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ANIMAL HUSBANDRY & VETERINARY SCIENCE | RESEARCH ARTICLE
Sex e ec in mu ual ol ac o y ela ionships
o indi idually caged abbi s
Alessand o Finzi, Paolo Neg e i, Gio anna Bianconi and Ped o González-Redondo
Cogen Food & Ag icul u e (2015), 1: 992154
Finzi e al., Cogen Food & Ag icul u e (2015),
1: 992154
h p://dx.doi.o g/10.1080/23311932.2014.992154
ANIMAL HUSBANDRY & VETERINARY SCIENCE | RESEARCH ARTICLE
Sex e ec in mu ual ol ac o y ela ionships
o indi idually caged abbi s
Alessand o Finzi
1
*, Paolo Neg e i
2
, Gio anna Bianconi
2
and Ped o González-Redondo
3
Abs ac :To assess he sex in luence on sni ing beha io o abbi s, se s o h ee
abbi s each we e loca ed o se en days in con iguous cages di ided by a me al
wall wi h holes ha p e en ed he neighbo ing abbi s o see each o he . A buck
was loca ed in he cen al cage, wi h a doe a each side. Rabbi beha io was ideo
eco ded o obse e animals sni ing wi h he muzzle nea he wall. The bucks
displayed an ol ac o y p e e ence owa ds one o he wo does, which dec eased in
ew days. The signi icance was p<0.01 o he i s h ee days, i lowe ed o p<0.05
in he nex h ee days and om he se en h, i u ned insigni ican (p>0.05). The
in e es o bucks owa ds he does was also cha ac e ized by a ene ic sc a ching
o he sepa a ion wall, con empo a y wi h in ense sni ing, displayed only o he
i s 35min o he i s day. The sni ing beha io o does a he cen al cage hous-
ing he male was no so ma ked as in bucks, and i p og essi ely changed ac oss he
ial (p<0.01). In conclusion, abbi s es ablish a ansi o y sex-o ien ed ol ac o y
ela ionship wi h he conspeci ics housed in con iguous cages, which looks no
longe necessa y once he abbi s ha e ecognized each o he .
Subjec s: Animal Beha io ; Ve eb a es; Rep oduc ion
Keywo ds: abbi a m cages; abbi social beha io ; abbi sexual beha io
*Co esponding au ho : Alessand o
Finzi, Rabbi Uncon en ional Keeping
Expe imen al Cen e, Conso zio ‘Coniglio
Ve de Lep ino di Vi e bo’ Via S. Ma ia,
43, 01030 Vasanello (VT), I aly
E-mail: [email p o ec ed]
Re iewing edi o :
Manuel Tejada Mo al, Uni e si y o
Se ille, Spain
Addi ional in o ma ion is a ailable a
he end o he a icle
ABOUT THE AUTHORS
The ac i i y o he esea ch g oup o he Rabbi
Uncon en ional Keeping Expe imen al Cen e
a Vi e bo (I aly) is mainly ela ed o al e na i e
keeping sys ems o imp o e abbi wel a e, o
minimizing he p oduc ion cos s, o p oduce high-
quali y mea in he indus ialized Coun ies, and
o imp o e ood secu i y in he de eloping ones.
The esea ch epo ed in his pape pe ains o a
line aimed a a be e unde s anding o he abbi
e hology unde indus ial a ming condi ions.
Indi idually caged abbi s a e conside ed dep i ed
o social ela ionship, bu p e ious ials ha e
shown ha a isual ela ionship is main ained.
The p esen esea ch demons a es ha abbi s
es ablish ol ac o y ela ionships e en hough hey
a e kep in indi idual cages.
PUBLIC INTEREST STATEMENT
Public conce ns agains indus ial a ming
include opposi ion o cage-based sys ems, unde
he eeling ha impede he social in e ac ions
among he animals. This in es iga ion
demons a es ha abbi s kep in con iguous
indi idual cages main ain social ela ionships by
ol ac o y ac i i y. This was con i med by a sni ing
ac i i y nea he wall, main ained o some days
when abbi s we e loca ed in cages sepa a ed
by solid walls wi h holes ha p e en ed hem o
see each o he bu allowed smelling. To check
whe he also an ol ac o y sexual ela ionship
exis s, a ial was pe o med by pu ing male
abbi s be ween wo emales in adjacen cages.
Male abbi s displayed a p e e ence owa ds
oneo he emales. The sni ing beha io o
emales was no so ma ked as in male abbi s.
Inbo h sexes, his sex-o ien ed beha io
dec eased du ing he i s week, sugges ing i
is no longe necessa y once he abbi s ha e
ecognized each o he because he smell is el
anyway.
Recei ed: 21 Oc obe 2014
Accep ed: 19 No embe 2014
Published: 09 Janua y 2015
© 2015 The Au ho (s). This open access a icle is dis ibu ed unde a C ea i e Commons A ibu ion
(CC-BY) 3.0 license.
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Finzi e al., Cogen Food & Ag icul u e (2015),
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h p://dx.doi.o g/10.1080/23311932.2014.992154
1. In oduc ion
The lack o social ela ionship is conside ed a wel a e cons ain in he indus ial abbi keeping
sys em, in which each doe has i s own cage, disposed as a pa o a ow along he building (T ocino
& Xicca o, 2006; Ve ga, 2000). To main ain isual con ac s among animals is speci ically ecom-
mended by Boe s e al. (2002), bu i was asce ained ha a mu ual isual ela ionship is always
es ablished, a leas among does loca ed in single cages in he same ow (Neg e i, Albani, & Finzi,
2004; Neg e i, Bianconi, & Finzi, 2008). As he impo ance o ol ac o y s imuli o elici speci ic
beha io s, mainly in sexual ela ionships, is well known (Maina di, 1992), his possibili y has also
been in es iga ed and i was possible o p o e ha does sni a each o he , hough his beha io is
obse ed only when he animals a e ecen ly loca ed in con iguous cages and i ends o disappea
in he lag o abou a week (Neg e i, Bianconi, & Finzi, 2010). Following his line o in es iga ion,
aimed a be e unde s anding how abbi s can main ain a social ela ionship hough loca ed in
single cages, a esea ch was ca ied ou o s udy wha peculia ol ac o y beha io can be obse ed
when a buck is loca ed in a cage be ween wo does. This expe imen is aimed only o asce ain i
sni ing beha io is in luenced by sex o he animals, since males a e no mally loca ed oge he ,
a he han among does, in he indus ial buildings.
2. Ma e ials and me hods
2.1. Expe imen al p ocedu e
The expe imen was pe o med u ilizing he same cage se u ilized in p e ious ials (Figu e 1; Neg e i
e al., 2004, 2008, 2010). The expe imen al se was o med by a ow o h ee con iguous cages loca ed
in he open ai in an o cha d (Vi e bo p o ince, I aly; 42° 25′ N, 12° 06′ E) o a oid he phe omones
sa u a ion o closed en i onmen s. The cages whe e limi ed by a solid in wall ha impai ed he ani-
mals o see each o he , while small holes (diame e 1.5mm; 4 lines; 6cm dis ance; 7 holes pe line)
allowed he ol ac o y pe cep ion o he con iguous animals. Adul abbi s (Lep ino o Vi e bo b eed;
ANCI-AIA, 2006), se en-mon h-old, we e loca ed in o he cages in he same ime. A buck was loca ed
in he cen al cage, while a doe was disposed a each side. This is no a disposi ion no mal in indus ial
sys ems whe e sexes a e aised in di e en a eas, bu , in his case, he aim was o check i does
showed an in e es o he male, sni ing owa ds he walls limi ing he cen al cages and i he bucks
showed same p e e ence o one o he does o no .
Figu e 1. Expe imen al cage
consis ing o h ee con iguous
indi idual compa men s
delimi ed by a solid in wall
ha impai he animals seeing
each o he , and p o ided
wi h small holes allowing he
ol ac o y pe cep ion o he
con iguous abbi s.
No es: The abbi a igh is
smelling a he wall.
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Animal beha io was eco ded 24h ound, o se en consecu i e days, wi h h ee eplica ions and
new animals each eplica ion. A h ee imes eplica ion was su icien o demons a e ha sni ing
ela ionships exis and o show ha beha io is s ongly a ec ed by indi iduali y, as in p e ious ex-
pe imen s whe e beha io al esponse was in ol ed (Finzi, Cio ba, & Macchioni, 2001; Neg e i e al.,
2004, 2008, 2010). Pho og ams we e obse ed o 1min each 5min o a o al o 2,184 obse a ions
pe each abbi , and single o ecip ocal sni ing a he wall was eco ded. Reco ds we e also ana-
lyzed o male beha io , which we e seen sc a ching ac i ely a he wall as i ying o go h ough i .
In his case, he bucks’ beha io was checked o 45 consecu i e minu es, jus a e pu ing he ani-
mals in he cages. Longe obse a ion ime was no necessa y because his beha io was, in case,
e y immedia e and ansi o y.
2.2. S a is ical analysis
In o de o analyze, o each single day and o he whole pe iod o obse a ion, (1) bucks showing
an ol ac o y p e e ence o one o he does loca ed a bo h sides, and (2) does showing o no an
ol ac o y p e e ence o he buck loca ed a he cen al cage, goodness-o - i χ2 es s we e pe o med.
Fo hese es s, he null hypo hesis ha animals p e e ed each one o bo h al e na i es in he same
p opo ion was assumed. To analyze he change o hese p e e ences ac oss he ial pe iod, χ2 es s
on con ingency ables we e pe o med. These analyses (Fe án, 1996) we e pe o med acco ding o
SPSS 15.0 (SPSS Inc., 2006).
3. Resul s and discussion
I was obse ed ha all bucks, despi e indi idual a iabili y, showed a signi ican ol ac o y p e e ence
o one o he does loca ed a bo h sides (nea 70%; p<0.001; Table 1; Figu e 2). This beha io was
pe sis en o he whole week ha las ed he ial, in he sense ha i did no change ac oss he ial
(χ2=4.182; p=0.653), bu i ended o dec ease slowly. The p e e ence was e y signi ican (p<0.01)
o he i s h ee days (72.8 s. 27.2%), and i lowe ed o p<0.05 in he nex h ee days (66.4 s.
33.6%). On he se en h day, he di e ence was s ill e iden (57.6 s. 42.4%), bu i los signi icance
(p=0.384).
The does’ sni ing in e es o he conspeci ic loca ed in he con iguous cage (Neg e i e al., 2010)
was mo e ma ked and in ense when males we e in ol ed. Ne e heless, as al eady shown, sni ing
a he wall ended o diminish a e he abbi s ecognized each o he , hey need no longe any spe-
ci ic beha io o smell he conspeci ic in neighbo ing cages.
Table 1. F equency o sni ing occu ences o males showing a p e e ence o one o he does se a bo h sides o he buck’s cage
Day Buck 1 Buck 2 Buck 3 To al
P e e ence No
p e e ence
P e e ence No
p e e ence
P e e ence No
p e e ence
P e e ence No
p e e ence
p
1 38 8 7 7 11 7 56 22 0.001
2 15 7 9 3 10 4 34 14 0.004
3 5 2 7 4 16 2 28 8 0.001
4 13 5 9 3 6 5 28 13 0.019
5 7 7 6 4 11 1 24 12 0.046
6 14 6 6 6 11 5 31 17 0.043
7 7 7 9 5 3 2 19 14 0.384
1–7 (media ±
DS, sample)
14.1 ± 11.2 6.0 ± 2.0 7.6 ± 1.4 4.6 ± 1.5 9.7 ± 4.2 3.7 ± 2.1 31.4 ± 11.9 14.3 ± 4.3 0.001
1–7 (media,
all he ime)
70.5 30.0 38.0 23.0 48.5 18.5 157.0 71.5
1–7 (%) 70.2 29.8 62.4 37.6 72.3 27.7 68.8 31.2
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The p e e ence o one o he does was ma ked and pe sis en o all he h ee bucks, while in he
p e ious ial (Neg e i e al., 2010), his beha io was shown, hough less ma ked, only by one
o  hedoes when animals o he same sex whe e es ed. The p e e ence o one o he does ound in
he p esen ial con i ms ha abbi s u ilize ol ac o y communica ion signals o iden i ica ion o
ma es (Ma ai & Rashwan, 2003).
The in e es o bucks owa ds he does was also shown by a ypical beha io o ene ic sc a ching
a he sepa a ion wall, con empo a y wi h in ense sni ing (Figu e 3), mainly when he does we e
nea o he wall, equen ly also sni ing a i . This beha io was e y ansien because i was
obse ed only o he i s 35min o he i s day a mos . P obably i depends on he ime he buck
ge s us a ed o he unsuccess ul sc a ching beha io . Also, indi iduali y was e iden as shown in
Figu e 3; one subjec s opped sc a ching a he wall nea ly immedia ely, while ano he pe sis ed in
his e o o hal an hou .
Figu e 2. A buck is displaying
an ol ac o y beha io owa ds
a doe loca ed in a con iguous
cage delimi ed by a solid in
wall p o ided wi h small holes.
Figu e 3. Du a ion o occu ence
o males sni ing and sc a ching
a he sepa a ion wall a e
being pu in o he cages.

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The beha io o does was no so ma ked as o males (Figu e 4), and i changed ac oss he ial
(χ2=20.517; p=0.002). Ne e heless, excep he i s day, when he beha io was mo e explo a i e
han sex o ien ed, sni ing a he cen al cage was obse ed whe e he buck was loca ed. Some imes
he signi icance le el (p<0.05) was eached in single days, bu o e all, he signi icance was high
(p<0.01).
4. Conclusions
The ial showed ha abbi s es ablish an ol ac o y ela ionship wi h he conspeci ics loca ed in
con iguous cages. This ela ionship is sex o ien ed. I looks ansi o y because when he animals
ha e ecognized each o he by sni ing, his beha io is no longe necessa y as ol ac o y s imuli,
di e en ly by isual ones, can be pe cei ed also when he animal a e no speci ically sni ing and
e en i hey ha e he heads o ien ed in di e en di ec ions. Fo his eason, isual ela ionship can
be obse ed as a pe sis en social ac i i y easily ecognized; on he con a y, he ol ac o y ela ion-
ship, hough ob iously pe sis en , can be s udied only o a sho e pe iod (days o e en minu es),
jus a e he abbi s ha e been loca ed in o con iguous cages.
Figu e 4. Pe cen age o
occu ences o does showing
a p e e ence o no p e e ence
o he male (mean o h ee
eplica ions).
No es: *—P < 0.05; **— P < 0.01;
***—P < 0.001; n.s.—P > 0.05.
Funding
To suppo his esea ch s age du ing which his ial
wasca ied ou , Ped o González-Redondo ecei ed
wog an s om he IV Plan P opio de In es igación o he
Uni e si y o Se ille (Spain) [g an numbe PP2010-05-
071]; Con oca o ia de Incen i os a Ac i idades de Ca ác e
Cien í ico y Técnico o he Conseje ía de Inno ación,
Ciencia y Emp esa (Jun a de Andalucía, Spain).
Au ho de ails
Alessand o Finzi
1
E-mail: [email p o ec ed]
Paolo Neg e i
2
E-mail: [email p o ec ed]
Gio anna Bianconi
2
E-mail: gio [email p o ec ed]
Ped o González-Redondo
3
E-mail: [email p o ec ed]
1
Rabbi Uncon en ional Keeping Expe imen al Cen e,
Conso zio ‘Coniglio Ve de Lep ino di Vi e bo’ ia S. Ma ia,
43, 01030 Vasanello (VT), I aly.
2
CRF Coope a i a Rice ca Finalizza a, Uni e si à To Ve ga a,
ia della Rice ca Scien i ica, snc., 00133 Roma, I aly.
3
Facul y o Ag icul u al Enginee ing, Depa men o
Ag o o es y Sciences, Uni e si y o Se ille, Ca e e a de
U e a, km 1, 41013 Se ille, Spain.
Ci a ion in o ma ion
Ci e his a icle as: Sex e ec in mu ual ol ac o y
ela ionships o indi idually caged abbi s, A. Finzi,
P.Neg e i, G. Bianconi & P. González-Redondo,
Cogen Food& Ag icul u e(2015), 1: 992154.
Co e image
Sou ce: Au ho .
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Finzi e al., Cogen Food & Ag icul u e (2015),
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h p://dx.doi.o g/10.1080/23311932.2014.992154
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