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Restoration of a bighorn sheep population impeded by Mycoplasma ovipneumoniae exposure

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Bighorn sheep (Ovis canadensis) were once extirpated from the Black Hills region of South Dakota, USA, mirroring declining populations throughout North America. Since the 1960s, several reintroductions have occurred in the Black Hills to reestablish populations with varying success. We translocated 26 bighorn sheep from Alberta, Canada to the Black Hills (February 2015) to restore bighorn sheep to their historic range. Due to prior examinations of cause-specific survival, subsequent genetic diversity and disease prevalence were required to evaluate success of the restoration effort. We measured a mean allelic diversity of 5.23 (SE=0.44 [mean number of alleles]) and an observed heterozygosity of 0.71 (SE=0.06; expected = 0.64 ± 0.05) in the translocated individuals. Translocated bighorn sheep tested negative for Mycoplasma ovipneumoniae at capture. An autogenous vaccine was administered prior to release in an attempt to safeguard the translocated bighorn sheep from infection with a strain known to be resident in adjacent bighorn sheep populations. However, the year following the translocation, a different strain of M. ovipneumoniae was associated with a pneumonia outbreak that resulted in 57.9% mortality. Our results suggest that allelic diversity and heterozygosity were sufficient for long-term herd establishment, reducing the potential for founder effects. However, the This article is protected by copyright. All rights reserved. Deadwood bighorn sheep disease and diversity overwhelming mortality associated with pneumonia, via the transfer of M. ovipneumoniae from an unknown source, limited the success or our reintroduction efforts. Successful attempts to restore bighorn sheep to their historic ranges must consider and mitigate potential routes for M. ovipneumoniae transmission pre-and post-reintroduction.
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RESEARCH ARTICLE
Restoration of a bighorn sheep population impeded by
Mycoplasma ovipneumoniae exposure
Ty J. Werdel1,,2 , Jonathan A. Jenks1, Thomas E. Besser3, John T. Kanta4, Chadwick P. Lehman5,
Teresa J. Frink6
Bighorn sheep (Ovis canadensis) were once extirpated from the Black Hills region of South Dakota, U.S.A., mirroring
declining populations throughout North America. Since the 1960s, several reintroductions have occurred in the Black
Hills to reestablish populations, with varying success. We translocated 26 bighorn sheep from Alberta, Canada, to the
Black Hills (February 2015) to restore bighorn sheep to their historic range. Due to prior examinations of cause-specic
survival, subsequent genetic diversity and disease prevalence analyses were required to evaluate success of the restoration
effort. We measured a mean allelic diversity of 5.23 (SE =0.44 [mean number of alleles]) and an observed heterozygosity
of 0.71 (SE =0.06; expected =0.64 ±0.05) in the translocated individuals. Translocated bighorn sheep tested negative for
Mycoplasma ovipneumoniae at capture. An autogenous vaccine was administered prior to release in an attempt to safeguard the
translocated bighorn sheep from infection with a strain known to be resident in adjacent bighorn sheep populations. However,
the year following the translocation, a different strain of M. ovipneumoniae was associated with a pneumonia outbreak that
resulted in 57.9% mortality. Our results suggest that allelic diversity and heterozygosity were sufcient for long-term herd
establishment, reducing the potential for founder effects. However, the overwhelming mortality associated with pneumonia,
via the transfer of M. ovipneumoniae from an unknown source, limited the success or our reintroduction efforts. Successful
attempts to restore bighorn sheep to their historic ranges must consider and mitigate potential routes for M. ovipneumoniae
transmission pre- and post-reintroduction.
Key words: bighorn sheep, disease, Mycoplasma ovipneumoniae,Ovis canadensis, pneumonia, reintroduction
Implications for Practice
It is critical for management agencies to consider poten-
tial sources of respiratory pathogens, including domes-
tic sheep (Ovis aries) and goats (Capra hircus), near the
area of bighorn sheep reintroductions, as pneumonia was
the primary cause of death within the Deadwood bighorn
sheep population.
Attempts to restore bighorn sheep populations in areas
with a likelihood of pathogen transmission between
domestic sheep and goats may risk high probabilities of
failure.
Continued monitoring of reintroduced populations, with
respect to genetic diversity, disease, and selenium sam-
pling, is necessary to assess long-term health and tness,
and, consequently, success of restoration efforts.
Introduction
Prior to extirpation across much of their historic range, bighorn
sheep (Ovis canadensis) were abundant (Seton 1929) and
widely distributed across western North America (Buechner
1960). Various factors contributed to population declines,
including uncontrolled harvest, pathogen spillover from
domestic sheep (Ovis aries) and goats (Capra hircus), forage
competition from domestic livestock, habitat loss, and habitat
fragmentation (Buechner 1960). Contact with domestic sheep
can result in transfer of pneumonia pathogens, which may
lead to adverse population-level effects (Smith 1954; Buech-
ner 1960; Foreyt 1990; Coggins 2002; George et al. 2008;
Wehausen et al. 2011; Cassirer et al. 2018). Cross-species
transmission of pneumonia pathogens generally involves
Author contributions: TJW, JAJ, JTK, CPL conceived and designed the study; TJW
conducted eld data collection; JTK led reintroduction efforts; TJW, TEB, JAJ
conducted data analyses; TJW, JAJ, TEB, JTK, CPL, TJF wrote the manuscript; JAJ
secured funding.
1Department of Natural Resource Management, Edgar S. Mcfadden Biostress Lab,
South Dakota State University, Brookings, SD 57007, U.S.A.
2Address correspondence to T. J. Werdel, email werdel@ksu.edu
3Department of Veterinary Microbiology and Pathology, Washington State
University, Pullman, WA 99164, U.S.A.
4South Dakota Game, Fish and Parks, 4130 Adventure Trail, Rapid City, SD 57702,
U.S.A.
5South Dakota Game, Fish and Parks, 13329 US Highway 16A, Custer, SD 57730,
U.S.A.
6Department of Applied Sciences, Chadron State College, Burkhiser Complex,
Chadron, NE 69337, U.S.A.
Present address: Department of Horticulture and Natural Resources, Kansas State
University, Manhattan, KS 66506, U.S.A.
© 2019 Society for Ecological Restoration
doi: 10.1111/rec.13084
Supporting information at:
http://onlinelibrary.wiley.com/doi/10.1111/rec.13084/suppinfo
Restoration Ecology 1
Deadwood bighorn sheep disease and diversity
nose-to-nose contact (Blaisdell 1972; Foreyt & Jessup 1982;
Onderka et al. 1988; Foreyt 1990; Wehausen et al. 2011).
Selenium deciency can occur in all animal species, but
may severely limit the immunity response to disease in small
domestic ruminants (sheep and goats), and these patterns likely
extend to bighorn sheep (Hefnawy & Tórtora-Pérez 2010).
Lungworms (Protostrongylus spp.) and bacteria (Mannheimia
haemolytica,Bibersteinia trehalosi,Mycoplasma ovipneumo-
niae) may become causative agents of pneumonia when present
in conjunction with weakened immune systems (Onderka et
al. 1988; Foreyt 1990; Hefnawy & Tórtora-Pérez 2010; Besser
et al. 2012, 2013). Spillover of M. ovipneumoniae from domes-
tic sheep likely causes epidemic pneumonia in bighorn sheep
(Besser et al. 2013, 2014) and may have contributed to observed
large-scale mortality events (Besser et al. 2012). Furthermore,
pneumonia has been linked with increased mortality in numer-
ous populations of bighorn sheep and is likely the primary factor
limiting population growth (Cassirer & Sinclair 2010; Cassirer
et al. 2018). Although bighorn sheep ewes can become immune
to the effects of M. ovipneumoniae, this immunity is not trans-
ferred to lambs, resulting in reduced lamb survival and stagnant
population growth (Plowright et al. 2013).
The Black Hills region of South Dakota, U.S.A., was included
in the historic range of bighorn sheep, until extirpation of the
species from this area in the early 1900s (Seton 1929; Witte &
Gallagher 2012). Several reintroduction attempts were initiated
in the 1960s with successful restorations occurring in the Custer
State Park, Spring Creek, Rapid Creek, Sheridan Lake, Hell
Canyon, and Elk Mountain areas (Zimmerman 2008; SDGFP
2013; Parr 2015). Recent habitat-suitability modeling indicated
that the Deadwood area of the northern Black Hills, an area with
no previous reintroductions, would likely be a suitable site for
contemporary restoration attempts (SDGFP 2013).
Since the 1950s, there have been >1,000 attempts to rein-
troduce bighorn sheep populations back to their historic range
that have resulted in varying levels of success (Berger 1990;
Singer et al. 2000; Hedrick 2014; Parr 2015; WAFWA 2015;
Werdel et al. 2018). Reintroductions are generally focused in
areas where bighorn sheep have been extirpated or where rem-
nant populations require enhanced abundances or increases in
genetic diversity to remain viable (Buechner 1960; Zimmer-
man 2008). Our objectives were to evaluate a current bighorn
sheep restoration attempt in the Deadwood region of the north-
ern Black Hills. Specically, we report on how disease exposure
affected a bighorn sheep reintroduction in this region.
Methods
Study Area
We captured bighorn sheep on the Luscar Mine in Alberta,
Canada (5880593, 473136, 11N [a reclaimed mine habitat
utilized by a population of 1,000 bighorn sheep and the
source of >350 bighorn sheep translocated throughout North
America]; Teck 2012), and translocated to our study area, the
Deadwood region, located in the northern Black Hills in west-
ern South Dakota, U.S.A. (602979, 4911453, 13N) (Fig. 1).
This area encompasses 8,177 ha of public (5,203 ha) and pri-
vate (2,974 ha) land and is located adjacent to the Deadwood,
Lead, and Central City communities in Lawrence County,
South Dakota. The area is located in the central core of the
Blacks Hills, which is typied by canyons, mountain peaks,
and broad valleys (Hoffman & Alexander 1987). Elevations
range from 1,073 to 2,209 m above sea level and soils consist of
limestones, dolomites, and sandstones (Hoffman & Alexander
1987). Ponderosa pine (Pinus ponderosa) was the dominant tree
species and occurred in monotypic stands intermixed with small
stands of quaking aspen (Populus tremuloides) and paper birch
(Betula papyrifera) (Mcintosh 1949; Orr 1959; Thilenius 1972;
Richardson & Peterson 1974; Hoffman & Alexander 1987).
Common plant species included Kentucky bluegrass (Poa
pratensis), timothy (Phleum pretense), smooth brome (Bromus
inermis), sedges (Carex spp.), western wheatgrass (Pascopyrum
smithii), prairie dropseed (Sporobolus heterolepis), eabane
(Erigeron spp.) and yarrow (Achillea spp.) (Uresk et al. 2009).
This region receives 156cm of precipitation (70% in the
form of snow) and is, on average, cooler (5C) than more
southern areas within the Black Hills (Hoffman & Alexander
1987; NOAA 2017). Ungulate species co-occurring in the area
included mule deer (Odocoileus hemionus), white-tailed deer
(Odocoileus virginianus), and elk (Cervus elaphus). Potential
bighorn sheep predators included mountain lions (Puma con-
color; Smith et al. 2014; Wilckens et al. 2016; Jenks 2018),
coyotes (Canis latrans), bobcats (Lynx rufus; Parr et al. 2014),
bald eagles (Haliaeetus leucocephalus), and golden eagles
(Aquila chrysaetos). All domestic livestock known to transmit
pathogens to bighorn sheep, including sheep (Ovis aries)
and goats (Capra hircus), were located 5 km outside of our
study area.
Translocation and Data Collection
In February 2015, we captured 26 bighorn sheep (24 adults,
2 juveniles [<1.5 years]) at the Luscar Mine (Hinton, Alberta,
Canada). We baited two sites with alfalfa (Medicago sativa;
Schmidt et al. 1978) for 1 week prior to capture. We created two
modied 18 m ×18 m electromagnetic drop-nets and positioned
them over bait sites the night prior to capture. We observed the
bait sites the following morning and activated drop-nets when a
sufcient number of bighorn sheep (n>25; high proportion of
breeding age bighorn sheep ewes presumed pregnant at capture)
were positioned directly under the net. Net-trapped individuals
were immediately restrained (e.g. hobbled and blind-folded) by
biologists and transferred to on-site processing stations.
We determined age of captured adult male bighorn sheep
based on horn annuli (Geist 1966) and adult females via tooth
eruption and wear (Hemming 1969; Krausman & Bowyer
2003). We tted 21 adult females and 1 adult male bighorn
sheep with store-on-board global positioning system (GPS;
Model 2110D; 154 –155 MHz) radio collars (Advanced Teleme-
try Systems, Isanti, MN, U.S.A.). We tted two adult female
bighorn sheep with very high frequency (VHF; Model 2520B;
154–155 MHz) radio collars (Advanced Telemetry Systems).
We tted one female bighorn lamb and one male bighorn
2Restoration Ecology
Deadwood bighorn sheep disease and diversity
Figure 1. Locations of Black Hills National Forest (BHNF) domestic sheep (South Dakota Game, Fish and Parks [SDGFP] survey 2015), bighorn sheep
range (specic ranges labeled within the map [SDGFP GPS and VHF collar data]), mountain goat range (Battle Creek range labeled within the map [SDGFP
GPS collar data]), and the reintroduced Deadwood bighorn sheep study area, located in the Black Hills of South Dakota, U.S.A.
lamb with VHF (Model M4200M; 154–155 MHz) expandable
break-away radio collars (Advanced Telemetry Systems). All
collars were equipped with mortality sensors (activated after
8 hours of inactivity).
We uniquely marked all captured bighorn sheep with ear
tags (All American 3-Star Tags; Y-Tex Corporation, Cody,
WY, U.S.A.). We collected blood samples (Tiger-top tubes;
Model 367985; Becton, Dickinson and Company, Sparks, MD,
U.S.A.) and swabbed nasal and pharyngeal passages (BBL Cul-
tureSwab EZ; Model 220144; Fisher Scientic, Waltham, MA,
U.S.A.) of all individuals for disease testing. Swab and blood
samples were sent to Washington Animal Disease Diagnostic
Laboratory (WADDL) to test for the presence of Mycoplasma
ovipneumoniae and other pathogens related to pneumonia
(polymerase chain reaction [PCR] for detection, competitive
enzyme-linked immunosorbent assay [cELISA] for detection
of antibodies, and Pasteurella aerobic culture for bacteria iso-
lates). We sent blood samples to The Holm Research Center,
University of Idaho, for selenium analysis (concentration of
selenium in whole blood; Poppenga et al. 2012), and to the
National Veterinary Services Laboratories (Ames, IA, U.S.A.)
to test for diseases including Brucella ovis,B. abortus,B. suis,
Restoration Ecology 3
Deadwood bighorn sheep disease and diversity
Bovine Parainuenza-3 Virus (PI-3), Bovine Viral Diarrhea
Virus , and Bacillus thuringiensis (PCR and cELISA). The
University of Alberta retained blood, tissue, and hair samples
for DNA extraction and analysis. In addition, we administered
aM. ovipneumoniae vaccine (autogenous [samples of the South
Dakota strain previously documented in Custer State Park and
Rapid City herds, and maintained by WADDL, were sent to
MVP Labs, Omaha, NE, U.S.A., for vaccine development])
to all captured bighorn sheep (intramuscular and intranasal).
All capture and handling methods followed guidelines set forth
by Sikes and ACUC (2016) and were approved by the South
Dakota State University Institutional Animal Care and Use
Committee (Approval No. 14-096A).
We transported captured bighorn sheep intwo 6 m commer-
cial livestock trailers 2,130 km (24 hours conned) from cap-
ture site to release site (3.5 km southwest of Deadwood, South
Dakota, on private land). All livestock trailers were sterilized
with bleach prior to transport. We relocated all radio-collared
bighorn sheep a minimum of ve times per week between
February–August 2015 and May July 2016, and a minimum
of 3–4 times per week September 2015 April 2016 and
August–December 2016. All individuals were relocated using
a hand-held directional antenna (Model RA-23K, Telonics,
Inc., Mesa, AZ, U.S.A.) and portable receiver (Model TR-2,
Telonics, Inc.). Mortality events were located within 12 hours
of receiving mortality signals from collars; however, if decayed
or signicantly scavenged, we did not collect samples and we
recorded the mortality cause as unknown (5.26% [1/19] of mor-
tality events; Werdel et al. 2018). We transported recovered
bighorn sheep carcasses to the South Dakota Game, Fish and
Parks (SDGFP) laboratory in Rapid City, South Dakota, and
performed a necropsy to determine mortality cause. We sent the
respiratory tract, including the lungs and trachea, to WADDL
to test for detection of M. ovipneumoniae using PCR analy-
sis (cELISA analysis was also conducted to test for antibodies
if blood serum was obtainable; Besser et al. 2013); if detec-
tion was positive, M. ovipneumoniae was strain-typed using
multi-locus sequence typing (MLST; 4-locus) to characterize
strains using partial DNA sequences (a low target copy num-
ber, PCR inhibitors within the sample, or presence of closely
related bacteria in the sample may interfere with strain typing;
Cassirer et al. 2017).
Data Analysis
M. ovipneumoniae sampled from three bighorn sheep mor-
talities were strain typed at WADDL. We compared strains
from Deadwood, Custer State Park, and Spring Creek bighorn
sheep populations using the Clustal Omega Multiple Sequence
Alignment tool (http://www.ebi.ac.uk/Tools/msa/clustalo/). We
used 4-locus strain-type data (Cassirer et al. 2017) to build
a neighbor-joining tree (FigTree 1.4.3) to compare M. ovip-
neumoniae samples present between populations. We struc-
tured our neighbor-joining tree using 17 M. ovipneumoniae
samples from pathogen carriers in the Black Hills (Deadwood
bighorn sheep =3, Custer State Park bighorn sheep =1, Spring
Creek bighorn sheep =1, Battle Creek mountain goat [Oream-
nos americanus]=1, and domestic sheep =11).
We extracted genomic DNA from founder bighorn sheep
blood, tissue, and hair samples with a Dneasy Tissue Kit
(Qiagen Inc., Valencia, CA, U.S.A.). PCR volumes (10 μL)
contained 1.0–3.0 μLDNA,1×reaction buffer (Applied
Biosystems, Foster City, CA, U.S.A.), 2.0mm MgCl2, 200 μm
of each dNTP, 1 μm reverse primer, 1 μm dye-labeled forward
primer, 1.5 mg/mL BSA, and 1 U Taq polymerase (Applied
Biosystems). PCR products were run in a 6.5% acrylamide gel
and visualized on a LI-COR DNA analyzer (LI-COR Biotech-
nology, Lincoln, NE, U.S.A.). We analyzed genomic DNA
samples (n=21) using 13 microsatellite markers: BM1225,
BM4505, BMC1222, FCB266, MAF209, MAF36, MAF64,
MAF65, OarAE16, OarCP26, Rt9, TGLA122, TGLA387
(Maudet et al. 2004; Luikart et al. 2008). We calculated descrip-
tive statistics using GenAlEx (Peakall & Smouse 2006) and
GenePop (Raymond & Rousset 1995) software. Additionally,
we calculated observed (HO) and expected (HE) heterozygos-
ity, allelic diversity (A), effective alleles (AE), and tested for
deviations from Hardy– Weinberg equilibrium (HWE). We
reanalyzed genomic DNA samples (n=6; remaining founder
bighorn sheep), utilizing the same methods, of surviving
founder bighorn sheep post hoc, to determine if genetic diver-
sity (HOand A) was lost during the study period (performed a
paired sample ttest to test for signicant differences).
Results
We did not detect Mycoplasma ovipneumoniae in individual
bighorn sheep prior to translocation (Table S1). Bacteria present
in individuals included Bibersteinia trehalosi, Beta hemolytic B.
trehalosi,Mannheimia spp., and Trueperella pyogenes (Tables 1
& S1). On average, selenium levels of captured bighorn sheep
were 0.46 μg/g (μg Se/g whole blood) prior to translocation
(range =0.28 –0.61 μg/g). Bovine parainuenza virus-3 was
present in 7.7% individuals (n=2), and remaining individuals
(n=24) were disease free.
Our prior study documented 19 mortalities (7 of 26 translo-
cated bighorn sheep survived the study period), 57.9% (n=11)
were pneumonia related, within the translocated Deadwood
bighorn sheep herd between February 2015 and January 2017
(Werdel et al. 2018). The only adult ram was euthanized due
to presumed contact with domestic sheep; however, the ram
displayed no signs of poor condition, and post-mortem analyses
revealed that it was PCR and cELISA negative for M. ovip-
neumoniae (Table S1). Eight carcasses tested positive (PCR;
cELISA positive =3; Table S1) for M. ovipneumoniae.We
euthanized three bighorn sheep ewes that displayed pneumonic
symptoms, and post-mortem investigations conrmed M. ovip-
neumoniae (PCR positive; cELISA positive =1; Table S1). The
11 M. ovipneumoniae–positive bighorn sheep mortalities dis-
played varying stages of consolidated lung tissue (lungs fused
to chest cavity) and infection (lesions exhibiting discolored
4Restoration Ecology
Deadwood bighorn sheep disease and diversity
Table 1 . Frequency and prevalence (%) of various pathogens in translocated Deadwood bighorn. Sheep sampled at capture (12 February, 2015). Washington
Animal Disease Diagnostic Laboratory (WADDL) tested swab and blood samples for the presence of Mycoplasma ovipneumoniae (polymerase chain reaction
[PCR] for detection and competitive enzyme-linked immunosorbent assay [cELISA] for detection of antibodies) and other pathogens related to pneumonia
(Pasteurella aerobic culture for bacteria isolates). Results for M. ovipneumoniae were negative among all PCR and cELISA tests. A more detailed description
of individual demographics, disease analyses, and selenium test results can be found in Table S1.
Mycoplasma
ovipneumoniae
Bibersteinia
trehalosi
Beta Hemolytic
B. trehalosi Mannheimia sp.
Trueperella
pyogenes
Deadwood bighorn sheep (n=26) 0 20 (76.9%) 6 (23.1%) 3 (11.5%) 1 (3.9%)
Figure 2. Neighbor-joining tree of 4-locus Mycoplasma ovipneumoniae strain types illustrating diversity among Black Hills South Dakota populations
created using FigTree 1.4.4 (http://tree.bio.ed.ac.uk/software/gtree/). Strain difference =horizontal line distance (scale is relative between samples);
identical strains connected by vertical line. Numbers and letters following “domestic sheep” indicate ock and sheep number (i.e. domestic sheep 1a-2011 is
from ock “1”, is individual “a”, and was sampled in 2011). Deadwood bighorn sheep are highlighted and BH numbers following “Deadwood bighorn
sheep” are unique identication numbers.
discharge) during necropsy (Werdel et al. 2018). M. ovipneu-
moniae detected in mortality samples of the translocated Dead-
wood bighorn sheep herd was strain typed (n=3) and an iden-
tical, single strain was detected. This outbreak strain differed
from M. ovipneumoniae strains detected in Black Hills bighorn
sheep, domestic sheep, and mountain goat populations (Fig. 2).
We genotyped and analyzed 21 unique (viable samples
appropriate for analysis) hair samples collected from indi-
vidual bighorn sheep. Observed heterozygosity (HO)ofour
bighorn sheep population was 0.71 (SE =0.06) and expected
heterozygosity (HE) was 0.64 (SE =0.05). Heterozygosity per
locus ranged from 0.10 to 0.95. Number of alleles per locus
(A) ranged from 2 to 7 (mean =5.23, SE =0.44) and aver-
age number of effective alleles (AE) was 3.19 (SE =0.32)
(Tables 2 & 3). We found a single deviation from HWE at locus
BMC1222 (p=0.04). Mean HOof surviving founder bighorn
sheep (n=6), analyzed post hoc, was not signicantly different
(p=0.72, HO=0.69 [SE =0.08]), while mean of Awas signif-
icantly lower (p<0.001, HO=3.62 [SE =0.39]) from genetic
diversity (HOand A) at capture (Fig. 3).
Discussion
Bighorn sheep translocated from a healthy, genetically diverse
native population in Alberta succumbed to a pneumonia out-
break the year following their release into the Black Hills
of South Dakota. The translocated sheep were naïve to the
pneumonia pathogen M. ovipneumoniae known to be present
in adjacent bighorn sheep populations, but were inoculated
with an autogenous M. ovipneumoniae vaccine prior to release.
However, pneumonia-related mortalities were associated with
aM. ovipneumoniae infection that differed from the vaccine
strain. Although we found that individual translocated bighorn
sheep were also carriers, at the time of capture, of multiple
bacteria that have been implicated in pneumonia epidemics, we
only observed disease-induced mortality following infection
with M. ovipneumoniae. This is consistent with previous studies
that have identied M. ovipneumoniae as the primary etiologic
agent for epizootic pneumonia in bighorn sheep (Besser et al.
2012). Similar extensive bighorn sheep mortality events have
been documented as early as 1924 (Marsh 1938), but more
recently in multiple studies on bighorn sheep (Festa-Bianchet
1988; Cassirer & Sinclair 2010; Besser et al. 2012; Smith et al.
2014), as well as mountain goats (Blanchong et al. 2018), and
Restoration Ecology 5
Deadwood bighorn sheep disease and diversity
Table 2 . Summary of genetic variation in the translocated Deadwood
bighorn sheep herd population. N=number of samples, A=number of
alleles per locus (allelic richness), AE=number of effective alleles per
locus, HO=observed heterozygosity, and HE=expected heterozygosity
in translocated Deadwood bighorn sheep sampled at capture (12 February,
2015).
Locus NAA
EHOHE
BM1225 21 5 3.89 0.81 0.74
BM4505 21 4 2.43 0.76 0.59
BMC1222 21 2 1.21 0.10 0.17
FCB266 21 4 2.58 0.62 0.61
MAF209 21 4 2.71 0.76 0.63
MAF36 21 4 3.14 0.91 0.68
MAF64 21 7 4.18 0.76 0.76
MAF65 21 5 4.01 0.81 0.75
OarAE16 21 7 5.80 0.95 0.83
OarCP26 21 7 3.79 0.86 0.74
Rt9 21 6 3.12 0.76 0.68
TGLA122 21 7 2.01 0.43 0.50
TGLA387 21 6 2.58 0.67 0.61
Mean 21.00 5.23 3.19 0.71 0.64
SE 0.00 0.44 0.32 0.06 0.05
their susceptibility to M. ovipneumoniae. The strain of M. ovip-
neumoniae found in the translocated Deadwood bighorn sheep
(n=3) post-release differed from M. ovipneumoniae strains
previously discovered within populations of bighorn sheep,
domestic sheep, and mountain goats occupying varying regions
of the Black Hills. This suggests that the underlying cause was
contact with an unrecognized non-bighorn sheep reservoir host,
or possibly an individual bighorn sheep that was not sampled.
We were unable to assess the efcacy of the vaccine adminis-
tered at capture, as we were unable to obtain sufcient heart
blood from carcasses to evaluate titers for M. ovipneumoniae
(cELISA). The strain of M. ovipneumoniae utilized in the vac-
cine development was not observed in the Deadwood bighorn
sheep; the vaccine may not have induced an antibody response,
induced antibodies may not have been protective, antibody
levels may have diminished between inoculation and exposure,
or antibodies may not have been protective across strains.
The translocated Deadwood bighorn sheep herd had average
selenium level of 0.46μg/g, with a range of 0.280.61 μg/g.
These results suggest that the original habitat utilized by the
translocated Deadwood bighorn sheep provided more than
adequate levels of selenium, but slightly lower than reported
by Parr (2015) (0.54– 1.42 μg/g, mean =0.83 μg/g) in bighorn
sheep occurring in the Elk Mountain region of the Black Hills.
This disparity is likely a result of high selenium levels found in
soils in the Elk Mountain region, where vertical transmission
of selenium likely takes place (Rosenfeld & Beath 1964; Parr
2015). Due to our relatively high selenium levels, we do not
believe that background levels affected the immunity of the
Deadwood bighorn sheep; however, it is a factor that may be
important in other translocations.
Heterozygosity (the condition of having differing alleles at
a single locus) and allelic diversity (average number of alleles
per locus) are measurements of genetic diversity; higher levels
of genetic diversity are associated with improved tness (Miller
et al. 2012). We found high levels of observed heterozygosity
(HO) and allelic diversity (A) in our translocated Deadwood
bighorn sheep population at capture. Furthermore, our ndings
are higher compared to previous studies in South Dakota (Zim-
merman 2008; Parr et al. 2016), Oregon, and Nevada (Whit-
taker et al. 2004). This comparison is complicated, however,
because different loci were sampled in each study. After cen-
soring bighorn sheep mortalities from genetic analysis post hoc,
there was a considerable decline in remaining levels of HO
and A(difference in Awas statistically signicant [p<0.001]).
High levels of genetic diversity in the founder population mit-
igated the loss of genetic diversity post pneumonia die-off in
the Deadwood bighorn sheep population, but there was not an
observed benet of increased resistance to M. ovipneumoniae;
the small population size will also contribute to a loss of genetic
diversity in subsequent generations if supplemental rams are
not introduced. Future restoration efforts should maximize indi-
vidual releases of adult ewes to ensure high genetic diversity
Table 3 . A compilation of four studies comparing population size (N), year sampled, observed heterozygosity (HO), average number of alleles (A), and
effective number of alleles (AE) (Whittaker et al. 2004; Zimmerman 2008; Parr 2015). *Comparisons of HO, A,andAEare indirect due to differing loci
sampled between studies.
Population NYear HO*A*AE* Source
Deadwood, SD 21 2015 0.71 5.23 3.19 This paper
Elk Mountain, SD 100 2013 0.59 4.33 2.55 Parr (2015)
Badlands National Park, SD 83101 1992 0.51 4.20 2.23 Zimmerman (2008)
Badlands National Park, SD 71–72 1996 0.54 3.20 2.1 Zimmerman (2008)
Badlands National Park, SD 66 1998 0.50 3.20 2.03 Zimmerman (2008)
Badlands National Park, SD 67 2004 0.47 2.20 1.66 Zimmerman (2008)
Hart Mountain, OR 270 1999 0.31 2.22 Unk Whittaker et al. (2004)
Aldrich Mountain, OR 205 1998 0.28 2.22 Unk Whittaker et al. (2004)
John Day River, OR 310 1999 0.36 2.44 Unk Whittaker et al. (2004)
Steens Mountain, OR 185 1999 0.29 2.22 Unk Whittaker et al. (2004)
Leslie Gulch, OR 125 1999 0.29 2.33 Unk Whittaker et al. (2004)
Santa Rosa Mountains, NV 295 2000 0.53 3.78 Unk Whittaker et al. (2004)
6Restoration Ecology
Deadwood bighorn sheep disease and diversity
Figure 3. Boxplots of observed allelic diversity (A) and observed heterozygosity (HO) of Deadwood bighorn sheep at the time of capture (12 February,
2015), compared with Aand HOafter the Deadwood bighorn sheep pneumonia die-off event (10 January, 2017).
post mortality, and because rams can initiate M. ovipneumo-
niae epizootics via interactions with domestic livestock, releases
must balance maintenance of genetic diversity with risk of dis-
ease transmission when deciding on number of rams to include.
Translocated animals are much more vulnerable to disease risk
(Plowright et al. 2013), so placing emphasis on a genetically
diverse source population for translocations is essential. Despite
the epizootic, the Deadwood bighorn sheep population con-
sisted of 23 bighorn sheep (2 rams, 16 ewes, 5 lambs) as of
September 2019. Our ndings may be relevant to other species
involved with restoration efforts when risk of disease transmis-
sion is high (e.g. black-footed ferrets [Mustela nigripes]).
For future reintroductions of bighorn sheep to be successful,
intensive pre- and post-sampling and monitoring (i.e. disease
risk, genetic diversity) is required. Our study suggests that suc-
cess of bighorn sheep reintroductions is related to transmission
of pneumonia agents from resident bighorn sheep and domestic
sheep and goat hosts. Wildlife managers must identify potential
pathogen transmission routes originating from bighorn sheep
or domestic livestock. Reoccurring testing of nearby livestock
is encouraged if restoration efforts for bighorn sheep popula-
tions are to be successful. Creating a complementary relation-
ship between local wildlife agencies and livestock producers
will benet both bighorn sheep and domestic sheep and goats.
If there is no reasonable presumption of complete separation
of bighorn sheep and domestic sheep and goats, reintroductions
will likely have a high probability of failure, and should be
avoided (WAFWA 2012).
Acknowledgments
Financial support for this project was provided by Federal
Aid to Wildlife Restoration administered through South Dakota
Department of Game, Fish and Parks (Study Number 7556). We
thank South Dakota Department of Game, Fish and Parks, Civil
Air Patrol, Deadwood Police Department, Lawrence County
Sheriff’s Ofce, and private property owners in the Deadwood
area for their assistance and property access. We thank B. Juarez
for assistance with data analyses. We thank T. Hafey, K. Cud-
more, J. Doyle, J. Clark, and C. Werdel for their assistance
with monitoring, capturing, and euthanizing bighorn sheep dur-
ing the study period. We thank A. Ahlers for review of the
manuscript.
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Supporting Information
The following information may be found in the online version of this article:
Table S1. Translocated Deadwood bighorn sheep (n=26) demographics, dis-
ease analyses (conducted by Washington Animal Disease Diagnostic Laboratory),
and selenium test results (conducted by The Holm Research Center, University
of Idaho).
Coordinating Editor: Jacob Bowman Received: 19 September, 2019; First decision: 21 October, 2019; Revised: 4
November, 2019; Accepted: 15 November, 2019
Restoration Ecology 9
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Resumen Los lineamientos para el uso de especies de mamíferos de vida silvestre en la investigación con base en Sikes et al. (2011) se actualizaron. Dichos lineamientos cubren técnicas y regulaciones profesionales actuales que involucran el uso de mamíferos en la investigación y enseñanza; también incorporan recursos nuevos, resúmenes de procedimientos y requisitos para reportes. Se incluyen detalles acerca de captura, marcaje, manutención en cautiverio y eutanasia de mamíferos de vida silvestre. Se recomienda que los comités institucionales de uso y cuidado animal (cifras en inglés: IACUCs), las agencias reguladoras y los investigadores se adhieran a dichos lineamientos como fuente base de protocolos que involucren mamíferos de vida silvestre, ya sea investigaciones de campo o en cautiverio. Dichos lineamientos fueron preparados y aprobados por la ASM, en consulta con profesionales veterinarios experimentados en investigaciones de vida silvestre y IACUCS, de quienes cuya experiencia colectiva provee un entendimiento amplio y exhaustivo de la biología de mamíferos no-domesticados. La presente versión de los lineamientos y modificaciones posteriores están disponibles en línea en la página web de la ASM, bajo Cuidado Animal y Comité de Uso: (http://mammalogy.org/uploads/committee_files/CurrentGuidelines.pdf). Recursos adicionales relacionados con el uso de animales de vida silvestre para la investigación se encuentran disponibles en (http://www.mammalsociety.org/committees/animal-care-and-use#tab3).
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The book covers population dynamics, diet, nutrition, diseases, behavior, and genetics of mountain lions occupying the Black Hills region. It explores the impact of a changing prey base on population growth and decline, movements within and away from the region, and hunting on the species; discusses interactions between the cats and livestock; and examines local people’s evolving perceptions of mountain lions. Provides a unique look into how a large, secretive predator recolonized an isolated region of North America.