 The 

wildlife pet trade is another form of translocations contributing to tularemia outbreaks.136,137

Wildlife population impacts by tularemia are of a temporary nature. Widespread, major epizootics have reduced wild 

beaver and muskrat populations, temporarily reducing fur 

harvests.13 Epizootics assumed to be caused by tularemia on 

the Upper Red River and Hudson Bay were reported to have 

persistent negative impacts on beaver populations and on 

those who depend on them for cultural and economic purposes for years.164 Other impacts have been associated with 

the cottontail rabbit, the most frequently hunted game animal 

in the United States.174 Fear of tularemia has reduced hunting 

cottontails in some areas, resulting in lost revenues for local 

Table 19. Examples of environmental persistence of Francisella tularensis.

Environmental substrate Survival time Comments

Water 14 weeks

90 days

4 months

3 months

3 weeks

Field samples stored at 7oC180

?27

At 4–6oC25

Tap water19

At 20–21oC in presence of carcass of a water vole dead 

from tularemia.142

Soil 14 weeks

30 days

62 days

Mud samples stored at 7oC25

Humid soil27,181

Mud232

Fodder 4 months

6 months

133 days

Grain, straw at 4–6oC25

Dry straw litter19

Wheat grain27

Live ticks 764 days

701 days

700 days

Virulence maintained within body of Ornithodoros 

turicata27

Ornithodoros parkeri19

Dermacentor marginatus25

Animal carcass 3 to less than 4 weeks

At least 20 days

4 + 31 days

General survival in carcass tissues180

Hides of water rats that died of tularemia (15–20oC)181

Urine in bladder of beaver dead of tularemia and 

storage of that urine at 15–28oC181

Laboratory culture 22 years At 10oC27 (Culture media not reported.)

DESTRUCTIVE FACTORS

Heat 10 minutes At 56–58oC27

Direct sunlight 3 hours At 29oC19,27
communities.144 For example, half of 160 farmers interviewed 

in a Wisconsin survey curtailed cottontail rabbit hunting 

because of “rabbit fever.”106 Conversely, the role of tularemia 

as a population regulation factor for small rodents is often 

considered a benefit.12,230 However, epidemic-like spread of 

tularemia among humans has been associated with a periodic 

cycling of mouse populations and tularemia in the former 

Soviet Union27 and in Central Europe.45,56

Disease Prevention and Control

The heavy use of the outdoors is part of the American 

lifestyle and is a factor relative to the potential for humans to 

contract tularemia. During 1996, 77 million people, or about 

40 percent of the population 16 years of age or older, enjoyed 

some recreational activity in the USA relating to fish and 

wildlife.231 Also, for people who have a subsistence-based 

lifestyle, contacts with wildlife and the environment provide 

more opportunities for exposure to F. tularensis than for those 

who are outdoors for recreational purposes.

However, tularemia has become the “forgotten disease” in 

many areas of North America despite its prominence during 

the first half of the 20th century. This perspective is reflected 

in current statements that refer to tularemia as a rare infectious disease.26 Nevertheless, tularemia remains persistent in 

nature and can cause serious illness in humans. 

The multiple routes for exposure (Fig. 15), and the high 

degree of invasiveness and infectiousness of F. tularensis

complicate prevention of human cases of tularemia in enzootic areas. Nevertheless, people can minimize their potential 

exposure to F. tularensis. The general population is best 

protected from tularemia by avoiding contact with arthropod 

vectors, animal hosts, and contaminated environments. To a 

great extent, actions should be guided by public education, 

the availability of timely information of tularemia activity, 

and the selective use of immunizations for high-risk segments 

of society if a suitable vaccine is developed (Box 8). 

Monitoring and surveillance of wildlife for tularemia activity in enzootic areas provides assessments useful for public 

health advisories and guidance for managers of public use 

areas such as National Parks and other outdoor recreation 

areas. The recent resurgence of tularemia in an enzootic 

geographic area extending over parts of Austria, the Czech 

Republic, and West Slovakia was clearly evident in hares 

prior to becoming an epidemic involving more than 200 

human cases in West Slovakia alone.233,234

Monitoring activities need to be appropriately focused for 

the geographic area being evaluated, as “one size does not fit 

all.” In some instances monitoring relatively resistant species, 

such as coyote, which prey upon highly susceptible species 

involved in the transmission of tularemia, such as jackrabbits, may be the best approach. For other situations, monitoring might be focused on arthropod vectors, such as ticks, or 

focused on surface waters. Monitoring approaches should 

be guided by the fact that specific foci for tularemia generally involve only a small number of primary species despite 

the broad host range of species susceptible to F. tularensis.

11 

Species other than those of primary importance tend to have 

incidental exposures and are not reliable indices for tularemia 

activity.

Surveillance for tularemia should be integrated with 

broader wildlife disease diagnostic activities and with that 

for domestic animals and human health. The diagnosis of 

tularemia as the cause of mortality in a beaver at a National 

Wildlife Refuge in Wisconsin during routine wildlife disease 

diagnostic activities provided early detection of tularemia 

activity. Wildlife managers temporarily closed portions of the 

refuge to minimize the potential for human exposure to tularemia. In another instance, the diagnosis of tularemia in an 

endangered Delmarva fox squirrel found by a hiker provided 

evidence of disease activity in a terrestrial environment (Fig. 

14); actions followed to modify human use of the area and 

reintroduction plans for the fox squirrel.235

A reasonable precaution is to avoid drinking untreated 

water from lakes, rivers, and streams. This precaution also 

provides protection against a variety of other diseases such 

as giardiasis. In addition, avoid contact uses of water where 

dead rodents, hares, or rabbits are observed in those or adjacent environments.

As for other arthropod transmitted diseases, the use of 

insect repellant and protective clothing can provide effective 

barriers against exposure when in areas where insect vectors are the primary means for transmission of F. tularensis. 

Frequent body searches and prompt removal of ticks can also 

greatly reduce the risk for human infections from tularemia 

and other tick-borne diseases. Companion animals such as 

dogs and cats can bring infected ticks into the home, potentially infecting their owners. The use of tick collars, routine 

inspection of pets, and the careful removal of ticks are other 

actions that can be taken for disease prevention.170 Figure 14. An endangered Delmarva fox squirrel that was a 

postrelease casualty of tularemia.

Photo by James Runningen

Disease Prevention and Control 49
50 Tularemia

Tularemia—Who Is At Risk?

The overall global risk for contracting tularemia has decreased greatly during recent years. 

Within the USA, the reduced number of annually reported cases was a major factor in 

the 1994 removal of tularemia from the list of nationally notifiable diseases. Because of 

increased threats of bioterrorism, tularemia was reinstated to the list in 2000.4 Nevertheless, tularemia remains a well-entrenched zoonosis. Areas historically known for this 

disease continue to have periodic outbreaks and tularemia sporadically appears in new 

places. The adage that, “one size fits all,” does not apply to either the risk for exposure to 

tularemia or guide preventive actions that should be considered. In general, risk for infection is related to personal lifestyle and occupation.

Highest Risk Situations

Moderate Risk Situations

Lower, but moderate risks for exposure to F. tularensis are 

commonly associated with a variety of nonlaboratory activities. Historically, activities such as hunting,241 trapping,78

and butchering wild game33 have been closely associated 

with human cases of tularemia, especially when those 

activities have involved the taking of rabbits, hares, beaver, 

muskrat, and water voles.44,144,147,185,242 Within the USA and 

many other countries, market hunting of wild game has 

been banned. As a result, “rabbit fever,” which was often 

contracted by those who sold and butchered cottontail 

rabbits, is no longer a problem for commercial butchers.36

In addition, trapping of species typically associated with 

tularemia has declined greatly. However, many native 

peoples and others continue to pursue these activities as 

part of their culture, livelihood (i.e. hunting guides), and for 

subsistence. The subsistence use of wildlife often involves 

salient species in the ecology of tularemia. Because these 

activities often take place in areas where tularemia in 

wildlife is common, it is likely that this segment of society 

has an elevated exposure rate to F. tularensis. For example, 

as many as 62 percent of native men in Alaska have tested 

positive for tularemia, most likely type B infections. Serologic evidence also indicates that large numbers of cases 

have occurred within North America in muskrat trappers.

Under some circumstances, farmers are also placed in 

moderate risk situations for exposure to F. tularensis. Hay 

Box 8

Laboratory-acquired infections are a significant risk for 

those involved in diagnostic and other laboratory investigations with Francisella tularensis.

238 Factors that elevate 

risk within this work environment include the potential for 

aerosol exposure associated with laboratory work, the low 

number of organisms required for aerosol infections, and 

the high concentration of organisms often present in the 

investigative materials. Because of these factors, laboratory investigators are often vaccinated, although, within 

the USA, the vaccines in use have been experimental. 

The Working Group on Civilian Biodefense recommends 

that the live vaccine strain [an attenuated (low virulence) 

form of F. tularensis] be used only in laboratory personnel 

routinely working with F. tularensis. Protection afforded 

by the live vaccine has been considerably better than that 

provided by the killed vaccine.4

and water supplies in rural areas have been the source 

for numerous human cases of tularemia following their 

contamination by small rodents. Aerosol exposure from 

handling contaminated hay infected more than 676 people 

during one event.128 High population densities of small 

rodents such as mice, voles, and lemmings in tularemia 

enzootic areas are a warning sign for potential outbreaks of 

this disease and should trigger surveillance for tularemia 

activity in those populations. Findings from that surveillance are important for risk assessment and for guiding 

actions to protect human health within farming communities. A persistent foci of tularemia, with a high percentage 

of pneumonic cases, on Martha’s Vineyard, Massachu- Photo by Milton Friend

Photos by Milton Friend
Photo by Milton Friend

setts, since 2000 has placed landscapers at risk. The wearing of protective face masks has been recommended for 

those engaged in such activities at that location.5,133

Military personnel also have experienced major exposures 

to F. tularensis. The largest tick-borne cluster of tularemia 

cases within the USA occurred among troops on maneuvers in Tennessee.79 Tens of thousands of Russian and 

German troops on the eastern front contracted tularemia 

in a series of outbreaks that occurred during World War II. 

However, it has been suggested that the outbreaks may 

have resulted from biological warfare rather than naturally 

acquired infections.4

The emergence of tularemia in prairie dogs, in combination 

with the popularity of these animals as wildlife pets and 

the inadequacy of health evaluation requirements for these 

animals, results in elevated risks for humans to contract 

tularemia from prairie dogs.136,137

Normal Risk Situations

The best prevention against tularemia is sound information about the presence of active disease in areas where outdoor activities are to be carried out 

and general knowledge of the ecology of this disease. The sound application 

of this information provides a basic foundation for enjoying and working in 

the outdoors in a manner that minimizes risks for exposure to F. tularensis, 

even when disease is present.

Wildlife disease investigators, biologists, and law enforcement agents along with veterinary clinicians are others 

with potential elevated risks for exposure to F. tularensis, 

depending on the circumstances of their field activities 

and clinical practice.

Field biologists and wildlife law enforcement agents are 

often the initial personnel to encounter wildlife mortality 

events, often of unknown causes, and gather specimens 

for evaluation by disease specialists. Exposures to such 

mortality events have inherent risks that differ somewhat 

with the wildlife species involved.

Veterinarians with on-farm activities encounter a variety 

of diseases in the animals they treat, as do clinicians who 

provide services for zoological collections and wild animal 

parks.243 Tularemia has been the cause of illness and death 

of numerous animals in these types of environments,244,245

including recent outbreaks in zoos in Arizona that killed 

several primates.

246 Zoo outbreaks of tularemia often 

involve an interface with wild rodents, which also could 

be a potential source for human exposure. In addition, the 

increasing number of cases of tularemia in companion 

animals, especially the domestic cat, provides another 

potential source for veterinarians to become exposed to F. 

tularensis.

In most instances, wildlife disease specialists are the least 

likely of those within this risk group to encounter “surprise” 

exposures to tularemia. Field observations made by those 

reporting wildlife mortality events, past history of disease 

events on the area involved, and, in many instances, 

preliminary diagnostic evaluations from specimens already 

submitted often provide wildlife disease specialists with 

an initial foundation for their investigations.

Because tularemia is strongly linked to rabbit, hare, and 

rodent populations, human contact with these animals is 

risky when tularemia is active. Hiking, camping, fishing, hunting, and other forms of outdoor recreation are 

activities where humans could have contact with infected 

animals, be bitten by infected arthropods such as ticks, or 

have contact with contaminated surface waters. Numerous cases of tularemia have been associated with humans 

capturing sick wildlife by hand. Healthy wildlife are seldom 

approachable by humans so it’s best to avoid contact with 

animals easily captured and possibly diseased.

Also, the potential for human exposure to F. tularensis by 

means other than contact with diseased animals should 

not be underestimated. Contact entry of F. tularensis via 

contaminated water has occurred though small abrasions 

in the skin, aerosol exposures by sprays and splashes 

resulting from human activities in those waters, and 

by ingestion.49,51,118,119,172,181,200 For example, a major, but 

unusual, outbreak of tularemia occurred in Spain among 

people fishing for crayfish in a contaminated stream.49

Tularemia—Who is at Risk? 51 Photo by Milton Friend Photo by Milton Friend
Consumption of infected

wild game

Contact with infected

wildlife

Aerosols of contaminated

hay

Laboratoryacquired infectionsIngestion of

contaminated water

Contact with contaminated

water

Arthropod bites

Contaminated mouth parts

and claws of companion

animals

Routes For Human Exposure to Francisella tularensis

52 Tularemia

Figure 15. Humans can acquire tularemia by many routes and from numerous sources. (Mouse and tick photographs courtesy of 

the Center for Disease Control, microsope photograph by James Runningen, other photographs by Milton Friend.)
The use of rubber or latex gloves should be standard for 

hunters, trappers, and others who process wildlife for food 

or hides, especially those species commonly associated with 

tularemia (i.e., rabbits, hares, muskrats, etc.). Game should be 

thoroughly cooked when used for food.

Current numbers of tularemia cases in humans do not warrant reducing targeted vertebrate and invertebrate populations 

that are sources for disease maintenance and transmission. 

Within the USA, and in many other countries, such actions 

would invoke strong public outcry in opposition to the concept and its application. Also, tularemia may serve as a natural control of rodent populations that would otherwise cause 

significant negative impacts.230 The rapid rodent population 

crashes often associated with tularemia may prevent enzootics 

of sylvatic plague in species susceptible to both diseases.12 

Vaccination of high-risk individuals, such as hunters, 

trappers, and laboratory workers, has often been proposed 

and explored to some extent.236 Immunization of humans was 

initiated in the former Soviet Union in the 1930s because of 

the high incidence of tularemia in that country. Many millions 

living in tularemia-endemic areas were given a live attenuated vaccine.237 However, vaccination has generally not been 

widely applied elsewhere. Vaccination of individuals may 

become feasible within the United States in the near future, 

especially those with high risk for tularemia (Box 8). A live 

attenuated vaccine is being tested as an investigational new 

drug, but protection afforded has been uneven. Some of the 

volunteers were not protected against aerosol challenges with 

virulent F. tularensis. Data from the investigations undertaken 

are under review by the U.S. Food and Drug Administration 

(FDA) to determine the future availability of the vaccine.4 

Treatment

Infection of humans by F. tularensis is treatable by antimicrobial therapy. Treatment recommendations have been 

developed for circumstances when a high degree of focus on 

the infected individual is possible as well as for large-scale 

events where this type of focus is not possible.4

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Glossary

Terms are defined relative to meaning within this publication.

Aerobic bacteria Requires the presence of oxygen for survival, in contrast to anaerobic bacteria that only exist in the 

absence of free oxygen.

Amphibians Cold-blooded vertebrates that live both on land 

and in water, have limbs instead of fins, have no claws on 

their toes, and have moist skin unprotected by external covering (e.g., scales, feathers, or hair); salamanders, newts, frogs, 

and toads.

Annelids Elongated, segmented metazoan invertebrates, 

above the lower worms; have a coelom (epithelium-lined 

space between the body wall and the digestive tract), like 

earthworms and leeches.

Anorexia Lack of appetite; severe and prolonged inability 

or refusal to eat.

Antigen Foreign proteins and other substance that, upon 

entering the body, stimulates the hosts immune system to produce specific substances, such as an antibody, to react with 

the antigen as a means for protecting the host from harmful 

invasion.

Antilocapridae A family of antelope containing the single 

living genus and species, the pronghorn Antilocarpa americana, that occurs in open grasslands and desert areas of 

western North America from southern Manitoba, Canada, to 

northern Mexico.

Arthropods Invertebrates belonging to the Phylum Arthropoda, here referring to members of the Classes Arachnida (spiders, ticks, mites, and scorpions) and Insecta (e.g., 

mosquitoes, flies, lice, fleas) that are disease vectors (e.g., 

mosquitoes and West Nile fever; ticks and tularemia).

Bacteremia The presence of bacteria in the blood.

Bacterium Singular of bacteria.

Bedbugs Small, wingless, flattened, oval, reddish, bloodsucking insects of the genus Cimex that feed on humans (e.g., 

Cimex lectularius), usually at night, and are found in houses, 

furniture, and unclean beds.

Biological vectors Arthropods in which the infecting 

organism develops or multiplies to become infective for other 

species.

Bioterrorism The use of biological agents, such as pathogenic organisms or agricultural pests, for terrorist purposes.

Biovar In the classification of bacteria, strains with sufficiently distinct characteristics (e.g., chemical, molecular) to 

be considered a subspecies of a taxonomic species.

Biowarfare Biological warfare; the use of biological weapons by one nation against another.

Bioweapons Any weapon usable in biological warfare and 

bioterrorism.

Birds Warm-blooded vertebrates with wings and feathers 

(although the wings are poorly developed for some species 

and they are flightless); belonging to the Class Aves.

Birds of prey Birds that primarily feed on the flesh of animals (e.g., amphibians, reptiles, mammals and other birds). 

Typically hawk-like birds, owls, eagles, condors, and vultures.

Biting flies Insects of the Order Diptera with mouthparts 

adapted to biting and piercing vertebrate animals; examples 

include deer flies and horse flies.

Biological transmission Disease transfer requiring an amplification host (often an arthropod) for development and/or 

multiplication of the disease agent necessary for infection of 

another host.

Blackflies Small, dark-colored, biting flies in the Family 

Simuliidae, whose larvae attach to rocks in flowing water; 

important vectors of Leucocytozoan spp., blood parasites of 

birds.

Boreal forests Predominantly coniferous (evergreen) native 

forests of northern latitudes.

Bubonic plague A severe bacterial disease of humans due 

to infection by Yersinia pestis; acute regional enlargement 

and inflammation of lymph nodes (buboes) is typical of this 

most common form of plague in humans. The “black death” 

of earlier times.

Buzzards Large hawk-like birds of prey, including New 

World vultures.

Caddis flies Insects of the Order Trichoptera with four 

membranous wings, slender antennae, and aquatic larvae; 

important food source for fish and birds.

Camels Primarily domesticated species of one-humped 

(Camelus dromedarius) and most two-humped camels; the 

only two-humped camel in a wild state (C. bactrianus) inhabits the Gobi Desert in Mongolia.

Canids Mammals within the Family Canidae (e.g., wolves, 

coyote, jackals, foxes, and other dog-like animals).

Carnivores Mammals with teeth and other body adaptations 

for feeding on flesh; primarily species belonging to the Order 

Carnivora (e.g., wolves, bears, raccoons, weasels, civets, 

hyenas, and tigers).

Catfish Bottom-feeding finfish with a scaleless skin, a 

broad, flat head and a strong single spine associated with 

both the dorsal and pectoral fins; barbels (fleshy appendages) 

are present on the face area. North American species include 

catfish, bullhead, stonecat, and madtoms.

Chicken hawk An informal name often used for a variety of 

hawk species.

Cloacal contents Fecal, urinary, and other discharges found 

in a common chamber at the end of the intestinal tract for 

most birds, reptiles, amphibians, and many fishes.

Companion animals Animals maintained by humans as pets 

(e.g., dogs, cats, captive wildlife, horses).

Glossary 63
64 Tularemia

Conjunctiva The mucous membrane that lines the inner 

surface of the eyelid and the exposed surface of the eyeball.

Contagious disease Disease capable of being transmitted 

from one individual to another; communicable. All contagious diseases are infectious, but not all infectious diseases 

are contagious, as some must be vectored by infected insects 

or other means.

Coryza Acute, profuse, free discharge from the nostrils associated with inflammation of the nasal mucus membrane and 

air passages of the head and throat.

Coxal fluid Body fluid of ticks that may be discharged if 

limbs become detached when attempting to remove attached 

and engorged ticks.

Crayfish A freshwater crustacean that resembles a lobster in 

appearance except for its small size.

Crustaceans Fauna with a chitinous exoskeleton, such as 

crabs, lobsters, and shrimps, including barnacles, sow bugs, 

water fleas, and beach hoppers.

Cutaneous Pertaining to the skin.

Disease carriers Animals infected with infectious agents 

and showing no clinical signs of disease, but are capable of 

transmitting the infection.

Doves Pigeon-like birds belonging to the Family Columbidae. Domestic pigeons are often referred to as rock doves. 

Within North America, mourning doves, and white-winged 

doves are the most abundant wild species.

Edema Accumulation of abnormal amounts of fluid in the 

intercellular spaces within tissues of the body; generally in 

subcutaneous tissues but can be systemic, as well as localized.

Emerging infectious diseases Infectious diseases that have 

newly appeared and/or increased in frequency of occurrence 

within the past three decades, or threaten to increase in the 

near future relative to populations affected, geographic distribution, or magnitude of effects.

Endemic A disease that commonly is present within a human population or a geographical area.

Endotoxins Heat-stable toxins released from disrupted cells 

of some species of gram-negative bacteria, such as vibrios 

and brucellae; large doses can produce hemorrhagic shock 

and severe diarrhea, smaller doses cause fever and other 

manifestations.

Enzootic An animal disease that commonly is present within 

a population or a geographical area.

Epidemic An outbreak of disease affecting a disproportionately large number of humans within a population, community, or region during a period of time.

Epizootic A disease affecting a greater number of animals 

than normal; typically involving many animals in the same 

region at the same time.

Epoch An extended period of time characterized by distinctive development and/or events; a division of geologic time.

Eurasia The geographic area encompassing Europe and 

Asia.

Fairy shrimp Transparent freshwater branchiopod crustaceans of the Order Anostraca.

Fish Refers to finfish (e.g., cold-blooded strictly aquatic vertebrates with a well differentiated skull and a bony skeleton), 

in contrast to shellfish (invertebrates) and jawless fishes.

Fleas Small, wingless, bloodsucking insects within the 

Order Siphonaptera with laterally compressed bodies and legs 

adapted for jumping; some are important vectors of zoonotic 

diseases, such as plague.

Fluorescent antibody A laboratory assay system utilizing 

fluorescent dyes as stains for the detection of antibody against 

specific pathogens.

Foals Young (of the year) horses.

Foxes In North America, term pertains to arctic, red, kit 

(swift), and gray fox.

Frogs Amphibians that, along with toads, are within the Order Anura. Adult specimens of both have short, squat bodies, 

powerful hind legs, and lack a tail (see Toads).

Gerbils Old World burrowing desert rodents belonging to 

the genus Gerbillus (and related genera) with long hind legs 

adapted for leaping. 

Giardiasis A common parasitic zoonoses resulting from infection of the small intestine by protozoans within the Genus 

Giardia. Humans typically become infected via contaminated 

food and water.

Gnats Small, biting flies within the Order Diptera.

Gram-negative coccobacillus Oval- shaped bacterial cells 

intermediate between spherical (coccus) and rod-shaped (bacillus) forms; gram-negative bacteria do not retain the purple 

dye when treated by Gram’s stain for differentiating bacteria 

into two major groups (gram-negative and gram positive).

Ground squirrels Typically, burrowing small rodents of the 

Family Sciuridae (e.g., in the USA, thirteen-lined ground 

squirrel, rock squirrel, and antelope ground squirrel), but this 

term often includes species in other genera, such as chipmunks and prairie dogs.

Grouse Ground-dwelling, chicken-like birds of the Family 

Tetronidae with short to medium length tails (in contrast to 

pheasants); referring here to the ruffed grouse (Bonasa umbellus), unless specified otherwise.

Hard ticks Arthropods of the Family Ixodidae that are important for disease transmission; includes ticks of the genera 

Dermacentor, Amblyomma, Ixodes, and Haemaphysalis.

Hardwood forest Forests primarily composed of deciduous 

trees of hardwood (e.g., beech, birch, and maple are types of 

forests).

Hares Lagomorphs of the Family Leporidae whose young 

are furred at birth, have open eyes, and are able to run a few 
minutes after birth, in contrast to rabbits, which are born 

naked, blind, and helpless.

Holarctic The biogeographic region encompassing the Nearctic and Palearctic subregions (the northern parts of the Old 

World and New World).

Infectious disease A disease caused by the invasion of a 

host by pathogenic microorganisms. The pathogen may be 

a bacterium, virus, fungus, parasite or a prion (infectious 

protein).

Intraperitoneal Within the peritoneal cavity (in mammals, 

the double-layered sac that lines the area around the viscera 

below the diaphragm).

Invertebrates Animals lacking a spinal column (e.g., insects, crustaceans).

Kite Falcon-like hawks of the Family Accipitridae.

Lagomorphs Mammals within the Order Lagomorpha (rabbits, hares, and pikas).

Lesion Pathological change in the appearance of tissues or 

loses of normal function due to pathogens, injury, or other 

causes.

Lice Small, wingless, usually flattened insects that are 

parasitic on animals and/or plants and derive their nutrition by 

feeding on their hosts blood or other body components; true 

lice infest animals, including humans, and transmit several 

important diseases.

Lymphatics The system of lymph and lymph vessels that 

drain the tissue fluids of the body and return lymph to the 

blood.

Lymphatic glands The aggregation of cells within the lymphatic system into functional areas for the secretion or excretion of lymph within the body (e.g. lymph nodes).

Lymphatic system That part of the body’s circulating system 

that recovers fluids and proteins which have exited cells and 

tissues and returns those materials to the blood; cellular debris 

and foreign materials are cleaned in this system by phogocytosis (e.g., white blood cell engulfment and consumption of 

foreign materials) and filtration.

Lymph nodes Rounded, encapsulated aggregations of 

lymphoid tissue distributed throughout the body along the 

lymphatic system. These nodes filter the flow of lymph circulating within the body.

Malaise A vague, general, and unfocused feeling of illness 

and fatigue.

Mammals Warm-blooded vertebrate animals that possess 

hair during some part of their life and suckle their young.

Mechanical transmission Disease transfer involving contact 

with surfaces contaminated by pathogens; this may occur 

from bites, scratches, contact with inanimate objects, and by 

other means allowing disease causing levels of the pathogen 

to enter the host.

Microbe Minute, microscopic living organisms that perform 

various biological functions essential for life processes (i.e., 

digestion); some microbes are referred to as germs because of 

their capacity to cause disease and include various forms of 

bacteria, fungi, protozoa (single-cell parasites), and viruses.

Migratory birds Species of birds that undertake seasonal 

geographic movements to meet their living and life-cycle 

requirements (e.g., waterfowl, shorebirds, many passerines).

Midges Very small, two-winged flies, many of which render 

painful bites and some of which vector infectious diseases.

Mice Small rodents with a pointed snout, relatively small 

ears, elongated body, and slender, nearly hairless tail; species 

primarily are within the genus Mus.

Miocene Period from 11 million to 25 million years ago 

during which the formation of high mountains occurred (e.g., 

Alps, Rockies, Himalayas).

Mites Minute arthropods related to spiders and usually 

having transparent or semitransparent bodies; parasitic forms 

for humans and animals feed primarily on the skin, causing 

various types of irritation of the tissue and also vector some 

infectious diseases.

Mollusks In general, shell-bearing invertebrates that have 

soft, unsegmented bodies (e.g., snails, clams, conchs, shells, 

scallops, oysters); also highly specialized carnivores often 

lacking an external shell and having long flexible tentacles, 

eyes, and a powerful beak (e.g., squid and octopi).

Moribund Being in a state of dying.

Mosquitoes Blood-sucking, small dipteran insects of the 

Family Culicidae that are important vectors for disease transmission (e.g., West Nile fever, malaria).

Nearctic The biogeographic subregion that includes Greenland, arctic America, and the parts of North America north of 

tropical Mexico (see Fig. 1).

Palearcarctic The biogeographic subregion that includes 

Europe, Asia north of the Himalayas, Arabia, and Africa 

north of the Sahara (See Fig. 1).

Paratuberculosis Johne’s disease (Mycobacterium paratuberculosis), an infectious bacterial disease of wild and 

domestic ruminants that clinically resembles tuberculosis 

(Mycobacteruim tuberculosis) but is different.

Parenteral inoculation Entry by injection other than 

through the alimentary canal (e.g., subcutaneous, intramuscular, etc.).

Pathogens Typically microorganisms capable of inducing 

disease, but broadly includes all disease-inducing agents.

Pathogenesis The progression of agent-caused events 

within the body following exposure to a pathogen (disease 

agent) that results in disease, morbidity, and/or death.

Pheasant Long-tailed and often brightly colored Old World 

gallinaceous birds of the Family Phasianidae.

Glossary 65
66 Tularemia

Pikas Short-eared, small rabbit-like mammals within the 

Order Lagomorpha; also referred to as coney and rock rabbit.

Pleomorphic An organism that has multiple distinct forms 

(e.g., a specific bacterium that can appear as spherical and 

rod-like forms).

Pliocene Period from 1 million to 11 million years ago during which the Antarctic Ice Age set in; on land, rapid evolution of mammals occurred.

Quail Any of various small, short-tailed gallinaceous birds 

of the Family Phasianidae.

Rabbit Small, long-eared mammals within the Family Leporidae (hares and rabbits) of the Order Lagomorpha (pikas, 

rabbits, and hares). Rabbits are born naked, blind, and helpless in a fur-lined nest; hares are born fully haired, with open 

eyes, and are able to run within minutes after birth. Some 

species commonly referred to as rabbits are actually hares 

(e.g., jack rabbit and snowshoe rabbit) while the Belgian hare 

is actually a rabbit.

Rain forest Tropical woodlands having an average annual 

rainfall of at least 100 inches and also characterized by lofty 

broad-leaved evergreen trees forming a continuous canopy.

Reptiles Vertebrates of the Class Reptilia that breathe by 

means of lungs and have external coverings of scales or bony 

plates; includes snakes, lizards, crocodiles, turtles, and dinosaurs.

Reservoir host The host that maintains the disease agent in 

nature and that provides a source of infection to susceptible 

hosts (see Fig. 9).

Rodent A diverse group of mammals characterized by incisor teeth that grow throughout life and must be worn away by 

cutting and gnawing hard materials. Species within the Order 

Rodentia include squirrels, mice, rats, voles, chipmunks, gophers, lemmings, beaver, porcupines, and many others.

Scavengers Animals that feed on dead carcasses, other carrion, and refuse (e.g., vultures, crows, hyenas, and jackals).

Septicemia Blood poisoning; persistence of pathogenic 

microorganisms and/or their toxins in the blood.

Serology Laboratory evaluations of the serum portion of 

blood for the purpose of detecting and measuring host antibody response to infectious agents and other antigens.

Serotype A group of closely related microorganisms distinguished by a characteristic set of antigens.

Snails Mollusks of the Class Gastropoda; most have a 

single enclosing shell or valve (usually spiral). Snails are a 

mobile, predatory species (often carnivores) that are important developmental hosts for pathogens causing several major 

parasitic diseases.

Snakes Scaled, limbless, sometimes venomous reptiles of 

the Suborder Serpentes having long, cylindrical tapering bodies.

Snapping turtles Any of numerous large freshwater turtles 

within the Family Chelydridae that have rough shells and 

powerful hooked jaws capable of closing suddenly.

Soft ticks Eight-legged arthropods of the Family Argasidae 

characterized by their soft, membranous external shells.

Spiders Invertebrates within the arachnids (spiders, mites, 

scorpions, and ticks) having an unsegmented abdomen that 

is constricted at the base and two or more pairs of abdominal 

spinnerets for producing silk threads for cocoons for their 

eggs or webs to capture prey.

Squirrel Tree squirrels of the Family Sciuridae; small to 

medium-sized arboreal rodents having long bushy tails and 

strong hind legs.

Systemic infections Those affecting the body as a whole.

Tabanids Bloodsucking biting flies, such as horseflies and 

gadflies, that can inflict painful bites and may mechanically 

vector infectious disease.

Ticks Blood-sucking, parasitic arthropods that have a hard 

body (ixodid ticks) or a soft body (argasid ticks); ticks are 

important disease vectors.

Toads In general, anurans with less smooth skin than that of 

most frogs; toads are also more terrestrial than frogs and hop 

rather than jump.

Translocation Human capture of wildlife at one geographic 

area and their transportation and release at a different geographic area.

Transovarian Transovarial; transmission of pathogens from 

the maternal organism (parent) by invasion of the ovary and 

infection of eggs, to individuals of the next generation (common in mites and ticks).

Tuberculosis A serious disease resulting from infection by 

bacteria within the genus Mycobacterium; M. tuberculosis

is the primary cause of tuberculosis in humans, M. bovis for 

other mammals, and M. avium intracellular for birds. However, humans have been infected by all three species, and M. 

tuberculosis also affects nonhuman primates.

Turtles Reptiles with shells that cover the body; some 

species are found in freshwater habitats, others in marine 

environments (sea turtles), and still others are terrestrial 

(tortoises).

Upland game birds Chicken-like terrestrial birds commonly 

hunted for sport and food (i.e., chachalacas, grouse, partridges, pheasants, prairie-chicken, ptarmigan, quail, and turkeys).

Virulence The degree or ability of a pathogenic organism to 

cause disease.

Vertebrates All animals having spinal columns; mammals, 

birds, reptiles, amphibians, and boney and cartilaginous 

fishes.
Glossary 67

Voles Small rodents of the genus Microtus (and related 

genera) that typically have a stout body, rather blunt nose (in 

contrast to mice), and small ears.

Waterbirds Bird species that utilize water environments as 

primary habitat (e.g., waterfowl, wading birds, gulls, terns, 

cormorants, and many others).

Waterfowl Birds within the Family Anatidae, collectively; 

all species of ducks, geese, and swans.

Zoonoses Infectious diseases transmissible between animals 

and humans, and vice versa.

Edited by Gail Moede Rogall

Layout and illustrations by Marta Anderson, Frances Jeanne 

Bergmann, Elizabeth Ciganovich, John M. Evans, Erinn Dornaus, 

Jennifer Rodriguez, and Rosemary Stenback.

Front cover photos of a veterinary examination of a cat, a ground 

squirrel, a jackrabbit, and the trapping of a snowshoe hare by 

Milton Friend, U.S. Geological Survey; muskrat photo by Terry 

Spivey, U.S. Department of Agriculture, U.S. Forest Service.


Milton Friend —Tularemia—Circular 1297

Printed on recycled paper