Sex effect in mutual olfactory relationships of individually caged rabbits

Page 1 o 7 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. Page 2 o 7 Page 3 o 7 Finzi e al., Cogen Food & Ag icul u e (2015), 1: 992154 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. Page 4 o 7 Finzi e al., Cogen Food & Ag icul u e (2015), 1: 992154 h p://dx.doi.o g/10.1080/23311932.2014.992154 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 Page 5 o 7 Finzi e al., Cogen Food & Ag icul u e (2015), 1: 992154 h p://dx.doi.o g/10.1080/23311932.2014.992154 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. Page 6 o 7 Finzi e al., Cogen Food & Ag icul u e (2015), 1: 992154 h p://dx.doi.o g/10.1080/23311932.2014.992154 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 . Re e ences ANCI-AIA. (2006). No me ecniche del lib o genealogico e del egis o anag a ico della specie cunicola. [Technicals anda ds o he abbi species s ud book] Rome: Au ho . Boe s, K., G ay, G., Lo e, J., Mahmu o ic, Z., McCo mick, S., Tu co e, N., & Zhang, Y. (2002). Com o able qua e s o abbi s in esea ch ins i u ions. In V. Reinha d & A. Reinha d (Eds.), Com o able qua e s o labo a o y animals (pp. 43–49). Washing on, DC: Animal Wel a eIns i u e. Fe án, M. (1996). SPSS pa a Windows. Análisis es adís ico. [SPSS o windows. S a is ical analysis] Mad id: Osbo ne-McG aw-Hill. Finzi, A., Cio ba, P., & Macchioni, P. (2001, May 23–24). E aluación compa ada del bienes a del conejo en sis emas al e na i os de c ía [Compa a i e e alua ion o abbi wel a e in al e na i e b eeding sys ems]. In Page 7 o 7 Finzi e al., Cogen Food & Ag icul u e (2015), 1: 992154 h p://dx.doi.o g/10.1080/23311932.2014.992154 © 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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Publishing wi h Cogen OA ensu es: • Immedia e, uni e sal access o you a icle on publica ion • High isibili y and disco e abili y ia he Cogen OA websi e as well as Taylo & F ancis Online • Download and ci a ion s a is ics o you a icle • Rapid online publica ion • Inpu om, and dialog wi h, expe edi o s and edi o ial boa ds • Re en ion o ull copy igh o you a icle • Gua an eed legacy p ese a ion o you a icle • Discoun s and wai e s o au ho s in de eloping egions Submi you manusc ip o a Cogen OA jou nal a www.Cogen OA.com P oceedings o he XXVI Symposium de Cunicul u a de ASESCU-I Symposium Ibé ico de Cunicul u a APEZ-ASPOC (pp. 164–167). A ei o,Po ugal. Maina di, D. (1992). Diziona io di E ologia [Dic iona y o e hology]. Tu in: Einaudi. Ma ai, F. M., & Rashwan, A. A. (2003). Rabbi s beha iou unde mode n comme cial p oduc ion condi ions—A e iew. A chi Tie zuch , 46, 357–376. Neg e i, P., Albani, A., & Finzi, A. (2004, Sep embe , 7–10). Loca ion and social beha iou o young abbi s bucks. InP oceedings o he 8 h Wo ld Rabbi Cong ess (pp.1257–1263). Puebla, Mexico. Neg e i, P., Bianconi, G., & Finzi, A. (2008, June, 10–13). Mu ual isual ela ionships o abbi s aised in indi idual cages. In P oceedings o he 9 h Wo ld Rabbi Cong ess (pp.1213–1216). Ve ona, I aly. Neg e i, P., Bianconi, G., & Finzi, A. (2010). Sho communica ion: Mu ual ol ac o y ela ionships in abbi s aised in indi idual cages. Wo ld Rabbi Science, 18, 33–36. h p://dx.doi.o g/10.4995/WRS SPSS Inc. (2006). Manual del Usua io de SPSS Base 150 [SPSS base 15.0 use ’s guide]. Chicago, IL: Au ho . T ocino, A., & Xicca o, G. (2006). Animal wel a e in ea ed abbi s: A e iew wi h emphasis on housing sys ems. Wo ld Rabbi Science, 14, 77–93. Ve ga, M. (2000, July, 4–7). In ensi e abbi b eeding and wel a e: De elopmen o esea ch, ends and applica ions. In P oceedings o he 7 h Wo ld Rabbi Cong ess (pp. 491–509). Valencia, Spain.