J o u r n a l o f W i l d l i f e D iseases, 4 8 (1 ), 2 0 1 2 , p p . 6 8 -7 6
© W ild life D is e a s e A s s o cia tio n 2012
PREVALENCE OF ANTIBODIES TO CANINE PARVOVIRUS AND
DISTEMPER VIRUS IN WOLVES IN THE CANADIAN
ROCKY MOUNTAINS
Brynn Nelson,^ Mark Hebblewhite,^^^ Vanessa Ezenwa,^^^ Todd Shury,^ Evelyn H. Merrill,"^
Paul C. Paquet,® ® Fiona Schm legelow/ Dale Selp,® Geoff Skinner,® and Nathan Webb^°
^ W ildlife Biology Program, D epartment of Ecosystem and C onservation Sciences, University of M ontana, Missoula,
M ontana 59812, USA
^ W ildlife Biology Program, Division of Biological Sciences, University of Montana, Missoula, Montana 59812, USA
^ Departm ent of V eterinary Pathology, W estern College of V eterinary Medicine, Saskatoon, Saskatchewan S7N 5B4,
Canada
"* Departm ent of Biological Sciences, University of Alberta, Edmonton, A lberta T6G 2E9, Canada
® R alncoast C onservation Foundation, PO Box 86, Denny Island, British Colum bia VOT 1B0, Canada
® Faculty of Environmental Design, University of Calgary, 2500 University Drive NW, Calgary, A lberta T2N 1N4, Canada
^ Departm ent of Renewable Resources, University of Alberta, Edmonton, A lberta T6G 2E9, C anada
® British Colum bia M inistry of Forests, 1011 4th Ave., Prince George, British Colum bia V2L3H9, Canada
® PO Box 10, Parks Canada, Jasper National Park, Jasper, A lberta T1K 1M0, C anada
Departm ent of Biological Sciences, University of Alberta, Edmonton, A lberta T6G 2E9, Canada
C urrent address: Odum School of Ecology, University of Georgia, Athens, Georgia 30602, USA
Corresponding author (email: m ark.hebblew hlte@ um ontana.edu)
W ild cam lvores are often exposed to diseases via co n tact w ith p erid o m estic host
species th a t travel thro u g h th e w ildland-urban interfaces. To d eterm in e th e antibody prevalences
an d relationships to h u m an activity for twro com m on can id p athogens, w e sam pled 99 wolves
(Canis lupus) from 2000 to 2008 for antibodies to canine parvovirus (CPV) an d canine d istem p er
virus (CE)V) in B anff and Jasp er N ational Parks an d su rro u n d in g areas o f th e C anadian Rockies.
This p o pulation was th e source for wolves re in tro d u c ed into th e N o rth ern Rockies o f th e US. O f 99
wolves sam pled, 94 h ad d etectab le antibody to CPV (95% ), 24 w ere antibody-positive for CD V
(24% ), and 24 h a d antibodies to b o th pathogens (24% ). W e te ste d w h e th e r antibody prevalences
for CPV and C D V w ere h ig h er closer to h u m an activity (roads, tow n sites. F irst N ation reserves)
an d as a function o f sex and age class. W olves > 2 yr old w ere m ore likely to b e have antibodies to
CPV. F o r CD V , m ale wolves, wolves ^ 2 yr, an d those closer to F irst N ation reserves w ere m ore
likely to have antibodies. Overall, how ever, w e fo u n d m inim al su p p o rt for h u m an influence on
antibody prevalence for C D V an d CPV. T he sim ilarity b etw een o u r antibody p revalence results
an d results from re c e n t studies in Yellowstone N ational P ark suggests th a t at least in th e case of
CD V , an d p erh ap s CPV, th ese could b e im p o rta n t p athogens w ith p o ten tial effects on w olf
populations.
Key words: B anff N ational Park, canine d istem p e r virus, canine parvovirus, Canis lupus,
carnivore, Jasp er N ational Park, wolf.
ABSTRACT;
INTRODUCTION
D isease Jias b e e n re c e n tly re c o g n iz e d as
a grow ing w o rld w id e c o n serv atio n th re a t
fo r m an y carn iv o res (M u rra y e t ah, 1999).
F o r exam ple, w olves {Canis lu p u s) a n d
m an y o th e r carn iv o res have th e p o te n tia l to
b e e x p o sed to c a n in e parv o v iru s (CPV ) a n d
ca n in e d is te m p e r virus (C D V ) n o t only
fro m o th e r wolves, b u t also fro m h o sts su ch
as d o m estic a n d fe ra l dogs (C anis fa m iliaris) a n d a lte rn a te h o sts su ch as coyotes
(C a n is la tra n s) a n d r e d foxes (V u lp es
v u lp e s ; L a u r e n s o n , 1998; C le a v e la n d
e t ah, 2000; A lm b e rg e t ah, 2010). P rev a-
len c e o f in fectio n witJi carn iv o re patJiogens
sucJi as C P V a n d C D V te n d s to in c rea se
a m o n g Irosts in u rb a n areas b e c a u se o f
increased contact am ong individuals (W oodro ffe e t a l , 2004), in c re a sin g spillover
transm ission rates from th e reservoir hosts
for wild canids (Steinel e t al., 2001). F o r
ex am ple, M ain k a e t al. (1994) fo u n d
th a t dom estic dogs w ere th e m ain source o f
C P V a n d C D V in fectio n s in g ian t
p andas (Ailuropoda m elanoleuca) in China.
D om estic and feral dogs have also b ee n
identified as th e m ajor reservoir hosts for
C PV an d C D V in Africa (L aurenson e t al.,
1998; C leaveland e t al., 2000).
68
NELSON ET AL.—WOLE SEROLOGY IN THE CANADIAN ROCKIES
B o th C P V a n d C D V a re p rim a rily
s p re a d b y c o n ta c t b e tw e e n in d iv id u als,
a n d th e y c a n s p r e a d r a p id ly b e c a u s e
c a rn iv o re s s u c h as w o lv es h a v e h ig h
d isp e rsa l ra te s, d isp e rse o v er w id e d is­
ta n c e s , a n d h a v e la rg e h o m e ra n g e s
(M u rra y e t ah, 1999; W o o d ro ffe e t ah,
2004). C a n in e p arv o v iru s is o fte n s p re a d
th ro u g h fecal-o ral c o n ta c t, it cau ses d ia r­
rh e a , fe v e r, a n d d e h y d ra tio n (M u rra y
e t ah, 1999; S o b rin o e t ah, 2008), a n d it
in fe c ts a b r o a d ra n g e o f age classes;
h o w e v e r, m o rta lity p rim a rily o c c u rs in
p u p s less th a n 4 m o o ld (S tein el e t ah,
2001; C a rm ic h a e l, 2005). C a n in e d is te m ­
p e r virus is a m o rb illiv iru s th a t in fe c ts all
ages o f c a n id s (S o b rin o e t ah, 2008),
c a u s in g p n e u m o n ia , e n c e p h a litis , a n d
so m e tim e s d e a th (M u rra y e t ah, 1999;
Z a rn k e e t ah, 2004). C a n in e p arv o v iru s has
a lo w e r c a s e fa ta lity r a te th a n C D V
(M u rra y e t ah, 1999). F o r m o re d etail
a b o u t C P V a n d C D V , see M u rra y e t al.
(1999), S o b rin o e t al. (2008), a n d A lm b e rg
e t al. (2010). B o th C P V a n d C D V in fe c t
m a n y c a rn iv o re sp ecies, a n d th e y a re o fte n
s p re a d b y d o m e stic ca n id s (M u rra y e t ah,
1999; W o o d ro ffe e t ah, 2004). C a rn iv o re
r e in tr o d u c tio n a n d r e s to r a tio n e ffo rts
m u st th e re fo re c arefu lly c o n s id e r d isease
as an im p o rta n t risk fa c to r in c o n serv atio n
p la n s (M u rra y e t ah, 1999).
R e c e n t w o lf re in tro d u c tio n su ccess in
th e w e s te rn U S (B angs a n d F ritts , 1996;
U S F ish a n d W ildlife Service, 2009) has
re s u lte d in a p o p u la tio n o f o v e r 1,500
w olves. R ecen tly , in th e C r e a t L akes a n d
Y ellow stone N a tio n a l P a rk w o lf p o p u la ­
tio n s, M ech e t al. (2008) a n d A lm b e rg
e t al. (2009) re p o r te d e v id e n c e th a t C P V
a n d C D V in fe c tio n h a d n eg ativ e effects o n
p u p survival a n d h e n c e p o p u la tio n grow th.
E ffectiv e w o lf m a n a g e m e n t p la n s sh o u ld
a c k n o w le d g e th e p o te n tia l p o p u la tio n
im p a c ts o f d isease o u tb re a k s o n w olves
(e.g., M o n ta n a F ish , W ildlife, a n d P arks,
2002). M an y re c o v e rin g w o lf p o p u la tio n s
a re e x p o sed to o v e rla p p in g h o st sp ecies
a n d a re clo se to h u m a n activity, p o te n tia lly
in c re a s in g d ise a se e x p o su re . F lo w ev er,
69
c o m p a re d to A frican carn iv o res, little is
k now n a b o u t th e effects o f h u m a n activity
o n w o lf diseases.
W e e x a m in e d p re v a le n c e o f a n tib o d ie s
to C P V a n d C D V in th e C a n a d ia n R ockies,
th e o rig in a l s o u rc e fo r r e in tr o d u c e d
w olves in to th e n o rth w e st U S (B angs an d
F ritts, 1996). W e p r e d ic te d th a t p re v a ­
le n ce s o f a n tib o d ie s to b o th p a th o g e n s
w o u ld in c re a se clo se r to h u m a n activity
(e.g., tow ns), b e c a u se o f h ig h e r p o p u la tio n
d e n s itie s o f h o s t re s e rv o irs (d o m e stic
dogs) a n d a lte rn a te h o sts in valley b o t­
tom s. W e also p re d ic te d th a t a n tib o d y
p re v a le n c es w o u ld b e h ig h e r n e a r F irst
N atio n reserv es, b e c a u se feral do g p o p u la ­
tions asso ciated w ith F irs t N atio n reserv es
are o fte n u n v a c c in a ted (e.g., W o odroffe
e t ah, 2004). W e d e te rm in e d th e o c c u r­
re n c e o f th e se p a th o g e n s in w olves at
v ary in g d ista n c e s fro m h u m a n activ ity
m e a s u re d as d ista n c e s to to w n s. F irs t
N atio n reserv es, a n d roads. W e ex am in ed
th e effects o f age a n d sex on C P V a n d C D V
a n tib o d y p re v a le n c e (Z arnke e t ah, 2004),
a n d p re d ic te d th a t p re v a le n c e w o u ld in ­
c re a se w ith age a n d h o m e ra n g e size
b e c a u se o f th e in c re a s e d lik elih o o d o f
e x p o su re in o ld e r w olves a n d g r e a te r
ex p o su re ra te s (A lm berg e t ah, 2009).
MATERIALS AND METHODS
Study area
O u r study area in clu d ed B anff N ational Park,
Jasp er N ational P ark (52“15 N, 115“30 W ), and
ad jacen t areas to th e east and n o rth (Fig. 1),
covering approxim ately 80,000 km^ (Thiessen,
2007). T h ree m ajor highways, secondary roads,
an d tow ns an d cities o ccur th ro u g h o u t th e
study area, an d Jasp er an d B anff N ational Parks
each receive two to th ree m illion visitors p e r
year. T h e n o rth e rn p o rtio n o f th e study area has
few er resid en ts an d roads, so th e re is a south to
n o rth g rad ien t o f d ecreasin g h u m an activity.
W ithin th e study area, th e re are F irst N ation
reserves belonging to th e C ree, N akota Sioux,
an d o th e r F irs t N ations p eoples (Statistics
C anada, 2006). See D ek k er e t al. (1995) and
H eb b lew h ite e t al. (2002) for details o f th e
study area.
W olves in o u r study area w en t th ro u g h two
p erio d s o f scarcity, once in th e 1900s to 1920s
70
JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2011
V
P-
S 4 Y ^ ;;
Legend
W o lf Territories
r
1
Wo f Buffers
A lberta/B C Boundary
Towns
First Nation Reserves
Roads
Banff and Jaspe r National Parks
3 25 50
// ■
^
200
'''v
^
'
‘‘’p ’iP iP jp .
K ilo m e te r s
F i g u r e 1.
Study area in th e C anadian Rocky M ountains o f A lberta—B ritish C olum bia (BC), show ing
locations o f w olf territo ries (from tele m e try data) a n d b u ffere d w olf (Canis lupus) c ap tu re locations (buffers)
from w hich w olf blood sam ples w ere analyzed for antibodies to canine d istem p e r virus (CDV) a n d canine
parvovirus (CPV), 2000—2008. Locations o f towns, Banff, Jasper, K ootenay, a n d Yoho N ational Park, m ajor
roads, a n d F irst N ation R eserves are show n. W olf data w ere collected d u rin g previous studies (e.g.,
Ffebblew hite e t ah, 2002; W hittington e t ah, 2005; N eufeld, 2006; W ebb, 2009).
b ecau se o f poisoning an d d estru c tio n o f p rey
an d again in th e 1950s b ecau se o f poisoning
(G unson, 1992). S tarting in th e 1970s, wolves
n atu rally reco lo n ized o u r study area from
n o rth ern A lberta (G unson, 1992; D ekker e t al.,
1995). W olves are p ro te c te d from h u n tin g and
trap p in g in N ational Parks, although th e y are
still subject to h u m a n -cau sed m ortality from
ro ad and railway m ortality (H eb b lew h ite e t a l,
2002). In b o th A lberta an d B ritish C olum bia,
w olf m a n ag em en t consists o f liberal harvest
th ro u g h h u n tin g an d trap p in g w ith th e goal of
m a in ta in in g sta b le p o p u la tio n s (G u n so n ,
1992). P opulation genetics rese arch by T h ies­
sen (2007) con firm ed th a t this en tire area
functions as one large population. A lternate
h o st species for canid diseases include feral
dogs, coyotes, m ustelid species (Mustela spp.),
an d occasionally re d foxes. Raccoons (Procyon
lotor) do n o t occur.
Wolf capture and blood sampling
W e ca p tu red wolves using foothold traps,
helico p ter n e t gunning, an d g ro u n d o r h elico p ­
te r d a rt cap tu re from 2000 to 2008 as p a rt of
ongoing research projects (H ebblew hite e t al.,
2002; W h ittin g to n e t a l, 2005; N eufeld, 2006;
W eb b , 2009). C ap tu re m ethods w ere approved
by ap p ro p riate anim al care protocols (U niver­
sity o f A lberta 353112, Parks C an ad a B N P004753 an d JN P-2007-952, A lberta G P4816
an d C N 087, W IL K A lO l-07, British C olum bia
V I07-31411). F o r ea ch w o lf c a p tu re d , we
r e c o rd e d age class, b a s e d on to o th w ear
(G ipson e t al., 2000), as pu p s an d yearlings
( < 2 yr) or subadults an d adults ( > 2 yr), sex,
cap tu re location, an d w olf pack. B lood sam ples
w ere collected from ju g u lar o r cephalic veins
into seru m sep arato r tubes o r silicone-coated
tu b es an d allow ed to clot. C lo tted sam ples w ere
c e n trifu g e d , a n d se ra w e re p ip e tte d in to
NELSON ET AL.—WOLE SEROLOGY IN THE CANADIAN ROCKIES
separate vials and sto red at —20 C for u p to 8 yr.
Sera w ere te ste d for antibodies to CPV and
C D V at th e W estern College o f V eterinary
M edicine at Saskatoon, Saskatchew an, C anada,
using a hem agglutination inhibition assay and
virus n e u tra liz a tio n assay (T izzard, 2000),
respectively. T iters > 1 :4 0 w ere co n sid ered
p o sitiv e fo r CPV , a n d tite rs > 1 :1 2 w ere
co n sid ered positive for CDV.
Human activity
B ecause m ost (90% ) anim als w ere rad io ­
collared, w e estim a ted w olf pack territories
b ased on th e 100% m inim um convex polygons
(M C P; M ohr, 1947) from very high-freq u en cy
(V H F) radio and global positioning system
(GPS) te lem etry d ata (e.g., H eb b lew h ite e t a l,
2002; W h ittin g to n e t a l, 2005; N eufeld, 2006;
W ebb, 2009). W e u sed w olf pack M C Ps to
assign each pack an average h u m a n activity
level to w hich each individual w ithin th e pack
was assum ed to b e exposed. W e u sed th e M C P
ra th e r th a n ca p tu re locations o f individual
wolves to reflect th e average exposure at the
p ack level. F o r individual wolves from u n ­
k now n packs (n = 17), w e d re w a circular
b u ffe r o f 1,000 km^ a ro u n d th e c a p tu re
lo c a tio n to e s tim a te e x p o su re to h u m a n
activity. T he b u ffe r size was e stim a ted using
th e average M C P ho m e range area across all
ra d io c o lla re d packs. M e a su re s o f h u m a n
activity w ithin each w olf pack territo ry w ere
b ased on average distance o f each pixel in the
en tire M C P to th e closest paved road. F irst
N ation reserve, an d tow ns. Spatial d ata on
h u m a n activity w ere o b ta in ed from th e N a­
tional T opographic Survey (available at h ttp ://
geogratis.cgdi.gc.ca). W e first m e asu red dis­
tan ce to th e th re e h u m a n activity layers using
th e spatial analyst distance function in A RC G IS 9.2 (E S R I, R edlands, California, USA),
w hich calculates a raste r distance layer (30-m^
resolution). W e th e n m e asu red th e average
d istan ce to p av ed an d u n im p ro v e d roads,
tow ns, and F irst N ation reserves for th e en tire
w olf-pack M C P using zonal statistics. W e
s c re e n e d fo r c o llin e a rity b e tw e e n sp atial
m e asu res o f h u m a n activity, an d d id n o t
in c lu d e variab les if |r |> 0 .3 (H o sm e r an d
L em eshow , 2000).
Statistical analyses
W e te ste d o u r m ain hypotheses for the
effects o f distances to h u m an activity (towns,
roads, and F irst N ation reserves), age, sex, and
y ear on th e prev alen ce o f CPV an d CD V
antibodies using logistic regression to m odel
th e probability o f a w olf b ein g exposed to
e ith e r C D V o r CPV (H osm er an d Lem eshow ,
71
2000). W e a d d e d age an d sex classes to a null
m odel (re p re sen tin g co n stan t exposure), and
ad d e d all possible com binations o f individual
an d co m b in ed covariates for o u r can d id ate set
o f m odels (15 m odels for each). W e re p o rt
odds ratios for covariates to te st for effects on
antib o d y prev alen ce, an d ev alu ated signifi­
cance at a = 0 .1 . To te st o u r hypotheses ab o u t
th e effects o f h u m a n activity on exposure to
canine diseases, w e p re d ic te d th e coefficient
o f d istan ce to b e negative if viral antibody
p rev alen ce in c re ase d closer to h u m an activity.
T h e b e st C D V an d CPV m odel was selected
a n d c o m p a re d u sin g A kaike’s in fo rm atio n
criteria (AIC) follow ing B u rn h am an d A n d er­
son (1998). In th e case o f m odel selection
u n certain ty , w e m o d el-averaged across th e to p
0 ^ AAIC (B u rn h am an d A nderson, 1998).
W e also co n sid ered a ran d o m effect for each
individual pack (including u nknow n pack) to
accom m odate p o te n tia l b etw een -p ack h e te ro ­
g eneity in exposure to diseases (Gillies e t a l,
2006). D esp ite o u r b e s t field efforts, how ever,
wolves w ere n o t c a p tu re d ran d o m ly o r evenly
across th e study area, w hich m ight bias disease
exposure results if age, sex, o r packs varied
over tim e. T h erefo re, b efo re statistical analy­
ses for risk factors, w e co n d u c te d chi-square
(X^) tests for significant differences across tim e
for th e sex, age, and packs th a t w e c a p tu re d
wolves from .
RESULTS
F ro m 2000 to 2008, w e sa m p le d 99
w olves fro m 42 packs (Fig. 1). O n ly five
w olves w e re c a p tu re d m o re th a n o n ce,
an d , b e c a u se th e s e re c a p tu re s o c c u rre d on
average 2.5 y r a p a rt, a n d b e c a u se th e five
w e re n o t originally an tib o d y -p o sitiv e, w e
c o n s id e re d th e se sam p les in d e p e n d e n t.
F ro m a sam p lin g v iew point, th e re w ere
n o sig n ifican t d iffe re n c es in th e fre q u e n c y
o f sexes (x^ P = 0 .5 1 ), ages (x^ P = 0 .3 1 ), o r
p acks (x^ P = 0 .4 1 ), co n firm in g no signifi­
c a n t sam p lin g bias. N in e ty -fo u r w olves
(95% ) w e re c o n sid e re d C P V antib o d y p o sitive (tite r ra n g e < 1 :6 —1:972) a n d 24
(24% ) w e re c o n sid e re d C D V antib o d y p o sitive (tite r ra n g e < 1 :2 0 —1:20,480), c o n ­
firm in g a h ig h e r an tib o d y p re v a le n c e to
C P V th a n C D V (b in o m ial te s t fo r overall
p re v a le n c e o f C P V vs. C D V a n tib o d y
P = 0 .0 0 1 ; T ab le 1). P u p s a n d yearlings
h a d a lo w er C PV ex p o su re th a n o ld e r
72
JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2011
1.
M ean a n d sta n d ard deviation (SD ) o f th e prevalence (% ) o f antibodies to canine parvovirus (CPV)
an d canine d istem p e r virus (CDV ) in wolves (Canis lupus) b y age class a n d sex across all packs in the
C anadian Rocky M ountains o f A lberta a n d B ritish C olum bia, 2000—2008.
T a b le
Age cla5S^ and sex
n
CPV (%)
SD
CDV (%)
SD
M ale < 2
M ale 2:2
F e m ale < 2
F e m ale S 2
U nknow ns
8
35
9
35
11
87.5
97
78
100
91
< 0 .0 0 5
0.38
< 0 .0 0 5
0.51
0.09
0
17
0
49
9
< 0 .0 0 5
0.12
< 0 .0 0 5
0.17
0.09
^ Pups and yearlings were < 2 yr old, and subadults and adults were ^ 2 yr of age when captured.
age classes (T ab le 1). F e m a le su b a d u lts
a n d a d u lts h a d a h ig h e r p ro b a b ility o f
ex p o su re to C D V th a n m ale su b a d u lts a n d
ad u lts (T ab le 1).
Effects of human activity
M odel selection show ed th a t for CPV
an tib o d y p rev alen ce, th e re w e re several
m odels b etw een AAIC 0.0 an d 2.0 (Table 2),
indicating m o d el selection uncertainty, e sp e­
cially for h u m a n effects o n C PV exposure.
T h e to p m odels in clu d ed th e variables age,
sex, an d distance to tow ns, roads, an d F irst
N ation reserves. T h e null m odel (constant)
was AAIC = 7.9 an d was n o t rep o rted . T h ere
was also n o su p p o rt for hetero g en eity am ong
packs in exposure to C PV becau se th e similar
m odel w ith ran d o m effects h a d substantially
low er m odel w eight (A A IC =4.9). T h erefore,
w e consid ered only th e fixed effects from th e
logistic m odel. A lthough th e top m odel for
C PV was a function o f distance to roads + age
(A A IC = 0.00, A IC w eight= 0.25; Table 2),
because th e re was substantial m odel selec­
tion uncertainty, a posteriori, w e m odel
averaged coefficients for CPV as a function
o f all covariates in Table 3 (CPV as a function
o f distance to tow ns, distance to roads,
distance to F irst N ation reserves, age class,
year, and sex). This “averaged” m odel was
also th e b e st C D V m odel (Table 2), m aking
com parisons easier. T he full C PV m odel was
m arginally significant (x^= 9.97, P = 0 .0 8 3 ),
y et still explained 29.9% (pseudo R^) o f
th e variation in C PV antibody prevalence
(Table 3). E xposure to C PV was m ore likely
in snbadnlts and adults (Table 3). M ales had
slightly g reater odds o f exposure to CPV th an
fem ales (Table 3). A ntibody prevalence to
CPV h a d w eak and nonsignificant relation­
ships to h u m an covariates, likely in p a rt
b ecause o f th e high prevalence o f CPV
relative to C D V an tib o d y (T able 3 and
Fig. 2).
2. T op canine parvovirus (CPV) a n d canine d istem p e r (CDV ) m odels for wolves (Canis lupus) in the
C anadian Rocky M ountains o f A lberta a n d B ritish C olum bia, 2000—2008. C ovariates u se d w ere age, sex, year,
an d distance to h u m an use. M odel stru c tu re , sam ple size (n), n u m b e r o f p a ram ete rs (K), log likelihood,
change in Akaike’s inform ation criteria (AIC), a n d A IC w eights are provided.
T a b le
n
K Log likelihood AAIC
75
75
75
75
75
75
4
2
4
5
4
4
- 1 1 .3 6
- 1 2 .6 9
- 1 2 .0 7
- 1 1 .2 6
- 1 2 .5 7
- 1 2 .6 9
0.00
0.42
1.41
2.08
2.42
2.65
0.24
0.20
0.12
0.08
0.07
0.06
1. D istance to towns + roads + F irst N ation reserves + age + sex 78
78
2. D istance to F irst N ation reserves + age + sex
6
6
- 3 0 .3 4
- 3 3 .4 4
0.00
1.55
0.63
0.29
Model structure
AIC weights
T op C PV m odels
1.
2.
3.
4.
5.
6.
D istance to road + age
A pproxim ate age
D istance to tow n + age
D istance to road + age + sex
D istance to F irst N ation reserve + age + sex
Age + sex
T op C D V m odels
NELSON ET AL.—WOLE SEROLOGY IN THE CANADIAN ROCKIES
73
3.
M easures o f m odel fit (likelihood ratio [LR], chi-square test, a n d R^} a n d odds ratios, P-values,
sta n d ard e rro r (SE) and P-values for th e influence o f w olf age class, sex, a n d distance functions (km) on
prevalence o f antibodies to canine parvovirus (CPV) a n d canine d istem p e r virus (CDV) for th e full logistic
regression m odel from T able 2. C anadian Rockies, A lberta, C anada, 2000—2008. P aram eters in b old are
statistically significant at P = 0 .f 0 from th e full m odel.
T a b le
LR
test
CPV
CDV
9.97, P=0.083
38.16, P<0.005
0.299
M ale
Age a 2
D istance to tow n
D istance to road
D istance to F irst N ation reserve
SE
P-value
Odds ratio
SE
P-value
1.22
8.89
1.026
1.930
0.994
1.464
2.36
0.087
1.09
0.21
0.81
0.06
0.48
0.247
0.70
0.225
3.91
0.981
0.789
1.038
0.170
6.97
0.022
0.096
0.013
0.045
0.51
0.54
0.109
0.004
F o r C D V , th e r e w e re only tw o m o d els
in th e to p fo u r A A IC , a n d th e to p m o d el
fo r C D V w as a fu n c tio n o f all covariates
(AAIC = 0.00, A IC w e ig h t= 0 .6 2 8 ; T a b le 2).
T h e n u ll m o d e l w as sim ilarly p o o r-fittin g as
c o m p a re d to th e C PV m o d e l (AAIC = 8 .I).
T h e to p m o d e l w as significant (x ^ = 3 3 .9 ,
P < 0 .0 0 5 ) a n d e x p la in e d 4 3 .4 % o f th e
v ariatio n in C D V (T ab le 3). S im ilar to
C PV , th e r e w as n o su p p o rt fo r a ra n d o m
e ffe c t o f p a c k (A A IC = 5.9). E x p o su re to
C D V in w olves w as m o re likely fo r adults
a n d su b a d u lts relativ e to p u p s a n d yearlings
CO CN -
0
50
0.434
Odds ratio
100
150
D istance to Indian Reserve (km)
I O b se rv e d CPV
P red icted CPV
' O b se rv e d CDV
• P red icted CDV
F i g u r e 2.
O bserved a n d p re d ic te d canine p a r­
vovirus (CPV) and canine d istem p e r (CDV ) antibody
prevalences as a function o f distance to closest F irst
N ation reserve for gray wolves (Canis lupus) in the
C anadian Rocky M ountains o f A lberta a n d B ritish
C olum bia from 2000 to 2008. O nly th e relationship
b e tw ee n C D V antibody prevalence a n d distance was
statistically significant (see T able 3 ) .
(th e in te rc e p t), a n d m ales h a d su bstantially
lo w e r o d d s o f e x p o su re to C D V th a n
fem ales (T able 3). E x p o su re to C D V was
also significantly m o re likely w ith g re a te r
d istan ces to F irs t N a tio n reserv es, alth o u g h
th e e ffe c t size w as sm all (T able 3 a n d
Fig. 2). E x p o su re to C D V sh o w e d w eak,
n o n sig n ifican t declin es w ith d istan c e from
ro ad s b u t re m a in e d stab le w ith d istan c e
fro m tow ns (T able 3).
DISCUSSION
W e f o u n d th a t tw o c o m m o n w o lf
p a th o g e n s h a d d iffe re n t an tib o d y p re v a ­
le n ce s a n d age/sex d iffere n c es, sim ilar to
o th e r stu d ie d w o lf p o p u la tio n s. W e fo u n d
h ig h C P V a n tib o d y p re v a le n c e s in th e
C a n a d ia n R ockies, in d ic a tin g alm o st all
w olves sa m p le d h a d b e e n ex p o sed to CPV.
T h e m o re v iru le n t C D V h a d , as e x p e cte d ,
lo w e r a n tib o d y p r e v a le n c e (T a b le I).
C o m p a re d w ith o th e r stu d ies, o u r C PV
a n tib o d y p re v a le n c e (95% ) w as h ig h e r
th a n values re p o rte d fro m M o n ta n a (Jo h n ­
son e t ah, 1994: 6 5 % ), A laska (Z arnke
e t ah, 2004: 3 5 % ), P o rtu g a l (S antos e t ah,
2009: 3 2% ), a n d S pain (S o b rin o e t ah,
2008: 6 2 % ) b u t sim ila r to th e 100%
p r e v a le n c e in w o lv e s in Y e llo w sto n e
(A lm b erg e t ah, 2009, 2010). In c o n tra st,
p re v a le n c e o f C D V a n tib o d y in o u r stu d y
(24% ) w as sim ilar to o r slightly h ig h e r
(9—2 4% ) th a n th o se r e p o rte d fo r th e se
74
JOURNAL OF WILDLIFE DISEASES, VOL. 48, NO. 1, JANUARY 2011
sam e p o p u la tio n s (Jo h n so n e t al., 1994;
Z arn k e e t al., 2004; S o b rin o e t al., 2008;
A lm b e rg e t al., 2009) a n d o n e p o p u la tio n
in S can d in av ia (A k e rste d t e t ak, 2010:
10% ). T h e re w e re im p o rta n t a n d c o n sis­
te n t effects o f age a n d sex class o n C P V
a n d C D V a n tib o d y p re v a le n c e th a t w e re
also sim ilar to p re v io u s stu d ies. As r e p o r t­
e d e lse w h e re , e x p o su re to b o th C D V a n d
C P V w as h ig h e r in w olves > 2 y r old
(Z arn k e e t ak, 2004; S o b rin o e t ak, 2008).
T h e fa c t th a t n o p u p s o r y earlin g s sh o w ed
e x p o su re to C D V , c o m p a re d to C PV , is
likely a fu n c tio n o f th e h ig h e r v iru le n c e o f
C D V a n d re s u lta n t h ig h m o rta lity a m o n g
p u p s , w h ic h goes u n d e te c te d in serologic
tests (A lm b erg e t ak, 2009). W e fo u n d
w e a k e r d iffe re n c es in e x p o su re b e tw e e n
m ales a n d fem ales fo r b o th C P V a n d C D V
c o m p a re d to o th e r stu d ie s (Z arn k e e t ak,
2004).
In c o n tra st to o u r h y p o th e se s a b o u t th e
p o te n tia l effects o f h u m a n activity o n w o lf
diseases, w e fo u n d o n ly w eak ev id e n c e fo r
h u m a n im p acts o n ex p o su re to C D V o r
C PV , w ith th e p o te n tia l ex cep tio n o f F irs t
N a tio n reserv es. V ery little is k n o w n a b o u t
th e re la tio n sh ip s o f C P V a n d C D V to
h u m a n activity in N o rth A m erica c o m p a re d
to stu d ies in A frican carn iv o res (L a u re n so n
e t ak, 1998; C leav elan d e t ak, 2000). O u r
resu lts su g g est th a t th is m ay b e d u e to
d iffe re n c es in d isease ecology b e tw e e n th e
tw o c o n tin e n ts. In o u r study, th e p re v a ­
le n c e o f C P V a n tib o d y w as essen tially h ig h
e n o u g h su ch th a t all w olves w e re exposed,
a n d d e te c tio n o f any spatial p a tte r n was
th e re fo re difficult. Z arn k e e t al. (2004)
fo u n d h ig h e r a n tib o d y p re v a le n c es to C P V
a n d o th e r ca n in e p a th o g e n s in re m o te areas
c o m p a re d to lo cations n e a r h u m a n se ttle ­
m e n ts in Alaska. W e also fo u n d th a t C D V
a n tib o d y p re v a le n c e in c re a se d p rim a rily
fu rth e r fro m F irs t N a tio n reserv es, n o t
closer, as p re d ic te d , sim ilar to re su lts o f
Z arn k e e t al. (2004) fo r CPV. T h e o p p o site
e ffec t o f F irs t N a tio n re se rv e s w as puzzling,
b u t it c o u ld b e ex p lain ed b y h ig h e r h a rv e st
o f w olves b y F irs t N a tio n tra p p e rs n e a r
reserv es, le a d in g to lo w er w o lf p o p u la tio n
density, a n d th u s lo w er C D V transm ission.
O u r resu lts are also co n siste n t w ith p e rsis­
te n c e in m u ltih o st c o m m u n ities, fo r exam ­
p le, w ith coyotes, sim ilar to re c e n t resu lts
fro m Y ellow stone N atio n a l P a rk (A lm berg
e t ak, 2010). O u r ability to d isc ern effects o f
h u m a n s o n carn iv o re diseases th ro u g h feral
dogs via in d ire c t m e an s is p ro b a b ly lim ited
a n d w ill re q u ire m o re d e ta ile d m u ltih o st
stu d ies to u n d e rs ta n d tran sm issio n d y n am ­
ics (A lm berg e t ak, 2010).
In th e la rg e r p o p u la tio n o f w olves in th e
C a n a d ia n R ockies, w e p re s e n t th e first
in fo rm a tio n a b o u t b a se lin e in fec tio n p re v ­
ale n ce fo r th e se tw o im p o rta n t c a n in e
p a th o g e n s. D e s p ite th e fa ct th a t w e fo u n d
lim ite d e v id e n c e fo r h u m a n effects on w o lf
diseases in th e C a n a d ia n R ockies, c a n in e
diseases m ay still have p o te n tia l p o p u la ­
tio n im p ac ts, fo r ex am ple, th ro u g h r e ­
d u c e d p u p su rv iv al d u r in g o u tb re a k s
(M ec h a n d C oyal, 1993; A lm b e rg e t ak,
2010). O u r re su lts co n firm th a t c an in e
disease dynam ics m ay b e sim ilar to th o se
k no w n fro m o th e r p o p u la tio n s, fo r ex am ­
p le , d iffe re n c es in C P V a n d C D V ex p o ­
su re , a n d sex a n d age d iffe ren c es. T h e
sim ilarity b e tw e e n o u r re su lts a n d resu lts
fro m n e a rb y re c o v e rin g w o lf p o p u la tio n s
in Y ellow stone N a tio n a l P ark, w h e re a
p o te n tia l p o p u la tio n im p a c t o f C D V was
p rev io u sly d e te c te d (A lm b erg e t ak, 2009),
suggests th a t C P V a n d C D V a re significant
a n d c o m m o n p a th o g e n s o f w o lf p o p u la ­
tio n s th a t will b e im p o rta n t to u n d e rs ta n d
fo r w o lf p o p u la tio n m a n a g e m e n t (M ech
e t ak, 2008). R eg a rd le ss o f th e p o te n tia l
ro le o f disease on p o p u la tio n dynam ics,
th e m o st im p o rta n t d e m o g ra p h ic effects o f
h u m a n s a re th ro u g h d ire c t h a rv e st o r ro ad
m o rtality in th e C a n a d ia n R ockies (W eb b
e t ak, 2011).
ACKNOWLEDGM ENTS
W e th a n k biologists for h elp in g us obtain
sam ples in th e field, in clu d in g B. W eckw orth,
P. F ram e, L. N eufeld, S. Slater, N. D eC esare,
S. H azen b erg , H. S paedtke, G. Kuzyk, B.
C ulling, D. C ulling, an d B ighorn H elicopters.
F u n d in g for this study was p ro v id ed by
A lb erta C onservation Association, A lberta F ish
NELSON ET AL.—WOLE SEROLOGY IN THE CANADIAN ROCKIES
an d W ildlife Division, B ritish C olum bia M in­
istry o f E nv iro n m en t, B ritish C olum bia M in­
istry o f F orests, C anadian A ssociation of
P etro leu m P rod u cers, Parks C anada, Boyal
D u tc h Shell, an d W o rld W ildlife F u n d . W e
th a n k D. P letsch er and two anonym ous
review ers for helpful com m ents on previous
versions o f this m anuscript.
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