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D op dead! Female ma e a oidance in an explosi ely b eeding og
© 2023 The Au ho s. Published by he Royal Socie y
Published e sion
Di ich, Ca olin; Rödel, Ma k-Oli e
Di ich, C., & Rödel, M.-O. (2023). D op dead! Female ma e a oidance in an explosi ely
b eeding og. Royal Socie y Open Science, 10(10), A icle 230742.
h ps://doi.o g/10.1098/ sos.230742
2023
oyalsocie ypublishing.o g/jou nal/ sos
Resea ch
Ci e his a icle: Di ich C, Rödel M-O. 2023
D op dead! Female ma e a oidance in an
explosi ely b eeding og. R. Soc. Open Sci. 10:
230742.
h ps://doi.o g/10.1098/ sos.230742
Recei ed: 30 May 2023
Accep ed: 21 Sep embe 2023
Subjec Ca ego y:
O ganismal and e olu iona y biology
Subjec A eas:
beha iou /e olu ion/ecology
Keywo ds:
dea h eigning, Eu opean common og,
expe ience, sexual con lic , hana osis,
onic immobili y
Au ho o co espondence:
Ca olin Di ich
e-mail: [email p o ec ed]
Elec onic supplemen a y ma e ial is a ailable
online a h ps://doi.o g/10.6084/m9. igsha e.c.
6858610.
D op dead! Female ma e
a oidance in an explosi ely
b eeding og
Ca olin Di ich
1,2,3
and Ma k-Oli e Rödel
1,3
1
Museum ü Na u kunde Be lin, Leibniz Ins i u e o E olu ion and Biodi e si y Science,
In alidens aße 43, 10115 Be lin, Deu schland
2
Depa men o Biology and En i onmen al Sciences, Uni e si y o Jy äskylä, Jy äskylä,
Finland
3
Be lin–B andenbu g Ins i u e o Ad anced Biodi e si y Resea ch (BBIB), Be lin, Ge many
CD, 0000-0002-4447-4481; M-OR, 0000-0002-1666-195X
Males’and emales’ ep oduc i e s a egies may di e ,
po en ially leading o sexual con lic . Inc eased e o s by
males (ha assmen , o ced copula ion, in imida ion) o gain
access o emales could e en nega i ely a ec emale su i al
and hus lead o ep oduc i e ailu e o bo h indi iduals. In
anu ans, a highe mo ali y isk o ma ing emales has been
epo ed in explosi e b eeding species. Du ing hese ma ing
e en s, se e al males cling o a emale, which a e mos ly
unable o ge id o he unwan ed males. This can lead o he
emale’s dea h. F om he li e a u e, i seems ha emales o
explosi e b eeding ogs ha e no means o ejec unwan ed
males. He e we desc ibe emale ma e a oidance beha iou s
in he Eu opean common og. We obse ed h ee emale
a oidance beha iou s, namely ‘ o a ion’,‘ elease call(s)’and
onic immobili y (dea h eigning). These beha iou s we e
signi ican ly associa ed wi h smalle emale body size, and
smalle emales we e mo e success ul in escaping amplexus.
Tonic immobili y as a ac ic o a oid ma ing o male
ha assmen has only been obse ed in a hand ul o species
and only in one o he amphibian. Ou obse a ions show
ha emales in explosi e b eeding ogs may no be as
passi e and helpless as p e iously hough .
1. Backg ound
In classical sexual selec ion heo y, sexual selec ion is mos ly
d i en by emale choice and male comba [1]. Acco ding o his
heo y, bo h sexes aim o maximize hei ep oduc i e i ness.
Whe eas males could ma e wi h se e al emales o inc ease he
numbe o o sp ing, emales a e limi ed by hei ep oduc i e
cycle and he numbe o po en ial o sp ing wi hin one o hose
cycles, which is usually unchangeable [2]. Hence he cos s,
bene i s and in e es s o bo h sexes may di e , which could lead
© 2023 The Au ho s. Published by he Royal Socie y unde he e ms o he C ea i e
Commons A ibu ion License h p://c ea i ecommons.o g/licenses/by/4.0/, which pe mi s
un es ic ed use, p o ided he o iginal au ho and sou ce a e c edi ed.
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o sexual con lic [3] and sexual coe cion [4]. The mos d ama ic examples o sexual con lic a e
in an icide, i.e. he so-called ‘B uce e ec ’, whe e he dea h o o sp ing s imula es o ula ion in he
mo he s o some mammalian species [5,6], o he o ced copula ion beha iou o male wa e owl,
which leads o an a ms ace educing he isk o o ced copula ion and unwan ed e iliza ion [7].
Thus, sexual con lic di ec ly gene a es selec i e p essu es and a ec s e olu iona y p ocesses [8].
Inc eased e o s by males (ha assmen , o ced copula ion, in imida ion) o gain access o emales
could lead o ep oduc i e ailu e o indi iduals in ol ed and e en nega i ely a ec emale su i al
(ducks: [9], ogs and oads: [10], mammals: [11]).
In ogs and oads, a highe isk o mo ali y in ma ing emales has been epo ed, pa icula ly in
explosi e b eeding species. This b eeding sys em is cha ac e ized by an (o en) male-biased
ope a ional sex a io, synch onized emale ecep i i y and low sexual selec ion [12]. In explosi e
b eeding anu an species, pai o ma ion is mainly d i en by male sc amble compe i ion o emales.
Females could ei he be a ac ed by male ad e isemen calls o emain passi e, depending on he
densi y a he b eeding si e [13]. Being ac i e as a emale includes he isk o being amplec ed by
se e al males [13], which could lead o dea h o he espec i e emale [10,14,15].
The Eu opean common og, Rana empo a ia Linnaeus, 1758, is an explosi e b eede , o ming dense
b eeding agg ega ions in ea ly sp ing [16]. Recen li e a u e, including comp ehensi e e iews, s a es ha
emales a e passi e du ing cou ship and ep oduc i e beha iou [16], which is a ibu ed o sexual
coe cion, pa icula ly emale ha assmen , by males. Howe e , he e is published e idence ha
R. empo a ia emales a e no passi e du ing ep oduc ion. Mo e han 250 yea s ago, Rosenho [17]
epo ed ha emales p oduce g un ing sounds like male elease calls [18]. This beha iou was obse ed
a e emales ha e deposi ed eggs, hus signalling non- ecep i i y o a male [19]. In addi ion o hese calls,
Sa age [19] obse ed emales showing onic immobili y (we he ein use his neu al e m ins ead o he
mo e an h opocen ic ‘dea h eigning’) [20], when g abbed by a male, some imes o se e al hou s.
Female common ogs a e he e o e unlikely o be de enceless agains sexual coe cion by males.
He e we desc ibe emale ma e a oidance beha iou s obse ed du ing a ecen s udy o male ma e
choice [21]. Ou obse a ions sugges ha emale common ogs a e no as passi e as is usually
assumed, and ha age and expe ience may play a key ole in he pe o mance o hese beha iou s.
2. Me hods
In sp ing 2019, we collec ed male and emale common ogs (Rana empo a ia) o es whe he males show
a p e e ence o emale body size [21]. We placed wo di e en ly sized emales oge he wi h a male in a
wa e - illed box (40 × 60 × 40 cm, 5 cm o wa e ) and allowed hem o mo e eely o one hou . We
eco ded he ma ing beha iou in each box using a webcam (LogiTech 920). Female a oidance o male
ma ing a emp s was obse ed by e iewing he ideo oo age. Fo de ails on loca ion and handling
see Di ich e al. [21]. All aw da a and sc ip s o ep oducing he analysis a e s o ed in an online
eposi o y [22].
We coun ed he occu ence o beha iou s alone, and in all possible combina ions (e.g. calls wi h
o a ion and/o onic immobili y, e c.). We used a pai wise - es wi h p-adjus men o mul iple
es ing ( alse disco e y a e) [23] o de e mine whe he emale body size di e ed when pe o ming
speci ic beha iou s. We es ed his o he mos common ypes o beha iou s (sample size g ea e
han i e). We modelled escape p obabili ies using a binomial logi model o emale body size pe se
and he body size a io be ween emales and males. A body size a io abo e one means ha he
emale is la ge han he male, and ice e sa i below one. We used he R s a is ical en i onmen [24]
o all analyses and g aphs. We used he packages ggplo 2 [25], g idEx a [26], png [27] and ggsigni
[28] o plo g aphs, MuMIn [29] o calcula e he likelihood- a io adjus ed R
2
o he binomial models
and ply o coun he numbe o occu ences [30].
3. Resul s
We obse ed h ee emale a oidance beha iou s, namely ‘ o a ing’,‘ elease call(s)’and onic immobili y.
We de ined ‘ o a ing’as a emale s a ing o o a e a ound he own body axis when amplexed by a male,
while he male ies coun e ac ing he o a ion wi h i s hind ee (elec onic supplemen a y ma e ial,
ideo S1). Release calls a e emi ed when he emale is amplexed by he male and she begins o call.
Two di e en calls a e p oduced, a g un and a squeak (elec onic supplemen a y ma e ial, audio S2
and S3, see de ails in [18]). Tonic immobili y is de ined as he s i ening o he emale—a ms and legs
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ou s e ched om he body—a e being amplexed by a male (elec onic supplemen a y ma e ial, ideo
S4). All h ee beha iou s we e obse ed when he ogs we e in wa e , bu we also obse ed one ins ance
o onic immobili y in he e es ial habi a , be ween an 83 mm male and a 79 mm sized emale
(elec onic supplemen a y ma e ial, igu e S5).
In ou expe imen s, a o al o 54 emales we e amplexed by a male. The mos common emale ma e
a oidance beha iou was o a ing, which was exhibi ed by 83% o all amplexed emales, ei he alone o
in combina ion wi h he o he wo beha iou s. We also obse ed emale body o a ion in he na u al
habi a se e al imes, sugges ing ha i is a common beha iou . Release calls we e emi ed by 48% o
amplexed emales, and calls we e always associa ed wi h o a ing ( igu e 1a). Tonic immobili y
occu ed in 33% o all clasped emales, mos o en in combina ion wi h o a ing and calling (13/18).
The occu ence o all h ee beha iou s oge he was signi ican ly associa ed wi h smalle emale body
size, whe eas o a ing in combina ion wi h calling was associa ed wi h la ge emale body size
(pai wise - es wi h d co ec ion, p= 0.02, igu e 1b).
Displaying o ma e a oidance beha iou esul ed in he escape o 25 emales (46% o all emales in
amplexus). The p obabili y o escape showed a end o inc ease wi h dec easing emale body size
(binomial GLM; p= 0.06, igu e 2a), and wi h dec easing emale- o-male SVL a io (smalle emales,
binomial GLM; p= 0.09, igu e 2b).
4. Discussion
Eu opean common og emales displayed body o a ions, elease calls and onic immobili y in o de o
escape amplec ing males. Small emales used all h ee ma e a oidance beha iou s mo e equen ly han
la ge emales and had highe escape p obabili ies.
While se e al ma e a oidance beha iou s we e exhibi ed by emales, body o a ion was he mos
common beha iou when a emale was clasped by a male. In o de o main ain an up igh posi ion
and o keep holding he emale, males coun e ac ed he o a ion by using hei s e ched hind ee .
This beha iou has been desc ibed by Sa age [19] bu was ne e subsequen ly epo ed o ci ed.
The e could be se e al easons o he e ec i eness and high equency o emale o a ion. Ro a ing
he male unde he emale and he eby unde wa e migh o ce males o elease emales o a oid
d owning and enables emales o b ea he. Female o a ions could also be a s a egy es ing he
s eng h and endu ance o males. Ma ing wi h a s onge male could inc ease a emale’s su i al
p obabili ies. I a male can kick-o i als and hus p e en he o ma ion o a ‘ma ing ball’, he emale
is mo e likely o su i e he ep oduc i e season [10,14,15]. Females may he e o e es po en ial
ma es. Howe e , es ing po en ial ma es can also be cos ly [31], pa icula ly i a emale ecei es mo e
a en ion h ough his beha iou bu canno de end he sel agains sexual coe cion om mul iple
15
10
5
0
o a ing
o a ing
onic immobili y o a ing +
calling
o a ing +
calling
o a ing +
onic immobili y
o a ing +
calling +
onic immobili y
o a ing +
calling +
onic immobili y
emale a oidance beha iou SVL emales (mm)
none
55 60 65 70 75 80 85 90
app oached emales showing a oidance beha iou
a oidance beha iou s
(a)(b)
Figu e 1. (a) Coun da a o all di e en a oidance beha iou s in common og emales, (b) emale body size in mm and a oidance
beha iou displayed. Females displaying all h ee beha iou s we e on a e age signi ican ly smalle han emales displaying o a ing
and calling (pai wise - es wi h d co ec ion, p= 0.02). La ge whi e do s ep esen mean body size, whiske s he 95% con idence
in e al. Do s a e ji e ed o be e isibili y.
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males. I emains o be de e mined which (pheno ypic o geno ypic) ai (s) is (a e) unde selec ion,
leading o ma e accep ance o ejec ion, and wha bene i s and cos s, i any, a e associa ed wi h ma e
choice by emale R. empo a ia. The e seem o be no ob ious di ec bene i s o choosing a pa icula
male, as males p o ide no pa en al ca e o de end any esou ces. Di ec bene i s, such as inc eased
e iliza ion success by la ge o size-asso ed males ha e been disp o ed; in ac , e iliza ion success
has been ound o be independen o size asso men [32]. We also de ec ed a high a e o mul iple
pa e ni y in ou s udy popula ion (80% [33]), p obably due o ‘s ay spe m’, which would minimize
he po en ial adap i e e ec s o p ecopula o y emale ma e choice.
In e es ingly, smalle emale common ogs we e mo e success ul a escaping an amplexus by o a ing
han la ge emales. This may be due o mechanical g ip cha ac e is ics. I emales a e (much) smalle
han he amplexing male, he male may no be able o hold hem igh enough o main ain he
amplexus. In Cane oads (Rhinella ma ina) i has been shown ha males wi h sho e a ms a e be e
a holding on o emales han males wi h longe a ms. The la e a e mo e o en eplaced by o he
males because hey canno hold he emales p ope ly [34]. Likewise in he Common oad (Bu o bu o),
male akeo e s we e mo e success ul when pai s we e no size asso ed, i.e. size misma ch led o
weake bonding in amplexus [35]. In ou s udy popula ion, we ound size-asso a i e ma ing [21,32],
whe e he males a e usually smalle han he emales. A highe escape p obabili y o smalle emales
amplexed by la ge males could be due o mechanical g ip p ope ies o he pai and suppo s he
p e iously documen ed size-asso a i e pa e ns in he absence o male ma e choice [21,32].
Tonic immobili y is known o occu h oughou he animal kingdom, anging om in e eb a es o
e eb a es [20]. I is mainly in e p e ed as a de ensi e s a egy agains p eda ion [36]. As a s ess
esponse o an immedia e h ea o p eda ion (o a s ong ac ile s imulus), i is an ‘e olu iona y
conse ed de ensi e mechanism o las eso ’[37]. Tonic immobili y as a ac ic o a oid ma ing,
ep oduc i e cannibalism o male ha assmen , has been obse ed in a hand ul o species, mainly in
a h opods such as spide s [38] and d agon lies [39], and in one o he amphibian species, he sha p-
ibbed new (Pleu odeles wal l; [40]). Sa age [41] epo ed a emale R. empo a ia ha showed onic
immobili y ( eigned dea h) o wo hou s a e being amplexed by a male. The male called equen ly
du ing his ime bu did no le he go. We ha e obse ed onic immobili y by emales equen ly, bu
mo e o en in smalle and he e o e younge emales. The smalle emales also showed he ull
epe oi e o beha iou s mo e o en han he la ge emales. We he e o e specula e ha his
beha iou may be ela ed o age o expe ience o emales. S ess inc eases co icos e one ci cula ing in
he blood, which could inhibi ep oduc i e beha iou [42] and is posi i ely co ela ed wi h he
du a ion o onic immobili y [37]. Less expe ience wi h ep oduc ion may esul in mo e s essed
emales [20,43,44]. In he Ame ican wood og (Li hoba es syl a icus), a species which is e y simila in
mo phology and beha iou o he Eu opean common og, emales showed a highe s ess esponse
1.00 1.00
0.75
0.50
0.25
0
0.75
0.50
0.25
0
escape p obabili y
60 70
SVL emale (mm) SVL a io ( emale/male)
80 90 0.8 1.0 1.2 1.4
(a)(b)
Figu e 2. (a) Escape p obabili y o emale common ogs du ing a oidance beha iou as a unc ion o emale body size (SVL),
o (b) he emale- o-male SVL a io. Do s ep esen indi idual emales and hei espec i e a oidance beha iou , ligh o ange =
o a ing, o ange = o a ing and calling, ed = o a ing, calling and onic immobili y. Do s a e ji e ed o be e isibili y.
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du ing b eeding when male sc amble compe i ion was high [45]. An impo an sou ce o s ess, ha
could igge onic immobili y, is he equen ly obse ed o ma ion o ‘ma ing balls’, which o en
esul in he dea h o emales and males by d owning [10,14,15]. Whe he d owning (lack o oxygen)
is he main ac o leading o dea h is no en i ely clea , especially as his species is able o abso b
oxygen om he wa e h ough he skin and pa ly hibe na es in ponds o s eams [41]. I may be a
mix u e o ac o s ha lead o he dea h o indi iduals du ing hese ma ing balls. Tonic immobili y
can lead o b adyca dia and he e o e an inc ease in pe iphe al esis ance [37], which could educe
oxygen up ake h ough he skin. Du ing he igh , wa e may en e he lungs, u he educing
oxygen up ake. B eeding begins immedia ely a e hibe na ion and indi iduals do no eed be o e
joining he b eeding g oup [46], esul ing in high ene gy demands ha may no be me , leading o
allos a ic o e load and dea h [47]. Ano he ac o could be he high p essu e exe ed by he amplexed
males, which could damage he emale’s o gans and lead o egg ex usion [10]. Anyhow, wha he
p oxima e ac o killing he emales may be, onic immobili y may be a be e op ion o a emale han
igh ing he way ou o he amplexus, as any mo emen in a la ge ma ing g oup au oma ically
a ac s a en ion o u he nea by males and hus inc eases he p obabili y o a ma ing ball
o ma ion. Wi h hese conside a ions in mind, i would be in e es ing o measu e s ess co icos e one
le els in emale R. empo a ia and in es iga e how hey co espond o age and sex a io in b eeding
agg ega ions [45,48].
Fu u e s udies should conside in es iga ing di e en og densi ies, sex a ios and age classes, o es
o ma e choice and he po en ial cos s associa ed wi h ep oduc ion. Howe e , ou s udy p o ides clea
e idence ha emale ogs, e en in dense ma ing agg ega ions o explosi e b eede s, a e less helpless
han gene ally assumed.
E hics. The go e nmen om Lowe F anconia issued esea ch pe mi s (55.2 DMS 2532-2-316) and he Ba a ian s a e
o es y depa men pe mission o access he o es ponds. All animal beha iou al expe imen s ollowed he guidelines
p o ided by ASAB.
Da a accessibili y. The aw da a a e deposi ed oge he wi h a eadme ex ile o me ada a, desc ip ion o a iables and
he R-sc ip o ep oduce all analysis and igu es. The DOI is p o ided in he e e ences [22]. h ps://doi.o g/10.7479/
s00 - a45.
The audio and ideo iles a e p o ided in elec onic supplemen a y ma e ial [49].
Decla a ion o AI use. We ha e no used AI-assis ed echnologies in c ea ing his a icle.
Au ho s’con ibu ions. C.D.: concep ualiza ion, da a cu a ion, o mal analysis, unding acquisi ion, in es iga ion,
me hodology, p ojec adminis a ion, w i ing—o iginal d a , w i ing— e iew and edi ing; M.R.: concep ualiza ion,
unding acquisi ion, in es iga ion, me hodology, esou ces, supe ision, w i ing— e iew and edi ing.
All au ho s ga e inal app o al o publica ion and ag eed o be held accoun able o he wo k pe o med he ein.
Con lic o in e es decla a ion. We decla e ha ing no compe ing in e es s.
Funding. This s udy was suppo ed by a PhD schola ship om he s a e o Be lin (Elsa Neumann Founda ion) awa ded
o CD. Ma e ial cos s we e co e ed by he Museum ü Na u kunde Be lin.
Acknowledgemen s. We hank he ollowing people o hei suppo du ing ieldwo k and sigh ing o ideo ma e ial.
Melanie Tie je, Ya a Ha idy, Guillaume Dema e and Ju ek Ri z. We hank he s a o he ecological ield s a ion,
Uni e si y o Wü zbu g, p o iding access o c ucial in as uc u e. We a e indeb ed o he go e nmen om Lowe
F anconia o esea ch pe mi s and he Ba a ian s a e o es y depa men o access pe mission o he o es
ponds. The og icon used in he igu es is p o ided by la icon.com unde he Fla icon licence. Thanks o he
au ho Vic o ule o he c ea ion. We hank he edi o and wo anonymous e iewe s o hei aluable commen s.
Re e ences
1. Da win C. 1871 The descen o Man, and
selec ion in ela ion o Sex. London, UK: Mu ay.
2. T i e s R. 1972 Pa en al in es men and sexual
selec ion. In Sexual selec ion and he descen o
Man 1871–1971 (eds B. Campbell), pp. 136–179.
Chicago, IL: Aldine Publishing Company.
3. Pa ke GA. 1979 Sexual selec ion and sexual
con lic . In Sexual selec ion and ep oduc i e
compe i ion in insec s (eds MS. Blum, NA.
Blum), pp. 123–166. New Yo k, San F ancisco,
London, UK: Academic P ess.
4. Clu on-B ock TH, Pa ke GA. 1995 Sexual
coe cion in animal socie ies. Anim. Beha . 49,
1345–1365. (doi:10.1006/anbe.1995.0166)
5. Palombi RA. 2015 In an icide as sexual con lic :
coe olu ion o male s a egies and emale
coun e s a egies. Cold Sp ing Ha b. Pe spec .
Biol. 7, a017640. (doi:10.1101/cshpe spec .
a017640)
6. Zipple MN. 2020 When will he B uce
e ec e ol e? The oles o in an icide, e icide and
ma e nal dea h. Anim. Beha . 160, 135–143.
(doi:10.1016/j.anbeha .2019.11.014)
7. B ennan PL, P um RO, McC acken KG, So enson
MD, Wilson RE, Bi khead TR. 2007 Coe olu ion
o male and emale geni al mo phology in
wa e owl. PLoS ONE 2, e418. (doi:10.1371/
jou nal.pone.0000418)
8. Pa ke GA. 2006 Sexual con lic o e
ma ing and e iliza ion: an o e iew. Phil.
T ans. R. Soc. B 361, 235–259. (doi:10.1098/
s b.2005.1785)
9. McKinney F, De ickson SR, Mineau P. 1983
Fo ced copula ion in wa e owl. Beha iou 86,
250–293. (doi:10.1163/156853983X00390)
10. T au h SE, McCallum ML, Ca w igh ME. 2000
B eeding mo ali y in he wood og, Rana
syl a ica (Anu a: Ranidae), om no hcen al
A kansas. J. A k. Acad. Sci. 54, 154–156.
11. Cassini MH. 2021 Sexual agg ession in
mammals. Mam. Re . 51, 247–255. (doi:10.
1111/mam.12228)
oyalsocie ypublishing.o g/jou nal/ sos R. Soc. Open Sci. 10: 230742
5
Downloaded om h ps:// oyalsocie ypublishing.o g/ on 23 Oc obe 2023
12. Emlen ST, O ing LW. 1977 Ecology, sexual
selec ion, and he e olu ion o ma ing sys ems.
Science 197, 215–223. (doi:10.1126/science.
327542)
13. Wells KD. 1979 The social beha iou o anu an
amphibians. Anim. Beha . 25, 666–693.
(doi:10.1016/0003-3472(77)90118-X)
14. Da ies NB, Halliday TR. 1979 Compe i i e ma e
sea ching in male common oads, Bu o bu o.
Anim. Beha . 27, 1253–1267. (doi:10.1016/
0003-3472(79)90070-8)
15. Howa d RD. 1980 Ma ing beha iou and ma ing
success in wood ogs Rana syl a ica.Anim.
Beha . 28, 705–716. (doi:10.1016/S0003-
3472(80)80130-8)
16. Gollmann B, Bo kin L, G ossenbache K,
Weddeling K. 2014 Rana empo a ia Linnaeus
1758 –G as osch. In Handbuch de Rep ilien
und Amphibien Eu opas, ol 5/IIIA: F oschlu che
(Anu a) IIIA, (Ranidae I) (eds K. G ossenbache ),
pp. 305–437. Wiebelsheim: Aula-Ve lag.
17. Rosenho A. 1758 His o ia na u alis ana um
nos a ium in qua omnes ea um p op ie a es,
p aese im quae ad gene a ionem ipsa um
pe ine , usius ena an u : Die na ü liche
His o ie de F ösche hiesigen Landes, wo innen
alle Eigenscha en de selben, sonde lich abe ih e
Fo p lanzung, ums ändlich besch ieben we den.
Nü nbe g: Fleischmann.
18. Di ich C, Rödel M-O. 2020 Desc ip ion o
emale elease calls o he Eu opean common
og, Rana empo a ia (Anu a: Ranidae).
Salamand a 56,91–94.
19. Sa age RM. 1934 The b eeding beha iou o he
common og, Rana empo a ia empo a ia
Linn., and o he Common oad, Bu o bu o bu o
Linn. P oc. Zool. Soc. Lond. 104,55–65. (doi:10.
1111/j.1469-7998.1934. b06220.x)
20. Humph eys RK, Rux on GD. 2018 A e iew o
hana osis (dea h eigning) as an an i-p eda o
beha iou . Beha . Ecol. Sociobiol. 72, 22.
(doi:10.1007/s00265-017-2436-8)
21. Di ich C, Tie je M, Rödel M-O. 2022 La ge is
no be e : no ma e p e e ence by Eu opean
common og (Rana empo a ia) males.
Beha iou 159, 1133–1150. (doi:10.1163/
1568539X-bja10169)
22. Di ich C, Rödel M-O. 2023 Da ase : D op dead!
Female ma e a oidance in an explosi ely
b eeding og. Da a Reposi o y a Museum ü
Na u kunde, Be lin. (doi:10.7479/s00 - a45)
23. Benjamini Y, Hochbe g Y. 1995 Con olling he
alse disco e y a e: a p ac ical and powe ul
app oach o mul iple es ing. J. R. S a is . Soc. B
57, 289–300. (doi:10.1111/j.2517-6161.1995.
b02031.x)
24. R Co e Team. 2022 R: a language and
en i onmen o s a is ical compu ing. Vienna,
Aus ia: R Founda ion o S a is ical Compu ing.
See h ps://www.R–p ojec .o g/.
25. Wickham H. 2009 ggplo 2: elegan g aphics o
da a analysis. New Yo k, NY: Sp inge .
26. Auguie B. 2017 g idEx a: miscellaneous
unc ions o ‘g id’g aphics. R package e sion
2.3. See h ps://c an. -p ojec .o g/web/
packages/g idEx a/index.h ml.
27. U banek S. 2022 png: ead and w i e PNG
images. R package e sion 0.1-8. See h ps://
CRAN.R-p ojec .o g/package=png.
28. Ahlmann-El ze C, Pa il I. 2021 ggsigni : R
package o displaying signi icance b acke s o
‘ggplo 2’.PsyA xi . (doi:10.31234/os .io/7awm6)
29. Ba on K. 2023 MuMIn: mul i–model in e ence.
R package e sion 1.47.5. See h ps://CRAN.R-
p ojec .o g/package=MuMIn.
30. Wickham H. 2011 The spli –apply –combine
s a egy o da a analysis. J. S a . So w. 40,
1–29. (doi:10.18637/jss. 040.i01)
31. Jennions MD, Pe ie M. 1997 Va ia ion in ma e
choice and ma ing p e e ences: a e iew o
causes and consequences. Biol. Re . 72,
283–327. (doi:10.1017/S0006323196005014)
32. Di ich C, Rod íguez A, Sege O, D akulićS,
Feldhaa H, Vences M, Rödel M-O. 2018
Tempo al mig a ion pa e ns and ma ing ac ics
in luence size-asso a i e ma ing in Rana
empo a ia.Beha . Ecol. 29, 418–428. (doi:10.
1093/beheco/a x188)
33. Di ich C, Hus e J, Rödel M-O, Feldhaa H.
2019 Ma iline e ec s on me amo phic ai s in
a na u al sys em in he Eu opean common og
(Rana empo a ia). Ecol. E ol. 9, 3075–3088.
(doi:10.1002/ece3.4811)
34. Cla ke GS, Shine R, Phillips BL. 2019 May he
(selec i e) o ce be wi h you: spa ial so ing
and na u al selec ion exe opposing o ces
on limb leng h in an in asi e amphibian.
J. E ol. Biol. 32, 994–1001. (doi:10.1111/jeb.
13504)
35. Höglund J. 1989 Pai ing and spawning pa e ns
in he common oad, Bu o bu o: he e ec s o
sex a ios and he ime a ailable o male-male
compe i ion. Anim. Beha . 38, 423–429.
(doi:10.1016/S0003-3472(89)80035-1)
36. Toledo LF, Sazima I, Haddad CFB. 2010 Is i all
dea h eigning? Case in anu ans. J. Na . His .
44, 1979–1988. (doi:10.1080/
00222931003624804)
37. Roge s SM, Simpson SJ. 2014 Thana osis. Cu .
Biol. 24, R1031–R1033. (doi:10.1016/j.cub.
2014.08.051)
38. Bilde T, Tuni C, Elsayed R, Peká S, To S. 2006
Dea h eigning in he ace o sexual cannibalism.
Biol. Le . 2,2–25. (doi:10.1098/ sbl.2005.0392)
39. Kheli a R. 2017 Faking dea h o a oid male
coe cion: ex eme sexual con lic esolu ion in a
d agon ly. Ecology 98, 1724–1726. (doi:10.
1002/ecy.1781)
40. Janssenswillen S, Bossuy F. 2016 Male
cou ship phe omones induce cloacal gaping in
emale new s (Salamand idae). PLoS ONE 11,
e0144985. (doi:10.1371/jou nal.pone.0144985)
41. Sa age RM. 1961 The ecology and li e his o y o
he common og ( ana empo a ia empo a ia).
London: Si Isaac Pi man and Sons, L d.
42. Ca JA. 2011 S ess and ep oduc ion in
amphibians. In Ho mones and ep oduc ion o
e eb a es, olume 2 –amphibians (eds D.
No is, K. Lopez), pp. 99–116. London,
Bu ling on, San Diego: Academic P ess.
43. Reading CJ. 2001 Non- andom pai ing wi h
espec o pas b eeding expe ience in he
common oad (Bu o bu o). J. Zool. 255,
511–518. (doi:10.1017/S0952836901001595)
44. Rome o-Diaz C, Gonzalez-Jimena V, Fi ze PS.
2019 Co icos e one media ed ma e choice
a ec s emale ma ing eluc ance and
ep oduc i e success. Ho m. Beha . 113,1–12.
(doi:10.1016/j.yhbeh.2019.04.011)
45. Swie k L, G aham SP, Langkilde T. 2014 The s ess
o sc amble: sex di e ences in beha io and
physiological s ess esponse in a ime-cons ained
ma ing sys em. Beha . Ecol. Sociobiol. 68,
1761–1768. (doi:10.1007/s00265-014-1784-x)
46. Jönsson KI, He czeg G, O’Ha RB, Söde man F,
Te Schu e AFH, La sson P, Me ilä J. 2009 Sexual
pa e ns o p eb eeding ene gy ese es in he
common og Rana empo a ia along a
la i udinal g adien . Ecog aphy 32, 831–839.
(doi:10.1111/j.1600-0587.2009.05352.x)
47. McEwen BS, Wing ield JC. 2003 The concep o
allos asis in biology and biomedicine. Ho m. Beha .
43,2–15. (doi:10.1016/S0018-506X(02)00024-7)
48. Bo odo i syna O, Tkaczynski JA, Co be CM,
Lowe h JA, Chandle DJ. 2022 Age-and sex-
dependen changes in locus coe uleus
physiology and anxie y-like beha io ollowing
acu e s esso exposu e. F on . Beha . Neu osci.
16, 808590. (doi:10.3389/ nbeh.2022.808590)
49. Di ich C, Rödel M-O. 2023 D op dead! emale
ma e a oidance in an explosi ely b eeding og.
Figsha e. (doi:10.6084/m9. igsha e.c.6858610)
oyalsocie ypublishing.o g/jou nal/ sos R. Soc. Open Sci. 10: 230742
6
Downloaded om h ps:// oyalsocie ypublishing.o g/ on 23 Oc obe 2023