Interactive effects of past and present environments on overwintering success : a reciprocal transplant experiment
Full text
In e ac i e e ec s o pas and p esen en i onmen s on
o e win e ing success—a ecip ocal ansplan expe imen
Tuula A. Oksanen1, Minna Koi ula2, Esa Koskela3, Tapio Mappes1& Ca l D. Soulsbu y3
1Cen e o Excellence in E olu iona y Resea ch, Depa men o Biological and En i onmen al Science, Uni e si y o Jy ¨
askyl¨
a, Finland
2MTT, Bio echnology and Food Resea ch, Biome ical Gene ics, Jokioinen, Finland
3Depa men o Biological and En i onmen al Science, Uni e si y o Jy ¨
askyl¨
a, Finland
Keywo ds
Delayed densi y dependence, li e his o y,
Myodes gla eolus, popula ion dynamics,
ecip ocal ansplan expe imen
Co espondence
Tuula A. Oksanen, Cen e o Excellence in
E olu iona y Resea ch, Depa men o
Biological and En i onmen al Science, P.O. Box
35, FI-40014 Uni e si y o Jy ¨
askyl¨
a, Finland;
E-mail: [email p o ec ed]
Funded by he Academy o Finland g an s o
T.A.O., M.K., E.K. and T.M. and he Cen e o
Excellence in E olu iona y Resea ch in he
Uni e si y o Jy ¨
askyl¨
a.
Recei ed: 11 May 2011; Re ised: 28 Oc obe
2011; Accep ed: 31 Oc obe 2011
Ecology and E olu ion 2012; 2(5): 899–907
doi: 10.1002/ece3.82
Abs ac
Li e-his o y ai s a e in luenced by en i onmen al ac o s h oughou he li espan
o an indi idual. The ela i e impo ance o pas e sus p esen en i onmen on
indi idual i ness, he e o e, is a ele an ques ion in popula ions ha ace he
challenge o empo ally a ying en i onmen . We s udied he in e ac ing e ec s
o pas and p esen densi y on body mass, condi ion, and su i al in enclosu e
popula ions o he bank ole (Myodes gla eolus) using a ecip ocal ansplan design.
In connec ion wi h he cyclic dynamics o na u al ole popula ions, ou hypo hesis
was ha indi iduals bo n in low-densi y enclosu es would do be e o e win e ing
in low-densi y enclosu es han in high-densi y enclosu es and ice e sa. Ou esul s
show ha he e ec o summe (pas ) densi y was s ong especially on su i al and
body mass. The esponse o body mass o summe densi y was nega i e in bo h
win e (p esen ) densi y g oups, whe eas he esponse o su i al p obabili y was
nonlinea and di e ed be ween he win e densi y g oups. In pa icula , ou da a
show a end o highe o e win e ing success o indi iduals o igina ing om he
lowes summe densi ies in low win e densi y and ice e sa. We he e o e conclude
ha he capaci y o indi iduals o espond o a change in densi y was cons ained
by he delayed densi y-dependen e ec s o en i onmen expe ienced in he pas .
These e ec s ha e he po en ial o con ibu e o ole popula ion dynamics. Possible
mechanisms media ing he e ec s o pas en i onmen in o p esen pe o mance
include bo h in insic and en i onmen al ac o s.
In oduc ion
Condi ions du ing ea ly de elopmen , such as en i onmen-
al o pa en al e ec s, can ha e long- e m consequences on
indi idual li e his o ies (Becke man e al. 2002). Mo eo e ,
many species a e capable o de eloping apid esponses o
changes in hei immedia e en i onmen such as bu s s o
compensa o y g ow h (Me cal e and Monaghan 2001). Va i-
a ion in indi idual li e his o ies may he e o e be conside ed
an ou come o he in e ac ion be ween genes and en i on-
men al ac o s bu also an in e ac ion be ween en i onmen al
ac o s ope a ing du ing he di e en phases o he li e cycle
(Monaghan 2008). This idea was i s adop ed by esea che s
ocusing on compensa o y g ow h, ha is accele a ed g ow h
a e a pe iod o es ic ed de elopmen ha enables indi-
iduals o ca ch up wi h/ o hei non es ic ed conspeci ics
(Ho nick e al. 2000; Me cal e and Monaghan 2001, 2003).
The impo ance o compensa o y g ow h on indi idual li e
his o ies has been widely examined, o example, in ela ion
o he leng h o li espan (Ozanne and Hales 2004; Inness
and Me cal e 2008), dominance s a us (Royle e al. 2005),
and me abolism (C iscuolo e al. 2008). In a mo e gene al
ecological con ex , he li e-his o y e ec s o changes in ood
quali y ha e been demons a ed by se e al ood manipula-
ion s udies (e.g., Plais ow e al. 2006; Tabo sky 2006; Ba e
e al. 2009; Helle e al. in p ess).
Food esou ces and die quali y a e en i onmen al ac o s
ha ypically a y ac oss he li espan o an indi idual, and
a e he e o e biologically meaning ul a ge s o he esea ch
on delayed li e-his o y e ec s. Addi ionally, ano he po en-
ially impo an a iable in his con ex is popula ion densi y
(Becke man e al. 2002). Fo many species, including small
c
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899
Su i al E ec s o Pas and P esen Densi ies T. A. Oksanen e al.
mammals, he li e-his o y e ec s o popula ion densi y a e
well documen ed and conside ed o be e olu iona ily sig-
ni ican . Fo example, high popula ion densi y is known o
supp ess sexual ma u a ion (P e o –Jullia d e al. 1999; E -
gon e al. 2001a), dec ease ep oduc i e success (Koskela e al.
1999), and educe he g ow h a e o ju eniles (Os eld and
Canham 1995). In cyclical popula ions, he e is commonly
obse ed pa e n known as he Chi y e ec (Chi y 1967;
Boons a and K ebs 1979), in which indi iduals a e la ge
du ing he inc ease and peak phase o luc ua ions han in
he declining and low phase. In he con ex o p edic able
densi y luc ua ions, i has e en been sugges ed ha emales
may modi y he pheno ype o hei o sp ing acco ding o
he densi y o he popula ion o imp o e hei i ness (Lacey
1998). This could be achie ed h ough adap i e ma e nal
e ec s, ha is, an adap i e ela ionship be ween o sp ing
pheno ype and he en i onmen expe ienced by he mo he
(Rossi e 1996; Mousseau and Fox 1998; Ma shall and Ulle
2007).
A he indi idual le el, densi y-induced changes in he
li e-his o y ai s o small mammals a e mos likely based on
pheno ypic plas ici y ha enables quick esponses o changes
in he en i onmen (Ag ell e al. 1995; No dahl and Ko -
pim¨
aki 2002). Fo example, E gon e al. (2001b) conduc ed
an ex ensi e ield ansplan expe imen by mo ing ield oles
(Mic o us ag es is L.) be ween si es ha di e ed in a e age
o e win e ing body mass. Thei esul s showed ha ans-
plan ed oles did no e ain he cha ac e is ics o hei sou ce
popula ion and ha he immedia e en i onmen he e o e
had an o e iding ole in shaping he body size. Mo eo e , as
ep oduc ion s a ed ea lie in si es wi h highe body mass,
adjus ing body size o he immedia e en i onmen ca ied
a clea bene i by enabling ep oduc ion concu en ly wi h
he es o he popula ion and con ibu ing o he popula ion
g ow h a e. Howe e , acco ding o ou knowledge, he e
ha e been no p e ious expe imen s on small mammals using
a ecip ocal ansplan design ha has manipula ed densi y.
We aimed o s udy he e ec s o pas and p esen densi ies
on he body mass, condi ion, and su i al o young bank
oles (Myodes gla eolus Sch ebe ) (Fig. 1), by designing an
expe imen whe e indi iduals bo n in an enclosu e popula-
ion o 8, 12, 16, 20, o 24 adul indi iduals we e ansplan ed
in ei he a low (9–10 adul indi iduals) o a high (18 adul
indi iduals) densi y enclosu e o o e win e . We hypo he-
sized ha a change in popula ion densi y would lead o a
misma ch be ween an immedia e adap i e esponse and u-
u e en i onmen , and he eby o lowe ed indi idual i ness
(Ba eson e al. 2004). This idea pa allels he concep o p e-
dic i e adap i e esponses (PAR) o human e olu ion, which
s a es ha o ganisms p ese hei physiology acco ding o he
cues o hei p ena al en i onmen in expec a ion ha pa ic-
ula physiology will ma ch hei u u e en i onmen (Gluck-
man e al. 2005). In ou s udy, howe e , we canno quan-
Figu e 1. S udy species, he bank ole Myodes gla eolus is a small oden
species common in no he n Eu ope. The main habi a s a e o es s and
ields, and he die ypically consis s o o bs, shoo s, seed, be ies, and
ungi. Pho o c edi : Ma i Laine.
i y how he popula ion densi y expe ienced by he mo he s
ansla ed in o he in au e ine en i onmen expe ienced by
he s udy animals.
In ole popula ions, densi y and densi y- ela ed ac o s
(e.g., a ailabili y o ood esou ces and ee b eeding e i-
o ies) ha e been ound o a ec se e al li e-his o y ai s
such as ma u a ion, ep oduc i e success, and suscep ibil-
i y o he cos s o ep oduc ion (Bujalska 1985; Koskela e al.
1999; P e o –Jullia d e al. 1999; Oksanen e al. 2007; Mappes
e al. 2008). Popula ion densi y is he e o e likely o ha e a
subs an ial e ec on he de elopmen o young indi iduals. I
was p edic ed ha he summe densi ies expe ienced by indi-
iduals du ing ea ly de elopmen would in luence hei li e-
his o y ajec o ies, and ha he ecip ocal ansplan design
would challenge he indi iduals o espond o he changed
condi ions wi hin he limi s o hei capaci y o u he phe-
no ypic plas ici y. Mo e speci ically, we es ed i indi iduals
bo n in low summe densi ies would do be e o e win e ing
in low win e densi y han in high win e densi y and ice
e sa. This is meaning ul in he con ex o ole popula ion
cycles because i indi iduals ha a e bo n du ing he peak
phase o luc ua ions ha e ela i ely low i ness du ing he
declining phase, i could speed up he decline in popula ion
densi y and so ampli y he luc ua ions.
Ma e ials and Me hods
S udy si e
Expe imen al animals we e young bank oles aised in en-
closu e colonies a Konne esi Resea ch S a ion. Colonies
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2012 The Au ho s. Ecology and E olu ion published by Blackwell Publishing L d.
T. A. Oksanen e al. Su i al E ec s o Pas and P esen Densi ies
o igina ed om labo a o y-bo n descendan s o wild indi-
iduals o iginally cap u ed a ou s udy si e (Konne esi, cen-
al Finland 62◦37N, 26◦20E). The e was densi y a ia ion
in he enclosu es (8, 12, 16, 20, o 24 adul indi iduals pe
0.2-ha enclosu e) ha had been es ablished o an ea lie en-
closu e expe imen (see Oksanen e al. 2007). These densi ies
we e all ela i ely high and co espond o he peak phase o
he mul iannual popula ion cycles o na u al bank ole pop-
ula ions (Yoccoz e al. 2001). Howe e , due o una oidable
na u al mo ali y he densi y o eigh indi iduals was consid-
e ed a sui able s a ing poin o he low-densi y ea men .
Densi y o 24 indi iduals (120 indi iduals/ha) co esponds
o a e y high bu no unusual densi y in na u al popula-
ions. These densi ies, ha is he densi ies p e ailing when
he expe imen al animals we e bo n a e e e ed o as sum-
me densi ies. Sex a io o adul indi iduals in he enclosu es
was 1:1.
The 11 0.2-ha s udy enclosu es we e si ua ed in an old ield.
To moni o he animals, 20 mul iple-cap u e li e aps we e
dis ibu ed in each enclosu e in a 5 ×4 g id wi h a dis ance o
10 m be ween aps. Each ap was co e ed wi h a gal anized
shee me al chimney ha educed exposu e o p ecipi a ion
and empe a u e ex emes.Enclosu e ences we e cons uc ed
o 1.25-m high gal anized shee me al ha was embedded
0.5 m in o he g ound. The ences we e high enough o en-
close he s udy popula ions, bu did no p e en p eda ion by
mammalian and a ian p eda o s. The oles we e dependen
on na u ally occu ing ood esou ces excep du ing apping
pe iods, when he aps we e bai ed wi h oa s and sun lowe
seeds.
Recip ocal ansplan expe imen
Following he end o he b eeding season in Oc obe , all in-
di iduals (adul indi iduals and he o sp ing bo n du ing
he b eeding season) we e apped om he enclosu es and
ans e ed o he labo a o y. O sp ing om he i s li e o
each adul emale we e measu ed wi h an elec onic scale o
hei body mass ( o nea es 0.01 g) and wi h a digi al calipe
o hei head wid h ( o nea es 0.1 mm) and eleased back
in o six enclosu es in wo di e en densi ies o o e win e .
In o al, his ecip ocal ansplan expe imen included 73
indi iduals eleased a ca. 91 days o age (42 males and 31
emales). Fou o he win e enclosu es had low densi y (nine
o 10 indi iduals) and wo win e enclosu es had high densi y
(18 indi iduals). These densi ies a e e e ed o as he win e
densi ies. Ra ios o males and emales in each enclosu e we e
adjus ed as close o 1:1 as possible. App oxima ely one-hal o
he indi iduals o igina ing om each summe densi y class
(8, 12, 16, 20, o 24) we e assigned o low win e densi y
enclosu es and he o he hal was assigned o high win e
densi y enclosu es. Indi iduals o igina ing om he same li -
e (24 li e s in o al) we e di ided in o di e en ea men s
Table 1. Numbe o indi iduals ecip ocally ansplan ed om summe
densi ies o win e densi ies. Summe densi ies a e 8, 12, 16, 20, and 24
indi iduals pe enclosu e in he pa en al gene a ion and win e densi ies
a e ei he 9–10 (low) o 18 (high) expe imen al indi iduals pe enclosu e.
Summe densi y Win e densi y
Enclosu e Densi y Low High
1823
7822
11 8 8 8
21221
91266
31622
10 16 3 3
42000
52033
62443
82455
To al 168 37 36
and eplica e enclosu es o andomize he e ec s o common
o igin and o a oid inb eeding. The bi h o hese indi iduals
had been moni o ed in labo a o y du ing an ea lie expe i-
men by Oksanen e al. (2007), and he bi h da e, mo he ,
and numbe o siblings o hese indi iduals we e he e o e
known. The emales and hei li e s we e eleased back in o
he enclosu e, he day ollowing he bi h o he pups and he
o al ime he emale spen in he labo a o y was on a e age
ou o i e days.
S udy design is desc ibed in Table 1. Indi iduals assigned o
he high and low win e densi y g oups did no di e in hei
age, body mass a au umn, o he size o he li e in which
hey had been ea ed (mean age [days] ±SE, high: 91.59 ±
0.84,low: 91.39±1.27,Independen samples - es : =0.136,
n=73, P>0.8; mean body mass [g] ±SE, low: 16.8 ±0.2,
high: 16.9 ±0.2, Independen samples - es : =–0.219, n=
73, P>0.8; mean li e size ±SE, low: 5.4 ±0.2, high: 5.3 ±
0.2, Independen samples - es : =0.200, n=73, P>0.8).
Rep oduc i e his o y o hese indi iduals was no eco ded
du ing he b eedingseason; howe e ,basedon he bi hda es,
each indi idual had had a possibili y o ep oduce a leas 1–2
imes be o e he b eeding season was o e . The animals we e
apped again in sp ing (Ma ch) be o e he nex b eeding
season s a ed and ans e ed back o he labo a o y whe e
hei bodymassandheadwid hwasmeasu ed.Condi ionwas
es ima ed as a s anda dized esidual om a linea eg ession
o body mass on head wid h (Schul e–Hos edde e al. 2005).
Indi iduals ha we e no caugh a e an in ensi e apping
e o we e eco ded dead. The p o ocol and he p ocedu es
employed we e e iewed and app o ed by he expe imen al
animal commi ee o he Uni e si y o Jy ¨
askyl¨
a.
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Su i al E ec s o Pas and P esen Densi ies T. A. Oksanen e al.
Da a analysis
Da a we e analyzed using linea (LMM) o gene alized
(GLMM) linea -mixed e ec s models (Bolke e al. 2009),
using he lme4 (Ba es and Maechle 2009) package in R (R
De elopmen Co e Team 2009). Sex ( emale/male) and win-
e densi y (low/high) we e used as ixed ac o s and summe
densi y and li e size as con inuous co a ia es. The p obabil-
i y o su i ing o he end o he expe imen (sp ing) was an-
alyzed wi h GLMM wi h binomial dis ibu ion and logi link
unc ion. Su i al did no i a linea esponse wi h summe
densi y (see Fig. 2A), so we used a quad a ic e m (summe
densi y2) o e alua e i su i al a ied nonlinea ly wi h sum-
me densi y. Models including he quad a ic e m we e signi -
ican ly be e han wi hou i (LR es : χ2=9.67, P=0.008).
We s a ed om a model ha included all ele an ac o s as
main e ec s and hei wo-way in e ac ions. The model was
hen hie a chically simpli ied by emo ing he in e ac ions
and main e ec s wi h nonsigni ican P- alues. Howe e , in
he analyses o log ans o med body mass and condi ion,
we decided o include he e ec s o sex and sex-win e den-
si y in e ac ion, because hey a e biologically meaning ul due
Figu e 2. E ec s o summe and win e densi y on su i al.
(A) The p opo ion o indi iduals ha su i ed a low (open ba s) and
high ( illed ba s) win e densi y and (B) he p edic ed p obabili y o su -
i al o e he win e . Open ci cles and dashed line, low win e densi y;
illed ci cles and solid line, high win e densi y. Equa ion o he cu e o
he low-densi y g oup is y =–0.0099x2+ 0.2989x – 1.4345 and equa-
ion o he cu e o he high densi y g oup is y =–0.0017x2+ 0.0853x
– 0.2883.
o he sexual size dimo phism obse ed in he s udy species
(Koskela e al. 2009).
Models ou pu s we e examined o homogenei y and no -
mali y o esiduals. P- alues o Gaussian e o dis ibu ions
we e es ima ed by compa ison o a p obabili y dis ibu ion
ob ained by 10,000 Ma ko chain Mon e Ca lo simula ions
(Baayen 2007). Fo all a iables, we epo e ec sizes and
95% con idence in e als (CI) (Nakagawa and Cu hill 2007).
In he analysis o da a collec ed in Oc obe , he uni o sam-
plesizeisali e (n=24 o ansplan ed li e s o 57 o all
li e s bo n du ing he summe ) and in he analysis o da a
collec ed in Ma ch, he uni o sample size is an indi idual
(n=35 [body mass and condi ion] o 73 [su i al]).
Resul s
Body mass o he ansplan ed indi iduals be o e he ecip-
ocal ansplan p ocedu e had a s a is ically signi ican neg-
a i e ela ionship wi h summe densi y and li e size (li e
mean o body mass [g] ±SE: 16.8 ±0.2, indi idual ange:
13.7–20.5; LMM 10 enclosu es, 24 li e s: summe densi y:
=–2.31, P=0.038, =–0.52, 95% CI =–0.75/–0.06; li e
size: =–3.67, P=0.002, =–0.70, 95% CI =–0.84/–0.35;
andom e ec o s udy enclosu e: <0.001 ±<0.001. The
s ong in luence o densi y on li e size was demons a ed by
a s a is ically signi ican nega i e co ela ion be ween sum-
me densi y and li e size o e all 57 li e s whose bi h had
been obse ed in he labo a o y (Spea man’s ho =–0.468,
n=57, P≤0.001). Condi ion, howe e , was clea ly no e-
la ed o ei he o hese co a ia es ( ange: –1.9 o 2.88; LMM:
10 enclosu es, 24 indi iduals, summe densi y: =–0.704,
P=0.480, =–0.18, 95% CI =–0.57/0.32; li e size: =
–1.272, P=0.232, =–0.32, 95% CI =–0.65/0.19; andom
e ec o s udy enclosu e: 0.248 ±0.498).
Fo y-eigh pe cen o he ansplan ed indi iduals su -
i ed o e he win e ( om Oc obe o Ma ch). Su i al was
signi ican ly a ec ed by summe densi y (Table 2). The e-
sponse o su i al o summe densi y a ied nonlinea ly in
bo h win e densi y g oups (Table 2, Figs. 2A, B). Though he
in e ac ion e m be ween summe and win e densi ies was
only close o signi ican (Table 2), i s ongly sugges ed ha
he dis ibu ion o su i al p obabili ies o indi iduals bo n
in high densi ies was highe a high win e densi ies, while
he con e se was ue o low summe densi ies (Figs. 2A, B).
The esponses o body mass and condi ion o summe den-
si y we e linea and nega i e in bo h win e densi y g oups
(Figs. 3A, B). The esponse o body mass was s a is ically sig-
ni ican , whe eas he esponse o condi ion was weake and
only ma ginally signi ican (Table 3). In e ac ion e ms be-
ween summe and win e densi ies in hese models we e no
signi ican and only sugges ed a weak end o an in e ac i e
e ec in body mass (Table 3).
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2012 The Au ho s. Ecology and E olu ion published by Blackwell Publishing L d.
T. A. Oksanen e al. Su i al E ec s o Pas and P esen Densi ies
Table 2. P obabili y o su i al. Binomial GLMM wi h summe densi y
(SD) and win e densi y (WD) as independen a iables (n=73). The
in e cep co esponds o an indi idual in low win e densi y. Random
e ec o s udy enclosu e is included in o he model (es ima ed pa am-
e e o a iance componen ±SD: 0.297 ±0.545). E ec size ( )and
noncen al 95% con idence in e als (CI) a e shown o each a iable.
Con en ions o e ec sizes: small e ec , =0.10, medium e ec , =
0.30, la ge e ec , =0.50 (Cohen 1988).
Es ima e SE zP CI
In e cep −8.543 3.305 – –
WD 4.988 4.512 1.11 0.269 0.11 −0.09/0.30
SD 1.343 0.490 2.74 0.006 0.27 0.07/0.44
SD (quad a ic) −0.045 0.016 −2.84 0.004 −0.28 −0.09/–0.45
WD ×SD −0.964 0.658 −1.46 0.143 0.15 −0.05/0.34
WD ×SD −0.038 0.021 1.81 0.070 0.19 −0.02/0.37
(quad a ic)
Discussion
We conduc ed a simple enclosu e expe imen whe e bank
oles aised in a ying popula ion densi ies we e ansplan ed
ei he in low o high densi y o o e win e . Ou aim was o
s udy he in e ac ion be ween summe and win e densi y on
pheno ypic a ia ion in body mass, condi ion, and su i al.
The ela i e impo ance o pas and p esen en i onmen on
indi idual i ness has p e iously been s udied mainly by ma-
nipula ing ood esou ces while, acco ding o ou knowledge,
his was he i s expe imen u ilizing a densi y-manipula ion
app oach.
Bank ole popula ionsinFennoscandiashowbo h seasonal
and mul iannual cyclic luc ua ions in popula ion densi y
(Kallio e al. 2009), and indi idual oles, he e o e, equen ly
ace densi y- ela ed changes in hei en i onmen (Hansson
and Hen onen 1985; Ko pim¨
aki e al. 2005). The ac ual
densi y luc ua ions, howe e , canno be easily in eg a ed
in o expe imen al designs, and p e ious s udies on densi y-
dependen e ec s on indi idual cha ac e is ics ha e mos ly
elied on co ela i e da a (Tkadlec and Zejda 1998; No dahl
and Ko pim¨
aki 2002) and compa isons be ween popula ions
wi h di e en densi ies ei he in na u al (P e o –Jullia d e al.
1999; E gon e al. 2001a) o in semina u al en i onmen s
(Os eld e al. 1993; Os eld and Canham 1995; Koskela e al.
1999). Al hough ou design ei he does no include densi y
luc ua ions compa able o na u al ole cycles, i indica es he
po en ial o indi iduals o espond o changes in popula ion
densi y, which is impo an in he con ex o delayed li e-
his o y e ec s (Becke man e al. 2002). Delayed li e-his o y
e ec s a e po en ially a key mechanism in linking en i on-
men al condi ions o popula ion le el esponses such as ma-
e nally media ed densi y e ec s o he ole cycles (Inchaus i
e al. 1998). We he e o e o mula ed ou hypo hesis in he
con ex o ole popula ion cycles, and p edic ed ha indi id-
uals bo n in low densi ies would do be e o e win e ing in
low-densi y han in high-densi y en i onmen and ice e sa.
This could con ibu e o he cycles, o example, by speeding
up he decline phase o he cycle.
Acco ding o ou esul s, he e ec o summe densi y was
s ong on mos o he measu ed a iables. Summe densi y
had a nega i e e ec on he size o he li e s om which he
expe imen al indi iduals o igina ed and on he body mass
o hese indi iduals be o e he ecip ocal ansplan . Mo e-
o e , summe densi y induced a nonlinea esponse in he
p obabili y o su i al and had a nega i e e ec on he body
mass a e he o e win e ing pe iod (Tables 2, 3 and Figs.
2, 3A). The aw da a sugges ha he o e win e ing success
o indi iduals o igina ing om he lowes summe densi ies
was be e in low win e densi y han in high win e den-
si y and ice e sa (Fig. 2A). The in e p e a ion based on
Table 3. Indi idual body mass and condi ion in sp ing. LMM ou pu s o he e ec s o sex, summe densi y (SD), and win e densi y (WD) (n=
35). In e cep co esponds o a emale in low win e densi y. Random e ec o s udy enclosu e is included in o he models (es ima ed pa ame e o
a iance componen ±SD: 0.004 ±0.061, 0.088 ±0.297, espec i ely). E ec size ( ) and noncen al 95% con idence in e als (CI) a e shown o
each a iable. Con en ions o e ec sizes: small e ec , =0.10, medium e ec , =0.30, la ge e ec , =0.50 (Cohen 1988).
Fixed e ec s Es ima e SE P CI
Body mass In e cep 3.021 0.145 – –
Sex 0.048 0.044 0.63 0.669 0.10 −0.21/0.39
WD −0.322 0.145 −1.39 0.113 −0.22 −0.48/0.10
SD −0.0113 0.007 1.85 0.047 0.29 −0.02/0.53
Sex ×WD 0.082 0.094 0.87 0.315 0.14 −0.18/0.42
WD ×SD 0.010 0.009 1.53 0.094 0.24 −0.07/0.50
Condi ion In e cep 0.628 1.348 – –
Sex 0.523 0.518 1.01 0.331 0.17 −0.17/0.46
WD −2.472 1.543 −1.60 0.120 −0.27 −0.53/0.07
SD −0.094 0.050 −1.88 0.065 0.31 −0.02/0.56
Sex ×WD 0.546 0.642 0.85 0.403 0.15 −0.19/0.44
WD ×SD −0.085 0.058 1.46 0.152 0.25 −0.09/0.51
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2012 The Au ho s. Ecology and E olu ion published by Blackwell Publishing L d. 903
Su i al E ec s o Pas and P esen Densi ies T. A. Oksanen e al.
Figu e 3. E ec o summe densi y on body mass and condi ion.
A) Body mass in sp ing and (B) body condi ion in sp ing. Figu es a e
p oduced om he aw da a and he cu es i ed a e linea .
ou bes i ing model (Table 1, Fig. 2B), howe e , is no as
s aigh o wa d. The in e ac i e e ec s o summe and win e
densi ies on he p obabili y o o e win e ing su i al sugges
ha he esponse o he su i al p obabili y o he summe
densi y was di e en be ween he low and high win e den-
si y g oups. The esponse in he low win e densi y g oup
was clea ly quad a ic wi h a peak su i al p obabili y a a
summe densi y o app oxima ely 16 (Fig. 2B). In e p e ing
he esul s om he poin o iew o he high win e den-
si y g oup is mo e complica ed as appea s ha ou summe
densi y se ies was no long enough o ca ch he ull shape o
he cu e o he peak alue o he p edic ed p obabili y o
su i al (Fig. 2B). Tendency o ela i ely low su i al in low
densi y may be explained by he possible bene i s o inc eased
social ole ance du ing he non ep oduc i e season ha has
been obse ed in se e al ole species. Fo example, oles a e
less e i o ial, less ac i e, and sha e nes s and hoa ds o ood
(e.g., Webs e and B ooks 1981; Wol and Lidicke J 1981;
Ecca d e al. 2011). In high-densi y condi ions, hese beha -
io s may ansla e in o mo e e ec i e he mo egula ion and
co-ope a i e de ense agains o he species. The o e all win-
e su i al a e (48%) was simila o a su i al a e om an
ea lie s udy (51%) conduc ed in he same s udy enclosu es
(Oksanen e al. 2001), sugges ing ha no hing excep ional
happened, o example, in he wea he condi ions du ing he
win e .
The nega i e e ec o li e size on body mass be o e o e -
win e ing (i.e., age o ca. 91 days) was expec ed as a ade-o
be ween bank ole li e size and o sp ing g ow h and body
size has been con i med in nume ous ea lie s udies (Mappes
e al. 1995; Koskela 1998; Oksanen e al. 2001, 2002; Mappes
and Koskela 2004). Howe e , as li e size was nega i ely e-
la ed o popula ion densi y as well, in heo y, he e ec o
popula ion densi y on body mass could ha e been posi i e.
The nega i e e ec o summe densi y on body mass he e-
o e sugges ed ha densi y e ec s we e no media ed by li e
size exclusi ely, bu ha densi y had mo e di ec e ec s on
body mass as well.
Compa ed o p e ious s udies wi h simila designs, ou e-
sul s only weakly suppo he indings o he ield ole ans-
plan expe imen (E gon e al. 2001b), which sugges ed an
o e iding ole o he immedia e en i onmen in shaping li e-
his o y ai s and he eby enabled disca ding in insic mech-
anisms as an explana ion o a ia ion in hem. Recen ly, an
o e iding e ec o an immedia e en i onmen has been e-
p o e d in ano he ole ansplan expe imen as well. Helle
e al. (in p ess) s udied he long- e m e ec s o ju enile and
adul en i onmen s manipula ed by ood suplemen a ion in
enclosu e popula ions o he bank ole. Thei s udy showed
ha he ep oduc i e success o emales was de e mined by
he quali y o he adul en i onme whe eas he su i al o
males and he cha ac e is ics o he li e s we e de e mined
by he ju enile en i onmen . In ou expe imen , he im-
media e en i onmen seemed o challenge he e ec o pas
en i onmen only in he e ms o o e win e ing su i al as
demons a ed by he shi in he dis ibu ion o he p edic ed
su i alp obabili ies(Fig. 2B).Innon-mammalians udysys-
ems, Tabo sky (2006) and Ba e e al. (2009) s udied he
in e ac ing e ec s o die a y condi ions du ing di e en de-
elopmen al pe iods on he li e-his o y ai s in cichlids and
cock oaches, espec i ely. Bo h o hese s udies conclude ha
he li e-his o y ai s measu ed we e in luenced by ju enile
g ow h condi ions a he han by esou ce a ailabili y la e in
li e. The esul s o he cu en s udy suppo hei conclusions
wi h he excep ion o he weak in e ac ion be ween he pas
and he p esen densi ies in body mass. These a he con a-
dic o y esul s sugges ha he ela i e signi icance o pas
e sus p esen condi ions may a y be ween s udy species
as well as ai s, mechanisms, and condi ions unde exami-
na ion. Building up a gene al unde s anding abou delayed
li e-his o y e ec s, he e o e, will no be an easily a ainable
goal.
The s onges suppo o ou esul s comes om an in e -
eb a e sys em (Plais ow e al. 2006). A ood manipula ion
expe imen in soil mi es showed ha he in e gene a ional
e ec s o pa en al nu i ional condi ions can be con ex de-
penden and ha e complex e ec s on popula ion dynamics
(Plais ow e al. 2006). Fu he mo e, he pe sis ence and sig-
ni icance o he e ec s o pa en al ood en i onmen (low,
904 c
2012 The Au ho s. Ecology and E olu ion published by Blackwell Publishing L d.
T. A. Oksanen e al. Su i al E ec s o Pas and P esen Densi ies
medium, o high) a ied be ween he ood en i onmen s o
he descendan s, and ha he e ec s o pa en al en i onmen s
we e mos p onounced when he descendan en i onmen
was no es ic ing, ha is, in high ood condi ions (Plais ow
e al. 2006). This esul is compa able o ou esul s on su -
i al p obabili y, which sugges ed ha he e ec o summe
densi y on su i al p obabili y di e ed be ween he win e
densi y g oups and ha he esponse was mo e dis inc when
he e was less compe i ion o e esou ces, ha is when he
win e densi y was low.
Ou da a does ha e some sho comings; in pa icula , due
o he limi ed numbe o indi iduals a ailable o he ecip-
ocal ansplan expe imen , i was no possible o include
he co a iance among indi iduals bo n in o he same li -
e o he co a iance among indi iduals o igina ing om
he same enclosu e in he s a is ical models. Mo eo e , i is
una oidable ha indi iduals a ailable o he ansplan ep-
esen a non- andom subse o he o sp ing bo n du ing
he summe as iabili y selec ion occu s o e he b eeding
season. Howe e , ou esul s on body mass and he p obabil-
i y o su i al gene ally seem o suppo he hypo hesis ha
he li e-his o y ajec o ies o bank oles a e in luenced by
popula ion densi y expe ienced du ing ea ly de elopmen .
Fu he mo e, ou esul s on su i al p obabili y sugges ha
a la ge-scale change in popula ion densi y has a po en ial
o in luence indi idual i ness. The esul s he e o e sugges
ha delayed densi y-dependen e ec s may indeed play a
ole in he cyclic dynamics o ole popula ions. In enclosu e
en i onmen , possible mechanisms media ing he e ec s o
ma e nal en i onmen in o o sp ing pe o mance include
ma e nal e ec s such as li e size- ela ed ac o s, ma e -
nallyde i ed immuni y,andea lyp og ammingo indi idual
me abolism. Howe e , pu ely en i onmen al e ec s such as
p eda ion o en i onmen al pa hogens canno be uled ou
ei he .
Mo eo e , he esul s sugges ha in p edic able en i on-
men s, i would be possible o indi iduals o imp o e hei
i ness by adjus ing hei ep oduc i e e o (i.e., li e size) o
he o hcoming densi y condi ions (Gluckman e al. 2005).
Howe e , in unp edic able en i onmen s, he capaci y o in-
di iduals o espond o changes in popula ion densi y may
be cons ained by he delayed densi y-dependen e ec s o
he pas en i onmen . In bank oles, his is likely o inc ease
he complexi y o easons leading o cyclic popula ion dy-
namics and he di icul ies aced in explaining hem. The e-
sul s, howe e , a e no only in e es ing in he con ex o ole
popula ion dynamics and he possible in insic and ex in-
sic causes con ibu ing o hem, bu also in conside ing o he
species including humans, which ace he challenge o empo-
ally a ying en i onmen , and he eby a possible misma ch
be ween immedia e adap i e esponses and u u e en i on-
men (Ba eson e al. 2004; Gluckman e al. 2005; Ricka d and
Lummaa 2007; on Bonsdo e al. 2011).
Acknowledgmen s
We hank Konne esi Resea ch S a ion and he Expe imen-
al Animal Uni o he Uni e si y o Jy ¨
askyl¨
a o p o iding
he acili ies, and Nigel G. Yoccoz as well as he anonymous
e iewe s o use ul commen s on he p e ious e sions
o he pape . The s udy was inancially suppo ed by he
Academy o Finland (g an numbe s: 104568 and 108955 o
T.A.O.; 71425, 72896 o M.K.; 115961 and 119200 o E.K.;
and 118603, 109165, and 204284 o T.M.) and he Cen e
o Excellence in E olu iona y Resea ch in he Uni e si y o
Jy ¨
askyl¨
a.
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