RESEARCH ARTICLE Open Access
In e speci ic in o ma ion on p eda ion isk
a ec s nes si e choice in a passe ine bi d
Je e Tol anen
1,8*
, Janne-Tuomas Seppänen
2,3
, Mikko Mönkkönen
4
, Robe L. Thomson
5,6
, Hannu Ylönen
7
and
Jukka T. Fo sman
1,8
Abs ac
Backg ound: B eeding si e choice cons i u es an impo an pa o he species niche. Nes p eda ion a ec s
b eeding si e choice, and has been sugges ed o d i e niche seg ega ion and local coexis ence o species. In e speci ic
social in o ma ion use may, in u n, esul in copying o ejec ion o he e ospeci ic niche cha ac e is ics and hus a ec
ealized niche o e lap be ween species. We es ed expe imen ally whe he a mig a o y bi d, he pied lyca che
Ficedula hypoleuca, collec s in o ma ion abou nes p eda ion isk om indi ec cues o p eda o s isi ing nes s o
he e ospeci ic bi ds. Fu he mo e, we in es iga ed whe he he mig a o y bi ds can associa e such in o ma ion wi h a
speci ic nes si e cha ac e is ic and gene alize he in o ma ion o hei own nes si e choice.
Resul s: Ou esul s demons a e ha lyca che s can use he a e o he e ospeci ic nes ing a emp s in hei own nes
si e choice, bu do so selec i ely. Young lyca che emales, when making he decision quickly, associa ed he a e o an
a i icial nes wi h nes -si e cha ac e is ics and a oided he cha ac e is ic associa ed wi h highe nes p eda ion isk.
Conclusions: Copying nes si e choices o success ul he e ospeci ics, and a oiding choices which led o ailed
a emp s, may ampli y o coun e e ec s o nes p eda ion on niche o e lap, wi h impo an consequences o
be ween-species niche di e gence-con e gence dynamics, species coexis ence and p eda o -p ey in e ac ions.
Keywo ds: Social in o ma ion, Nes si e choice, P eda ion isk, Realized niche, Species coexis ence, In aspeci ic a ia ion
Backg ound
The niche concep is a cen al ene in he heo y o spe-
cies coexis ence and communi y ecology, s a ing ha wo
species canno coexis wi hou adequa e niche di e ences
[1–4]. One impo an axis o he species niche is he cha -
ac e is ics o o sp ing p oduc ion si e (nes , den, e c).
Choice o he o sp ing p oduc ion (b eeding) si e de e -
mines he a ailable esou ces and h ea s ha he animal
and i s o sp ing encoun e , making i an impo an
i ness- ela ed decision. Resou ces and p eda ion isk a e
also a ec ed by he decisions o o he indi iduals in he
communi y, including hose o o he species.
B eeding si e choice d i en by a ying nes p eda ion
p essu e has been shown o be an impo an mechanism
a ec ing species coexis ence [5–7]. This idea is based on
unc ional esponses o nes p eda o s o highe o e all
nes densi y in a speci ic mic ohabi a when wo o mo e
species p e e he same mic ohabi a [5,7,8]. Inc eased
nes p eda ion a es in each species would hen selec o
niche di e gence in mic ohabi a o nes si e choice, and
he eby acili a e local coexis ence o he species [5–7].
Besides a ec ing species coexis ence, nes p eda ion is an
impo an gene al selec i e o ce in animals [9,10]. I usu-
ally esul s in comple e b ood loss and o sho -li ed
species, ailing e en a single b eeding a emp may esul
in ze o li e- ime ep oduc i e success. Howe e , nes p e-
da ion isk a ies in space and ime (e.g. [11–13]). Conse-
quen ly, he abili y o indi iduals o espond o cues on
he ela i e isk o nes p eda ion in di e en habi a s and
imes should be highly adap i e.
Di ec obse a ions o o en s eal hy, widely anging and
quickly mo ing nes p eda o s a e ela i ely a e e en s
o an obse e , and he e o e o e li le in o ma ion o
decision-making. Encoun e s wi h nes p eda o s may also
h ea en he obse e i sel (e.g. [14,15]). Ye , o example,
bi ds can clea ly espond o he densi y o nes p eda o s
* Co espondence: [email p o ec ed]
1
Depa men o Ecology and Gene ics, Uni e si y o Oulu, 90014 Oulu,
Finland
8
Cu en Add ess: Na u al Resou ces Ins i u e Finland (Luke), Uni e si y o
Oulu, Paa o Ha aksen ie 3, 90014 Oulu, Finland
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Tol anen e al. BMC E olu iona y Biology (2018) 18:181
h ps://doi.o g/10.1186/s12862-018-1301-3
when making habi a choices [16] and o sp ing in es -
men decisions [17]. A po en ial mechanism o es ima e
p eda o incidence wi hou di ec isual o acous ic de ec-
ion is cueing on indi ec signs o p eda o s such as odou ,
exc emen s o o he aces [18–22]. Beha iou , b eeding
si e choices and success o o he conspeci ic o he e ospe-
ci ic indi iduals may also p o ide in o ma ion abou p e-
da ion isk [23–25]. A po en ially p o i able s a egy is o
ollow he decisions and he esul ing success (e.g. nes
dep eda ed o no ) o hose he e ospeci ics which b eed a
li le ea lie han he obse e [24,26]. B eeding a emp s
o such he e ospeci ics could p o ide he mos up- o-da e
in o ma ion abou nes p eda ion isk.
He e ospeci ic social in o ma ion use is expec ed o be
mos use ul be ween ecologically simila species [24], in
his case be ween species ha a e h ea ened by a simila
se o p eda o s. Ins ances o social in o ma ion use, such
as he e ospeci ic a ac ion and copying o beha iou s (e.g.
[26–30]) can esul in posi i e i ness e ec s o he in o -
ma ion use [27]. Thus social in o ma ion use may a o
main aining o inc easing ecological simila i y be ween
species in a communi y. Howe e , ecological simila i y
also inc eases compe i ion o sha ed esou ces (e.g. ood,
nes si es), a o ing dec easing ecological simila i y
be ween compe ing species: niche di e gence ia cha ac e
displacemen is a cen al pa adigm o species coexis ence
heo y [1–4]. Nes p eda ion may he e o e igge bo h
di e gence and con e gence o ealized niches, and bo h
could concei ably be ampli ied by social in o ma ion use.
Resul ing dynamics can be complex, scale-sensi i e, and
highly dependen on local condi ions and communi y
composi ion.
He e, we es ed expe imen ally whe he a mig a o y,
ca i y-nes ing bi d, he pied lyca che (Ficedula hypo-
leuca), collec s in o ma ion abou nes p eda ion isk
om indi ec cues o p eda o s isi ing nes s o a he -
e ospeci ic esiden bi d, he g ea i (Pa us majo ).
We hen in es iga ed whe he he mig a o y bi d can
associa e such in o ma ion wi h a speci ic nes si e
cha ac e is ic, a e able o gene alize he pe cei ed in o -
ma ion and use i in guiding hei own nes -si e choice.
G ea i s and lyca che s a e pu a i e compe i o s [31,
32], ye lyca che s use i s as a sou ce o in o ma ion
in many c ucial decisions, such as b eeding si e choice
ando sp ingin es men [27,30,33,34]. I pied
lyca che s can associa e p eda ion isk wi h a pa icu-
la nes -si e cha ac e is ic o hei pu a i e compe i o s,
we expec hem o p e e acan nes si es exhibi ing
he same cha ac e is ic as he ‘low- isk’nes si es o
he e ospeci ics.
Me hods
We conduc ed he ield expe imen in no he n Finland
(N 65°, E 25°) du ing b eeding seasons in 2013–2016.
The expe imen al design consis ed o sepa a e nes box
si es se up in habi a s sui able o b eeding pied ly-
ca che s, a leas one kilome e apa o imp o e inde-
pendence. Each si e included wo pai s o nes boxes (see
Fig. 1 o a schema ic illus a ion o he expe imen al
design). In one pai ( he ‘in o ma ion box pai ’)wecon-
s uc ed inside bo h nes boxes a i icial g ea i nes s o
Fig. 1 Schema ic illus a ion o he expe imen al se up
Tol anen e al. BMC E olu iona y Biology (2018) 18:181 Page 2 o 8
moss and sheep hai . We assume lyca che s pe cei ed
hese a i icial nes s as genuine i nes s, o a leas as he -
e ospeci ic nes s, because hei own nes s consis solely o
plan ma e ial (wood ba k, hay) and a e clea ly dis in-
guishable om i nes s.
The a i icial nes s we e andomly assigned o ea -
men s wi h o wi hou simula ed nes p eda o isi s.
One o he boxes ep esen ed he ‘high- isk’nes si e,
whe e we sp ayed aeces and u ine o mus elids (Mus ela
ni alis ni alis,Mus ela e minea and Ma es ma es;
abundan nes p eda o s in he s udy a ea) dissol ed in
wa e inside and ou side he nes box and on he base o
he ee he nes box was a ached o. The wa e -exc e-
men mix was made by mixing sawdus con aining mus-
elid u ine and aeces wi h wa e and le ing he u ine
and aeces dissol e in he wa e o e wo days (see [19]
o mo e de ailed in o ma ion). Sawdus con aining mus-
elid aeces and u ine was ob ained om cages o cap i e
indi iduals a Konne esi Resea ch S a ion and Ranua
Zoo. In addi ion, we pu wo pieces o mus elid aeces
and ew agmen s o a common hen (Gallus Gallus
domes icus) egg on op o he nes . The o he nes box
wi hin he ‘in o ma ion box pai ’was ea ed using only
wa e in sp aying and pu ing wo pieces o black s ing
(con ol o mus elid aeces) on op o he nes , wi hou
any egg agmen s.
We hen a ached a neu al symbol, made o whi e plas-
ic, a ound he en ance hole (3.2 cm diame e ) o each
box wi hin he box pai ; one box go a iangle and he
o he one a ci cle, diame e o side dimension 7.5 cm.
Ac oss he expe imen al si es we sys ema ically andom-
ized which symbol was associa ed wi h he ‘high- isk’nes
si e ( he nes wi h simula ed p eda o isi ) so ha in hal
o he si es a iangle was associa ed wi h he ‘high- isk’
si e and ice e sa. Ins ead o using some na u ally occu -
ing nes -si e di e ence, such as ca i y en ance heigh o
diame e o ee species, we pu pose ully used a no el,
neu al cha ac e is ic pai wi h jus one e y salien bu
simple con as (shape), o which bi ds should no ha e
any in insic o lea ned esponse. Such designs isola e
beha io al ai s unde in es iga ion om con ounding
ac o s [33,35] and ha e been success ully applied in ea l-
ie nes -si e choice s udies (e.g. [30,33]). The boxes wi hin
he ‘in o ma ion box pai ’we e se up ca. 10 m apa in
ees o same size and species.
Abou 20 m away om he ‘in o ma ion box pai ’we se
up ano he box pai , he ‘choice box pai ’. This box pai
included wo acan nes boxes ca. wo me e s apa , again
se up in simila ees. We pu 1.5 l o clean sawdus in o
each o he ‘choice box pai ’boxes o make hese acan
boxes mo e a ac i e nes ing si es han he wo in he ‘in-
o ma ion box pai ’. Flyca che s s ongly p e e building
hei nes on op o exis ing nes ma e ials, such as
dummy [36] o dese ed (pe s. obs.) i nes s, and se ling
in he ‘in o ma ion box pai ’would yield no da a on ly-
ca che ’s abili y o associa e neu al symbol wi h nes p e-
da ion isk. Howe e , clean sawdus in he nes box is
p e e ed e en mo e s ongly han i nes s [37].
Finally, we andomly assigned he wo symbols, i-
angle and ci cle, o he ‘choice box pai ’boxes. This
c ea ed a se ing whe e wo equally a ac i e acan
nes ing si es we e a ailable immedia ely adjacen o each
o he , o lyca che o choose be ween. These nes si es
di e ed only in he ype o symbol a ached a ound he
ca i y en ance, while he nea by ‘in o ma ion box pai ’
ea u ed associa ion be ween one o he symbols and
nes p eda ion isk. The dis ance be ween he box pai s
had o be ela i ely sho o ensu e ha he bi ds se ling
in he ‘choice box pai ’mos likely encoun e he simu-
la ed in o ma ion in he ‘in o ma ion box pai ’be o e
cons uc ing hei own nes . Due o he small spa ial
scale his expe imen al design is conse a i e: i is con-
cei able ha bi ds may pe cei e p eda ion isk o be uni-
o m in he gene al a ea, i.e. equal in all nes boxes
wi hin a si e, and consequen ly do no espond o he
symbol- isk associa ion. Finding a signi ican esponse
would hus gi e s ong suppo o he exis ence o abil-
i ies in bi ds o i) de ec indi ec cues o p eda ion isk
om obse ing he e ospeci ic nes ing a emp s and ii)
associa e nes ing si e cha ac e is ics wi h ha p eda ion
isk in o ma ion and iii) de elop p e e ence o “sa e ”
cha ac e is ics in hei own nes -si e choice.
We moni o ed he se lemen and b eeding o pied ly-
ca che s by isi ing he si es usually e e y second day
(occasionally e e y hi d day). Du ing each isi we
e eshed he ea men s wi hin he ‘in o ma ion box
pai ’( epea ed he sp aying and ensu ed ha aeces/
s ings and egg agmen s con inued o be obse able)
and checked he lyca che nes s a us in he ‘choice box
pai ’. We eco ded he eme ging lyca che nes s acco d-
ing o a ou -le el classi ica ion: some nes ma e ial in
he box, bu box loo s ill isible (le el 1), hal nes (box
loo no isible) bu no cup-shape (le el 2), cup-shape
o ming, bu cup no ye comple ed (le el 3) and eady
nes o laying (cup comple ed; le el 4). Usually he bi ds
ini ially b ough some nes ma e ial o bo h o he
‘choice’boxes, bu e en ually comple ed he nes in only
one o hem. We de ined he choice o ha e happened
once we obse ed a leas a wo-le el di e ence be ween
he adjacen acan nes boxes.
Pied lyca che males usually a i e o b eeding si es
be o e emales and de end a e i o y ha may include
se e al po en ial nes ca i ies (e.g. bo h nes boxes in ou
‘choice box pai ’), while he emale builds he nes and
hus p esumably has mo e in luence han he male on he
nes -si e choice ([14]; bu see [38]). We he e o e concen-
a ed on emale beha io . We app oxima ed emale a -
i al ime as he nes ini ia ion day, de ined as he day
Tol anen e al. BMC E olu iona y Biology (2018) 18:181 Page 3 o 8
when a le el 1 nes was i s obse ed, o as he p e ious
day in case he nes was i s obse ed as a u he le el
nes . We cap u ed emales om he s ill ac i e nes s du -
ing incuba ion ( wo nes we e abandoned ea lie ), de e -
mined hei age as young (1-yea -old) o old (a leas 2
yea s old) based on plumage cha ac e is ics [39]and
measu ed hei a sus leng h as a p oxy o body size.
The alue o social in o ma ion is expec ed o show
empo al deg ada ion as he ime lag be ween he eme -
gence o in o ma ion (beha io o success o he in o -
ma ion sou ce) and i s applica ion (by he in o ma ion
use ) inc eases [24]. I is hus expec ed ha indi iduals
using social in o ma ion would apply he in o ma ion
quickly a e ob aining i . In addi ion, in o ma ion based
on social cues is o en mo e easily a ailable compa ed o
in o ma ion collec ed di ec ly om he en i onmen
(e.g. by obse ing p eda o s). Thus, indi iduals ha base
hei decisions on social in o ma ion a e expec ed o
make as e decisions han hose who use di ec pe sonal
obse a ions o ob ain in o ma ion [40–42]. To ake he
ime used o make he nes si e (symbol) choice in o ac-
coun , we calcula ed a a iable ‘decision ime’as he di -
e ence be ween he choice da e (day when a leas a
wo-le el di e ence in he nes s age was obse ed) and
he app oxima e a i al da e. I social in o ma ion use
esul s in as e decision-making, we expec bi ds using
he simula ed in o ma ion o ha e sho e decision ime
han hose no using he in o ma ion (i.e., making
andom symbol choice).
S a is ical analyses we e pe o med using gene alized
linea models wi h binomial e o dis ibu ion in P o-
g am R ( e sion 3.3.1; [43]). The ull model included
he a iables emale age, a sus leng h, a i al ime
(bo h linea and quad a ic e ms), decision ime, yea
(2013–2016) and chosen symbol ( iangle o ci cle).
In addi ion, we i ed wo-way in e ac ions be ween
emale age and a sus leng h, a i al ime and deci-
sion ime, as well as wo-way in e ac ions be ween
a sus leng h and a i al ime and decision ime. Con-
inuous explana o y a iables we e mean-cen e ed (a -
i al ime o yea -speci ic means) p io o analyses.
Since he analysis o he ull da a indica ed an in e -
ac ion ela ed o emale age, we epea ed he analyses
o old and young emales sepa a ely. In hese
analyses he ull model was he same as o he ull
da a, bu wi hou he emale age a iable and i s
in e ac ions.
A e de ining he ull model, all biologically eason-
able models unde he ull model we e i ed o he
da a and Akaike’s in o ma ion c i e ion [44] co ec ed
o small sample size, AICc, was used o ank he
models. To ake model selec ion unce ain y in o
accoun we de i ed op model se s ha included all
models wi h ΔAICc < 6, bu wi h he cons ain ha
models ha we e mo e complex e sions o a model
wi hlowe AICcwe eomi ed[45]. I mo e han one
model was included in he inal op model se , we
e alua ed he ela i e suppo be ween he models
using e idence a ios ( a ios o model Akaike weigh s;
[46]). We also p esen e ec sizes wi h 95% con i-
dence in e als o a iables in he bes suppo ed
models. Collinea i ies o con inuous explana o y a i-
ables we e es ima ed using Pea son co ela ion coe i-
cien s, bu all pai -wise co ela ions we e low ( <
0.29). Bo h ull and inal models wi hin he op model
se s (i included a leas wo explana o y a iables)
we e also es ed o o e all mul icollinea i y using
a iance in la ion ac o s (VIF), bu all VIFs we e
accep able (< 2.8). Also o e dispe sion le els o ull
and inal models we e accep able (sum o squa ed
Pea son esiduals / esidual d < 1.14).
Resul s
We eco ded 113 pied lyca che nes si e choices wi hin
he ‘choice box pai s’, bu wo nes s we e abandoned
be o e we could cap u e he emales. The e o e he da a
se used in he analysis included 111 nes si e choices, o
which 62 we e made by old emales and 49 by young
emales. O e all, lyca che s chose he symbol depic ing
‘low- isk’nes si e in 62 o 111 (56%) cases; old emales
in 32 o 62 (52%) and young emales in 30 o 49 (61%)
cases. Only 15 lyca che pai s se led on op o he sim-
ula ed i nes s (se en and eigh pai s on op o nes s
wi h and wi hou simula ed nes p eda o isi , espec -
i ely) showing ha adding sawdus in he ‘choice box
pai s’was an e icien way o ge he lyca che s o se le
wi hin he desi ed box pai .
The analysis o he ull da a se (n=111 choices)
esul ed in a op model se o wo models. The bes sup-
po ed model included he in e ac ion be ween emale age
and decision ime (Table 1), and was conside ably be e
suppo ed han he second, in e cep -only model (ΔAICc
= 4.29; e idence a io 0.9 / 0.1 = 9.0). Da a was he e o e
analysed sepa a ely o old and young lyca che emales.
Table 1 Pa ame e es ima es and hei 95% con idence in e als
in he bes -suppo ed models o ull da a, old and young emale
da a. S a is ics o s a is ically signi ican a iables (95% CI excluding
ze o) in explaining pied lyca che nes si e choices in bold
Da a se Va iable Es ima e 95% CI
Full da a In e cep 0.058 −0.443 –0.561
Age_young 0.363 −0.443 –1.185
Decision ime 0.037 −0.128 –0.214
Age_young:Decision ime −0.474 −0.845 –−0.142
Old emales In e cep 0.065 −0.435 –0.567
Young emales In e cep 0.523 −0.105 –1.194
Decision ime −0.437 −0.770 –−0.151
Tol anen e al. BMC E olu iona y Biology (2018) 18:181 Page 4 o 8
The op model se o old emales only included he
in e cep -only model. The in e cep did no di e om
ze o indica ing andom nes si e choice in espec o he
symbol a ound he en ance hole (Table 1).
Fo young emales he op model se included only one
model indica ing s ong nega i e e ec o decision ime
(Table 1). We illus a e he e ec o decision ime on he
nes si e choice o young emales in Fig. 2a, and o com-
pa ison illus a e he same e ec on choices o old emales
in Fig. 2b. Bo h igu es a e based on he models including
only he e ec o decision ime ( he bes model o young
and he hi d bes model o old emale da a). Those
young emales ha made he nes si e (symbol) choice
ela i ely quickly, decision ime < 3 days, p e e ed he
‘low- isk’symbol: 18 o 23 (78%) emales chose he
‘low- isk’symbol. The p e e ence o ‘low- isk’symbol de-
c eased wi h inc easing decision ime and disappea ed
when decision ime eached 5 days o mo e (Fig. 2a).
The e a e e y ew da a poin s a longes decision imes
(n= 4 o decision ime > 6 days), hus e e sal o p e e -
ence a la ge alues should no be in e ed, despi e he
g aphical appea ance. Decision ime was no ela ed o
nes si e choice in old emales (Fig. 2b).
Discussion
Ou esul s demons a e ha lyca che s a e able o use
he a e o p eceding he e ospeci ic nes ing a emp s in
hei own nes -si e choice –bu do so selec i ely. Young
lyca che emales, when making he decision quickly, as-
socia ed he simula ed a e o an a i icial he e ospeci ic
nes wi h a neu al nes -si e cha ac e is ic and p e e ed
he cha ac e is ic associa ed wi h lowe nes p eda ion isk
(o a oided he cha ac e is ic associa ed wi h highe isk).
The choices o old emales we e andom i espec i e o
he ime used in decision-making.
P e ious s udies ha e shown ha bi ds may ob ain in-
o ma ion abou p eda o s indi ec ly ia ol ac ion [18,
21] o by obse ing exc emen s o mammalian p eda o s
and a oid nes si es ha p eda o s appa en ly had isi ed
[19,20,22]. Ou expe imen demons a es a mo e com-
plica ed esponse whe eby bi ds de i e in o ma ion on
nes p eda ion isk om he e ospeci ic nes ing a emp s
(ano he dimension o indi ec in o ma ion) and associ-
a e he in o ma ion o a speci ic nes si e cha ac e is ic.
This de i ed in o ma ion may hen be applied o o he
nes si e loca ions wi h simila cha ac e is ics. Fo ex-
ample, ege a ion cha ac e is ics a e o en consis en ly
associa ed wi h high and low p eda ion isk [5–7] and by
linking he obse ed success o o he s and ege a ion
cha ac e is ics, indi iduals could choose sa e nes si es
(o a oid isky si es) acco dingly. I is likely ha nes ing
a emp s o he e ospeci ics and he associa ed mic o-
habi a ea u es a e mo e easily obse ed han p eda o s
hemsel es, making hei associa ion an a ailable in o -
ma ion sou ce o indi iduals. Howe e , he alue o
such in o ma ion depends on he spa io- empo al a i-
a ion in p eda o ype and beha io and i is expec ed o
dec ease wi h inc easing dis ance and delay om he
e en ha gene a ed he in o ma ion [24].
Gi en ha nes p eda ion poses a signi ican h ea o
b eeding bi ds [9,10], i is expec ed ha indi iduals
would collec in o ma ion abou p eda o incidence in
speci ic nes si es o a eas. Why hen did no all he ly-
ca che emales p e e he ‘low- isk’nes si es in ou
expe imen ? Social in o ma ion use s a egies ha e been
obse ed o exhibi age-speci ic a ia ion [34,47–50],
p obably due o di e ences in pe sonal expe ience o
abili y and oppo uni y o collec in o ma ion pe sonally.
Old (a leas 2-yea -old) emales p obably ha e p io
b eeding expe ience and may be be e in collec ing
in o ma ion pe sonally (i.e. di ec ly, no indi ec ly ia
o he indi iduals). They may mo e eadily ely on
Fig. 2 The p obabili y o (a) young and (b) old pied lyca che
emales o choose he nes si e wi h he ‘low- isk’symbol a ached
a ound he en ance hole in ela ion o he decision ime. Dashed
lines along he solid ed line ( he p edic ed p obabili y) depic he
95% con idence in e als. Ve ical dashed line depic s he expec ed
p obabili y le el (0.50) unde andom nes si e choice. Do s
ep esen da a poin s (each do may include se e al da a poin s).
No e he di e en scale o he x-axis be ween (a) and (b)
Tol anen e al. BMC E olu iona y Biology (2018) 18:181 Page 5 o 8

pe sonal in o ma ion, despi e also ha ing ob ained he
social in o ma ion. Fo example, old emales may ha e
pe cei ed he simula ed social in o ma ion bu hen may
ha e obse ed ha he e a e no p eda o s p esen in he
a ea (any mo e) and hus selec ed he nes si e andomly
in espec o he symbol. Young (1-yea -old) emales do
no ha e p io b eeding expe ience and may hus p e e
o use social in o ma ion. Due o he small spa ial dis-
pe sion o he expe imen al nes boxes, mo e expe i-
enced old emales may also ha e pe cei ed he p eda ion
isk o be equal among all he boxes esul ing in andom
nes si e choice.
We obse ed a ia ion also among he young emales:
only hose ha made hei nes si e choice decisions quickly
used he simula ed social in o ma ion. This is consis en
wi h he hypo hesis ha he alue o social in o ma ion de-
c eases wi h inc easing delay be ween he e en gene a ing
he in o ma ion and he applica ion o ha in o ma ion by
he obse e [24]. On he o he hand, social in o ma ion
use also enables as e in o ma ion collec ion and hus also
as e decision-making compa ed o using (only) pe sonal
in o ma ion [40–42]. Ou di ec obse a ions o lyca che
beha iou a he expe imen al si es showed ha emales
may isi and he e o e de i e in o ma ion om all he nes
boxes wi hin a si e in jus a ew minu es. By elying on he
in o ma ion a ailable in he o he nes s hey could he e o e
make he nes si e choice immedia ely a e a i ing o he
si e. Nes si e choice by emales ha ook longe o make a
decision was indi e en o symbols and hei associa ed
p eda ion ea men , and is consis en wi h hem ob aining
nes si e quali y in o ma ion pe sonally. Females making
slowe decisions may also ha e explo ed he su oundings
and encoun e ed o he expe imen al si es wi h con as ing
symbol-in o ma ion associa ions ( hese we e andomized
ac oss si es) inc easing he likelihood o andom choices.
These esul s p o ide empi ical e idence o he hypo heses
o as e decision-making when elying on social in o ma-
ion [40–42] as a esponse o deg ading in o ma ion alue
wi h ime ([24]; see also [51]), mainly obse ed in g oup
o aging o da e [52,53].
Cueing on nes p eda o p esence ia indi ec sou ces
h ough he e ospeci ic nes ing a emp s conside ably
inc eases he amoun o a ailable in o ma ion ha can be
acqui ed sa ely and quickly by b eeding bi ds. This beha -
io may ha e impo an implica ions o ealized niche
o e lap be ween species and he e o e o species coexis -
ence, communi y ecology, and ul ima ely e olu ion.
Whe eas nes p eda ion pe se selec s o niche di e gence
in nes si e choice o coexis ing species [5–7], he e ospeci-
ic in o ma ion use in ela ion o nes p eda ion isk, and
mo e speci ically copying o nes si e cha ac e is ics o sa e
nes si es, may esul in main enance o simila i y and
e en enhanced con e gence in o he ‘low- isk / p eda o
ee niche space’. On he o he hand, a oidance o
cha ac e is ics o isky nes si es esul s in di e gence in
he ‘high- isk niche space’. Since nes p eda ion exe s a
s ong selec ion p essu e in bi ds [9,10], niche e olu ion
should p oceed owa ds sa e nes si es in bo h in e ac ing
species (in o ma ion sou ce and in o ma ion use ). I simi-
la cha ac e is ics de ine sa e nes si es in bo h species,
hey should show niche con e gence. He e ospeci ic in o -
ma ion use could hen add on he independen species
-speci ic e ec s and accele a e con e gence o he ealized
niches be ween he species. In o ma ion use and conse-
quen he e ospeci ic a ac ion also p o ide a po en ial
explana ion o he obse a ions whe e compe i o s sha e
simila mic ohabi a s despi e hey su e highe nes p e-
da ion han when b eeding alone (c . [7]).
On he o he hand, con e gence in nes si e cha ac e is-
ics ia he e ospeci ic in o ma ion use would esul in
highe nes densi y in speci ic nes si es. I nes p eda o s
espond unc ionally and begin o p e e such mic ohabi a s
in sea ching p ey, inc eased p eda ion isk in his mic o-
habi a would selec o di e gence in nes si e niche
be ween he wo species (c . [5–7]). As a esul , he in e ac -
ing species (in o ma ion sou ce and in o ma ion use )
could end up in luc ua ing ealized-niche di e gence
con e gence dynamics. Pace, ampli ude and spa ial scale o
hose dynamics would depend on he unc ional espon-
si eness and o he cha ac e is ics o he p eda o commu-
ni y and he p e alence o he e ospeci ic in o ma ion use
among he p ey species. S ong unc ional esponsi eness
o p eda o s coupled wi h equen he e ospeci ic in o ma-
ion use among he p ey species would esul in ela i ely
apid luc ua ions occu ing wi hin ew gene a ions, while
weake esponsi eness and less equen in o ma ion use
could yield modes luc ua ions o e longe empo al scales.
Spa ial a ia ion in p eda o and p ey communi ies and
hei esponsi eness and eliance on in e speci ic in o ma-
ion use would c ea e localized dynamics, and consequen ly
di e si y ecological in e ac ions (p eda o -p ey and in o -
ma ion use dynamics) a la ge spa ial scales.
Conclusions
This s udy demons a es ha bi ds i) can de ec indi ec
cues o p eda ion isk om obse ing he e ospeci ics nes -
ing a emp s and ii) can associa e nes ing si e cha ac e is ics
wi h ha p eda ion isk in oma ion and iii) can –bu only
condi ionally do –de elop p e e ence o “sa e ”cha ac e -
is ics in hei own nes si e choice. Such in e speci ic social
in o ma ion use in ela ion o nes p eda ion isk may a ec
ealized niche dynamics among coexis ing species wi h im-
po an implica ions o species coexis ence and commu-
ni y dynamics. These indings also add o he accumula ing
e idence o be ween-indi idual a ia ion in social in o ma-
ion use pa e ns; bo h due o age- ela ed di e ences and
also due o wi hin-age-g oup a ia ion. Gi en he subs an-
ial po en ial o indi idual le el a ia ion in beha iou o
Tol anen e al. BMC E olu iona y Biology (2018) 18:181 Page 6 o 8
a ec key ecological and demog aphic p ocesses, also in-
cluding species coexis ence and communi y ecology and
e olu ion [54–57], we should aim o ho oughly unde s and
he a ia ion in in o ma ion use.
Addi ional ile
Addi ional ile 1: The da a se suppo ing he a icle. (XLSX 16 kb)
Abb e ia ions
AICc: Akaike’s in o ma ion c i e ion co ec ed o small sample size;
VIF: Va iance in la ion ac o ; ΔAICc: Di e ence in AICc uni s o he ocal
model compa ed o he model wi h lowes AICc
Acknowledgemen s
We hank Mikko Ka jalainen o help in he ield and he Konne esi Resea ch
S a ion and he Ranua Zoo o p o iding ma e ials. Commen s om wo
e iewe s in Pee age o Science imp o ed he manusc ip .
Funding
This s udy was unded by Socie as p o Fauna e Flo a Fennica, Oska Ö lunds
S i else (g an s o JT), Kone Founda ion (JTF) and Academy o Finland (g an s
#122665, #125720 o JTF and #138049 o RLT).
A ailabili y o da a and ma e ials
All da a analysed du ing his s udy a e included in his published a icle as a
supplemen a y ile (Addi ional ile 1).
Au ho s’con ibu ions
All au ho s concei ed he ideas and designed me hodology. JT collec ed
and analysed he da a and led he w i ing o he manusc ip . All au ho s
con ibu ed c i ically o he d a s and ga e inal app o al o publica ion.
E hics app o al and consen o pa icipa e
Handling o bi ds was done acco ding o he guidelines o he Finnish Ringing
Cen e. O he e hics app o al no applicable.
Consen o publica ion
No applicable.
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
Publishe ’sNo e
Sp inge Na u e emains neu al wi h ega d o ju isdic ional claims in published
maps and ins i u ional a ilia ions.
Au ho de ails
1
Depa men o Ecology and Gene ics, Uni e si y o Oulu, 90014 Oulu,
Finland.
2
Na u e and Game Managemen T us , Dege by, Finland.
3
Open
Science Cen e, Uni e si y o Jy askyla, PO Box 35, 40014 Uni e si y o
Jy askyla, Jy äskylä, Finland.
4
Depa men o Biological and En i onmen al
Sciences, Uni e si y o Jy askyla, PO Box 35, 40014 Uni e si y o Jy askyla,
Jy äskylä, Finland.
5
Sec ion o Ecology, Depa men o Biology, Uni e si y o
Tu ku, 20014 Tu ku, Finland.
6
Pe cy Fi zPa ick Ins i u e o A ican O ni hology,
DST-NRF Cen e o Excellence, Uni e si y o Cape Town, 7701 Rondebosch,
Sou h A ica.
7
Depa men o Biological and En i onmen al Science,
Uni e si y o Jy askyla, Konne esi Resea ch S a ion, 44300 Konne esi, Finland.
8
Cu en Add ess: Na u al Resou ces Ins i u e Finland (Luke), Uni e si y o
Oulu, Paa o Ha aksen ie 3, 90014 Oulu, Finland.
Recei ed: 28 Feb ua y 2018 Accep ed: 20 No embe 2018
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