Small Ruminant Research 62 (2006) 39–41

The significance of the vomeronasal organ for offspringrecognition in sheep�

K.K. Booth

Department of Anatomy and Physiology, Faculty of Veterinary Science, University of Pretoria,Private Bag X04, Onderstepoort 0110, South Africa

Available online 8 September 2005

Abstract

Three groups of 10 Dorset ewes each were randomly selected to determine the importance of the vomeronasal organ foroffspring recognition during nursing. The ewes in treatment group 1 were rendered anosmic by two irrigations of their olfactorymucosa with a zinc sulfate–procaine solution. The vomeronasal organs of the ewes in treatment group 2 were rendered non-functional by electro-cauterization of the nasoincisive duct. The nasal cavities in the ewes in treatment group 3 were just irrigatedwith normal saline. Each ewe received a 1-day-old alien lamb and nine behavioural recordings were collected for the 10-min trial.Analyses of variances revealed that the ewes with non-functional vomeronasal organs were unable to distinguish alien lambsfrom their own and allowed alien lambs to suckle as if they were their own lambs. Both groups with functional vomeronasalorgans rejected alien lambs at the udder. Thus, it was concluded that the vomeronasal organ is used as a final determinant foroffspring recognition during nursing in sheep.© 2005 Elsevier B.V. All rights reserved.

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eywords: Sheep; Neonate recognition; Vomeronasal organ; Maternal behaviour

. Introduction

It is generally considered that visual and auditoryues are used by many female animals for offspringecognition at a distance. However, it has been demon-trated that female goats only require 5 min of initialontact immediately after birth to discriminate theirwn kids from aliens after several hours of separation.

� This paper is part of a special issue entitled Keynote Lectures ofhe 6th International Sheep Veterinary Congress—Guest Edited byr. George C. Fthenakis and Prof. Quintin A. McKellar.

E-mail address: ken.Booth@up.ac.za.

Such quick recognition could not come from normmemorization of visual and/or auditory cues.

Several studies have concluded that olfactiothe primary cue used by female animals to recogtheir offspring during close contact activities, suas nursing. This recognition is believed to be baupon the offsprings’ individual olfactory signature temanates from their body coat, specifically fromanal region. Many of the odors from the anal regiomost animals have been associated with pheromthat are specifically detected by the vomeronasal oand that influence a variety of reproductive activifrom sexual maturation to maternal behaviour.

921-4488/$ – see front matter © 2005 Elsevier B.V. All rights reserved.doi:10.1016/j.smallrumres.2005.07.029

40 K.K. Booth / Small Ruminant Research 62 (2006) 39–41

The vomeronasal organ is morphologically con-structed for detection of pheromones. It consists oftwo blind-ending, epithelial-lined tubes situated oneither side of the base of the nasal septum. Each tube isenclosed in a “C”-shaped cartilage and each tube hasonly one rostral opening into the nasoincisive duct.The nasoincisive ducts open onto the floor of the nasalcavity, just caudally to the nasal vestibule and into theoral cavity on the incisive papillae, just caudally to thedental pad. The sensory epithelium, which lines oneside of the vomeronasal organ, possesses chemicalreceptors specific for pheromones. These specificreceptors are not found on the olfactory epithelium ofthe nasal cavity. The vomeronasal sensory epitheliumgives rise to nerves that pass to the accessory olfactorybulb. Secondary nerve fibers from the accessory olfac-tory bulb finally reach the medial preoptic area and themedial hypothalamus. Thus, the vomeronasal organhas connections to areas of the brain identified withsexual behaviour and production of gonadotrophins.

The well-known lip curl or “flehman” behaviourin male ruminants is considered an example of deliv-ery of pheromones from female urine into the malevomeronasal organ. In the procedure, a sample of urineis delivered via the tongue to the incisive papilla. Then,the fluid is sucked through the nasoincisive duct to thevomeronasal organ as the curled lips block the exter-nal nasal openings. Pronounced flehman behaviour hasnot been observed in most female animals. However,a so-called “maternal flehman” behaviour has beeno s. Ast zlingt henl sivep vioui thee thato

tert ass tionb ectc os-s thev hert g atb hata s is

supported by the observation that removal of the amni-otic fluid from lambs before ewes had the chance toclean their offspring disrupted the development of theinitial mother-offspring bond. Thus, an investigationwas initiated to determine whether the vomeronasalorgan is used as a determinant for offspring recogni-tion in sheep.

2. Materials and methods

Oestrus was synchronized in 30 Dorset-breed eweswith two intramuscular injections of lutalyse (10 mg)administered 10 days apart. Ewes were mated 1 dayafter the second injection and then randomly dividedinto three groups.

Ewes in treatment group 1 were rendered anos-mic by two irrigations of their olfactory mucosa witha solution of zinc sulfate (1.5%) and procaine (3%)under surgical anesthesia. The first irrigation occurredat 4 weeks and the second irrigation occurred at 3weeks before parturition. The vomeronasal organs ofthe ewes in treatment group 2 were rendered inacces-sible to stimuli by permanently occluding the entirenasoincisive duct via electro-cauterization under sur-gical anesthesia. Complete mucosal scaring over thenasal and oral openings of the nasoincisive duct wasobserved 1 month after surgery. The ewes in treatmentgroup 3 had their olfactory mucosa irrigated with a

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bserved in female sheep during suckling episodehe lamb engages the udder, the ewe is seen nuzhe lamb’s anal region with her muzzle. The ewe ticks her muzzle and runs her tongue over the inciapilla as she closes the nasal openings. This beha

s believed to deliver some neonatal pheromone towe’s vomeronasal organ in a similar manner toccurring during flehman in the male.

Non-volatile dyes have been shown to enhe vomeronasal organ during activities, suchelf-grooming, social grooming and consumpehaviour. Since grooming by licking is the first dirontact a dam has with her newborn, it is very pible that a neonatal pheromone is delivered toomeronasal organ via the incisive papilla from eithe skin or the amniotic fluid that covers the offsprinirth. It is possible that this neonatal pheromone is wewe would recognize at the time of suckling. Thi

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normal saline solution under surgical anesthesia;acted as controls.

Each treatment group was housed in separateities and all ewes were synchronized into parttion with an intramuscular injection of betamethaz(20 mg) on the evening of gestation day 144, followby a 10 mg betamethazone injection on the morningestation day 145, if necessary. Lambs remainedtheir dams at least until the end of the first suckepisode and then, they were removed from their dfor a minimum of four hours to stimulate hunger ateat-seeking activities.

Each ewe received a 1-day-old alien lamb or la(in the case of twins) of equal size as her own fdifferent housing facilities. The following behaviourecordings were collected for the 10-min trial:

1. Number of low-pitched, closed mouth bleats.2. Number of high-pitched, open-mouth bleats.

K.K. Booth / Small Ruminant Research 62 (2006) 39–41 41

3. Number of smelling episodes from ewe.4. Number of maternal flehmans.5. Number of udder acceptances.6. Number of suckling episodes of 5-s duration.7. Number of udder rejections.8. Number of aggressive behaviour.9. Number of changes of position of ewe.

The above-described behavioural trial was repeated24 h later using the same lamb or lambs as in the firsttrial. After each trial, each ewe was presented with herown lamb and the same behavioural data collected.

The data were analyzed using the GLM procedure ofthe SAS system (Version 6.11, 1989–1996) with treat-ment and trial as the independent variables. Probabil-ities less than 0.05 were considered significant. Meancomparisons were evaluated by the Bonferroni test.Within a treatment group, data for the two behaviourtrials did not differ. Thus, a single mean value for eachbehaviour frequency was calculated for each ewe.

3. Results and discussion

Ewes in the cauterized group (treatment group 2)emitted more low-pitched bleats than in the othertwo groups with functional vomeronasal organs. Therewere no significant differences between treatmentgroups with regards to high-pitched bleats. Theseobservations indicated that the cauterized group ofewes showed more interest in alien lambs and they weren henc ups.

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flehmans during both 10-min trials than the ewes withfunctional vomeronasal organs in the other two treat-ment groups. Each time a cauterized ewe would sniffa lamb and perform a maternal flehman, they appearedto be confused and would repeat the procedure morethan the ewes in the other two groups. This repeatedbehaviour indicated that they failed to detect a recog-nition signal and tried repeatedly to get one.

Total number of udder acceptances and total suck-ling time was greater for the cauterized group of ewesthan for the other two treatment groups. Rejection oflambs at the udder, display of aggression and changesof position of ewe away from the alien lamb was lowerfor the cauterized group of ewes when compared totreatment groups 1 and 3. These observations are insupport of the previous conclusions. As a result of theinability, within the cauterized group of ewes, to detecta recognition signal through their blocked vomeronasalorgans, these ewes could not discriminate alien lambsfrom their own and thus, allowed alien lambs to suckle.

This inability to discriminate alien lambs from ownlambs was reinforced when own lambs were returnedto the ewes. The ewes in each group accepted theirown lambs at the udder. This acceptance was imme-diate for the control group and the procaine treatedgroup. However, the initial behaviour of the cauterizedgroup of ewes towards their own lambs was identicalto that demonstrated towards the alien lambs. Repeatedsniffing of their own lamb’s anal region and repeatedmaternal flehmans further demonstrated their inabilityt

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ot distressed by the presence of the alien lambs wompared to the ewes in the other two treatment gro

The cauterized group of ewes also spent mime sniffing the lambs and performed more mate

o detect a recognition signal.Thus, it was concluded that the vomeronasal o

s used as a final determinant for offspring recogniuring nursing in sheep.