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Special Section on Mountain Sheep Management
Pneumonia in Bighorn Sheep: Risk and
Resilience
E. FRANCES CASSIRER,
1
Idaho Department of Fish and Game, 3316 16th Street, Lewiston, ID 83501, USA
KEZIA R. MANLOVE, Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, WA 99164, USA
EMILY S. ALMBERG, Montana Department of Fish, Wildlife, and Parks, 1400 South 19th St., Bozeman, MT 59717, USA
PAULINE L. KAMATH, School of Food and Agriculture, University of Maine, Orono, ME 04469, USA
MIKE COX, Nevada Department of Wildlife, 6980 Sierra Center Parkway, Suite 120, Reno, NV 89511, USA
PEREGRINE WOLFF, Nevada Department of Wildlife, 6980 Sierra Center Parkway, Suite 120, Reno, NV 89511, USA
ANNETTE ROUG, Utah Division of Wildlife Resources, 1594 W. North Temple, Suite 2110, Salt Lake City, UT 84116, USA
JUSTIN SHANNON, Utah Division of Wildlife Resources, 1594 W. North Temple, Suite 2110, Salt Lake City, UT 84116, USA
RUSTY ROBINSON, Utah Division of Wildlife Resources, 1594 W. North Temple, Suite 2110, Salt Lake City, UT 84116, USA
RICHARD B. HARRIS, Washington Department of Fish and Wildlife, 600 Capitol Way North, Olympia, WA 98501, USA
BEN J. GONZALES, Wildlife Investigations Laboratory, California Department of Fish and Wildlife, 1701 Nimbus Road, Rancho Cordova,
CA 95670-4503, USA
RAINA K. PLOWRIGHT, Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA
PETER J. HUDSON, Center for Infectious Disease Dynamics, Penn State University, University Park, PA 16802, USA
PAUL C. CROSS, U.S. Geological Survey, Northern Rocky Mountain Science Center, Bozeman, MT 59715, USA
ANDREW DOBSON, Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA
THOMAS E. BESSER, Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, WA 99164, USA
ABSTRACT Infectious disease contributed to historical declines and extirpations of bighorn sheep (Ovis canadensis)in
North America and continues to impede population restoration and management. Reports of pneumonia outbreaks in free-
ranging bighorn sheep following contact with domestic sheep have been validated by the results of 13 captive commingling
experiments. However, ecological and etiological complexities still hinder our understanding and control of respiratory disease
in wild sheep. In this paper, we review the literature and summarize recent data to present an overview of the biology and
management of pneumonia in bighorn sheep. Many factors contribute to this population-limiting disease, but a bacterium
(Mycoplasma ovipneumoniae) host-specific to Caprinae and commonly carried by healthy domestic sheep and goats, appears to
be a primary agent necessary for initiating epizootics. All-age epizootics are usually associated with significant population
declines, but mortality rates vary widely and factors influencing disease severity are not well understood. Once introduced, M.
ovipneumoniae can persist in bighorn sheep populations for decades. Carrier females may transmit the pathogen to their
susceptible lambs, triggering fatal pneumonia outbreaks in nursery groups, which limit recruitment and slow or prevent
population recovery. The demographic costs of disease persistence can be equal to or greater than the impacts of the initial
epizootic. Strain typing suggests that spillover of M. ovipneumoniae into bighorn sheep populations from domestic small
ruminants is ongoing and that consequences of spillover are amplified by movements of infected bighorn sheep across
populations. Therefore, current disease management strategies focus on reducing risk of spillover from reservoir populationsof
domestic sheep and goats and on limiting transmission among bighorn sheep. A variety of techniques are employed to prevent
contacts that could lead to transmission, including limiting the numbers and distribution of both wild and domestic species. No
vaccine or antibiotic treatment has controlled infection in domestic or wild sheep and to date, management actions have been
unsuccessful at reducing morbidity, mortality, or disease spread once a bighorn sheep population has been exposed. More
effective strategies are needed to prevent pathogen introduction, induce disease fadeout in persistently infected populations,
and promote population resilience across the diverse landscapes bighorn sheep inhabit. A comprehensive examination of
disease dynamics across populations could help elucidate how disease sometimes fades out naturally and whether population
resilience can be increased in the face of infection. Cross-jurisdictional adaptive management experiments and transdisciplinary
collaboration, including partnerships with members of the domestic sheep and goat community, are needed to speed progress
toward sustainable solutions to protect and restore bighorn sheep populations. Ó2017TheWildlifeSociety.
KEY WORDS bighorn sheep, domestic goats, domestic sheep, Ovis canadensis, respiratory disease, spillover,
wildlife-livestock interface.
Received: 28 November 2016; Accepted: 23 May 2017
1
E-mail: frances.cassirer@idfg.idaho.gov
The Journal of Wildlife Management 82(1):32–45; 2018; DOI: 10.1002/jwmg.21309
32 The Journal of Wildlife Management 82(1)
Infectious disease has influenced bighorn sheep (Ovis
canadensis) population dynamics at least since the westward
expansion of the United States, and plausibly since the
Spanish colonization of Mexico and the American South-
west. The importance of disease in the historical decline and
extirpation of bighorn sheep across much of their range from
southern Canada to Mexico is unique among North
American ungulates. Early naturalists described catastrophic
die-offs and suggested that disease outbreaks and disappear-
ance of wild sheep might be attributed to the introduction of
domestic sheep and goats into bighorn sheep range (Brooks
1923, Grinnell 1928). Shillinger (1937) reported on an
experiment in which Rocky Mountain bighorn sheep (O. c.
canadensis), after surviving well in captivity by themselves, all
died when healthy-appearing domestic sheep were intro-
duced to the enclosure. Shillinger speculated “The only
evident explanation is that some infectious organism well
tolerated by the domestic sheep...was transferred to the wild
animals with disastrous results” (Shillinger 1937:301). Since
then, many more disastrous disease outbreaks have occurred
in free-ranging wild sheep populations and another 12
domestic-wild sheep commingling experiments have been
conducted with similar deadly results for bighorn sheep
(Wehausen et al. 2011, Besser et al. 2012a). Together these
observations have culminated in the recognition that
management of bighorn sheep also involves management
of pathogen transmission from domestic sheep (Council for
Agricultural Science and Technology 2008, Western
Association of Fish and Wildife Agencies Wild Sheep
Working Group 2012, The Wildlife Society 2015).
The susceptibility of bighorn sheep to infectious agents
carried by domestic sheep is not unexpected given that
genetic similarity with domestic hosts is a key risk factor for
pathogen spillover and associated disease-induced popula-
tion declines in wildlife (Pedersen et al. 2007). The bighorn
sheep is the only North American ungulate with a congeneric
domesticated relative. Although species divergence occurred
over a million years ago (Rezaei et al. 2010), domestic and
bighorn sheep are still sufficiently similar that they can
interbreed and produce viable offspring (Young and Man-
ville 1960). Bighorn and domestic sheep and goats share
lineages of immune-associated genes in the major histo-
compatibility complex (Gutierrez-Espeleta et al. 2001), but
inherent differences in immune systems likely contribute to
the disparity in effects of pathogens across species (Silflow
et al. 1989, Dassanayake et al. 2009, Highland et al. 2016).
Understanding and acknowledging the importance of
pathogen spillover from domestic sheep and goats has
provided valuable perspective and direction for management
of respiratory disease in bighorn sheep and, at the same time,
has complicated it. Wildlife biologists managing bighorn
sheep are now faced with an uncomfortable choice between
promoting connectivity and gene flow to restore remnant
populations and increasing fragmentation and limiting
dispersal to reduce the risk of pathogen spillover and
transmission. The impact of disease persistence in the
aftermath of all-age epizootics is also a serious obstacle to
population management. In this paper, we review the
literature and include a synthesis of data from our respective
jurisdictions and from members of the Western Association
of Fish and Wildlife Agencies Wild Sheep Working Group
to provide an overview of the current state of knowledge
about pneumonia in bighorn sheep. We report on impacts to
individuals and populations, describe current management
directions, and discuss potential strategies for moving
forward.
CAUSES OF PNEUMONIA IN BIGHORN
SHEEP
Pneumonia in bighorn sheep is a microbiologically complex
disease, and many diverse bacteria are detected in the lungs of
fatally affected animals, including pathogens that
cause pneumonia and other diseases in livestock such
as Mannheimia haemolytica,Pasteurella multocida, and Fuso-
bacterium necrophorum. Some of these pathogens are toxigenic
and lethal to captive bighorn sheep in experimental trials
(Foreyt et al. 1994, Dassanayake et al. 2009), but they do not
exhibit a clear and consistent association with disease
epizootics in free-ranging populations (Singer et al. 2000b,
Weiser et al. 2003, Rudolph et al. 2007, Besser et al. 2012b,
Shanthalingam et al. 2016). Over time, paradigms of disease
etiology have shifted, reflecting the diversity of pathogens and
nonpathogenic agents detected in the lungs of pneumonic
bighorn sheep. Suspected causes have ranged from lungworm
infection (Protostrongylus spp.) to leukotoxin positive Pasteur-
ellaceae, to a multi-factorial respiratory disease complex
(Besser et al. 2013). Much attention has focused on virulent
Pasteurellaceae bacteria where problems with accurate detec-
tion and classificationhave also complicated efforts to establish
an associationwith pneumonia outbreaks in wild sheep(Angen
et al. 2002, Walsh et al. 2012, Miller et al. 2013,
Shanthalingam et al. 2014, Walsh et al. 2016).
In 2006, by applying culture-independent methods to
high-quality samples of the lung microbiome obtained from
free-ranging bighorn lambs in early stages of disease,
researchers discovered that Mycoplasma ovipneumoniae was
the pathogen that first invaded the lungs and predisposed
affected animals to polymicrobial pneumonia (Besser et al.
2008). This pathogen does not act alone but appears to be a
necessary agent for initiating epizootics. Further research is
needed on the role of co-infection by known and perhaps as
yet unrecognized pathogens as well as other factors that may
contribute to disease outcomes by affecting transmission,
carriage, and immunity (Dassanayake et al. 2010, Besser et al.
2012b, Fox et al. 2015, Wolff et al. 2016). Clarity on the
significance of these interactions will help provide a more
complete understanding of the variation observed in the
course of infection and disease. We focus our discussion of
microbial etiology on M. ovipneumoniae because, based on
the experimental and empirical data which we review here, it
currently presents the most parsimonious and well-supported
model for a primary agent of bighorn sheep respiratory
disease. For this reason it is also an important focus for
management.
M. ovipneumoniae better meets Hill’s (1965) causal criteria
relevant to infectious diseases: strength of association,
Cassirer et al. Pneumonia in Bighorn Sheep 33
temporality, plausibility, experimental evidence, and analogy
than any competing proposed etiology (Besser et al. 2013).
M. ovipneumoniae also fulfills Koch’s postulates (Evans 1976,
Walker et al. 2006) for a primary causal agent, with minor
modifications. The strong association with disease (i.e.,
Koch’s first postulate) is one of the most convincing lines of
evidence for M. ovipneumoniae. Besser et al. (2013) detected
M. ovipneumoniae in all free-ranging bighorn sheep
populations affected by pneumonia epizootics where samples
were available for testing (n¼36) and 91% (29/32) of
bighorn sheep populations unaffected by pneumonia lacked
evidence of exposure. Pneumonia outbreaks were associated
with introduction of M. ovipneumoniae in 10 previously
unexposed free-ranging bighorn sheep populations where
testing was done before and after the epizootic (Besser et al.
2008, Bernatowicz et al. 2016; M. Cox, Nevada Department
of Wildlife, unpublished data; J. Kanta, South Dakota
Game, Fish, and Parks, unpublished data; J. Shannon, Utah
Division of Wildlife, unpublished data; L. Jones, U.S. Fish
and Wildlife Service, unpublished data). Limited informa-
tion also suggests that free-ranging Dall’s sheep (Ovis dalli)
in Alaska and bighorn sheep populations in northern Alberta
where bacterial pneumonia epizootics are not reported, have
not been exposed to M. ovipneumoniae (Zarnke and Soren
1989, Besser et al. 2013).
Equally compelling, in 2 recent experiments 5 of 6 bighorn
sheep survived when commingled with domestic sheep in the
absence of M. ovipneumoniae (Besser et al. 2012a, Kugadas
2014). In contrast, virtually no (2%) bighorn sheep survived
in 12 previous commingling experiments with domestic
sheep, including only 1 of 26 in 4 experiments where
presence of M. ovipneumoniae was reported or could be
confirmed retrospectively (Foreyt and Jessup 1982; Foreyt
1989, 1990; Lawrence et al. 2010; Table S1, available online
in Supporting Information).
Although Koch’s second postulate (i.e., isolation of the
agent in pure culture; Walker et al. 2006) has been repeatedly
fulfilled, the ability of those cultures to reproduce the disease
in healthy bighorn sheep (i.e., Koch’s third postulate) is
limited, perhaps because of virulence attenuation during
cultural passage (Gilmour et al. 1979, Niang et al. 1998a,
Besser et al. 2008). However, nasal washes from M.
ovipneumoniae-colonized domestic sheep, treated to remove
any detectable viable bacterial species other than Mycoplasma,
do reproduce the disease in healthy bighorn sheep and the
challenge strain of M. ovipneumoniae can be recovered from
the pneumonic lungs of the affected animals, thereby
fulfilling postulate 4 (i.e., re-isolation of the originally
inoculated pathogen; Besser et al. 2014).
Many Mycoplasma spp. are host-specific, and the host range
of M. ovipneumoniae is considered to be limited to Caprinae
(Nicholas et al. 2008). Respiratory disease following
infection with M. ovipneumoniae also has been reported in
captive Dall’s sheep and other wild Caprinae, including
mountain goats (Oreamnos americanus), and muskox (Ovibos
moschatus; Black et al. 1988, Handeland et al. 2014, Wolff
et al. 2014). In a recent National Animal Health Monitoring
System survey, Sheep 2011, the Animal and Plant Health
Inspection Service tested up to 16 adult females each in 453
randomly selected domestic sheep flocks from across the
United States for M. ovipneumoniae nasal carriage and serum
antibody. Most flocks (88%) tested positive for carriage (as
determined by polymerase chain reaction [PCR] on nasal
swabs). Larger operations were more likely to be PCR
positive and all flocks with 500 adult females were PCR
positive (USDA Aphis Veterinary Services 2015). Less
extensive surveys of domestic goats reported 37.5–88% of
flocks to be PCR positive on nasal swabs. Larger flocks were
more likely to be positive for carriage (Heinse et al. 2016;
Table S2, available online in Supporting Information). A
host-specific pathogen commonly carried by domestic sheep
and goats is consistent with the high mortality observed in
captive bighorn sheep when commingled with domestic
sheep but not when commingled with non-Caprinae
livestock including cattle, horses, and llamas (Foreyt 1992,
Foreyt and Lagerquist 1996, Besser et al. 2012a).
Additional evidence for M. ovipneumoniae as an epidemic
agent is the transmission of 1 (or occasionally 2) multi-locus
sequence types (strains) within an outbreak and a diversity of
strains across outbreaks (Besser et al. 2012b, Cassirer et al.
2017). These strains of M. ovipneumoniae also link the all-
age epizootics to the recurrent lamb pneumonia epizootics
that follow (Cassirer et al. 2017). Strains detected in
domestic sheep differ from those detected in domestic goats,
suggesting host adaptation and coevolution within old world
Caprinae (Maksimovic et al. 2017). This divergence also
provides a means for inferring the host species of origin.
CHARACTERISTICS OF RESPIRATORY
DISEASE IN INDIVIDUALS
The diverse histopathologic lesions observed in experimental
and naturally occurring bighorn sheep pneumonia, range
from those typical of Mycoplasma infections (lymphocytic
cuffing around airways and hypertrophy of the bronchial
respiratory epithelium) to the often more dramatic and severe
hemorrhagic, edematous, and necrotic lesions resulting from
secondary bacterial infections (Miller 2001, Besser et al.
2008, Wood et al. 2017). This polymicrobial pneumonia is
thought to occur when M. ovipneumoniae binds to and
degrades the cilia of the trachea and bronchi, resulting in
disruption of the mucociliary escalator (Niang et al. 1998c),
the physiologic process for clearing bacteria from the lower
respiratory tract. The impaired host immune defenses then
allow inhaled opportunistic pathogens to establish multiple
simultaneous infections of lung tissues with often fatal
results.
The clinical course of bighorn sheep pneumonia may
appear dramatic and short, but evidence from naturally
occurring and experimental infection indicates that sub-
clinical disease exists for several days to several weeks prior to
development of obvious symptoms (Besser et al. 2008, Besser
et al. 2014, Cassirer et al. 2017). This delay presumably
represents the time required for M. ovipneumoniae to infect
the airways and disrupt the mucociliary escalator. The latent
period has important implications for management because
animals might appear healthy for several weeks following
34 The Journal of Wildlife Management 82(1)
infection. By the time disease is evident, M. ovipneumoniae
and other pneumonia pathogens already could be widespread
in the population, even in individuals that still look healthy.
The original focus of M. ovipneumoniae research was
infection in domestic sheep and goats where it is documented
as an important, and probably under-diagnosed, cause of
pneumonia in lambs and kids (Lin et al. 2008, Rifatbegovic
et al. 2011). Differences in the disease across host species
suggest potential focal areas for research that may reveal why
the disease is so devastating in wild sheep (Table 1). Higher
nasal carriage rates (x2
1¼35.49, P<0.001) and lower
antibody prevalence in domestic sheep (x2
1¼33.78,
P<0.001; Table 1, Table S2) are consistent with an evolved
tolerance of M. ovipneumoniae, defined as the ability to shed
high levels of a pathogen with minimal morbidity or
mortality (Råberg et al. 2009). Bighorn sheep resist infection
and react to M. ovipneumoniae exposure with dramatic
humoral immune responses, which could reduce carriage
(Table 1), but also might trigger an auto-immune reaction.
Such a reaction has been described in domestic lambs that
develop respiratory disease associated with M. ovipneumoniae
infection (Niang et al. 1998b). Robust bighorn sheep
immune responses may also contribute to their disease.
Although M. ovipneumoniae may be associated with early
pneumonia in domestic lambs (Bottinelli et al. 2017),
juvenile domestic sheep are usually resistant to M.
ovipneumoniae prior to weaning. Lambs born in persistently
infected flocks often become infected during their third
month of life (Table S3, available online in Supporting
Information). Bighorn lambs are apparently completely
susceptible to infection from birth (Besser et al. 2013),
despite the similar magnitude and timing of passive transfer
of maternal immunity in both species (Herndon et al. 2011,
Highland 2016). Passively transferred bighorn sheep
antibodies might not protect from colonization or it could
be that other forms of immunity are more important than the
maternally transferred antibody-mediated immune response
in defending the host from this pathogen (Plowright et al.
2013).
Domestic sheep herds usually harbor multiple strains of M.
ovipneumoniae simultaneously (Thirkell et al. 1990; Ionas
et al. 1991a,b; Parham et al. 2006). Therefore, intensive
sampling and strain typing are required to confirm or rule out
individual flocks as a source of M. ovipneumoniae transmis-
sion to bighorn sheep populations. In contrast, 1 or
occasionally 2 strains appear to predominate in bighorn
sheep populations (Cassirer et al. 2017). Immune response to
M. ovipneumoniae is apparently strain-specific in both
species, but disease outcomes of cross-strain infection are
more severe in bighorn sheep (Alley et al. 1999, Felts et al.
2016, Justice-Allen et al. 2016, Cassirer et al. 2017).
PNEUMONIA IN BIGHORN SHEEP
POPULATIONS
Die-Off Events
Many, if not most, bighorn sheep populations in the lower 48
states have endured all-age pneumonia die-offs (Western
Association of Fish and Wildife Agencies Wild Sheep
Working Group 2012). These epizootics are the most
obvious and dramatic manifestation of disease in bighorn
sheep populations. During pneumonia outbreaks when
animals are clinically ill, disease agents such as M.
ovipneumoniae and Pasteurellaceae, usually transmitted
through direct contact, may become airborne for short
distances (Dixon et al. 2002, Besser et al. 2014). Pathogens
can spread rapidly and expose nearly all individuals to
infection (Bernatowicz et al. 2016, Ramsey et al. 2016,
Cassirer et al. 2017). Severe, high mortality epizootics can
ultimately cause extirpation or functional extinction of
populations (Singer et al. 2000b); however, most pneumonia
outbreaks do not kill entire populations. We estimated a
median population decline of 48% (range ¼5–100%) in 82
bighorn sheep disease events reported in 7 states and 2
provinces (Fig. 1, Table S4). Causes of the considerable
divergence in mortality rates are not well understood but
might be explained by heterogeneity in host immunity,
pathogen virulence, and patterns of contact and transmission
(Hobbs and Miller 1992).
We detected 28 different strains of M. ovipneumoniae in 45
bighorn sheep populations tested in 6 western states (Fig.
2B,C; Tables S5 and S6, available online in Supporting
Information), each of which likely represents a separate
spillover event that caused an all-age epizootic when first
introduced. Domestic sheep and domestic goat M. ovipneu-
moniae lineages were both detected in bighorn sheep
populations, but most strains detected in bighorn sheep
fell within the domestic sheep clade (Kamath et al. 2016,
Cassirer et al. 2017; Fig. 2C).
Clusters of the same strain in inter-connected populations,
such as those along the border of Idaho, Oregon, and
Washington in Hells Canyon, USA; in the Pancake Range
Table 1. Comparison of M. ovipneumoniae infection in domestic and
bighorn sheep, USA, 1999–2016.
Bighorn sheep Domestic sheep
Infection outcome—
na€ıve adults
a
Bronchopneumonia No disease
Infection outcome—
lambs
a
Bronchopneumonia 20–
100% mortality
Coughing syndrome
<2% mortality
Age of lambs at
initial infection
a
<1 week Usually 8–12 weeks
Prevalence of
carriage
b
Low (median 22%) High (median 56%)
Seroprevalence
c
High (median 67%) Low (median 30%)
Strain diversity
within
populations
d
Usually 1 Usually many
a
Alley et al. (1999); Besser et al. (2008, 2014); Cassirer et al. (2013);
USDA (2011).
b
Samples (n¼1,267) from 40 bighorn sheep populations in California,
Idaho, Nevada, Oregon, Utah, and Washington and 47 domestic sheep
flocks (n¼2,508 samples) in 13 states across the United States (USDA
Aphis 2015).
c
Samples (n¼1,589) from 42 bighorn sheep populations in California,
Idaho, Nevada, Oregon, Utah, and Washington and 37 domestic sheep
flocks (n¼323 samples) across the United States (USDA Aphis 2015).
d
Parham et al. (2006), Cassirer et al. (2017).
Cassirer et al. Pneumonia in Bighorn Sheep 35
metapopulation of south-central Nevada, USA; and in the
southern Nevada metapopulation (Fig. 2B), likely reflect a
multiplier effect on a single spillover event when carrier
bighorn sheep spread the pathogen across neighboring
populations over time.
Multiple strains of M. ovipneumoniae observed within a
single bighorn sheep population (Fig. 2B) often represent
sequential pathogen invasion events. When a new strain is
introduced into a population with ongoing infection, it may
replace the existing strain or eventually fade out. Retrospec-
tive analysis in the intensively sampled Hells Canyon
metapopulation demonstrated a pattern of sequential spill-
overs and strain replacement or fadeout (Cassirer et al. 2017).
Additional data and genomic analyses will be useful for
confirming relationships among strains within and between
populations and for more rigorous modeling of the ancestral
phylogeny and transmission dynamics.
Pathogen Persistence
In 6 states (i.e., California, Idaho, Nevada, Oregon, Utah,
and Washington), 63% of 155 populations where infection
status is known, have been exposed to M. ovipneumoniae,
including most native (never extirpated) herds (Fig. 2A).
Exposure, as determined by the presence of M. ovipneumo-
niae-specific antibodies, indicates that at least some members
of the population have been infected during their lifetime.
Exposure does not confirm ongoing shedding, but infection
is often maintained in exposed populations by (generally)
asymptomatic carriers (Plowright et al. 2016, Cassirer et al.
2017).
Persistently infected populations have a high likelihood of
prolonged periods of disease in juveniles and occasionally
adults. High rates of pneumonia-induced lamb mortality
(20–100%) between 4 and 14 weeks of age are common and
reduce recruitment, limiting population growth or causing
declines when combined with other mortality factors (Ryder
et al. 1992, Enk et al. 2001, Smith et al. 2014, Smith et al.
2015). Some populations rebound (Coggins and Matthews
Figure 2. Exposure status and strain types of Mycoplasma ovipneumoniae detected in bighorn sheep populations in Washington, Oregon, Idaho, Utah,
California, and Nevada, USA. A) Exposure of bighorn sheep populations to M. ovipneumoniae, 1999–2016. We assigned exposure based on results of blood
serum samples (n10 from each population) submitted to the Washington Animal Disease and Diagnostic Laboratory for M. ovipneumoniae-specific serum
antibody testing. Populations were classified as positive if antibodies were detected in at least one sample. Populations were classifiedas negative if no antibodies
were detected from 15 samples. B) Spatial distribution of 28 M. ovipneumoniae genotypes (strains) obtained from bighorn sheep, 1984–2016. Each strain type
is identified by a different color (domestic sheep origin, n¼26) or hatching (domestic goat origin, n¼2). Strains of the same color represent well-supported
monophyletic clusters (posterior probability, PP >0.95) with 99.7% to 100% sequence identity (as in panel C). In general, strains that are shades of the same
colors are more closely related than strains of different colors. Pie charts indicate the proportional composition of strain types found at a given location over the
entire time period of sampling. Chart size is relative to sample size. C) Bayesian majority rule consensus phylogeny of M. ovipneumoniae strains derived from
bighorn sheep, with colors corresponding to strains shown in panel B. We based phylogenetic analyses on multilocus sequence typing data from 4 genetic loci
(16S, IGS, rpoB,gyrB). Node support is reported as PP, with circle size relative to value (only PP >0.60 shown). Scale bar indicates genetic distance in units of
nucleotide substitutions per site. Dashed line represents the M. ovipneumoniae lineage derived from domestic goats.
Figure 1. Population declines reported after pneumonia events in bighorn
sheep populations in Alberta and British Columbia, Canada; and Idaho,
Montana, Nebraska, Nevada, North Dakota, Oregon, Utah, and
Washington, USA, 1978–2016. Dashed line represents median mortality
of 48% in 82 pneumonia events. Data provided by state and provincial
agencies and the Western Association of Fish and Wildlife Agencies Wild
Sheep Working Group.
36 The Journal of Wildlife Management 82(1)
1992, Jorgenson et al. 1997), but in others there is no trend
towards recovery for decades (Manlove et al. 2016). In these
cases, the demographic costs of pathogen persistence can
outweigh the effects of the initial epizootic. Persistently
infected populations also pose a disease risk for adjacent
herds and, if they are used as source stock for translocations,
moving carriers can inadvertently spread infection over long
distances.
Chronically infected populations occasionally experience
years with no evidence of disease in juveniles or adults. In
approximately 20% of years following all-age disease
epizootics in Hells Canyon, lamb survival was high and
similar to that observed in unexposed populations (Cassirer
et al. 2013). These sporadic disease fadeouts may be due to a
delay or failure of M. ovipneumoniae transmission to
susceptible lambs, as opposed to local pathogen extirpation,
because pneumonia epizootics recur in subsequent years. A
single or even several years with apparently healthy rates of
lamb survival is not necessarily a harbinger of pathogen
fadeout and population recovery (Manlove et al. 2016).
Social behavior likely plays an important role in determin-
ing the patterns of pneumonia epizootics and disease
fadeout. Males are more likely to be directly associated
with spillover and spread within and across populations
during all-age outbreaks simply because they have larger
home ranges and make more long distance movements
(DeCesare and Pletscher 2006, O’Brien et al. 2014, Borg
et al. 2016). However, dam-lamb and lamb-lamb inter-
actions may be the most important routes of transmission in
persistently infected populations (Manlove et al. 2017).
Population substructure seems to protect some nursery
groups from pathogens (Manlove et al. 2014) perhaps
because no carrier dams are present. However, substructuring
also might decouple contact rates and associated pathogen
transmission from population size. If contact rates remain
high as populations decline, transmission may never drop
below the threshold required for pathogen extinction. This
form of frequency-dependent transmission is common in
social animals, and allows disease to persist at low population
sizes. This can ultimately lead to host extirpation especially
when combined with other stochastic events affecting small
populations (de Castro and Bolker 2005).
MONITORING POPULATIONS FOR
INFECTION AND DISEASE
All-age pneumonia epizootics are usually readily detected by
observations of sick and dying sheep where populations are
being actively monitored or are easily observed. However,
low mortality outbreaks and epizootics in small and remote
populations may be overlooked and underreported. Bighorn
sheep also die from other diseases and not all sheep with
clinical signs of respiratory disease (for example coughing)
have pneumonia. Necropsy and laboratory testing are
recommended when animals die from unknown causes, or
when pneumonia is suspected. Pneumonia epizootics should
be considered as a plausible cause when there is a sudden
decline in a bighorn sheep population, particularly if
followed by low recruitment.
Outside of all-age outbreaks, juvenile survival, particularly
during the first 4 months of life, is the best demographic
indicator of health status in bighorn sheep populations. Poor
survival to weaning, (4 months of age; Festa-Bianchet
1988), is the most sensitive signal of pneumonia-induced
mortality in lambs. In Hells Canyon, there was a 100%
probability of pneumonia being detected when survival to
weaning was <50% (Cassirer et al. 2013, Manlove et al.
2016; Fig. 3A); however, this relationship might differ in
areas with higher rates of non-disease-related neonatal
mortality. Recruitment of juveniles as yearlings and
population trend are less clear and specific metrics for
classification of health status. Although most populations are
stable or decline slowly during periods of persistent infection,
pneumonia also might be present when lamb:female ratios at
9–12 months (recruitment) are 0.30 (Fig. 3A), even if
populations are stable or slightly increasing (Fig. 3B, Table
S7 available online in Supporting Information).
Diagnostic testing procedures for respiratory disease are
continually changing as technology advances and knowledge
of the disease and disease agents evolve. Comprehensive
testing guidelines for wild sheep produced by the Western
Association of Fish and Wildlife Agencies Wildlife Health
Committee (2015) provide a good recent overview for a
broad array of pathogens. Sampling for M. ovipneumoniae
should be a part of any bighorn sheep health surveillance
protocol and can also be used to monitor potential sources of
domestic spillover. The most efficient diagnostic strategies
for detection vary by host species and by infection stage. In
acute infection (e.g., during all-age or lamb pneumonia
epizootics in bighorn sheep, or in 8–16-week-old domestic
lambs or kids in an enzootic flock), M. ovipneumoniae can be
detected by PCR tests in a high proportion of animals’ nasal
swabs or pneumonic lung tissues. Infection status of
domestic sheep and goat flocks is also best determined by
PCR tests on nasal swabs. Given the high M. ovipneumoniae
shedding prevalence in domestic sheep flocks (median 0.56;
Table 1), PCR testing on swab samples from 10 adults
should be sufficient (99% probability, binomial test) to detect
whether M. ovipneumoniae is present. Repeated sampling is
recommended to confirm negative status. In contrast,
determining the exposure status of chronically infected
bighorn sheep herds is most efficiently done by testing for
serum antibodies, given the relatively high seroprevalence
(median 0.67) and lower PCR prevalence in wild sheep
(Table 1). Blood serum samples from 15 animals are
generally adequate to determine exposure status if prevalence
is 0.25 (99% probability, binomial test). If no antibodies are
detected, the population can be considered unexposed, unless
samples are collected recently after transmission, prior to
immune response development. Nasal swabs from 18
animals should be adequate (85% probability) to detect
shedding by PCR in bighorn sheep populations with M.
ovipneumoniae prevalence of 0.10. Larger sample sizes may
be required to account for non-detection error associated
with field sampling and diagnostic testing (Walsh et al.
2016). Strain-type can be identified in PCR-positive
samples. Nasal or sinus swabs can also be collected from
Cassirer et al. Pneumonia in Bighorn Sheep 37
fresh or frozen dead animals including heads of hunter-
harvested bighorn sheep. Formalin-fixed paraffin-embedded
pneumonic lung tissue blocks routinely archived by most
diagnostic laboratories for histopathology also provide a
DNA source for investigating historical presence and strain
types of M. ovipneumoniae and other pathogens.
MANAGEMENT OF PNEUMONIA IN
BIGHORN SHEEP
Wildlife managers and veterinarians have tried many
techniques for controlling and mitigating respiratory disease
in wild sheep populations, including administering anti-
biotics (Coggins 1988, Rudolph et al. 2007, McAdoo et al.
2010), vaccination (Cassirer et al. 2001, Sirochman et al.
2012), mineral supplementation (Coggins 2006, Sirochman
et al. 2012), anthelmintic treatment (Miller et al. 2000,
Goldstein et al. 2005), selective culling (Edwards et al. 2010,
Bernatowicz et al. 2016, Ramsey et al. 2016), partial or
complete depopulation (Cassirer et al. 1996, McFarlane and
Aoude 2010, Bernatowicz et al. 2016), augmentation, and
limiting population size and dispersal. The variety of
methods employed, and the lack of clear successes, partially
reflects past uncertainty over the causative agents and
biological processes involved. The ad hoc nature of some of
the treatments also limits broader inference. More rigorous
testing of a broad ensemble of approaches for management is
needed to account for the inherent challenges and variability
associated with managing disease in free-ranging wildlife.
Large-scale pathogen eradication is rarely seen as a realistic
goal (Klepac et al. 2013), particularly in the presence of a
reservoir host, and indeed is not considered a viable option
for wild sheep respiratory disease. Instead, more practical
management objectives include controlling the spatial extent
or prevalence of the pathogen, facilitating natural pathogen
extinction, or reducing the demographic costs of infection
(Wobeser 2002, Joseph et al. 2013). Attempts to manage
bighorn sheep pneumonia fall broadly into 2 categories: 1)
strategies that directly aim to reduce exposure and
transmission such as preventing spillover, treatment with
antibiotics, vaccination, targeted culling of shedders, reduc-
ing population size or density, and population eradication;
and 2) strategies that aim to increase individual resistance or
herd resilience, including improving nutritional condition,
increasing genetic diversity, managing co-infection, or
increasing or modifying spatial structuring. Some approaches
(such as vaccination or density reduction) could conceivably
have application in both categories.
Preventing exposure, theoretically and in practice, offers
the most direct and effective method for disease control.
Managing transmission is a component of disease prevention
strategies for most zoonoses and other spillover diseases
(Ebinger et al. 2011, Viana et al. 2014) including test and cull
for brucellosis, oral vaccination for rabies, and reduction of
deer density for tuberculosis (Rupprecht et al. 1986, Schmitt
et al. 2002, Slate et al. 2005, Schumaker et al. 2012).
However, managing transmission can be a long-term and
costly endeavor. Promoting individual resistance and
population resilience has theoretical and empirical support
in a number of systems. In general, managing populations to
maximize their individual- or herd-level resilience makes
good sense (Stephen 2014). Whether increased resistance
and resilience can offset the costs of an exotic pathogen like
M. ovipneumoniae, which generally produces high mortality
rates in non-adapted but otherwise robust hosts, remains to
Figure 3. Receiver operating characteristic (ROC) curves identifying optimal lamb survival to weaning (black) and recruitment lamb:female ratios (gray) cut-
off values for correctly classifying A) presence of pneumonia and B) declining population trend in bighorn sheep populations in Hells Canyon, Idaho, Oregon,
and Washington, USA, 1997–2015 (Manlove et al. 2016). The yaxis indicates sensitivity and the xaxis indicates inverse specificity of lamb survival and
recruitment values. A perfect predictor would have a value of 1 on the yaxis and 0 on the xaxis for a score of 1 AUC (area under curve). The dashed line
represents values with no ability to predict categories (0.50 AUC). A) Lamb survival to weaning (AUC¼0.93) was an excellent predictor of health status and
performed better than recruitment (AUC ¼0.84). B) Recruitment (AUC ¼0.72) was a better predictor of population trend than juvenile survival to weaning
(AUC ¼0.66). Optimal cut-off values for assigning presence of pneumonia were juvenile survival to weaning of <0.60 (84% accuracy) or recruitment of <0.30
lambs:female (82% accuracy). The optimal cut-off value for classifying populations as declining was recruitment of <0.20 lambs:female (69% accuracy).
38 The Journal of Wildlife Management 82(1)
be seen. Below, we discuss past performance and future
potential of these management strategies in combating
bighorn sheep pneumonia.
Preventing Spillover and Pathogen Invasion
State and federal natural resource agencies have widely
instituted policies to prevent pathogen spillover by encour-
aging or requiring spatial separation between wild sheep and
domestic sheep and goats (Western Association of Fish and
Wildife Agencies Wild Sheep Working Group 2012, Bureau
of Land Management 2016). Federal and state policies are
informed by models, such as the USDA Forest Service’s
Bighorn Sheep Risk of Contact Tool (Woolever et al. 2015),
which incorporate bighorn sheep space use, habitat
preferences, foray probabilities, and demographics (Clifford
et al. 2009, Cahn et al. 2011, Carpenter et al. 2014, O’Brien
et al. 2014) to identify geographic locations with high risk of
domestic-wild sheep contact. These models allow compari-
son of proposed management alternatives and assessment of
population-level consequences for bighorn sheep. Resulting
actions may take the form of closing or retiring public
grazing allotments, altering their timing of use, trucking
rather than trailing sheep between pastures, or changing
grazing classification from domestic sheep or goats to other
livestock (USDA Forest Service 2010, Bureau of Land
Management 2017).
Other preventive management practices include capturing
or culling escaped domestic sheep on bighorn sheep ranges
and removing wild sheep observed near or commingling with
domestics. Outreach efforts on private and public lands have
encouraged landowner or public lands grazing permittee
cooperation in double-fencing domestic sheep flocks in wild
sheep habitat, using additional guard dogs, penning domestic
sheep and goats at night, not turning sick sheep out to
pasture, counting domestic sheep more frequently to better
detect and gather strays, notifying local wildlife officials if
wild sheep are observed near domestic sheep, and
encouraging use of other best management practices
(Western Association of Fish and Wildife Agencies Wild
Sheep Working Group 2012).
We are unaware of any formal evaluation of the success of
existing separation strategies in preventing new outbreaks,
though the regular appearance of new M. ovipneumoniae strains
in bighorn sheep herds suggests there is room for improvement.
Nevertheless, cross-species contact mitigation efforts almost
certainly play a crucial rolein reducing pathogen invasion. More
workisneededto assess the strengthsand weaknessesofexisting
approaches and to devise new andbetter strategies for managing
both domestic and wild sheep to reduce transmission risk.
Efforts are currently underway to investigate the feasibility of
developing and maintaining M. ovipneumoniae-free domestic
flocks, which could help reduce the significant risk of pathogen
transmission from small domestic sheep and goat herds on
private lands (Sells et al. 2015, Heinse et al. 2016, Cassirer et al.
2017).
Another paradigmatic approach to preventing pathogen
introduction is reducing density of wild sheep populations.
Associative studies (Monello et al. 2001, Sells et al. 2015)
report a positive relationship between wild sheep relative
density (or population size) and risk of respiratory disease
outbreaks. This relationship could mechanistically result
from larger or higher density populations occupying a greater
area and dispersing more widely or more often than smaller,
lower density herds, with the consequence that increased
density corresponds to increased contacts with neighboring
domestic sheep or infected wild sheep herds (Monello et al.
2001). Evidence, however, for a density-dependent relation-
ship in movements and dispersal in ungulates is limited and
equivocal (Loison et al. 1999, Long et al. 2008) and pre-
outbreak population sizes are often small (<50 to 200
animals) and do not differ from sizes of populations that
remain healthy (Monello et al. 2001, Shannon et al. 2014).
Many reintroduced bighorn sheep populations experience
robust or even exponential growth following initial
establishment. When these populations are exposed to
respiratory pathogens they often undergo die-offs followed
by a prolonged period of low lamb recruitment, limiting
recovery (Manlove et al. 2016). As a result, populations are
often largest just prior to outbreaks, leading to a statistical,
but not necessarily biological, association between popula-
tion size and outbreak risk. The expected biological processes
underlying a presumed density-dependent relationship are
not evident, such as declining population growth rate or
reduced juvenile recruitment (Jorgenson et al. 1997, Monello
et al. 2001). Therefore, it is unknown whether reducing
populations or keeping them small would actually mitigate
risk, or whether disease outbreaks are simply associated with
healthy, growing, and susceptible populations. Future work
could pursue the underlying mechanisms directly and
experimentally. Understanding the nature of observed
associations of pneumonia and population size in bighorn
sheep is needed to help minimize disease risk and maximize
the number and distribution of wild sheep on the landscape.
Translocations have been widely and successfully used to
increase the numbers, distribution, and genetic diversity of
bighorn sheep populations (Singer et al. 2000a, Hogg et al.
2006, Olson et al. 2012). Translocations also present a clear
risk for anthropogenically assisted pathogen introductions
and opportunities for exposure at release sites (Cunningham
1996, Deem et al. 2001, Sainsbury and Vaughn-Higgins
2012, Aiello et al. 2014). Moving animals known to be
positive for pneumonia pathogens into new ranges is risky
(Western Association of Fish and Wildlife Agencies
Wildlife Health Committee 2015). Mixing bighorn sheep
from populations known to harbor pathogens with na€ıve
animals, can and has, had poor results (Sandoval et al. 1987).
Even if a pathogen is present in both source and recipient
populations, immunity may not provide universal protection
(Dassanayake et al. 2009, Cassirer et al. 2017). Most state,
federal, and provincial agencies use health screenings to
inform wild sheep translocation decisions. Careful matching
of pathogen profiles, including relevant bacteria, viruses, and
parasites in source, recipient, and adjacent bighorn sheep
populations and selecting release sites with low risk of
contact with domestic sheep and goats are important for
translocation success. In practice, health surveys may be
Cassirer et al. Pneumonia in Bighorn Sheep 39
conducted a year in advance at the herd level and with
imperfect pathogen detection probabilities, resulting in
uncertainty surrounding an individual’s health status at the
time of translocation. Furthermore, M. ovipneumoniae strain
typing would not be expected to detect possible epitope
variation resulting in immune escape, and health screenings
are only as good as our knowledge of what to look for.
Improved molecular-based approaches for detecting and
describing pathogens and their associated virulence factors
are needed. Development of rapid animal-side tests is in
progress and, if successful, could also contribute to reducing
disease risks posed by translocations.
Reducing Transmission During and Post-Epizootics
A number of agencies have attempted to manage active
respiratory disease outbreaks. However, no management
action, absent population eradication, has successfully
stopped a pneumonia outbreak, and there is no evidence
that any intervention has consistently reduced morbidity,
mortality, or spread of disease. In part, this is due to the
unplanned nature of outbreaks and the inability to randomly
assign treatments and controls to matched populations to
reliably test for an effect. Nevertheless, efforts to halt
epizootics by administering antibiotic treatments (Sandoval
et al. 1987, Coggins 1988, Rudolph et al. 2007, McAdoo
et al. 2010), and by conducting random and selective culls
(Cassirer et al. 1996, Edwards et al. 2010, Bernatowicz et al.
2016, Ramsey et al. 2016) have generally had mixed or
negative results. In other wildlife species, depopulation has
been successfully employed to prevent spread between
populations, but culling zones or population segments to
stop the spatial spread of epidemics have met with limited
success (Wobeser 2002). Culling is rarely successful because
by the time an epidemic is detectable, transmission is usually
well under way; even if culling slows transmission, it is
unlikely to stop it given imperfect detection of symptomatic
animals, long infectious periods, ongoing contacts, and
undetected animal movements within and between pop-
ulations. Lack of success with antibiotics and vaccines
administered during or after outbreaks may be a function of
their low efficacy, targeting the wrong agent, or an inability
to administer them appropriately in most free-ranging
bighorn sheep populations.
Depopulation and reintroduction has occasionally been
used in an attempt to manage small, particularly poorly
performing herds struggling with persistent disease.
Although this method may be effective when all members
of the former herd are removed, significant effort is needed to
ensure complete removal and that the ongoing risk of
pathogen introduction is low. A current experimental
management effort offering an alternative to depopulation
of persistently affected populations exploits the relatively low
shedding prevalence of M. ovipneumoniae in bighorn sheep
by removing only chronic carrier females (Bernatowicz et al.
2016). The goal of this experiment is to stop the chain of
transmission from dams to lambs and facilitate pathogen
fade-out. If successful, this technique may be best applied to
small, accessible populations, where extensive testing is
feasible, and the stochastic mortality of chronic carriers may
bolster an active selective removal. In general, test-and-cull
success hinges on test sensitivity, animal handling opportu-
nity, pathogen prevalence, and the duration over which
management is implemented. Targeted removal works best
when a few individuals are responsible for most of the
transmission (Lloyd-Smith et al. 2005, Streicker et al. 2013)
and may require complete eradication of these carriers. For
example, although test-and-cull efforts to control brucellosis
in elk (Cervus canadensis) successfully met goals of reducing
local prevalence (Scurlock et al. 2010, Schumaker et al. 2012)
they never eradicated the disease, and upon the program’s
cessation, prevalence rapidly increased (Wyoming Game and
Fish Department 2016). Test-and-cull strategies would
ideally be timed to coincide with the lowest-possible
pathogen prevalence and the highest levels of immunity,
although we currently do not know when those minima and
maxima occur.
Managing for Resistance and Resilience
Managing disease by maximizing individual resistance or
population resilience has received renewed interest, partic-
ularly in the face of continuing challenges associated with
direct control of transmission. Theoretical and empirical
work across humans, domestic animals, and wildlife
suggests that manipulating physiological condition, genet-
ics, or co-infection can alter rates of morbidity and mortality
and reduce infection intensity, which may in turn feedback
on population-level dynamics (Beldomenico and Begon
2010). However, several studies have found that tradeoffs
often exist between enhancing disease resistance and
controlling transmission. For example, increasing food
supply can minimize parasite-induced mortality (Pedersen
and Greives 2008) but may also facilitate transmission
(Becker et al. 2015), managing co-infections can reduce
morbidity and mortality but can also accelerate pathogen
spread (Ezenwa and Jolles 2015), and metapopulation
structure can enhance disease spread while simultaneously
allowing higher numbers of hosts to survive (Hess 1996,
McCallum and Dobson 2002).
There are numerous examples of management actions
intended to bolster individual resistance and overall
population performance in struggling bighorn sheep
populations but little systematic evaluation as to their
efficacy. For example, there is no clear evidence of a causal
relationship between nutritional condition and susceptibility
to respiratory disease in bighorn sheep. Certainly the many
experiments in captivity show that optimally provisioned
bighorn sheep still succumb at high rates upon exposure to
respiratory pathogens. Disease resistance may be correlated
with genetic diversity (Luikart et al. 2008, Savage and
Zamudio 2011) and researchers continue to seek evidence of
host genetic resistance to respiratory disease, which might be
expected in herds that are demographically successful even in
the presence of long-term pathogen persistence but, to date,
a genetic basis has not been found for the susceptibility of
wild sheep to pneumonia (Gutierrez-Espeleta et al. 2001,
Boyce et al. 2011). Currently, multi-jurisdictional efforts are
40 The Journal of Wildlife Management 82(1)
underway to collect data on animal condition, genetics, and
pathogens to better understand their interactions with wild
sheep health.
At the population level, maximizing resilience might include
promoting large, widely distributed, genetically diverse
metapopulations with spatial structuring and a range of
behaviors (de Castro and Bolker 2005, Hess 1996). Indeed,
there is some evidence that larger wild sheep populations may
experience lower rates of mortality during pneumonia
epizootics and are more able to recover than their smaller
counterparts (Singer et al. 2001, Cassaigne et al. 2010).
Furthermore, increasing population substructure may create
asynchrony in transmission across groupsof animals. Although
this may not prevent epizootics and could actually increase
pathogen persistence at the herd or metapopulation level
(Grenfell and Harwood 1997, Swinton et al. 1998, Park et al.
2002), it might buffer against simultaneous population-wide
epizootics and facilitate stochastic pathogen extinction from
sub-herd or population segments (Cross et al. 2005). More
work is needed to determine whether or not spatial structuring
shields bighorn sheep populations from the worst outcomes of
disease and how population structure might affect disease
persistence. Current efforts are underway on a limited basis to
expedite formation of metapopulation structure by assisted
colonization of adjacent range. These manipulations may be
most applicable to large, healthy populations.
MANAGEMENT IMPLICATIONS
The extensive costs of pathogen introduction and transmis-
sion observed across a wide range of habitats and populations
indicate that preventing spillover is the most pressing
immediate priority for management of pneumonia in
bighorn sheep. Collaboration by wildlife and livestock
managers on research and in practice is needed to develop
more effective, sustainable approaches to reduce ongoing
pathogen transmission from domestic small ruminants to
wild sheep. Transmission risks posed by moving bighorn
sheep to expand populations are also recognized and should
be mitigated before translocations are conducted. In the
absence of spillover, selection on the host and the pathogen
may eventually lead to a less destructive relationship between
wild sheep and the bacteria involved in pneumonia.
However, considerable theory suggests that evolution toward
increased resistance or reduced virulence is not always
expected (Alizon et al. 2009, Osnas et al. 2015). Effective
tools are needed to actively restore persistently infected
stagnant or declining populations. A comprehensive exami-
nation of disease dynamics across populations to better
understand how recovery occurs naturally would be useful to
inform management of pneumonia in exposed populations.
In the long-term, agencies will need better strategies for the
management of larger interconnected bighorn sheep
populations for species viability. Engaging a diversity of
perspectives in the wildlife, domestic animal, and
health sciences through an inter- or trans-disciplinary
process could provide new directions or refine existing
approaches for management of healthy, resilient populations
(Choi and Pak 2007, Allen-Scott et al. 2015). Natural
experiments and designed experiments conducted in an
adaptive management framework can also accelerate learning
about complex natural systems (Walters and Green 1997,
Craig et al. 2012, Williams and Brown 2016). Inter-
jurisdictional collaboration can greatly facilitate and, in many
cases, is required for successful adaptive management.
Replicated interventions with clear hypotheses, objectives,
and defined expected outcomes accompanied by monitoring
of treatments and controls could greatly advance under-
standing in the face of uncertainty and speed progress
towards developing successful strategies for managing
pneumonia in wild sheep.
ACKNOWLEDGMENTS
Any mention of trade, firm or product names is for
descriptive purposes only and does not imply endorsement by
the U.S. Government. We thank J. Colby, H. Schwantje, W.
Jex, T. Nordeen, M. Nelson, B. P. Wiedmann, H. M.
Miyasaki, D. G. Whittaker, E. M. Rominger, and C. Ruhl
for providing data. This manuscript was improved by
comments from C. J. Butler, J. Gude, D. P. Walsh, and 2
anonymous reviewers and by discussions with the Western
Association of Fish and Wildlife Agencies Wild Sheep
Working Group Disease Management Venture. Additional
financial support was provided by Federal Aid to Wildlife
Restoration, Morris Animal Foundation grant D13ZO-081,
National Institutes of Health IDeA Program grants
P20GM103474 and P30GM110732, and Montana Univer-
sity System Research Initiative 51040-MUSRI2015-03.
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Associate Editor: Mark Boyce.
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Cassirer et al. Pneumonia in Bighorn Sheep 45
