A ian op p eda o and he landscape o ea : esponses o
mammalian mesop eda o s o isk imposed by he golden
eagle
Ma i S. Lyly
1
, Alexand e Ville s
1,2
, Elina Koi is o
1
, Pekka Helle
3
, Tuomo Ollila
4
& E kki Ko pim€
aki
1
1
Sec ion o Ecology, Depa men o Biology, Uni e si y o Tu ku, FI-20014 Tu ku, Finland
2
Cen e d’E udes Biologiques de Chiz
e UMR 7372, CNRS & Uni e si 
e de La Rochelle, 79360 Beau oi su Nio , F ance
3
Finnish Game and Fishe ies Resea ch Ins i u e, Oulu Game and Fishe ies Resea ch, Uni e si y o Oulu, POB 413, FI-90014 Oulu, Finland
4
Finnish Fo es and Pa k Se ices, Na u al He i age Se ices, POB 8016, FI-96101 Ro aniemi, Finland
Keywo ds
In aguild p eda ion, mesop eda o
supp ession, pine ma en, ap o , ed ox,
ophic in e ac ions.
Co espondence
Ma i S. Lyly, Sec ion o Ecology, Depa men
o Biology, Uni e si y o Tu ku, FI-20014
Tu ku, Finland.
Tel: +358 2333 5813; Fax: +358 2333 6568;
E-mail: [email p o ec ed]
Funding In o ma ion
The s udy was inancially suppo ed by Jenny
and An i Wihu i Founda ion (g an s o MSL),
and he Academy o Finland (g an s no.
123379, 136717 and 250709 o EKo ).
Recei ed: 21 May 2014; Re ised: 23
No embe 2014; Accep ed: 25 No embe
2014
Ecology and E olu ion 2015, 5(2):
503–514
doi: 10.1002/ece3.1370
Abs ac
Top p eda o s may induce ex ensi e cascading e ec s on lowe ophic le els,
o example, h ough in aguild p eda ion (IGP). The impac s o bo h mamma-
lian and a ian op p eda o s on species o he same class ha e been ex ensi ely
s udied, bu he e ec s o he la e upon mammalian mesop eda o s a e no
ye as well known. We examined he impac o he p eda ion isk imposed by a
la ge a ian p eda o , he golden eagle (Aquila ch ysae os, L.), on i s po en ial
mammalian mesop eda o p ey, he ed ox (Vulpes ulpes, L.), and he pine
ma en (Ma es ma es, L.). The s udy combined 23 yea s o coun ywide da a
om nes ing eco ds o eagles and wildli e ack coun s o mesop eda o s in
Finland, no he n Eu ope. The p eda ion isk o he golden eagle was modeled
as a unc ion o e i o y densi y, densi y o ledglings p oduced, and dis ance
o nea es ac i e eagle e i o y, wi h he expec a ion ha a high p eda ion isk
would educe he abundances o smalle sized pine ma ens in pa icula . Red
oxes appea ed no o su e om eagle p eda ion, being in ac mos nume ous
close o eagle nes s and in a eas wi h mo e eagle e i o ies. This is likely due
o simila p ey p e e ences o he wo p eda o s and he la ge size o oxes
enabling hem o escape eagle p eda ion isk. Somewha con a y o ou p edic-
ion, he abundance o pine ma ens inc eased om low o in e media e e i-
o y densi y and a close p oximi y o eagle nes s, possibly because o simila
habi a p e e ences o ma ens and eagles. We ound a sligh ly dec easing end
o ma en abundance a high e i o y densi y, which could indica e ha he
esponse in ma en popula ions is dependen on eagle densi y. Howe e , mo e
esea ch is needed o be e es ablish whe he mesop eda o s a e in imida ed o
p eda ed by golden eagles, and whe he such e ec s could in u n cascade o
lowe ophic le els, bene i ing he bi o ous species.
In oduc ion
The adi ional iew o ophic dynamics has emphasized
he impo ance o bo om-up e ec s in ecosys ems, bu
ecen s udies ha e p o ided inc easing e idence o show
ha op-down p ocesses a e also ex ensi e and in luen ial
in shaping communi ies (e.g., Hebblewhi e e al. 2005;
Bo all and Ebenman 2006; Te bo gh and Es es 2010). A
ypical case o such p ocess is op p eda o s p eying upon
and limi ing he numbe s o he bi o es. Indeed, op p e-
da o s a e o en key species in hei ecosys ems and may
induce ex ensi e cascading e ec s on he lowe ophic
le els (Es es e al. 2011; Ripple e al. 2014).
Ano he pa hway o op-down e ec s is in aguild p e-
da ion (IGP), whe e p eda o y species compe e o e
sha ed p ey bu also p ey on each o he (Polis e al. 1989;
Lou enc
ßo e al. 2014). Among e eb a es, IGP is ypically
in lic ed by la ge species on hei smalle compe i o s,
he kille species being usually mo e han h ee imes
la ge han he ic im species (Paloma es and Ca o 1999;
Se gio and Hi aldo 2008). In addi ion o di ec killing
and consump ion, IGP o en induces a oidance and
ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
This is an open access a icle unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s use,
dis ibu ion and ep oduc ion in any medium, p o ided he o iginal wo k is p ope ly ci ed.
503
isk-sensi i e habi a selec ion in he p ey, educing hei
b eeding success and su i al (Mi chell and Banks 2005;
Se gio and Hi aldo 2008; Mukhe jee e al. 2009). Top
p eda o s may hus ac as an impo an mo ali y ac o
o smalle p eda o s (Ri chie and Johnson 2009; Pasa-
nen-Mo ensen e al. 2013) and gene a e a “landscape o
ea ” whe e mesop eda o s expe ience di e ing le els o
p eda ion isk (Laund 
e e al. 2001; Swanson e al. 2014).
Howe e , i op p eda o popula ions decline, hey can
cease o limi popula ions o mesop eda o s, as is sug-
ges ed by he mesop eda o elease hypo hesis (Soul
e
e al. 1988; C ooks and Soul
e 1999; P ugh e al. 2009).
Fo example, in Aus alia, he absence o a op p eda o ,
he dingo (Canis dingo, Meye ), has esul ed in a meso-
p eda o elease, which in u n has caused de as a ing
cascading e ec s on he small ma supial auna (Johnson
e al. 2007).
Mos o he p e ious s udies on e eb a e IGP ha e
ocused on wi hin-class p eda o guilds (mammal–mam-
mal IGP: Paloma es e al. 1995; Cou champ e al. 1999;
Helldin e al. 2006; Le nic e al. 2011; bi d–bi d IGP:
Hakka ainen and Ko pim€
aki 1996; Fielding e al. 2003;
Se gio and Hi aldo 2008; Lou enҫo e al. 2011). Fo
example, s udies om No h Ame ica show ha he wol
(Canis lupus, L.) has a nega i e impac on he coyo e
(Canis la ans Say) no jus ia p eda ion bu also
h ough in imida ion and ood compe i ion (Be ge and
Gese 2007; Mille e al. 2012). Mo eo e , he e is a clea
in e ac ion ex ending o he ed ox (Vulpes ulpes, L.):
when wol es a e p esen , oxes a e mo e nume ous han
coyo es, whe eas when wol es a e absen , coyo es domi-
na e in numbe s (Newsome and Ripple 2014). None he-
less, obse a ions om he p ey emains o la ge ap o s
show ha mammalian mesop eda o s succumb o p eda-
ion by bi ds, oo (Sulka a e al. 1997, 2008; Wa son
2010). This sugges s ha la ge bi ds o p ey could also
a ec he abundance and dis ibu ion o mammalian mes-
op eda o s. Ye , such p eda o y in e ac ions ha e been
epo ed only in a ew a icles (Ko pim€
aki and No dahl
1989; Roeme e al. 2002; Moeh enschlage e al. 2007;
Salo e al. 2008).
One o he la ges ap o species in he No he n
Hemisphe e is he golden eagle (Aquila ch ysae os, L.).
Many o i s popula ions c ashed du ing he ea ly 20 h
cen u y, la gely due o pe secu ion (Whi ield e al. 2004;
Ollila and Koskimies 2006; Wa son 2010). Cu en ly
golden eagle popula ions a e mainly s able o inc easing,
bu hei eco e y has been slowed down by habi a ag-
men a ion and inc eased human dis u bance (Wa son
2010). The golden eagle is a op p eda o , which can p ey
o e a wide ange o species, om small bi ds, and
oden s e en o ungula es as la ge as dee . The main p ey
i ems come om he g oups o ha es (Lepo idae), g ouse
(Te aonidae and Phasianidae), and squi els (Sciu idae)
(Wa son 2010). Wha di e en ia es golden eagles om
many o he ap o s is he ela i ely high pe cen age o
mammalian p eda o s in hei die (Valkama e al. 2005;
Lou enҫo e al. 2011), ypically anging om 2% o as
much as 10–20% (Wa son 2010). The e o e, he pauci y
o absence o he golden eagle may ha e con ibu ed o
he inc ease o mesop eda o s in many ecosys ems du ing
he pas decades (Ko pim€
aki and No ds €
om 2004).
The aim o his a icle was o expand he unde s and-
ing o in aguild ela ionships be ween a ian op p eda-
o s and mammalian mesop eda o p ey. We do so by
examining whe he he Finnish golden eagle popula ion
impac s abundances o wo ca ni o ous mesop eda o s,
he ed ox, and he pine ma en (Ma es ma es, L.).
Bo h species a e common in Finland (Wikman 2010) and
known o be p eyed upon by eagles (ca. 1% o esh p ey
emains a nes si es each, Sulka a e al. 1999). We com-
bine wo coun ywide da a se s ga he ed om Finland
o e se e al decades: he nes ing in en o y da a o golden
eagles and he wildli e snow- ack census da a, which as
annual moni o ing scheme o mul iple species is unique
in i s ex en and longe i y. We use es ima ed eagle e i-
o y and ledgling densi ies oge he wi h dis ance o he
nea es eagle nes as p oxies o he p eda ion isk, he
impac o which we hen examine on mesop eda o abun-
dances. Howe e , he mechanism o such impac can be
ei he di ec p eda ion, dispe sal due o in imida ion, o
bo h, and he wo phenomena canno be se apa wi h
obse a ional da a. Ins ead, we s udy he o e all impac
o eagles on mesop eda o abundances. We p edic ha
he abundance o he pine ma en, simila in size wi h
he main p ey i ems o eagle, will be lowe in a eas whe e
he e a e mo e ac i e eagle e i o ies and ledglings p o-
duced, and also in he icini y o inhabi ed eagle nes s. In
con as , we expec he la ge ed ox, which is a he
uppe end o he weigh scale o eagle p ey, no o
espond o ou p oxies o p eda ion p essu e.
Ma e ials and Me hods
Golden eagle da a
In Finland, he golden eagle is dispe sed o e an a ea la -
ge han 150,000 km²(Fig. 1), mainly wi hin he eindee
(Rangi e a andus, L.) husband y a ea in he no he n
pa s o he coun y (Ollila and Ilmonen 2009). Du ing
he pas decades, he numbe o b eeding eagle pai s has
been inc easing (Ollila and Koskimies 2006; Fig. 2),
eaching 348 inhabi ed e i o ies in 2014 (Ollila 2014).
The nes ing da a o he golden eagle, p o ided by he
Finnish Fo es and Pa k Se ice, include in o ma ion
abou nes occupancy and b eeding success o eagles in
504 ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Eagle P eda ion Impac upon Ma en and Fox M. S. Lyly e al.
Finnish nes ing si es. The da a a e de i ed om an ongo-
ing la ge-scale moni o ing o all known e i o ies and
ac i e sea ching o new ones, ca ied ou annually by
some 40 olun a y bi d inge s.
In his s udy, we included all he known e i o ies
ha had eco ds o eagle p esence du ing 1988–2011
(n=477, 6569 indi idual eco ds). Nes s we e annually
ca ego ized in o wo classes acco ding o hei b eeding
success: (1) unsuccess ully b eeding pai s (p esen bu
no b eeding, wi h possible eco ds o a ailed b eeding
a emp , such as b oken egg shells o emains o
chicks); and (2) success ully b eeding pai s (p esen
wi h ≥1 ledglings p oduced). To analyze he impac o
golden eagles upon mesop eda o species, we hen used
he eagle nes loca ions o o m wo ypes o annual
eagle densi y maps. In he e i o y densi y (TD) maps,
all ac i e golden eagle e i o ies we e included (classes
1–2), whe eas ledgling densi y (FD) maps we e o med
using only he nes s wi h ledglings p oduced (class 2),
mul iplied wi h he numbe o ledged chicks (1 o 2).
The ob ained coun ywide densi y maps e lec he p e-
da ion p essu e –bo h di ec and indi ec –by he
golden eagle.
The eagle densi y maps we e p oduced by compu ing a
smoo hed in ensi y unc ion ( as e size 1 km) om he
nes loca ions, using he “densi y.ppp” unc ion om
he R package “spa s a ” (Baddeley and Tu ne 2005).
The densi y.ppp compu es a ke nel es ima e (Diggle
1985) o he in ensi y unc ion o a poin p ocess, which
gene a ed he pa e n o nes s (u). I compu es he con o-
lu ion o he iso opic Gaussian ke nel wi h poin masses
a each da a poin in u:
kðuÞ¼ X
n
i
kðxiuÞwi
()
eðuÞ(1)
In he in ensi y unc ion k(u), he poin s in he neigh-
bo hood o a single poin ua e gi en by x
i
and hei
weigh s by w
i
, equaling o 1 in ou case. The edge co ec-
ion ac o o he densi y unc ion is gi en by e(u). The
amoun o smoo hing (i.e., s anda d de ia ion) in Gauss-
ian smoo hing ke nel kis de ined by as ollows:
0 50 100 150 200
km
N
Figu e 1. Map o Finland showing he loca ions o wildli e iangles
( iangle symbols) and golden eagle nes ing si es (g ey a ea) included
in he s udy. The nes ing si es a e p esen ed wi h a andomized
≤10 km o se and a 10 km bu e zone. The sou he n bo de o
eindee husband y a ea is p esen ed wi h a da k g ey line.
0 100 200 300 400
Yea
Numbe o e i o ies/ ledglings
88 90 92 94 96 98 00 02 04 06 08 10
Figu e 2. Popula ion ends o he golden eagle du ing 1988–2011
in Finland. The numbe o ac i e e i o ies (solid line) and ledglings
p oduced (dashed line) a e shown annually.
ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 505
M. S. Lyly e al. Eagle P eda ion Impac upon Ma en and Fox
kðx;yÞ¼ 1
2p 2ex2þy2
2 2(2)
The co e o a golden eagle e i o y does no ypically
ex end mo e han 3 km om he nes , bu eagles egula ly
isi si es u he om hei nes (McG ady e al. 2002),
especially a e he chicks ha e ledged. The e o e, he spa-
ial ex en wi hin which he eagle p eda ion migh be
s onges was es ed by calcula ing he densi y maps a i e
di e en le els o smoo hing, a 1–5 km. An op imal
le el o was hen selec ed h ough model compa ison.
Game animal abundance da a
The abundance da a o game animals om he wildli e
iangle scheme comp ised o snow- ack coun s o se e al
mammalian species om 1989 o 2011, de i ed om
1610 indi idual iangles (17,808 indi idual eco ds)
(Fig. 1). Da a we e p o ided by he Finnish Game
Resea ch Ins i u e, which coo dina es he annual na ion-
wide census pe o med by hun e s. T iangle loca ions a e
ixed, and mos , bu no all, iangles a e censused e e y
yea . The ack coun s a e ca ied ou mainly du ing Feb-
ua y by moni o ing he iangula 3 94 km ansec
lines, es ablished h oughou he coun y (Lind
en e al.
1996; Pellikka e al. 2005). Old acks a e co e ed by
snow all o ack coun e s, and a e a su icien ack
accumula ion ime, new acks a e coun ed. Typically, he
esul s o he ack coun s a e exp essed as ack densi y
(c ossings pe 24 h pe 10 km) (Pellikka e al. 2005), bu
in his s udy he o iginal ack coun obse a ions we e
used, complemen ed by a a iable epo ing he ack
accumula ion ime in days. Obse a ions wi h an espe-
cially long accumula ion ime (>10 days) we e disca ded.
Addi ionally, isual sigh ings o g ouse a e eco ded du -
ing he census, and hese abundance da a we e also
employed in his s udy.
Abundance index da a o wo common mesop eda o
species, ed ox and pine ma en, we e used as esponse
a iables. These wo mesop eda o s a e ai ly ac i e du -
ing win e and a e hus well p esen ed in he snow- ack
coun s. The ed ox, as a la ge species, may also p ey on
he smalle pine ma en (Linds €
om e al. 1995). The
indices o moun ain ha e (Lepus imidus, L.), cape caillie
(Te ao u ogallus, L.), black g ouse (Te ao e ix, L.),
hazel g ouse (Te as es bonasia, L.), and willow g ouse
(Lagopus lagopus, L.) we e also employed as explana o y
p ey co a ia es. Obse a ions o all he bi d species we e
summed oge he as he a iable “g ouse”. T ack coun s,
when used as a co a ia e, we e scaled wi h ack accumu-
la ion ime.
Using he midpoin coo dina es o he wildli e ian-
gles, he obse ed game abundances o an indi idual
iangle we e linked wi h he eagle densi ies ex ac ed
om he TD and FD as e maps a he same loca ion. In
a gi en yea , he game obse a ions we e linked wi h TD
o he same yea and wi h FD om he p e ious yea .
The eason o his was ha TD co esponds well o eagle
densi y du ing he win e since adul eagles keep o hei
e i o ies yea - ound, apa om he no he nmos pop-
ula ions ha a e o ced o mig a e because o se e e win-
e condi ions (McG ady e al. 2002; Wa son 2010).
Meanwhile, FD is a good p oxy o he hun ing p essu e
posed by eagles du ing he summe and au umn, when
he ledglings mo e abou he e i o y and hei pa en s
hun la ge amoun s o ood o hei o sp ing and hem-
sel es (Wa son 2010). Thus, FD would mos likely a ec
he obse ed mesop eda o abundances in he ollowing
win e .
In addi ion o he densi y a iables, he dis ance o he
closes ac i e eagle nes om each wildli e iangle was
calcula ed o each yea . The a iable “dis ance o nea es
nes ” (DNN) was hen used as a compe ing explana o y
eagle a iable and compa ed wi h TD and FD. DNN
inc eases linea ly when mo ing u he om he nes , and
he e o e, i may be e desc ibe he p eda ion e ec o
eagle a he pe iphe y o he e i o ies. Howe e , he
e ec o DNN is o in e es only wi hin dis ances wi hin
which eagles and mesop eda o s mo e abou , as i is no
plausible ha eagles would educe mesop eda o numbe s
a ou side hei e i o y limi s. Densi y a iables TD and
FD app oach ze o qui e quickly when mo ing u he
away om he e i o y co e a ea, bu hei ad an age is
ha hey a e able o accoun o wo o mo e e i o ies
close o each o he , whe eas DNN does no e lec he
o e all local eagle abundance well.
Habi a da a
As mesop eda o abundances depend on landscape ea-
u es, a iables desc ibing habi a composi ion we e
inco po a ed in o ou analyses. Habi a in o ma ion was
acqui ed om CORILIS da a ( as e size 1 91 km),
which gi es he p opo ion o di e en Co ine Land
Co e (CLC) classes wi hin a smoo hing adius o 5 km
(Eu opean En i onmen Agency 2009). The da a a e
de i ed om Landsa sa elli e image y om 2000. The
p opo ions o a mland and o es in he landscape we e
calcula ed by summing he p opo ions o CLC classes
12–22 and 23–29, espec i ely. Habi a p opo ions we e
hen assigned o each wildli e iangle acco ding o he
as e cell in which he iangle midpoin was loca ed, so
ha he a iables gi e pe cen ages o a mland and o es
in he landscape wi hin a 5 km adius om he iangle
cen e s. The amoun o a mland and o es habi a
wi hin landscape has p e iously been ound o in luence
506 ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Eagle P eda ion Impac upon Ma en and Fox M. S. Lyly e al.
he abundances o ed oxes and pine ma ens (Ku ki
e al. 1998).
La i ude and longi ude a iables we e included in he
models as hey we e expec ed o explain he impac o
egionally a ying en i onmen al condi ions upon he
mesop eda o s. The p oduc i i y o he o es s in no h-
e n Finland is dis inc ly lowe han in he sou he n pa s
o he coun y (Pel ola 2009). Rela ed o his, condi ions
in no he n Finland a e ha she han in he sou h, as
empe a u es a e lowe and he e is ypically mo e snow-
all du ing he da k pola win e s. On he o he hand,
eindee husband y occu s only in he no he n pa s o
Finland (Fig. 1), and in his a ea, he die o he golden
eagle also includes eindee s, mainly in he o m o cal es
and ca casses (Nybakk e al. 1999; Sulka a e al. 1999;
No be g e al. 2006).
S a is ical analyses
Fo da a handling and analyses, we used R-so wa e, e -
sion 3.0.2 (R Co e Team 2013). S a is ical analyses we e
conduc ed wi h gene alized addi i e mixed model
(GAMM), using he “gamm” unc ion om he package
“mgc ” (Wood 2011).
To analyze he impac o golden eagle upon he abun-
dance indices o ed ox and pine ma en, we buil mod-
els wi h quasi-Poisson dis ibu ion. DNN, and TD and
FD wi h 1–5 km we e all se as explana o y a iables in
sepa a e models (11 models in o al). The in e ac ion o
longi ude and la i ude was included in he models o
accoun o la ge-scale spa ial au oco ela ion. Also, he
ollowing co a ia es we e cen e ed and scaled, ollowing
Schielze h (2010), and included in he model s uc u e:
he p opo ion o a mland, he p opo ion o o es ,
moun ain ha e abundance, g ouse abundance, and he
ime o mesop eda o ack accumula ion in days. In he
pine ma en models, he abundance o he la ge ed ox
was also included as a p eda o co a ia e. To accoun o
epea ed samples om he same iangles, ha is, o han-
dle pseudo- eplica ion issues (Hu lbe 1984), a andom
s uc u e o indi idual iangles and an AR1 co ela ion
s uc u e o iangle ID wi hin yea we e included in all
models.
Model selec ion was s a ed by i ing a smoo he o all
co a ia es excep he ack accumula ion day, which was
expec ed o ha e a linea ela ion wi h he esponse a i-
able. Fo o he a iables han eagle and coo dina es, he k
(uppe limi on he deg ees o eedom associa ed wi h a
smoo h) was cons ic ed o imp o e con e gence. F om
linea es ima es, he unnecessa y smoo he s we e emo ed
and hen he model was e i ed. A e his, all nonsigni i-
can a iables we e emo ed –only eagle a iables we e
always e ained as a minimal model s uc u e in o de o
imp o e he compa abili y o he models. The bes o
TD and FD was selec ed based on he amoun o de iance
explained in he inal models (in TD models 4 km o ed
ox, 5 km o pine ma en; in FD models 5 km o bo h
species, see Table 1). Resul s a e epo ed only o models
TD ,FD ,and DNN o ed ox and pine ma en ( o
a iables e ained in inal models, see Table 2).
Resul s
Red ox
The ela ionship be ween he e i o y densi y (TD,
4 km) and ed ox abundance was linea : he mo e eagles
he e we e, he highe ox numbe s we e ( =2.305,
P=0.021, Fig. 3A). In con as , ledgling densi y o
eagles in he p e ious yea (FD, 5 km) had no ob ious
associa ion wi h ox abundance ( =0.777, P=0.437,
Fig. 3B). The in luence o dis ance o nea es eagle nes
(DNN) was nonlinea , bu when examined only a close
dis ances (up o 30 km) i was ai ly linea : he sho e
he dis ance o ac i e eagle nes s was, he mo e oxes
he e we e (F=6.337, P<0.001, Fig. 3C).
Table 1. The amoun o de iance explained (DE) in all ed ox and pine ma en models. Models selec ed based on hei DE ha e bolded alues.
Red ox models DE Pine ma en models DE
Dis ance o nea es nes 95145.24 Dis ance o nea es nes 19079.21
Te i o y densi y, 4km 94824.11 Te i o y densi y, 5km 18762.96
Te i o y densi y, 3 km 94823.30 Te i o y densi y, 4 km 18750.45
Te i o y densi y, 5 km 94811.90 Te i o y densi y, 3 km 18668.46
Te i o y densi y, 2 km 94786.98 Te i o y densi y, 2 km 18639.04
Fledgling densi y, 5km 94778.21 Fledgling densi y, 5km 18630.63
Fledgling densi y, 4 km 94773.42 Fledgling densi y, 4 km 18607.4
Fledgling densi y, 3 km 94759.72 Fledgling densi y, 3 km 18597.67
Fledgling densi y, 1 km 94753.89 Fledgling densi y, 2 km 18581.58
Fledgling densi y, 2 km 94751.36 Fledgling densi y, 1 km 18568.67
Te i o y densi y, 1 km 94751.32 Te i o y densi y, 1 km 18567.63
ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 507
M. S. Lyly e al. Eagle P eda ion Impac upon Ma en and Fox

The impac o habi a a iables on ed oxes was he
same in all h ee models (see Table S1 o all esul s).
In e media e p opo ions o a mland and low o in e -
media e p opo ions o o es in he landscape we e mos
bene icial o oxes. As expec ed, he abundance o oxes
inc eased wi h inc easing moun ain ha e numbe s,
al hough his associa ion le eled o a e y high ha e
abundances. In spa ial e ms, he model p edic ed highes
ox abundances in ag icul u e- and o es -domina ed
sou hwes Finland, g adually dec easing owa d no heas ,
wi h a local dec ease in he eas e n pa s o Middle
Finland.
Pine ma en
Te i o y densi y (TD, 5 km) had a nonlinea ela ion-
ship wi h pine ma en abundance: om low o in e medi-
a e TD, he amoun o ma ens sligh ly inc eased, bu a
high TD, i appea ed o dec ease (F=5.300, P=0.004,
Fig. 4A). Howe e , wide con idence in e als esul ing
om ela i ely ew da a poin s a high eagle densi ies
necessi a e cau ion when in e p e ing he associa ion.
Fledgling densi y (FD, 5 km) had no ob ious associa-
ion wi h he ma en abundances ( =1.412, P=0.158,
Fig. 4B). Dis ance o nea es nes (DNN) had a nonlinea
impac on pine ma en abundance, which a close ange
o ac i e eagle nes s ansla ed o he sho e he dis ance,
he mo e ma ens he e we e (F=5.008, P<0.001,
Fig. 4C).
The esponse o ed ox abundance was signi ican and
iden ical in all o he h ee pine ma en models: he num-
be o ma ens obse ed inc eased sligh ly when he ox
abundance inc eased om low o in e media e ox abun-
dance, bu a high ox abundances he numbe o ma ens
dec eased (F=23.695, P<0.001, Fig. 5). To be conse a-
i e, he esul s a e epo ed om he DNN-model, which
had he lowes F- alue. Mo eo e , all h ee models p e-
dic ed pine ma en abundances o be highes when he
p opo ion o o es in he landscape was high (see Table
S1 o all esul s). The esponse o p opo ion o a m-
land was nonlinea , wi h lowes ma en abundances
occu ing a landscapes wi h in e media e amoun s o
a mland. Spa ially examined he highes ma en abun-
dances occu ed in sou he n and cen al Finland and he
lowes in he wes e n pa s o Middle Finland.
Discussion
We examined he abundances o wo mammalian meso-
p eda o s, he ed ox, and he pine ma en, in ela ion o
he p eda ion isk imposed by he golden eagle by com-
bining long- e m da a om moni o ing o game animal
abundances and eagle nes ing. We p edic ed ha ma en
abundance indices would be lowe in a eas whe e he e
a e mo e ac i e eagle e i o ies and ledglings p oduced,
and also when close o inhabi ed eagle nes s, whe eas ed
ox abundances would no espond nega i ely o hese
ac o s. Ou esul s show ha bo h mesop eda o s we e
mos abundan in a eas o high e i o y densi y and e y
close o ac i e eagle nes s. In ega ds o he pine ma en,
his was he opposi e o ou p edic ion. Howe e , he
esul s ga e some indica ion ha eagles could be ha m ul
o pine ma ens a e y high e i o y densi ies.
Acco ding o ou esul s, ed oxes seem o be abun-
dan in he icini y o ac i e golden eagle nes s. Al hough
he amoun o o es and a mland in he landscape was
accoun ed o , we suspec ha he e we e s ill some unex-
plained ac o s ha bo h eagles and oxes bene i om,
esul ing in inc eased densi ies o bo h species in he same
a eas. The golden eagle is sensi i e o any human dis u -
bance (Ollila and Koskimies 2006; Kaisanlah i-Jokim€
aki
e al. 2008), and he ed ox can manage well in emo e
a eas oo, al hough i bene i s om agmen ed landscapes
occu ing close o human inhabi a ion (Ku ki e al.
1998). Foxes and eagles p ey pa ly on same p ey species,
such as ha es, g ouse, and o he bi ds (Kauhala e al.
1998; Sulka a e al. 1999; Dell’A e e al. 2007). The
amoun o ha e and g ouse was aken in o accoun , bu
su icien a ailabili y o o he sha ed p ey could enable
he wo species o h i e in same a eas. Fo example, he
local a ailabili y o eindee ca casses would p o i bo h
species. All in all, i seems ha a he popula ion le el
Table 2. Re ained a iables in he selec ed GAMM models o ed ox and pine ma en. The a iables applied wi h smoo he s a e in i alics. In e -
ac ions a e ma ked wi h a symbol 9. E and N e e o la i udinal and longi udinal coo dina es and abb e ia ion acc.days o he snow- ack accu-
mula ion ime in days.
Response P eda o s Loca ion, habi a P ey, census ime
Red ox Te i o y densi y E9N, a mland, o es Moun ain ha e, acc. days
Red ox Fledgling densi y E9N, a mland, o es Moun ain ha e, acc. days
Red ox Dis ance o nea es nes E 9N, a mland, o es Moun ain ha e, acc. days
Pine ma en Te i o y densi y, ed ox E 9N, a mland, o es Moun ain ha e, acc. days
Pine ma en Fledgling densi y, ed ox E 9N, a mland, o es Moun ain ha e, acc. days
Pine ma en Dis ance o nea es nes , ed ox E 9N, a mland, o es Moun ain ha e, acc. days
508 ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Eagle P eda ion Impac upon Ma en and Fox M. S. Lyly e al.
oxes a e able o a oid he ha m ul impac s o eagle p e-
da ion o in imida ion, as hey did no espond o he
landscape o ea modeled by eagle p esence. This can
esul om he ac ha ed oxes a e usually o he same
weigh o e en la ge han golden eagles, whe eas in IGP,
he kille is ypically clea ly la ge han he p ey (Palo-
ma es and Ca o 1999; Se gio and Hi aldo 2008).
Te i o y densi y ( e i o ies/100 km²)
Red ox abundance ( acks obse ed/day)
(A)
01234
23456789
0.0 0.5 1.0 1.5
2.5 3.0 3.5 4.0 4.5 5.0
0 5 10 15 20 25 30
3.0 3.5 4.0 4.5 5.0
Fledgling densi y ( ledglings/100 km²)
Red ox abundance ( acks obse ed/day)
(B)
Dis ance o nea es nes (km)
Red ox abundance ( acks obse ed/day)
(C)
Figu e 3. Red ox snow- ack abundance es ima es a a ying golden
eagle e i o y densi y (TD, panel A), ledgling densi y (FD, panel B),
and dis ance o nea es nes (DNN, panel C), p esen ed wi h 95% CI
(dashed lines).
Te i o y densi y ( e i o ies/100 km²)
Pine ma en abundance ( acks obse ed/day)
(A)
Fledgling densi y ( ledglings/100 km²)
Pine ma en abundance ( acks obse ed/day)
(B)
0.0 0.5 1.0 1.5 2.0 2.5
0.0 0.5 1.0 1.5
0.0 0.5 1.0 1.5
0.0 0.5 1.0 1.5
0 5 10 15 20 25 30
0.0 0.5 1.0 1.5
Dis ance o nea es nes (km)
Pine ma en abundance ( acks obse ed/day)
(C)
Figu e 4. Pine ma en snow- ack abundance es ima es a a ying
golden eagle e i o y densi y (TD, panel A), ledgling densi y (FD,
panel B), and dis ance o nea es nes (DNN, panel C), p esen ed wi h
95% CI (dashed lines).
ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 509
M. S. Lyly e al. Eagle P eda ion Impac upon Ma en and Fox
Simila ly o he ed ox, he abundance o pine ma en
was ound o co ela e posi i ely wi h eagle e i o y den-
si y, speci ically when mo ing om low o in e media e
densi ies. This likely de i es om he ac ha he golden
eagle and he pine ma en bene i om simila habi a s.
Al hough he amoun o o es co e age was con olled
o in he analyses, he e is also a ia ion be ween o es
s ands in e ms o wood olume, ee densi y, and s and
age. Ma ens eside mainly in o es ed a eas and p e e o
mo e in old sp uce- and pine-domina ed s ands (B ain-
e d and Rols ad 2002). Golden eagles ypically nes in
la ge pines (Ollila and Koskimies 2006), bu habi a s p o-
iding hese ees a e limi ed in Finnish o es s. Thus,
excluding e y dense o es s ands ha a e di icul o
eagles o mo e in, he wo species likely eside in simila
ype o habi a s. This was also suppo ed by he ac ha
we obse ed highe ma en abundances wi hin sho e
dis ances om ac i e eagle nes s.
A densi y-dependen p eda ion impac was ound wi h
ed oxes on pine ma ens: a high abundances, oxes
could ac as an IG p eda o o ma en. Red oxes ha e
been obse ed o p ey on pine ma ens, o example, in
Sweden, whe e he dec ease o oxes in 1980s due o sa c-
op ic mange, caused by a pa asi ic mi e, was ollowed by
an inc ease in he numbe o ma ens (Linds €
om e al.
1995). Howe e , landscape-le el s udies om Fennoscan-
dia ha e epo ed con a y esul s (Ku ki e al. 1998).
Conside ing ed oxes and pine ma ens, i is impo an
o no e ha hese gene alis p eda o s may also compe e
o e he same ood esou ces, which likely in ensi ies hei
in e ac ion a high abundances. Die s udies ha e shown
ha he o e all p ey selec ion o he wo species is o e -
lapping, al hough ma ens ha e less la ge-sized p ey in
hei die han oxes do (Pulliainen and Ollinm€
aki 1996;
Kauhala e al. 1998).
Ou esul s emphasize he impo ance o he iming o
obse a ions; in con as o e i o y densi ies om he
same ime pe iod, mesop eda o abundances did no
espond o he ledgling densi y o eagles in he p e ious
summe . One eason o his could be ha a e ledging,
ju enile eagles mo e ou side he home ange o such an
ex en ha a clea p eda ion impac wi hin he e i o y
canno be obse ed. In addi ion, young eagles ypically
s a dispe sing al eady du ing la e au umn (Wa son
2010), a e which he p eda ion impac is gene a ed
solely by he adul s emaining a he e i o y. Fu he -
mo e, mo emen s o he mesop eda o p ey can dilu e
he e ec o eagle p eda ion. The e o e, a ime lag o o e
6 mon hs may be oo long o any p eda ion impac o
show on mesop eda o abundances. Ins ead, i could be
be e o s udy he impac o b eeding eagles and hei
ledglings on mesop eda o abundances in au umn. Es i-
ma ed eagle e i o y densi y, which is able o accoun o
mul iple close e i o ies, was pe haps he bes p oxy o
p eda ion isk, al hough he dis ance o eagle nes
explained he la ges amoun o a ia ion in he da a.
We expec ed o de ec a p eda ion impac o golden
eagle upon pine ma en abundance, bu he analyses did
no p o ide subs an ial suppo o his. Howe e , we
wish o no e ha he da a showed a dec easing end in
ma en abundance a high e i o y densi ies o eagles,
ha is, when he e is one o mo e esiden eagle pai
wi hin he a ea. As he impac o oxes was sepa a ely
con olled o in ou analyses, we do no belie e ha his
end was a esul o combined p eda ion p essu e by
eagle and ox. Ins ead, a esponse o he landscape o ea
shaped solely by he eagle emains a mo e plausible expla-
na ion. A e all, ma ens weigh app oxima ely only one-
hi d o he weigh o he eagle and a e hus an easie
p ey o he eagle o hun han oxes a e. I has p e iously
been no ed ha pine ma ens a oid e y open a eas and
clea cu s (B aine d and Rols ad 2002), and his local-
scale habi a p e e ence o ma ens could be ela ed o he
h ea o golden eagle p eda ion (Ko pim€
aki and No d-
s €
om 2004). In gene al, medium-size p eda o s ac i ely
a oid habi a s u ilized by apex p eda o s (Fed iani e al.
1999; Mukhe jee e al. 2009). Simila ly, he eagle could,
in addi ion o di ec killing, educe ma en numbe s by
in imida ion. Also, eagles may dis u b ma ens and ham-
pe hei o aging, hence dec easing hei i ness. In an
ea lie s udy, p eda ion isk imposed by he whi e- ailed
sea eagle (Haliaee us albicilla, L.) has been shown o
educe he swimming ips o ano he mus elid species,
he Ame ican mink (Neo ison ison, Sch ebe ) (Salo e al.
2008). In con as , s ong ood compe i ion among
golden eagles and pine ma ens is unlikely, as he die o
0 50 100 150 200
0.0 0.5 1.0 1.5 2.0
Red ox abundance ( acks obse ed/day)
Pine ma en abundance ( acks obse ed/day)
Figu e 5. Pine ma en snow- ack abundance es ima es a a ying
ed ox abundances, e ie ed om he dis ance o nea es nes
(DNN) model. 95% CI a e p esen ed wi h dashed lines.
510 ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d.
Eagle P eda ion Impac upon Ma en and Fox M. S. Lyly e al.
hese species is ai ly b oad ye no o e lapping much
(Pulliainen and Ollinm€
aki 1996; Wa son 2010). Resea ch
conduc ed a ine spa ial scales could help o es ablish
whe he an abundan eagle popula ion causes any educ-
ion in pine ma en numbe s, o example, ia beha io al
changes ha esul in lowe i ness. New in o ma ion on
he impac o he golden eagle could be acqui ed, o
example, by adio- acking habi a use o ma ens and
obse ing he p eda ion beha io o eagles.
When abundan , mesop eda o s hold he po en ial o
induce bo h ecological and economic cos s wi h hei ou -
b eaks (P ugh e al. 2009), and he e o e, unde s anding
p ocesses ela ed o hei abundance is impo an . Species
such as he ed ox, pine ma en, and Ame ican mink a e
sugges ed o limi o be he cause o decline o ha e and
bi d popula ions (Ma cs €
om e al. 1988; Linds €
om e al.
1994; Kauhala and Helle 2000; No ds €
om e al. 2002).
No su p isingly, IGP om a op p eda o upon mesop e-
da o s may also cause cascading impac s on he bi o es
(e.g., Henke and B yan 1999; Helldin e al. 2006; P ugh
e al. 2009). Elmhagen e al. (2010) showed ha when he
ecolonizing lynxes (Lynx lynx, L.) limi ed ox popula-
ions, his has an indi ec posi i e impac on moun ain
ha e abundance. Fielding e al. (2003) sugges ed ha
h ough supp essing medium-sized ap o s he golden
eagle could educe he o e all p eda ion p essu e on game
species. Howe e , such cascading e ec s wi h a ian–mam-
malian IGP ha e no eally been examined, e en hough
hey could ha e ex ensi e in luence on ecosys ems. Fo
example, on he Cali o nia Channel Islands (USA), he
in oduc ion o an exo ic p ey has enabled he golden
eagle o s ongly eshape he local mesop eda o commu-
ni y and indi ec ly a ec he g ani o e p ey (Roeme
e al. 2009). In no he n Eu ope, he eagle owl (Bubo
bubo) could also be ac ing as p ominen a ian op p eda-
o (Ko pim€
aki and No ds €
om 2004).
Based on he esul s p esen ed he e, i is no clea
whe he he bi o es (e.g., ha es and g ouse) would bene i
om eagles p eying upon and in imida ing ed ox and
pine ma en. None heless, i is impo an o keep in mind
ha he Finnish mesop eda o guild en ails se e al o he
species ha may be in luenced by eagles. Mo eo e , by
expanding hei ange in he u u e, golden eagles (Ollila
and Ilmonen 2009; Wa son 2010) as well as o he ap o s
may inc ease p eda ion on mesop eda o s in new a eas.
This could, in u n, imp o e he p o ec ion s a us o golden
eagles and ap o s in gene al i ap o -induced mesop eda-
o supp ession we e o bene i he bi o ous species. In
addi ion, he p eda ion impac s o ap o s could be com-
pa ed wi h hose caused by mammalian op p eda o s,
which in Finland include he inc easingly nume ous lynx
and bea (U sus a c os), as well as he less common and
p obably only locally ele an wol and wol e ine (Gulo
gulo, L.) (Wikman 2010). This ype o compa ison o he
s eng h o op-down supp ession would help o assess he
impo ance o ap o s in bo eal ecosys ems.
Conclusions
This s udy p o ides no el in o ma ion on a ian–mamma-
lian IGP by examining he ela ionship be ween he
golden eagle and i s po en ial p ey, he pine ma en and
he ed ox. We ound bo h mesop eda o species o be
mos abundan in p oximi y o he golden eagle sugges -
ing ha killing and in imida ion by eagles may no be a
ele an cause o dec ease o popula ions o ma ens and
oxes. Howe e , we su mise ha pine ma ens could su -
e om p eda ion a high densi ies o eagle e i o ies,
pa icula ly due o hei smalle size. The in o ma ion
epo ed in his a icle imp o es ou unde s anding o he
ole o a ian op p eda o s in e es ial communi ies, bu
u he long- e m s udies a e equi ed o o m a clea e
pic u e o he impac s ha eco e ing a ian op p eda-
o s, such as he golden eagle, ha e on p eda o guilds.
Ga he ing beha io al da a would also help us o unde -
s and in mo e de ail how mesop eda o s cope wi hin he
p esence o la ge a ian p eda o s. Po en ial cascading
e ec s o mesop eda o supp ession on lowe ophic
le els would be o g ea in e es , oo.
Acknowledgmen s
We hank all he olun ee s who ha e helped o collec
he golden eagle and game abundance da a. We also
hank E ic Le To o ec o e ising he language and he
edi o s and an anonymous e iewe o help ul commen s
on he d a manusc ip . The s udy was inancially sup-
po ed by Jenny and An i Wihu i Founda ion (g an s o
MSL), and he Academy o Finland (G an Nos. 123379,
136717 and 250709 o EKo ).
Con lic o In e es
None decla ed.
Da a Accessibili y
Da a used o his s udy can be ound in D yad da a
a chi e (ASCII ex ile, doi: 10.5061/d yad.qc6n ). The
loca ion da a a e no included o a oid endange ing nes -
ing si es o he golden eagle. Habi a da a come om he
Eu opean En i onmen Agency (2009).
Re e ences
Baddeley, A., and R. Tu ne . 2005. spa s a : an R package o
analyzing spa ial poin pa e ns. J. S a . So w. 12:1–42.
ª2015 The Au ho s. Ecology and E olu ion published by John Wiley & Sons L d. 511
M. S. Lyly e al. Eagle P eda ion Impac upon Ma en and Fox