Anita. Behav.

, 1985, 33, 739-745

The ontogeny of flehmen in horses

S H A R O N C R O W E L L - D A V I S * & K A T H E R I N E A. H O U P T t

*College of Veterinary Medicine, University of Georgia, Athens, Georgia 30602, U.S.A. tNew York State College of Veterinary Medicine, Cornell University, Ithaca, New York 14853, U.S.A.

Abstract. Flehmen behaviour in Welsh pony (Equus caballus) mares and foals living on pasture was observed during 807 h of focal sampling. A series of flehmens performed at one site was defined as a flehmen incident. Colts exhibited flehmen incidents and performed flehmen more frequently during an incident than did fillies or mares. Fillies exhibited flehmen incidents more frequently than did mares, but did not flehmen more frequently during an incident. Colts exhibited a peak frequency of performing flehmen and of flehmen incidents during weeks 1-4 with a subsequent linear decrease in frequency up to weeks 17-20. Usually, flehmen occurred without the subject having had direct contact of the nostrils, lips, or tongue with a possible stimulant. Twenty-six per cent of the flehmen incidents occurred during or after urination by another pony. Seven per cent of the incidents occurred during or after urination by the pony showing flehmen.

Flehmen is a behaviour pattern which has been observed in many mammalian species, including most ungulates. Estes (1972) described the typical form of flehmen for ungulates as consisting of the animal standing open-mouthed, with head extended and elevated, while the upper lip is retracted, wrinkling the nose and baring the gum. Flehmen in the horse was first described by Schneider (1930), who reported repeated, vigorous inhalations and exhalations immediately prior to actual lip-curling. During the actual lip-curl no breathing was detected through a stethoscope. The primary function of flehmen is probably urinalysis, through stimulation of either the vomeronasal organ (Estes 1972) or the nasal olfactory epithelium (Dagg & Taub 1970). In goats, flehmen has been shown to carry dye from the mouth to the vomeronasal organ (Ladewig & Hart 1980). The relation of flehmen to the vomeronasal organ has not been demonstrated in the horse, a species in which the incisive duct does not open into the oral cavity, and substances must be taken in through the nostril to be aspirated into the vomeronasal organ via the opening of the incisive duct into the nasal cavity at the rostral end of the ventral nasal meatus (Schummer et al. 1979; Lindsay & Burton 1983). However, Wysocki et al. (1980) have demonstrated such a transfer of urinary non-volatiles in the guinea pig, a species which also lacks an opening of the incisive duct into the mouth. The purpose of this" paper is to describe the ontogeny of flehmen in the horse, to compare flehmen rates in juvenile males and females, and to

examine the stimuli eliciting the performance of flehmen in foals.

METHODS A study of the developmental behaviour of foals was carried out from 1979 to 1981 on a Welsh pony breeding farm in Ithaca, New York. Twelve adult pony females (mares) and 21 foals, 13 females (fillies) and 8 males (colts), were the focal subjects for the study. The foals were sired by four different stallions, three of which were present during the study. One stallion which was not the sire of any of the subject foals, two geldings and several mares without foals were also in the same pastures as the subject animals during parts of the study. A foal and its mother were observed simultaneously as a focal dyad for a series of focal samples of their concurrent behaviour (Altmann 1974). A total of 2 h of 20-min (1979) or 15-min (1980 198l) focal samples were taken on each dyad during each week of the foal's life from its birth until its weaning by the farm management at 4.5-5.5 months of age. When circumstances prevented collection of all scheduled focal samples, all available data were used. A total of 807 h of observations were collected on the 12 mares, 511 h on the 13 fillies and 296 h on the 8 colts. All incidents of flehmen by the subjects were recorded to quantify the rate of flehmen by each sex at various ages. Temporally related behaviours, especially urination, defaecation and sniffing, were

739

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Animal Behaviour, 33, 3

Analyses of variance for linear regression were calculated in which age was considered to be the independent variable (x) and rates of flehmen or flehmen incidents were considered to be the dependent variables.

RESULTS

Flehmen Incidents
A total of 179 flehmen incidents were recorded. O f these, 157 occurred during an animal's own focal sample sessions. Twenty-two were 'ad lib' records and were used only for descriptions of the context and number offlehmens per incident. O f all 179 incidents, 90 were exhibited by colts, 71 by fillies and 18 by mares. Flehmen incidents by colts occurred at the rate of 0-26 incidents per hour, or once every 3.8 h (range, 1/2.0 h-1/17.6 h). Flehmen incidents by fillies occurred at the rate of once every 0.11 + 0-03 per hour or once every 9.1 h (range 1/3.0 h-0/h). Two fillies never showed flehmen. Thus, colts engaged in flehmen incidents 2.4 times as often as fillies. Mares engaged in flehmen incidents far less often than did their offspring, male or female. Three mares never showed flehmen. The highest rate of flehmen incidents for any mare was once every 20.6 h. The mean was 0.02+0.01 incidents per h, or once every 50-0 h. Colts engaged in flehmen incidents significantly more often than did fillies or mares ( T = 2 1 , P < 0 . 0 2 5 ; T = 0 , P<0-001; respectively). Fillies engaged in flehmen incidents significantly more than did mares ( T = 3 3 , P < 0.025).

Figure 1. Performance offlehmen by a foal, redrawn from photographs.

recorded to quantify the circumstances under which flehmen occurred in foals. 'Nosing' was defined as moving the nostrils immediately next to something (e.g. a pool of urine), with or without touching it. Flehmen was observed to occur in both mares and foals. The form was as described by Estes (1972), except that the mouth was not open (Fig. 1). Sometimes, following an initial showing of flehmen, the pony would lower its lip and head, but would then initiate another flehmen over the same site following a brief interval of sniffing, urination, self-grooming or other activities. Thus, several flehmens might occur successively. In the following descriptions, the term 'flehmen' refers to one raising of the head and upper lip, while the term 'flehmen incident' or 'incidents' refers to one or more flehmens in close succession and in the same locale. In most cases the distinction between incidents was clear, there being a temporal separation of several minutes as well as spatial changes and orientation to different stimuli. A criterion of at least 1 rain between successive flehmens was set to separate incidents. Overall rates of flehmen and flehmen incidents were calculated by dividing the total number of flehmens or flehmen incidents for an individual, by the total number of hours of observation on that individual. Mann-Whitney tests (Daniel 1978) were used to determine the significance of differences between means. To evaluate changes with age, rates were determined for each foal over 4-week periods, i.e. birth to 4 weeks, 5-8 weeks, etc.

Rate of Flehmen During Flehmen Incidents

Flehmen was shown only once during 60% of the colt's flehmen incidents, 82% of the filly's flehmen incidents and 83% of the mare's flehmen incidents. For colts, the number of ftehmens shown per incident ranged up to seven (mean + SE= 1!9 + 0' 1), for fillies up to six ( m e a n 1-4 and for mares up to three ( m e a n + s E = 1.2-t-0.1). Colts showed flehmen during a flehmen incident significantly more frequently than did fillies ( T : 1 9 , P < 0 - 0 5 ) or mares (T=8.5, P<0.005). There was no significant difference between fillies and mares in the number o f flehmens shown per incident ( T = 50, P > 0.10).

Crowell-Dav& & Houpt: Ontogeny offlehmen

Rate of Flehmen Colts showed flehmen 0-49 0-11 times per hour, or once every 2.0 h (range, 1/1 h-1/8.8 h). Fillies showed flehmen 0-15 + 0.06 times per hour, or once every 6.3 h (range, 1/1.8 h-0/h). Mares showed flehmen 0-03!-0.0t times per hour, or once every 33-3 h. Colts showed flehmen significantly more than did fillies ( T = 9 , P=0-001) or mares ( T = 0 , P < 0-001). Fillies showed flehmen significantly more than did mares ( T = 31, P=0.025).

741

ftehmen was 1 day. The rate of flehmen and flehmen incidents by fillies did not regress linearly with age ( F = 0 . 5 , P > 0.05; F = 1.67, P > 0.05). The sex difference in rates of flehmen and flehmen incidents varied with age. Values for both variables for the two sexes were compared during each 4-week period. Colts showed fiehmen more often at all ages tested. The difference in flehmen rate between sexes was significant during weeks 1-12 (weeks 1-4, T = 27, P < 0.05; weeks 5-8, T = 5, P < 0 . 0 0 1 ; weeks 9-12, T = l l . 5 , P<0-005). The rate of flehmen incidents was greater in colts than in fillies during weeks 5-8 ( T = 24, P < 0'025).

Effect of Age The youngest age at which a colt was observed to perform flehmen was 2 days. For colts, the rates of flehmen incidents and showing flehmen were greatest during the first 4 weeks of life when flehmen occurred, on the average, once every 1-2 h and flehmen incidents once every 1-9 h (Fig. 2). The rate of both decreased linearly ( F = 120.05, P < 0.001; F=261.99, P<0.001). By weeks 17-20, flehmen occurred only once every 5.6 h and ftehmen incidents occurred once every 12.5 h. The youngest age at which a filly was observed to perform Contexts of Flehmen Evaluation of the records of events immediately prior to, during and following a flehmen incident revealed a variety of contexts (Table I). Flehmen during or shortly after urination by another pony was common, accounting for 26% of all incidents. The details of this reaction varied. The urinating pony was sometimes immediately next to the foal or mare and at other times was several metres away. The initial flehmen of the incident sometimes occurred after an initial nosing of the urine, and at other times occurred without the pony which showed flehmen having had any close contact with the urine, either as a spray or as a puddle. In nosing the urine, the pony would lower its head so that its nostrils were immediately above the wet grass or earth. Sniffing was sometimes made evident by a repeated flaring of the nostrils. Then it would raise its head and show flehmen. Ponies were never observed to lick the urine, although during one incident a colt lowered his nose into a fresh pool of urine. When he subsequently raised his head, urine could be seen dripping off his nose. Nosing of urine or of a site with an unknown stimulus (see below) was sometimes the behaviour which interrupted individual performances of flehmen during an incident. All four performances of flehmen by a mare in response to urine of another pony were in response to mare urine. Fillies performed flehmen 12 times in response to their mother's urine, three times in response to the urine of other mares and once over a site where a mare and colt had just urinated. Colts performed fiehmen 11 times in response to their mother's urine, eight times in response to the urine of other mares, five times in response to the urine of fillies and once over a site where a mare and her filly

8 8 8 8 8 Colts 13 i 13 , 12 ~ 12 i I I i FiIlies 1.20 1.101.00.90.80-I.0

~- 70g .60
E 5040.30

-2.0 Ig

20
.10. .

-5.0

- I0.0

o ;

;
Age

,~ ,'G 2'o
of Fool (Weeks)

Figure 2. The mean rate of flehmen by foals at various ages. The standard error of the mean is shown as a vertical bar. An asterisk indicates a significant difference (P < 0.05) between colts and fillies.

742

Animal Behaviour, 33, 3

Table I. Frequency of various flehmen contexts for all incidents exhibited* Colts (N=8) 26 (29~o) 11 (12~o) 15 (17~o) 6 (7~) 18 (20~) 20 (22~) 3 (3~) 7 (8~) 11 (12~) 0 (0~o) 3 (3~o) 90 Fillies (N= 13) 16 (23~o) 12 (17~o) 4 (6~) 6 (8~) 17 (24~o) 12 (17~) 3 (4~) 9 (13~o) 9 (13~o) 0 (0~o) 4 (6~) 71 Mares (N= 12) 4 (22~o) 0 (0~) 4 (22~) 1 (6~o) 4 (22~) 5 (28~) 0 (0~) 0 (0~o) 1 (6~o) 2 (11~o) 1 (6~o) 18

Context of flehmen During or after urination by another pony Own mother Other During or after own urination Spontaneous After nosing object or grass After nuzzling udder or nursing Head at mother's hindquarters# Over faeces Noses or licks foal's hindquarters Other and unknown Total number of incidents

* The number offlehmen incidents in a given context refers to the number of incidents in which the first flehmen of the incident occurred. The percentage of total flehmen incidents for the given age-sex class, in the described context, is given to the right of the absolute number. The list items are not mutually exclusive, e.g. flehmen over a pile of faeces that another pony had just urinated on is recorded twice: (1) after urination by another pony and (2) over faeces. t Mare not urinating.

had just urinated. Thus, performance of flehmen after exposure to urine was almost entirely in response to mare urine. In 13 of the incidents ( 7 ~ of total) colts, fillies or mares showed flehmen during or immediately after their own urination. Nine of these incidents occurred without any prior urination by other ponies or nosing of the ground or a pile of faeces. As with urination by other ponies, the initial performance of flehmen was sometimes followed by nosing of the pony's own urine and subsequent showing of additional flehmens. Twenty-one flehmen incidents occurred over faeces. Ten o f these (48~) occurred after nosing or eating the faeces. The faecal material varied from fresh to dry. Once a colt showed flehmen when he was lying on a faecal pile that was about 1 m wide and 3 m long. Although behaviour by the stallions was not recorded quantitatively, it is important to note that the stallions were frequently observed to urinate over the faecal piles of the mares, as has been previously described by Tyler (1972), Feist and McCullough (1976) and Turner et al. (1981). Foals and mares were also observed to urinate over faecal piles (see below). Therefore, the actual

stimulus for showing flehmen over the faecal pile could have been prior, unobserved urination by another pony. On six occasions, foals were observed to show flehmen immediately after ceasing to nurse, or after they had nuzzled their mother's udder (Table I). On 16 occasions, there was no definitive stimulus of urination or defaecation when a foal showed flehmen, but the foal was walking immediately behind its mother or was standing with its head close to her hindquarters. Once, the foal had licked its mother's hindquarters immediately before showing flehmen. Twice, mares showed flehmen after nosing their foal's hindquarters. On one of these occasions the mare had also licked the foal's hindquarters. Performance of flehmen frequently occurred with no stimulus more evident than that the pony had had its nose in the grass or had nosed the ground or an object (e.g. a fence, a flowering plant) immediately prior to the incident (Table I). This accounted for 21~o of all flehmen incidents. The sites may have been urinated on earlier, when the observer was not present or did not have the locale in view. However, it is also possible that the pony

Crowell-Davis & Houpt: Ontogeny of flehmen

Table IL Elimination by ponies performing flehmen Colts (N = 8) 33 (37~o) 39 (43~o) 1 (l~o) 90 Fillies (N= 13) 13 (18~) 19 (27~) 0 (0~) 71 Mares (N = 12) 2 (11~) 3 (17~) 1 (1~o) 18

743

Type of elimination Urinated after first flehmen Urination by subject before, during or after it shows fiehmen Defaecated over site Total number of incidents

was responding to volatile substances other than urine. Performance of flehmen was observed to occur spontaneously in 22~o of the incidents (Table I). In these cases, the pony was standing or walking with its head in the air. It had not been feeding, nor had it nosed any object or pony immediately prior to the incident. There were no recent or concurrent urinations or defaecations and the pony was not standing over a pile of faeces. The pony would stop moving, raise its head, and perform flehmen. In 29 (74~o) of these incidents there was no subsequent orientation to a possible physical source of an olfactory stimulus. In the other 26~o of these incidents the pony would, after the initial flehmen, lower its head, nose the ground, then perfor m flehmen again, this process being repeated one or more times. In one instance a mare showed spontaneous flehmen when she was downwind from two stallions and two mares that were probably in oestrus.

urine flow hitting the site almost directly. In females, however, the urine flow almost invariably missed the site. Only rarely did females step far enough across the site to urinate directly onto it. Defaecation at the site was observed twice, once by a mare and once by a colt.

DISCUSSION The most noteworthy findings of this study are that the flehmen rate decreased from birth to the twentieth week of age, that juvenile males performed flehmen more than females, and that foals of either sex performed flehmen more than their mothers did. Descriptions of the contexts in which flehmen was observed provide the basis for more precise future evaluations of the context of flehmen. The literature on flehmen in ungulates has emphasized its occurrence in adult males (e.g. Schneider 1930; Dagg & Taub 1970; Estes 1972; Feist & McCullough 1976; Altieri & Mfiller-Schwarze 1980; Henderson et al. 1980), as they sample the urinary pheromones of females, presumably with the vomeronasal organ (Estes 1972). Dagg & Taub (1970), in a study of giraffes (Giraffa camelopardalis), observed flehmen twice in adult females and once in a calf, and believed that it was an abnormal behaviour resulting from captivity. Flehmen by adult female black-tailed deer (Odocoileus hemionus columbianus) is rare and apparently does not occur at all in fawns (Henderson et al. 1980). In contrast, Tyler (1972) frequently observed flehmen in New Forest pony mares and foals after they had sniffed urine or placentas or upon seeing another pony exhibiting flehmen. Feist

Urination Following Flehmen

An initial flehmen was followed by urination by the pony that had performed flehmen in 37~o of the incidents by colts, 18~oof the incidents by fillies and 11~o of the incidents by mares. Incidents in which the initial flehmen occurred immediately after or during urination by the pony were not included in this tabulation. The urination occurred over faeces, the urine of other ponies, and at sites where there was no substance visible to the observer which might have triggered the incident (Table II). When urinating over a site of known stimulus, e.g. a faecal pile, both males and females usually stepped over the site with their forelimbs, but not with their hindlimbs. In males, this resulted in the

744

Animal Behaviour, 33, 3

therefore in actual performance of flehmen more often than mares, were otherwise similar to mares. There was no significant difference between fillies and mares in the number of flehmens performed per incident and they had about the same likelihood of urinating after the initiation of a flehmen incident. Thus, while young foals of both sexes exhibited an early juvenile period of frequent flehmen response, adult patterns of sexual differentiation were already evident. Colts engaged in flehmen incidents more often than fillies. Fillies behaved, within the context of a flehmen incident, like adult mares. Colts, as far as it was possible to determine from this study, behaved within the context of the incident more like stallions. Flehmen usually occurs after direct contact of the nose, lips and/or tongue with urine, in deer (Miiller-Schwarze 1979), goats (Ladewig & Hart 1980), American buffalo (McHugh 1958), cats (Felis catus) (Verberne 1976), Asian elephants (Elephas maximus) (Rasmussen et al. 1982), and guinea pigs (Caviaporcellus) (Wysocki et al. 1980). This was not the case with the juvenile and adult female equids observed in this study. Twenty-two per cent of the performances of flehmen were spontaneous, that is, occurring without apparent stimulus. Post-urination flehmen occurred in the absence of direct contact with the urine. Thus, in horses, direct contact with urine is not necessary to stimulate flehmen. The differences in behaviour between horses and other species investigated may be due to the anatomical structure of the vomeronasal organ of the horse. In most ungulates, the incisive duct opens into both the oral cavity and the nasal cavity, but in equids it does not (Estes 1972). Instead, the vomeronasal organ of equids opens, via the vomeronasal and incisive ducts, entirely into the ventral aspect of the ventral nasal meatus (Estes 1972; Lindsay & Burton 1983), so that tongue contact with a substance would not facilitate entrance of a substance into the vomeronasal organ. Horses may sense volatile material which they aspirate into the vomeronasal organ. In conclusion, it has been shown that foals exhibit significant rates of flehmen which suggest that they are sensitive to certain volatile substances, possibly pheromones, in their environment. Colts and fillies exhibit different rates offlehmen and may be responding differentially to different substances. While pheromones detected by performing flehmen may affect maturation, definitive evidence of such an effect is not yet available in this species.

(1971) did not observe flehmen by any females among the Pryor Mountain wild horses and only observed it twice by colts. The differences between the two reports may be methodological; Feist observed his herd from 46 or more metres whereas Tyler could approach her herds more closely and made her observations at 9-46 m. Reinhardt (1983) observed performance of flehmen in Bos indicus calves older than one week, with males exhibiting flehmen more often than females. O'Brien (1982) observed that female feral goats (Capra hircus) fi'equently showed flehmen after sniffing their own or an unrelated neonate. McHugh (1958) observed performance of flehmen by cows and male and female calves of the American buffalo (Bison bison bison). Performance of flehmen has also been observed in the Holstein cow (Bos taurus) (Hurnik et al. 1975) and the Mithan cow (Bibosfrontalis Lambert 1837) (Scheurman 1975). The high rate of flehmen during the first 4 weeks of life in foals may be a response to oestrous urine, because mares usually come into oestrous 4-14 days following parturition and every 19-23 days thereafter (Roberts 1971). Because an adult stallion was present, the mares were bred and would not have been in oestrous after the foal was a month or two old. In experiments involving the destruction of the vomeronasal organ or its nerve, and in other experiments involving varying forms of exposure to male mouse (Mus musculus) urine, it has been demonstrated that the vomeronasal organ of juvenile female mice is the receptor organ for male pheromones which accelerate puberty (e.g. Kaneko et al. 1980; Drickamer & Assmann 1981; Lomas & Keverne 1982). M/iller-Schwarze (1979) found that two male black-tailed deer that were deprived of female urine from birth had lower body weights and smaller antlers than three control males. It may be that, in equid foals, detection of pheromones via the vomeronasal organ is also important for sexual maturation and/or growth. The behavioural differences between colts and fillies are similar to those between adult stallions and mares (Feist 1971). Colts urinated after the initiation of a flehmen incident twice as often as did fillies or mares. They were also more likely than fillies or mares to perform fiehmen more than once during an incident, had a significantly higher mean rate of flehmen during an incident than fillies, and had three times as high a rate of flehmen as mares. Fillies, while they engaged in flehmen incidents and

Crowell-Davis & Houpt: Ontogeny of flehrnen ACKNOWLEDGMENTS

Field work was carried out while D r CrowellDavis' research was being supported by the D e p a r t m e n t o f A n a t o m y , Cornell University. D r G. Hausfater provided m u c h useful advice during the initiation o f this project. J. Burnham, J. Carnevaele, C. Carini and L. K a n e ably assisted with the field observations. We would like to t h a n k M r and Mrs K. Butler for allowing the use o f their farm as a field site and D r J. Brown for assistance with the statistical analyses. P r e p a r a t i o n o f this manuscript was supported by V M E S G r a n t 84-118.

745

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(Received 14 December 1983; revised 14 September 1984," MS. number." A4211)