En i onmen al Change and Disease Dynamics: E ec s o
In ensi e Fo es Managemen on Puumala Han a i us
In ec ion in Bo eal Bank Vole Popula ions
Liina Vou ilainen
1,2
*, Sake i Sa ola
1
, E a Riikka Kallio
3,4
, Juha Laakkonen
5
, An i Vahe i
2,6
,
Olli Vapalah i
2,5,6
, Heikki Hen onen
1
1Finnish Fo es Resea ch Ins i u e, Van aa Resea ch Uni , Van aa, Finland, 2Depa men o Vi ology and Resea ch P og ams Uni , In ec ion Biology, Haa man Ins i u e,
Uni e si y o Helsinki, Helsinki, Finland, 3Depa men o Biological and En i onmen al Science, Uni e si y o Jy a
¨skyla
¨, Jy a
¨skyla
¨, Finland, 4Depa men o E olu ion,
Ecology and Beha iou , Ins i u e o In eg a i e Biology, Uni e si y o Li e pool, Li e pool, Uni ed Kingdom, 5Depa men o Ve e ina y Biosciences, Facul y o Ve e ina y
Medicine, Uni e si y o Helsinki, Helsinki, Finland, 6Helsinki Uni e si y Cen al Hospi al, HUSLAB, Helsinki, Finland
Abs ac
In ensi e managemen o Fennoscandian o es s has led o a mosaic o woodlands in di e en s ages o ma u i y. The main
oden hos o he zoono ic Puumala han a i us (PUUV) is he bank ole (Myodes gla eolus), a species ha can be ound in all
woodlands and especially ma u e o es s. We in es iga ed he in luence o o es age s uc u e on PUUV in ec ion dynamics
in bank oles. O e ou yea s, we apped small mammals wice a yea in a o es ne wo k o di e en succession s ages in
No he n Finland. Ou s udy si es ep esen ed ou o es age classes om young (4 o 30 yea s) o ma u e (o e 100 yea s)
o es s. We show ha PUUV-in ec ed bank oles occu ed commonly in all o es age classes, bu peaked in ma u e o es s.
The p obabili y o an indi idual bank ole o be PUUV in ec ed was posi i ely ela ed o concu en hos popula ion densi y.
Howe e , when popula ion densi y was con olled o , a ela i ely highe in ec ion a e was obse ed in oles apped in
younge o es s. Fu he mo e, we ound e idence o a ‘‘dilu ion e ec ’’ in ha he in ec ion p obabili y was nega i ely
associa ed wi h he simul aneous densi y o o he small mammals du ing he b eeding season. Ou esul s sugges ha
younge o es s c ea ed by in ensi e managemen can educe han a i al load in he en i onmen , bu PUUV is common in
woodlands o all ages. As such, he Fennoscandian o es landscape ep esen s a signi ican ese oi and sou ce o
han a i al in ec ion in humans.
Ci a ion: Vou ilainen L, Sa ola S, Kallio ER, Laakkonen J, Vahe i A, e al. (2012) En i onmen al Change and Disease Dynamics: E ec s o In ensi e Fo es
Managemen on Puumala Han a i us In ec ion in Bo eal Bank Vole Popula ions. PLoS ONE 7(6): e39452. doi:10.1371/jou nal.pone.0039452
Edi o : Dhanaseka an Vijayk ishna, Duke-NUS G adu e Medical School, Singapo e
Recei ed Feb ua y 6, 2012; Accep ed May 21, 2012; Published June 20, 2012
Copy igh : ß2012 Vou ilainen e al. This is an open-access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s
un es ic ed use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal au ho and sou ce a e c edi ed.
Funding: This s udy was inancially suppo ed by Maj and To Nessling Founda ion (www.nessling. i/en), Kone Founda ion (www.koneensaa io. i/en), Emil
Aal onen Founda ion (www.emilaal onen. i/eng.h m), Jenny and An i Wihu i Founda ion (www.wihu in ahas o. i/ ounda ion.h ml), Finnish Game and Fishe ies
Resea ch Ins i u e (www. k l. i/english), and he EU 6 h F amewo k P og amme (GOCE-2003-010284 EDEN, www.eden- p6p ojec .ne ). This s udy was pa ially
unded by EU g an FP7-261504 EDENex and is ca alogued by he EDENex S ee ing Commi ee as EDENex 014 (h p://www.edenex .eu). The con en s o his
publica ion a e he sole esponsibili y o he au ho s and don’ necessa ily e lec he iews o he Eu opean Commission. The unde s had no ole in s udy design,
da a collec ion and analysis, decision o publish, o p epa a ion o he manusc ip .
Compe ing In e es s: The au ho s ha e decla ed ha no compe ing in e es s exis .
* E-mail: liina. ou ilainen@helsinki. i
In oduc ion
Human ac i i y has changed he dis ibu ion and abundance o
many species. Consequen ly, he dis ibu ion and abundance o
pa hogens and pa asi es ha hese species ha bo may also be
al e ed. Se e al wildli e pa hogens can also in ec humans, i.e., a e
zoono ic. Fo example, han a i uses ( amily Bunya i idae) bo ne by
oden s and insec i o es cause hemo hagic e e wi h enal
synd ome (HFRS) and han a i us ca diopulmona y synd ome
(HCPS) in humans [1].
The mos common han a i al disease in Eu ope is neph opa hia
epidemica (NE), a mild o m o HFRS [2]. I is caused by Puumala
i us (PUUV) [3,4] which is ypically ound in he bank ole,
Myodes gla eolus. In he oden hos , PUUV is pe sis en [5] and
does no cause isible symp oms [5–7] al hough i can educe
win e su i al [8]. T ansmission in he hos is ho izon al and
occu s di ec ly and ia ae osol exc e ions [6,9]. The la e is
conside ed he main pa hway o oden -human ansmissions
[10]. Epidemic peaks o human NE ollow he seasonal and
mul iannual dynamics o bank ole abundance [11–18]. While he
i us and i s hos a e ound in mos Eu opean coun ies, he bulk
o human in ec ions occu in he bo eal zone o No h and No h-
eas Eu ope [2].
A eas o in ensi e ag icul u e ha e been associa ed wi h lowe
p e alence o PUUV in bank oles [19–21] and lowe incidence o
NE [14,20,22] han in mo e o es ed a eas in he empe a e zone.
In his s udy, we in es iga ed whe he ano he kind o en i on-
men al dis u bance, i.e., he in ensi e o es y p ac iced in bo eal
Fennoscandia could ha e simila e ec s on PUUV dynamics.
In ensi e managemen o Fennoscandian o es s has ans o med
he landscape in o a mosaic o g assy clea -cu s, plan a ions, and
a succession o o es s o a iable ma u i y. Fo es cu ing
p o oundly al e s g ound-le el ege a ion, when mosses and
Vaccinium sh ubs o ma u e o es loo s a e eplaced by g asses
in newly cu si es unde going e o es a ion [23,24]. In bo eal
Finland, land a ea is nea ly 80% o es ed, o which he as
PLoS ONE | www.plosone.o g 1 June 2012 | Volume 7 | Issue 6 | e39452
majo i y is in comme cial p oduc ion. Climax o es s (100+yea s)
ep esen app oxima ely 20% o managed o es s, whe eas he
p opo ion o young s ands (0–40 yea s) is oughly wice as la ge
[25].
Dea ing and Dizney [26] e iewed he mechanisms by which
en i onmen al dis u bance can in luence he in ec ion dynamics o
han a i us ia hei oden hos s. Fi s ly, dis u bance can al e hos
popula ion densi y, which in u n may a ec in aspeci ic con ac
a es. In ensi e managemen o bo eal o es s can educe bank
ole abundance since hey p e e climax o es s, p obably due o
hei ichness in ood sou ces (bilbe y, a bo eal lichens) and
shel e (moss, woody deb is) [27–29]. Ano he sugges ed d i ing
o ce, he so-called ‘‘dilu ion e ec ’’ [30–32], p oposes ha habi a
dis u bance can al e small mammal species ichness, in luencing
in aspeci ic con ac a e and he eby ansmission [26]. In bo eal
en i onmen s, small mammal communi ies a e o en mo e di e se
in young managed o es s as his is he p e e ed habi a o Mic o us
spp. [27].
In his s udy, we in es iga ed whe he in ensi e managemen o
bo eal o es s in luences he dynamics o PUUV in bank oles.
Gi en hei p e e ence o ma u e o es s, we expec ed he
abundance o PUUV-in ec ed bank oles o be posi i ely ela ed
o o es age. Fu he mo e, we expec ed bank ole densi y o be
posi i ely ela ed and he abundance o non-hos species o be
nega i ely ela ed o he p obabili y o bank oles being PUUV
in ec ed. To es hese p edic ions, we moni o ed small mammal
species abundance and he incidence o PUUV-in ec ed bank oles
in ou o es age classes o e ou yea s in no he n Finland. Wi h
his design, we we e able o explo e he ela ionships be ween
o es age, small mammal communi y s uc u e and in ec ion
dynamics o PUUV in bank oles.
Ma e ials and Me hods
E hics S a emen
Acco ding o he Finnish Ac on he Use o Animals o
Expe imen al Pu poses (62/2006) and a u he decision by he
Finnish Animal Expe imen Boa d (16
h
May, 2007), he animal
cap u e echnique, i.e., using aps ha ins an ly kill he animal, we
used is no conside ed an animal expe imen and he e o e
equi es no animal e hics license om he Finnish Animal
Expe imen Boa d. All animal apping ook place wi h pe mission
(1013/204/2002) on land owned by he Finnish Fo es and Pa k
Se ice. A pe mi (23/5713/2001) o cap u ing p o ec ed species
(So ex spp., Myodes u ocanus and Myopus schis icolo ) was g an ed by
he Finnish Minis y o he En i onmen . O he species cap u ed
in his s udy a e no p o ec ed in Finland and none o he cap u ed
species a e included in he Red Lis o Finnish Species.
S udy Si e and Design
The s udy was conduc ed wi hin an a ea o 875 km
2
in no he n
Finland (municipali ies o Tai alkoski and Pudasja¨ i: 65uN,
28uE) in he no he n bo eal ege a ion zone. Managemen o
each o es s and was eco ded in de ail by he Finnish Fo es and
Pa k Se ice and included da es on which clea -cu ing and
plan a ion ook place.
S ands in ou s udy ep esen ed ou age classes: managed
o es s wi h (1) 4–8, (2) 10–15, and (3) 25–30 yea s om plan a ion
a e clea cu ing, and non-managed o es s (4) olde han
100 yea s (see Figu e S1 o ep esen a i e pho og aphs). In each
age class, 10 o es si es o 5–76 ha (a e age 18 ha) we e chosen
o he s udy. Fo es s ands .100 yea s we e domina ed by
No wegian sp uce (Picea abies), whe eas he younge o es s we e
plan a ions o sp uce o Sco s pine (Pinus syl es is) wi h some
na u ally egene a ed bi ch (Be ula spp.), aspen (Populus emula) and
owan (So bus aucupa ia). In he unde s o y ege a ion, mosses
(Hylocomium splendens,Pleu ozium sch ebe i and Dic anum spp.)
oge he wi h bilbe y (Vaccinium my illus) we e dominan in
ma u e o es s. In 4–8 yea o es s ands, mosses we e eplaced by
g asses (mos ly Deschampsia lexuosa), i eweed (Epilobium angus i o-
lium) and aspbe y (Rubus idaeus). G asses we e s ill abundan 10–
15 yea s a e cu ing, bu less abundan han in he younges age
class. Sh ubs such as Vaccinium i is-idaea,Empe um nig um,
Vaccinium uliginosum and Rhododend on omen osum we e common. In
25–30 yea s ands, much o he g ound was shaded esul ing in
spa se unde s o y ege a ion han in o he age classes. G asses
we e a e, and some V. i is-idaea and V. my illus we e p esen .
Small Mammal T apping
Small mammals we e apped acco ding o he small quad a
me hod [33]. Wi hin each s and, small mammals we e apped in
i e 15615 m quad a s ha we e accessible by oo bu a leas
50 m apa . Twel e snap- aps we e bai ed wi h ye b ead and
placed on each quad a so ha h ee aps we e placed wi hin 2 m
om each co ne . T aps we e se o e wo consecu i e nigh s and
checked each mo ning. T appings we e pe o med on 200
quad a s on 40 s ands du ing he beginning (ea ly June) and end
(Sep embe ) o he b eeding season om 2007 o 2010. Each
apping pe iod las ed app oxima ely h ee weeks.
Once apped, small mammals we e placed in plas ic bags in
cooled, insula ed con aine s and ozen he same day a 220uC.
Animals we e la e dissec ed and hei species, sex, age, and weigh
de e mined. Age de e mina ion o bank oles (summe -bo n/
o e win e ed) was based on he de elopmen o pelage, and when
unce ain, on mola oo s [34]. The hea o each bank ole was
placed in an Eppendo ial and kep ozen un il sc eened o he
p esence o PUUV an ibodies. PUUV an ibodies a e p ese ed in
hea samples as well as in esh- ozen whole blood samples
(unpublished da a).
De e mina ion o PUUV In ec ion
The hea o each animal was dilu ed in 200 mL phospha e-
bu e ed saline (PBS) p io o an immuno luo escen an ibody es
(IFAT) o de ec PUUV-speci ic an ibodies [35]. PUUV-in ec ed
emale bank oles p o ide ma e nal an ibodies o hei o sp ing
[6,36] which may in la e he in ec ion a e in such cases. Following
Kallio and o he s [37], we expec ed he p opo ion o se oposi i e
indi iduals o dec ease wi h body mass un il a ce ain h eshold
whe e ma e nal an ibodies a e commonly los , and hen o
inc ease again wi h body mass, since olde and hea ie bank oles
a e o en PUUV in ec ed [37–39]. To de e mine he h eshold
be ween PUUV in ec ion and se oposi i i y due o ma e nal
an ibodies, we applied a gene alized addi i e mixed model
(GAMM) wi h binomial e o dis ibu ions and a logi link
unc ion (gamm4 unc ion o gamm4 package [40] in he R
so wa e package [41]). A body mass smoo he was used as
p edic o o he p obabili y o a bank ole being PUUV
se oposi i e, and a andom in e cep was allowed o each s and
and apping session. As summe -bo n animals we e only cap u ed
in he all, animals cap u ed in sp ing we e excluded om he da a
se .
S a is ical Analysis
The e ec o o es age on he numbe o PUUV-in ec ed bank
oles pe s and was s udied using GLMM (gene alized linea
mixed modeling) wi h Poisson e o dis ibu ions and a log link
unc ion. In he ull model, o es age ( ac o wi h ou le els), ole
densi y cycle phase (high; yea s 2007 and 2010/low; yea s 2008
In ensi e Fo es Managemen and Puumala Han a i us
PLoS ONE | www.plosone.o g 2 June 2012 | Volume 7 | Issue 6 | e39452
and 2009), season (sp ing/ all), and all hei wo-way in e ac ions
we e used as ixed ac o s. To accoun o epea ed measu emen s,
a andom in e cep was allowed o each o es s and, and o
accoun o o e dispe sion, o each obse a ion [42]. The ull
model was educed by emo ing ixed e ec s sequen ially i hei
inclusion did no dec ease AIC (Akaike in o ma ion c i e ion) by
mo e han wo uni s [43].
The p obabili y o a bank ole being in ec ed wi h PUUV was
s udied using GLMM wi h binomial e o dis ibu ions and a logi
link unc ion. Fo es age ( ac o wi h ou le els) and he mean-
cen e ed numbe s o bank oles and o he small mammals
de ec ed we e included as p edic o s. Fu he mo e, o exclude
he obse ed e ec s ha would esul om demog aphic a ia ion
in bank ole popula ions (i.e., con ounding e ec s), we added he
mean-cen e ed body mass as a p oxy o age, sex, and hei
in e ac ion as p edic o s. To accoun o epea ed measu emen s,
andom in e cep s we e allowed o each o es s and and apping
session. As we expec ed he anges o bo h he dependen and
independen a iables o a y be ween seasons, sepa a e models
we e applied o sp ing and all da a. In e ences we e d awn om
he ull models, since se e al independen a iables (e.g., he
numbe o bank oles and o he small mammals) we e expec ed o
con ound each o he . All models we e i ed using he Laplace
app oxima ion me hod (lme unc ion o lme4 package [44] in he
R so wa e [41]).
Resul s
Al oge he , 3 452 small mammals we e cap u ed du ing eigh
apping pe iods om June 2007 o Sep embe 2010. The mos
common species was he bank ole (N = 2 384, Figu e 1A). Fou
o he oden species ( ield ole Mic o us ag es is (N = 326), oo /
und a ole Mic o us oeconomus (N = 25), wood lemming Myopus
schis icolo (N = 33), g ay-sided ole Myodes u ocanus (N = 21)), and
ou sh ew (So icinae) species (common sh ew So ex a aneus
(N = 624), masked sh ew So ex caecu iens (N = 34), pygmy sh ew
So ex minu us (N = 3), and wa e sh ew Neomys odiens (N = 2)) we e
also cap u ed. Bank oles we e mos abundan in .100 yea
o es s, whe eas non-hos oden s (i.e., pooled numbe s o ield
oles, oo oles, g ey-sided oles and wood lemmings) we e mos
abundan in he 4–8 yea o es s. Sh ew abundance did no show
dis inc di e ences be ween o es age classes (Fig. 1A). All bank
oles cap u ed in sp ing had o e -win e ed and we e ep oduc i e,
whe eas mos in he all we e non-b eeding indi iduals bo n
du ing he summe . F om he sp ing ime apping pe iods, 148 o
he 318 bank oles sc eened ca ied PUUV an ibodies and we e
conside ed in ec ed (46.5%, Wald’s 95% CI: 41.1 o 52.0%). F om
he all apping pe iods, 513 o 1 947 bank oles (26.3%) sc eened
posi i e o PUUV-speci ic an ibodies. The p obabili y o ca ying
an ibodies in he all eached i s minimum a a weigh o 14.4
g ams (Figu e 2). Thus, in la e analyses se oposi i e bank oles
wi h a body mass ,14.4 g (N = 67) we e conside ed o be ca ying
ma e nal an ibodies and he e o e no in ec ed. Consequen ly,
in ec ion p e alence in he all apping pe iods was 22.9% (95%
CI: 21.1 o 24.8%). The e we e no disce nable di e ences in
PUUV in ec ion p e alence be ween he ou o es age classes
examined (Figu e 1B).
E ec o Fo es Age on he Abundance o PUUV-in ec ed
Bank Voles
PUUV-in ec ed bank oles we e mos abundan in 100+yea
o es s (Figu e 1A). The bes -suppo ed Gene alized Linea Mixed
Model (GLMM) analyzing he abundance o PUUV-in ec ed bank
oles included he main e ec s o o es age, season, and cycle
phase (Table 1), bu all hei wo-way in e ac ions we e d opped
du ing model selec ion. Compa ed o 100+yea o es s, he
p edic ed abundance o in ec ed bank oles in 25–30, 10–15, and
4–8 yea o es s was 61%, 46%, and 65% lowe , espec i ely
( ans o med om GLMM coe icien s in Table 1 by coe icien (%)
= [1-e
In e cep +Coe icien
/e
In e cep
]*100). All hese di e ences we e
s a is ically signi ican . Fu he mo e, PUUV-in ec ed oles we e
71% less abundan in sp ing han all and 95% less abundan
du ing low densi y yea s.
E ec s o Fo es y, Bank Vole Densi y and Non-hos
Species on PUUV In ec ion in Bank Voles
Bank oles in young o es s we e mo e likely o be PUUV
in ec ed han hose in old o es s (Figu e 3A–D, Table 2). In he
GLMM he p obabili y o a bank ole being PUUV in ec ed in
sp ing was signi ican ly lowe in 100+ han 25–30 yea o es s. In
he all model, he di e ence was also signi ican be ween animals
in 100+and 10–15 yea o es s. The p obabili y o in ec ion
ollowed he same pa e n in sp ing and all, i.e., 25–30.10–
15.4–8.100+yea o es s (Figu e 3A–D, Table 2). The
p obabili y o PUUV in ec ion inc eased wi h bank ole
abundance, he e ec being mo e p onounced in sp ing han in
all, bu s a is ically signi ican in bo h seasons (Figu e 3A–B,
Table 2). The abundance o o he small mammals had
a s a is ically signi ican and nega i e impac on he p obabili y
o a bank ole being PUUV in ec ed in sp ing, bu no in all
(Figu e 3C–D, Table 2). In sp ing, males we e signi ican ly mo e
likely o be in ec ed han emales bu he body weigh and he
in e ac ion o sex and weigh we e no signi ican (Figu e 3E,
Table 2). In all, bo h body weigh and he in e ac ion o sex and
weigh we e signi ican p edic o s o in ec ion s a us, so ha he
p obabili y inc eased by weigh mo e s eeply in males han
emales (Figu e 3F, Table 2). The model coe icien s (Table 2)
ep esen he e ec s o independen a iables ‘‘all o he hings
equal’’, so ha he p obabili y o PUUV in ec ion is highe in
young compa ed o old o es s a any gi en hos o non-hos
densi y (Figu e 3A–D). Likewise, in Figu es 3A–D he p edic ed
p obabili ies ep esen an a e age-weigh emale, whe eas p ob-
abili ies o males and hea ie indi iduals would be highe in any
gi en o es age class, o densi y o bank oles o o he small
mammals. Despi e he ac ha bank oles we e mo e o en
in ec ed in young o es s, hei highe densi y in old o es s
compensa ed, a leas in pa , o he habi a -a ibu ed dec ease
in in ec ion a e (Figu e 3A–B). All co ela ions be ween ixed
co a ia es we e lowe han 0.6, i.e., no collinea i y was ound ha
would ha e p e en ed hei inclusion in he same model.
Discussion
This s udy demons a ed ha bank oles in ec ed wi h Puumala
han a i us can be ound commonly in young o es s unde going
in ensi e managemen . Howe e , hey a e less abundan han in
ma u e o es s ands 100+yea s old. The p obabili y o a bank ole
being PUUV in ec ed was posi i ely ela ed o concu en bank
ole abundance and nega i ely ela ed o he abundance o o he
small mammals. Fu he mo e, bank oles inhabi ing young o es s
we e mo e likely o be PUUV in ec ed han hose in ma u e
s ands.
E ec s o Fo es y on PUUV-in ec ed Bank Vole Densi y
Du ing mos o he apping pe iods wi hin ou ou -yea s udy,
PUUV-in ec ed bank oles we e ound in all o es age classes,
being ela i ely common e en in young s ands. Hence, he
managed bo eal landscape o di e en aged o es s poses no
In ensi e Fo es Managemen and Puumala Han a i us
PLoS ONE | www.plosone.o g 3 June 2012 | Volume 7 | Issue 6 | e39452
ba ie o ei he bank oles o he sp ead o PUUV, unlike
ag icul u al land su ounding o es pa ches in empe a e Eu ope
[19–22,45]. As he s ands in his s udy ep esen ed a wide ange o
age classes, i is unlikely ha PUUV-in ec ed bank oles would be
sca ce o absen om succession s ages no co e ed by his s udy,
i.e., 30–100 yea old o es s. Thus, we assume ha he as
Figu e 1. Numbe s o small mammals (A) and Puumala han a i us p e alence (B) in ou o es succession s ages. a = 100+; b = 25–30;
c = 10–15; d = 4–8 yea s a e plan ing.
doi:10.1371/jou nal.pone.0039452.g001
Figu e 2. Di e en ia ion be ween Puumala han a i us in ec-
ion and ma e nal an ibodies. P edic ed p obabili y (solid line) wi h
95% CI (dashed lines) o bank oles cap u ed in all o ca y han a i us
an ibodies in ela ion o body mass. The do ed e ical line indica es
he h eshold alue (14.4 g) abo e which se oposi i e animals we e
ea ed as genuinely in ec ed. Sphe es indica e he numbe s o
obse ed da a poin s.
doi:10.1371/jou nal.pone.0039452.g002
Table 1. Bes suppo ed GLMM analyzing he numbe o
PUUV-in ec ed bank oles in a o es s and.
Pa ame e Es ima e (SE)
a
z
P alue
In e cep
b
2.062 (0.203) 10.2 ,0.0001
Fo es age (25–30 y) 20.945 (0.285) 23.3 0.00093
Fo es age (10–15 y) 20.621 (0.279) 22.2 0.02577
Fo es age (4–8 y) 21.039 (0.288) 23.6 0.00031
Cycle phase (low) 22.906 (0.209) 213.9 ,0.0001
Season (sp ing) 21.250 (0.145) 28.7 ,0.0001
Va iance a ibu able o andom o es s and e ec (40 g oups) was 0.23 wi h
s anda d de ia ion 0.48 and o andom obse a ion-le el e ec (320 g oups)
0.44 wi h s anda d de ia ion 0.66.
a
Es ima es a e gi en on na u al loga i hmic scale and s anda d e o s o
es ima es a e in pa en heses.
b
In e cep is calcula ed o a 100+yea s and in he all o a high densi y yea .
doi:10.1371/jou nal.pone.0039452. 001
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majo i y o Finnish o es s (i.e., 77% o land co e ) p o ide sui able
habi a o bank oles and enable high connec i i y among
popula ions o hos s and i al s ains. The e o e, we do no belie e
ha bo eal bank ole popula ions a e sensi i e o local s ochas ic
ex inc ion and coloniza ion e en s, which can impai he
pe sis ence o pa hogens in empe a e hos popula ions [19,21,46].
Al hough PUUV-in ec ed bank oles we e p esen in all o es
age classes, hey we e 46–64% less abundan in young han in
ma u e o es s ands. Gi en ha a la ge numbe o in ec ed
animals likely indica es a la ge numbe o bank oles shedding
PUUV, ma u e o es s may suppo a highe i al load and pose
a highe isk o ansmission o humans.
Whe eas o es dis u bance by ag icul u e is associa ed wi h low
human NE incidence, dis u bance due o in ensi e o es
managemen is no . The disease is app oxima ely h ee imes
mo e common in eas e n and cen al han in sou h-wes e n pa s
o Finland [47] ye he o es age s uc u e is qui e uni o m ac oss
he coun y [23]. The mos impo an eason o he epidemio-
logical pa e n seems o be he deg ee o cyclici y in oles. The e is
a s eep g adien in snow co e om sou h-wes e n o no he n and
eas e n Finland ha a ec s he communi y s uc u e o p ey and
hei p eda o s. Consequen ly, he ampli ude o ole popula ion
cyclici y inc eases om he sou hwes o he no h [29,48,49]. As
such, popula ion peaks in he no h likely cause a apid inc ease in
he numbe o PUUV-sp eading bank oles [50]. In addi ion,
sou h-wes e n Finland is cha ac e ized by a highe p opo ion o
ag icul u al and u ban en i onmen s less equen ed by bank
oles.
Figu e 3. Fac o s con ibu ing o he p obabili y o a bank ole being in ec ed by Puumala han a i us. P edic ed p obabili ies o a bank
ole being PUUV in ec ed in ela ion o o es age and concu en numbe s o bank oles on he s udy si e in sp ing (A) and all (B), in ela ion o
o es age and concu en numbe s o o he small mammals in (C) sp ing and (D) all, and in ela ion o sex and body mass in sp ing (E) and all (F).
P edic ed alues ep esen es ima es o ixed e ec s in Table 2. In A, B, C, and D, black line = 100+; ed = 25–30; g een = 10–15; blue = 4–8 yea o es
s and; all p edic ions a e made o a bank ole emale wi h a e age alues o o he con inuous co a ia es. In Eand F, solid lines indica e p edic ions
o emales, and dashed lines o males, bo h cap u ed om a 100+yea s and wi h a e age numbe s o bank oles and o he small mammals.
Sphe es indica e he numbe s obse ed, sphe e sizes be ween plo s a e no compa able. P edic ions a e only d awn on he ange o obse a ions on
each o es age class (A,B,C,D) and sex (E,F). Thick lines in A,B,C, and D ep esen he in e qua ile anges o obse a ions.
doi:10.1371/jou nal.pone.0039452.g003
In ensi e Fo es Managemen and Puumala Han a i us
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Fac o s Con ibu ing o he Likelihood o a Bank Vole
Being In ec ed wi h PUUV
Bank oles in 100+yea o es s we e less likely o be PUUV
in ec ed han hei conspeci ics in younge s ands. This obse a-
ion could be due o one o bo h o he ollowing easons; i s ly,
he lowe bank ole abundance in young o es s sugges s hey a e
less a o able habi a s [25]. The lack o esou ces in young o es s
could educe he condi ion o esiden bank oles and he eby
inc ease hei ulne abili y o pa hogens. This explana ion is
suppo ed by ou obse a ions o PUUV in ec ion a es peaking in
25–30 yea o es s, which appea o be he leas a o able habi a
since hey ha bo ed he lowes numbe o bank oles du ing mos
o he s udy pe iod. Secondly, en i onmen al condi ions in
younge o es s could a o he su i al o PUUV ou side he
hos . The highes in ec ion a es in bo h sp ing and all occu ed in
25–30 yea s ands, whe e dense canopies main ained high
humidi y, lowe empe a u e a g ound le el and blocked
ul a iole adia ion. These en i onmen al condi ions could
po en ially p olong he pe iod o e which i al pa icles emain
in ec i e ou side a hos [9].
We obse ed a posi i e ela ionship be ween he p obabili y o
being PUUV in ec ed and concu en hos popula ion densi y.
This esul implies ha ansmission inc eases wi h bank ole
densi y, ei he be ween in ec ed and suscep ible indi iduals o
be ween suscep ible indi iduals and an in ec ious en i onmen .
Se e al s udies ocusing on he PUUV han a i us and bank oles
ha e add essed he associa ion be ween in ec ion p e alence and
hos densi y [12,19,22,37,38,51,52], bu posi i e ela ionships ha e
only been ound occasionally, and in mos cases wi hou ime lags
[12,22,52].
We ound ha abundance o o he (non-hos ) small mammals
was nega i ely co ela ed wi h he likelihood o a bank oles being
PUUV in ec ed du ing he b eeding season. This esul is
consis en wi h o he s udies whe e han a i us p e alence was
nega i ely co ela ed wi h di e si y [53–55], p esence [56], o
p opo ion [19,57] (bu see [52]) o non-hos small mammals.
Howe e , we obse ed ha an inc easing numbe o non-hos
small mammals educed he likelihood o a bank ole being
in ec ed when hos densi y was cons an (Table 2, Figu e 3C).
The e o e, we conside he associa ion a ue dilu ion e ec in ha
he e ec o non-hos s on pa hogen p e alence occu s i espec i e
o hos densi y, in con as o an appa en one whe e non-hos s
egula e hos densi y. To da e, a ue dilu ion e ec has been
epo ed in h ee han a i us s udies [19,55,56] and has been
hypo hesized o ake place when non-hos species educe in-
aspeci ic con ac a es o hos s by al e ing hei beha io [31].
Among Fennoscandian bo eal oden s, Mic o us spp. and Myodes
u ocanus a e compe i i ely supe io o he bank ole [27,58,59].
Sh ews o genus So ex ha e been conside ed compe i i ely in e io
o neu al [60,61], bu expe imen al da a show ha bo h ield
oles and common sh ews can educe he home ange o b eeding
emale bank oles [62–64]. The e o e, one migh p esume ha in
sp ing when bank oles a e b eeding, bo h he p esence o non-
hos oden s o sh ews could al e he beha io o bank oles,
educing hei con ac a e wi h PUUV-in ec ed indi iduals o an
in ec ious en i onmen . In he all, mos bank oles we e sexually
inac i e and he e o e mo e ole an o conspeci ics [65]. As such,
in aspeci ic con ac a e and he p obabili y o acqui ing an
in ec ion may hen be less a ec ed by o he species, which could
explain why no dilu ion e ec was obse ed in he all.
In his s udy, and in se e al o he s conce ning han a i uses and
hei hos s [37–39,52,66], males we e mo e o en in ec ed han
emales. This obse a ion was limi ed o hea ie , ep oduc i e
indi iduals. Rega dless o whe he hese age- and sex- ela ed
di e ences esul om beha io al o immunological ac o s,
du a ion o exposu e, o biased weigh s o p egnan emales, we
emphasize he need o con ol o hese con ounding ac o s when
analyzing pa e ns o pa hogen p e alence o in ec ion p obabili y.
We obse ed ha young in ensi ely managed o es s a e
associa ed wi h lowe bank ole and highe non-hos densi ies.
Bo h hese cha ac e is ics o he small mammal communi y
educed he p obabili y o a bank ole being in ec ed wi h PUUV.
On he o he hand, we also obse ed a highe p obabili y o bank
oles being in ec ed when apped in young a he han old o es
s ands, i.e., a con a y e ec ha was no a ibu able o ei he hos
o non-hos densi y. In conclusion, we belie e ha he combined
e ec o hese h ee ac o s caused a homogeneous p e alence o
PUUV in bank oles among all o es age classes (Figu e 1B).
Table 2. GLMMs analyzing he p obabili y o a bank ole being PUUV in ec ed in sp ing and all.
Sp ing season Fall season
Pa ame e Es ima e
a
z P Es ima e
a
zP
In e cep
b
20.957 (0.387) 22.5 0.013 21.705 (0.149) 211.4 ,0.0001
Fo es age (25–30 y) 1.225 (0.454) 2.7 0.007 0.607 (0.221) 2.7 0.006
Fo es age (10–15 y) 0.547 (0.382) 1.4 0.152 0.458 (0.197) 2.3 0.020
Fo es age (4–8 y) 0.079 (0.421) 0.2 0.852 0.296 (0.223) 1.3 0.185
N o bank oles 0.059 (0.026) 2.3 0.023 0.017 (0.005) 3.3 0.001
N o o he small mammals 20.256 (0.109) 22.4 0.019 20.005 (0.009) 20.6 0.580
Sex (male) 0.626 (0.257) 2.4 0.015 0.158 (0.122) 1.3 0.196
Weigh 0.015 (0.057) 0.3 0.790 0.158 (0.019) 8.1 ,0.0001
Sex (male):Weigh 0.076 (0.082) 0.9 0.354 0.188 (0.039) 4.8 ,0.0001
In he sp ing, a iance a ibu able o andom o es pa e n e ec (39 g oups) was 0.10 wi h s anda d de ia ion 0.31 and o andom yea e ec (4 g oups) 0.22 wi h
s anda d de ia ion 0.47.
In he all, a iance a ibu able o andom o es pa e n e ec (40 g oups) was 0.05 wi h s anda d de ia ion 0.21 and o andom yea e ec (4 g oups) 0.00 wi h
s anda d de ia ion 0.00.
a
Es ima es a e gi en on logi scale and s anda d e o s o es ima es a e in pa en heses. Signi ican coe icien s a e in bold.
b
In e cep is calcula ed o a emale bank ole o a e age weigh , cap u ed om a 100+yea s and wi h a e age numbe s o bank oles and o he small mammals.
doi:10.1371/jou nal.pone.0039452. 002
In ensi e Fo es Managemen and Puumala Han a i us
PLoS ONE | www.plosone.o g 6 June 2012 | Volume 7 | Issue 6 | e39452
Conclusions
All o es age classes ha bo ed PUUV-in ec ed bank oles in he
cyclic peak phase, indica ing ha all o es habi a s, be hey
managed o old-g ow h, a e po en ial sou ces o NE in ec ion o
humans. In con as o he ag icul u al landscape in empe a e
Eu ope, in ensi e managemen o Fennoscandian o es s does no
c ea e signi ican ba ie s o he sp ead o bank oles and PUUV.
We ound bank oles apped in young o es s we e mo e likely
in ec ed, bu he mechanisms o his associa ion equi e u he
in es iga ion. We also ound in ec ion p obabili y o be hos
densi y dependen . Fu he mo e, we obse ed a s a is ically
signi ican dilu ion e ec in b eeding animals when hos densi y
was con olled o , bu no among non-b eeding indi iduals in he
all. Based on ou indings, i seems likely ha he species
composi ion o he small mammal communi y could indeed play
a ole in PUUV in ec ion dynamics.
Suppo ing In o ma ion
Figu e S1 Rep esen a i e pho og aphs o he ou
s udied o es age classes.
(TIF)
Acknowledgmen s
Da a on managemen his o y and loca ions o o es s ands in Tai alkoski
and Pudasja¨ i we e p o ided by he Finnish Fo es and Pa k Se ice. We
wish o exp ess ou since e g a i ude o h ee anonymous e e ees o hei
insigh ul c i icism and aluable ideas o imp o ing his manusc ip .
Au ho Con ibu ions
Concei ed and designed he expe imen s: SS HH. Pe o med he
expe imen s: SS LV. Analyzed he da a: LV ERK. Con ibu ed
eagen s/ma e ials/analysis ools: OV AV. W o e he pape : LV SS
ERK JL AV OV HH.
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In ensi e Fo es Managemen and Puumala Han a i us
PLoS ONE | www.plosone.o g 8 June 2012 | Volume 7 | Issue 6 | e39452