Spontaneous and odour-induced chin marking in domestic female rabbits

Anim. Behav., 1992, 43, 329-336

Spontaneous and odour-induced chin marking in domestic female rabbits

R O B Y N H U D S O N & T H O M A S V O D E R M A Y E R Institut fiir Medizinische Psychologie, Universitgit Miinchen, Goethestrasse 31, D-8000 Miinchen 2,

Germany

(Received 19 November; initial acceptance 28 January 1991; final acceptance 11 July 1991; MS. number: 3679)

Abstract. In the European rabbit, Oryctolagus euniculus, chin marking is one of the most conspicuous forms of olfactory communication. In an investigation of factors influencing the expression of this behaviour in females, the marking frequency of seven intact and three ovariectomized does was tested over a 12- month period by placing them individually for 10 min each day in an arena containing three bricks. In the intact does but not in the ovariectomized ones, the frequency of chinning was increased by experimental long days and suppressed by experimental short days within 1-2 weeks of reversing the light regime. These changes were accompanied by clear alterations in the size and colour of the vulva, indicating that oestrus was also suppressed under the short-day conditions. However, presenting does with bricks marked by donor animals resulted in a significant increase in the frequency of chinning independent of photoperiod. Moreover, does appeared to distinguish between donors, directing marks preferentially to bricks marked by males rather than females, bricks marked by long-day rather than short-day donors, and those marked with chin gland secretion rather than with donors' urine or with carrot or lemon juice. Thus, while the finding that chinning activity was positively correlated with oestrus is consistent with the hypothesis that in females this behaviour is a form of sexual advertisement, the differential response shown to the chin marks of individual donors, even by non-oestrous does, suggests other, non-sexual functions for the chemosignals in chin gland secretion.

For the investigation of olfactory communication and the olfactory regulation of mammalian social behaviour there can be few animals more suitable for study than the European rabbit, Oryctolagus cuniculus. Being mainly nocturnal and spending

much time underground, this gregarious species relies heavily on odour signals produced by a variety of skin glands and contained in urine and faeces for the regulation of most aspects of its social life (Mykytowycz 1972; Bell 1980, 1985; Mykytowycz et al. 1984).

One of the most conspicuous features of this olfactory communication is chinning. Rabbits of both sexes possess a submandibutar gland, the secretion from which they use to mark objects in their environment by rubbing the chin over them (Mykytowycz 1962; Lyne et al. 1964; Black- Cleworth & Verberne 1975). This behaviour has been best studied in males: both the frequency of chinning and the secretory activity of the gland correlate positively with social rank, testosterone levels and reproductive activity (Mykytowycz 1962, 1965; Mykytowycz & Dudzinski 1966; Wales & Ebling 1971; Black-Cleworth & Verberne 1975;

Bell 1985). Thus it seems likely that in males chin marking is involved in the establishment and maintenance of social rank and in territorial defence.

Although chinning has been less well studied in females, evidence suggests it to be an important component of oestrous behaviour. Not only is the frequency of marking highest in oestrous does, declining within hours of mating (Soares & Dia- mond 1982; Gonz~dez-Mariscal et al. 1990), but it can also be readily manipulated by the adminis- tration of steroid hormones (Hudson et al. 1990). While the current functional interpretation of chin marking by does in terms of sexual advertisement is attractive, it is based almost entirely on the observation of spontaneous levels of marking activity (Soares & Diamond 1982; Gonz~lez- Mariscal et al. 1990; Hudson et al. 1990). How- ever, the report that females may also respond to odour stimuli from conspecifics with an increase in chinning (Black-Cleworth & Verberne 1975), even when not in oestrus (unpublished data), suggests that the regulation of this behaviour is more complex.

0003-3472/92/020329 + 08 $03.00/0 �9 1992 The Association for the Study of Animal Behaviour 329

330 Animal Behaviour, 43, 2

Our aim in this study is (1) to investigate the relationship between reproductive state and chinning by recording spontaneous levels of marking activity in intact and ovariectomized does kept under long and short photoperiods and (2) to test whether females respond to chin marks from donors with a change in chinning behaviour and whether they differentiate between such marks. We describe four factors influencing the expression of chin-marking behaviour: (1) individual differences; (2) change in daylength; (3) the presence of odours from unknown conspecifics; and (4) rapid habituation to these.

M E T H O D S

Animals

Eleven mature does, four mature bucks, three ovariectomized does and two castrated bucks of an established chinchilla strain (Chbb-Ch; Thomae, Biberach, Germany) were used. The animals were kept separately caged in stainless steel cages measuring 60 x 45 x 45 cm under experimentally controlled light conditions at 21+2~ and fed rabbit pellets (Altromin).

Experimental Procedures

Test females and experimental light conditions were the same as in a previous study on emission of nipple-search pheromone (Hudson & Distel 1990). To investigate the influence of daylength on chin- marking behaviour, four multiparous, three virgin and the three ovariectomized does were separated from the breeding colony in late December and brought into light conditions corresponding to the summer daylength maximum for Munich (16:8 h light:dark). Following a 2-month stabilization period, the light regime was reversed (8:16 h light: dark) for 7 months and then switched back again to 16:8 h light:dark for a further 2 months. As vulva colour has been reported to correlate with ovarian activity and hence with oestrus (Rottmann & Bieniek 1982), we used this to monitor the does' reproductive state. For each of the 10 test does, vulva cotour was rated dai ly according to a five- point scale which ranged from pale greyish beige (1) through light pink, dark pink and cherry red to deep purplish red (5). �9 Spontaneous levels of chin marking were

recorded for 100 days distributed as follows: 30 days in 16:8h light:dark; 30 days in 8:16h light:

dark; a break of several months followed by 10 days of testing before the return to 16:8 h light:dark; and a further 30 days testing (Fig. 1). Responsiveness to the chin marks of donor animals was recorded under 8:16 h light:dark during the break in regular testing, and again under 16:8 h light:dark at the end of the study.

Behavioural Testing

We assessed spontaneous levels of marking activity for 10 min each day by placing does individually in a wire-mesh arena 1 m in diameter and 43 cm high, containing three 15-cm-high terracotta bricks placed in a triangle approximately 0.5 m apart. The number of times each doe rubbed her chin on the bricks, whether separately or in a series, was recorded.

Responsiveness to chin marks from donor animals was assessed as follows. To control for the effect of presenting new bricks free of the test females' own marks, does were first tested for 3 days in the arena with two fresh, unmarked bricks and one old brick from the previous photoperiod series (see Fig. 3 for an example). On each of the following 5 days, two of the three bricks were treated with odour stimuli (see below) and the number of chin marks directed to each brick was recorded. To control for possible positional effects, the bricks were rotated during testing so that in any session each brick occupied each position for an equal amount of time. Stimulus bricks were pre- pared either by giving them to donor animals to mark in their home cage and, in the case of short- day or castrated donors showing low spontaneous marking activity, also by systematically rubbing the four corners along the donor's jaw and chin. Where urine was used as the stimulus, 10 drops, taken from a metal tray placed beneath the donor's cage overnight, were collected on a cotton swab and this was wiped across the corners of the brick. Each brick was used for testing one odour stimulus only and each animal was tested only once each day with a break of at least 1 day allowed between experiments.

We conducted 14 such experiments on each doe during both short-day and long-day conditions: two each using marks from (1) two males, (2) two females, (3) one male and one female, and (4) two castrated male donors kept in long-day conditions; (5) two each using one male and one female kept in short-day conditions for 1 month; and (6) two

Hudson & Vodermayer: Chin marking by doe rabbits

using urine from (a) male and female long-day and (b) male and female short-day donors to see whether the response was specific to odours from the chin gland. Finally, to test the specificity of the chin-marking response, the does were presented with bricks that had been rubbed with a freshly cut lemon or carrot. The order of the experiments was randomized, and testing was carried out between 1100 and 1400 hours at least 1 h after feeding.

Data Analysis

As the chinning activity of the ovariectomized does was very low (Figs 1 and 4), only data from the intact animals were used for statistical analysis. To examine the influence of daylength, mean individual scores for the week immediately before and the week immediately after the change from 16:8 h to 8: 16 h light:dark, and for the 10 days immediately before and immediately after the change from 8: 16 h to 16:8 h light:dark were compared using the non-parametric Wilcoxon signed-ranks test cor- rected for ties. Stability of individual differences in chinning activity across these four conditions was tested using the Kendall coefficient of concordance (Siegel 1969). The response to stimulus odours was analysed using the Wilcoxon test, first by comparing individual mean scores from the 3-day baseline condition with individual scores for each of the 5 experimental days, and second, by comparing the number of marks directed by individual does on any one day to each of the two stimulus bricks, and to each of these compared to the control brick. To test the stability of individual differences in chinning activity across conditions, individual values from day 4 for each of the experiments were compared using the Kendall coefficient of concordance. Except for the photoperiod experiments, all Wilcoxon tests were two-tailed.

R E S U L T S

Spontaneous Marking Behaviour

It took only about a week from the start of the study for does to become accustomed to the arena and to start marking as soon as they were placed in it. Although for a given photoperiod the level of chinning activity remained quite constant (Fig. 1), there were considerable differences between the scores of the individual intact animals. Whereas active does marked up to 80 times per 10 min, the

331

least active animals rarely marked more than 20 times. The three ovariectomized females showed little or no chinning, marking less than five times per session in 85% of trials regardless of photoperiod (Fig. 1).

Effect of photoperiod

Whereas chinning scores for the intact does remained constant at a mean+sE of 30.5___9'6 marks per session under long-day conditions, reversing the lighting schedule to 8:16 h light:dark resulted in a clear decline in the marking activity of these does within 2-3 days, and in a significant decrease (T=0, N = 7 , P<0.01) to less than 10 marks per session within a week (Fig. 1). Whereas marking activity remained low during the 7 months in 8:16 h light:dark, the previously high levels were restored within 10 days of the return to 16:8 h light: dark (T=0, N=7 , P<0.01). In fact, this sudden return to long days appeared to result in a temporary overshoot in chinning activity, with does marking on average (_SE) 53 '3_ 12-4 times per session during the second week (Fig. 1).

Despite such marked changes in chinning activity, the rank of high to tow marking animals was generally maintained across conditions (k=4, s=384, W= 0"86, N=7 , P < 0.01; Fig. 4).

The changes in marking behaviour were paral- leled by changes in the appearance of the vulva (Fig. 2). Despite individual differences, under 16: 8 h light:dark the labia of the intact animals were typically large, symmetrical and evenly coloured. In contrast, the labia of the ovariectomized does were small, pale and asymmetrical, and unevenly patterned with violet flecks. Within 2 weeks of the change to 8:16 h light:dark there was a clear reduction in the size and colour of the labia of all intact animals. However, with the return to long days the first clear signs of an increase in vulva size, a reduction in asymmetry and development of a more intense and even coloration were already evident between the first and second week (Fig. 2).

Odour-induced Marking

Response to foreign chin marks

The effect of presenting the test does with bricks marked by unknown individuals was essentially the same for all 12 (2 • 6) experiments in which mature


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Figure 1. The mean number of chin marks made per day per 10-min test session in relation to changes in daylength and sustained short-day conditions (N= 7 intact does and 1 ovariectomized doe). Experimental alterations in the light regime are indicated by the vertical broken lines, and shading represents the SE.

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Figure 2. Vulva colour of the seven intact test does in relation to changes in daylength. Each point corresponds to a daily estimate of colour intensity for each doe according to a 5-point scale, with the palest grade at 1. Otherwise as for Fig. 1.

donors kept under 16:8 h light:dark were used (see Fig. 3 for an example). Thus, irrespective of the donors' identity, the presence of the stimulus bricks resulted in a clear increase in marking by all individuals, with the rank order of high to low frequency chinners being generally maintained across stimulus conditions (k=12, s=3038, W=0.75, N=7, P < 0.01; Fig. 4). Even the ovariectomized females responded with a slight increase in marking (Fig. 4), although without showing the long, intensive movements characteristic of intact does.

For all experiments, the use of two fresh bricks and one old one during the 3-day baseline period failed to elicit any change in the previous pattern of chinning behaviour, with no significant difference recorded in the mean number of marks directed to

the old or to the fresh, unmarked bricks (all experiments: T = 5 - t l , N=7, P>0.05). Despite the influence of daylength on the expression of spontaneous chinning described above, the pattern of response elicited by the stimulus bricks appeared to be independent of the photoperiod of the test does and was seen during testing under both short-day and long-day conditions (Fig. 4).

In these experiments qualitative changes in chinning were as noticeable as the quantitative changes. In contrast to the brief, isolated rubbing movements characteristic of the baseline condition, does marked with long, strong strokes and usually after having sniffed and also sometimes licked the stimulus bricks first. These chinning movements were typically performed as part of a series in which two

Hudson & Vodermayer: Chin marking by doe rabbits 333

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Figure 3. An example of three experiments showing the mean number of chin marks made per day per 10-min test session by the intact test does when tested under short-day conditions, in response to chin marks from donor animals kept under long-day conditions. []: untreated control bricks; II, []: bricks with marks from donor animals; (a) two males, (b) two females and (c) one male and one female.

or three strong strokes were interrupted by sniffing, sometimes for several seconds, before chinning was resumed.

In addition to the overall increase in the frequency and intensity of marking, presenting does with stimulus bricks resulted in marks being preferentially directed to the bricks from particular donors. Thus, when presented with bricks marked by two stud males, all does marked the brick from one of the individuals more often than the other for the first 3 days (four experiments; T=0, N=7, P<0.02; Fig. 3). The pattern of behaviour was essentially the same when female donors were used except that preferences for the bricks of particular individuals were less marked (Fig. 3). In the experiments in which a buck and a doe were used as

donors, the buck's brick was always the most frequently marked.

However, although the bricks were freshly marked by the donors each day, in all experiments responsiveness of the does declined steadily from the first to the last test run. Only on the first two days were scores for all experiments using intact long-day donors significantly greater than baseline (12 experiments; T=0-2 , N=7 , P~<0.05), and by day 5 this was no longer the case for any of the conditions (Fig. 3).

Quality and specificity of the signal Females responded to the marks of donors in

short days with a small, and for the first 3 days significant increase in marking behaviour (four


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Figure 4. An example of two experiments showing the number of chin marks made per day per 10-min test session by individual does kept under short-day and long-day conditions, in response to chin marks of donor animals (males, kept in long-day conditions). []: number made during baseline testing on day 3 of the experiment. [] § I1: number made on day 4 when the marks of the donor animals were first presented. A G : intact test does; OX: an ovariectomized female.

experiments; T = l - 2 , N = 7 , P<0.05), although only on the first day with a significant preference for the buck's brick (four experiments, T = 0-1, N = 7, P~<0-05). When the response to chin marks from either of the two castrated males was tested, does failed to differentiate between stimulus and control bricks, showing no significant change in the frequency of marking over baseline (four experiments; T = 7-13, N = 7, P > 0"05). Responses to urine were typically much weaker than to chin marks from the same animals, and a significant increase in total marking activity, due almost exclusively to the reaction to urine from the buck, was recorded only for the first day (four experiments, T = 1-2, N = 7, P<0.05). However, does appeared to have little difficulty perceiving the stimuli as they often spent considerable amounts of time sniffing the urine- marked bricks. When urine from the same donors was tested after they had been kept for over a month in 8:16 h light:dark the response of the does was indistinguishable from baseline.

Carrot and lemon juice had no measurable effect on marking behaviour although does showed great interest in the carrot-scented brick, sniffing, licking, biting and scratching at it vigorously. The lemon-scented brick, however, was largely ignored.

D I S C U S S I O N

Chin marking is clearly a robust and readily quan- tifiable component of the female rabbit 's behavioural repertoire and one readily performed under

experimental conditions. However, the regulation of chinning also seems rather complex and even under the simple laboratory conditions of this study four distinct factors could be identified influencing its expression: individual differences; change in daylength; the presence of odours from unknown conspecifics; and habituadon to these.

Individual differences in the frequency of marking appeared most robust and were maintained across change in photoperiod and the presentation of foreign odour stimuli. This pattern is broadly consistent with the results of previous studies. Thus, despite different breeds and test conditions, reliable individual differences have been reported for intact does by Black-Cleworth & Verberne (1975) and Gonz~ilez-Mariscal et al. (1990).

Because all these studies used individually caged, domestic rabbits, the origin or possible functional significance of such differences is not yet clear. How- ever, given reports that high ranking, wild does have particularly large chin glands (Mykytowycz 1965; Mykytowycz & Dudzinski 1966), and that in bucks gland size and marking activity correlate with social rank (Mykytowycz 1965; Mykytowycz & Dudzinski 1966; Bell 1981), it would be interest- ing to investigate whether in does, too, marking activity is correlated with social status.

Whatever the significance of these findings for the regulation of rabbit social life, any differences between individuals in absolute chinning frequency were clearly overridden by the effect of daylength. Female rabbits are reportedly very sensitive to

Hudson & Vodermayer: Chin marking by doe rabbits 335

experimental changes in photoperiod, responding to a decrease in daylength of as little as 1 h with a decline in emission of nipple-search pheromone, fecundity and willingness to mate within 2 weeks (Hudson & Distel 1984, 1990). This corresponds well with the rapid changes seen in vulva colour in this study, and the fact that the vulva remained small and pale throughout the 7 months does were kept under 8:16 h light:dark suggests that oestrus was suppressed for this entire short-day period.

Despite strong evidence for the hormonal regulation of spontaneous chinning, presenting does with odour stimuli from reproductively active, unfamiliar conspecifics resulted in a clear increase in the frequency of marking independent of photoperiod and thus of the does' reproductive state. In fact, even the ovariectomized females responded with a small increase in marking activity to these odour stimuli. This response appeared specific to odours from conspecifics as presenting bricks treated with plant juice had little effect on marking even though the animals showed great interest.

As notable as the increase in marking activity was the speed and reliability with which does habituated to these stimuli. Thus, three or four 10- min testing sessions 24 h apart were sufficient for the frequency of marking to drop to baseline levels in all experiments. This was not simply because of a change in the quality of the marks as the same bricks reliably induced a temporary increase when presented a few days later. Habituation presumably also accounted for the failure of does during the baseline conditions to differentiate between old and fresh bricks, and may serve in the wild to reduce superfluous responding to known marks.

The single most important factor influencing preferential responsiveness to the odour stimuli from conspecifics appeared to be the donors' reproductive status. This is supported by three sets of observations: (1) by the failure of stimuli from donors kept in short-day conditions to elicit strong increases in marking; (2) by the lack of response to the marks of the castrated males; and (3) by the observation that bricks marked by males were preferred to bricks marked by females. Taken together, these observations suggest that female rabbits are able to discriminate between chin marks from different animals according to the donors' hormonal state.

It is also possible that rabbits are capable of finer discriminations given that the test does not only preferentially mark the brick of a particular indi-

vidual when presented with stimuli from two donors of the same sex, but also responded more strongly to bricks from unfamiliar donor females than to the bricks of the baseline condition marked by only the other, presumably familiar, members of the test group. The possibility of finer discriminations by rabbits is supported both by the complex morphology and chemical composition of the chin gland (Lyne et al. 1964; Goodrich & Mykytowycz 1972; Goodrich 1983), and by reports of individual recognition on the basis of scent marks in other mammalian species (Thiessen & Rice 1976; Halpin 1986). Whatever the case, chin-marking behaviour should provide a ready means of testing the rabbit 's capacity for individual recognition, and eventually of identifying the nature of the signals transmitted.

Finally, with regard to the possible functional significance of the behaviour shown by does in this study, the findings on spontaneous marking are consistent with the hypothesis that chinning by female rabbits is a form of sexual advertisement accompanying oestrus (Soares & Diamond 1982; Gonzfilez-Mariscal et al. 1990; Hudson et al. 1990). However, the odour-induced marking also suggests that oestrus may be only one of several contexts relevant for the performance of this behaviour. Given the strong response to the marks of unfamiliar animals, even by non-oestrous females, it is possible, for example, that chinning also plays a role in the establishment and maintenance of group identity (Rasa 1973; Halpin 1986).

A C K N O W L E D G M E N T S

We thank Hans Distel for critical discussion and help with presentation of the figures, Alfred Halser for care of the animals, Astrid M/iller for the graphics and the Deutsche Forschungsgemeins- chaft for supporting this work (Hu 426/1; Po 121/13).

R E F E R E N C E S

Bell, D. J. 1980. Social olfaction in lagomorphs. Symp. zool. Soc. Lond., 45, 141 164.

Bell, D. J. 1981. Chemical communication in the European rabbit: urine and social status. In: Proceed- ings of the Worm Lagomorph Conference (Ed. by K. Myers & C. D. Mclnnes), pp. 271-279. Guelph: University of Guelph, Ontario.

Bell, D. J. 1985. The rabbits and hares: order Lagomorpha. In: Social Odours in Mammals (Ed. by R. E. Brown &


D. W. MacDonald), pp. 507-530. Oxford: Clarendon Press.

Black-Cleworth, P. & Verberne, G. 1975. Scent-marking, dominance and fiehmen behavior in domestic rabbits in an artificial laboratory territory. Chem. Sens. Flay., 1, 465494.

Gonzfilez-Mariscal, G., Melo, A. I., Zavala, A. & Beyer, C. 1990. Variations in chin-marking behavior of New Zealand female rabbits throughout the whole reproductive cycle. Physiol. Behav., 48, 361-365.

Goodrich, B. S. 1983. Studies of the chemical composition of secretions from skin glands of the rabbit Oryctolagus cuniculus. In: Chemical Signals in Vertebrates 111 (Ed. by R. M. Silverstein & D. Mfiller-Schwarze), pp. 275-289. New York: Plenum Press.

Goodrich, B. S. & Mykytowycz, R. 1972. Individual and sex differences in the chemical composition of pheromone-like substances from the skin glands of the rabbit, Oryctolagus cuniculus. .L Mammal., 53, 540-548.

Halpin, Z. T. 1986. Individual odors among mammals: origins and functions. Adv. Study Behav., 16, 39-69.

Hudson, R. & Distel, H. 1984. Nipple-search pheromone in rabbits: dependence on season and reproductive state. J. comp. Physiol. A., 155~ 13-17.

Hudson, R. & Distel, H. 1990. Sensitivity of female rabbits to changes in photoperiod as measured by pheromone emission. J. comp. Physiol. A., 167, 225-230.

Hudson, R., Gonzfilez-Mariscal, G. & Beyer, C. 1990. Chin-marking behavior, sexual receptivity and pheromone emission in steroid-treated, ovariectomized rabbits. Horm. Behav., 24, 1-13.

Lyne, A. G., Molyneux, G. S., Mykytowycz, R. & Parakkal, P. F. 1964. The development, structure and function of the submandibular cutaneous (chin) glands in the rabbit. Austral. J. Zool., 12~ 340-348.

Mykytowycz, R. 1962. Territorial function of chin gland secretion in the rabbit, Oryctolagus cuniculus L. Nature, Lond., 193, 799.

Mykytowycz, R. 1965. Further observations on the territorial function and histology of the submandibular cutaneous (chin) glands in the rabbit, Oryctolagus cuniculus L. Anim. Behav., 13, 400-412.

Mykytowycz, R. 1972. The behavioural role of the mammalian skin glands. Naturwissenschaften, 4, 133 139.

Mykytowycz, R. & Dudzinski, M. L. 1966. A study of the weight of odoriferous and other glands in relation to social status and degree of sexual activity in the wild rabbit, Oryctolagus cuniculus (L.). CSIRO Wildl. Res., 11, 31~47.

Mykytowycz, R., Goodrich, B. S. & Hesterman, E. R. 1984. Methodology employed in the studies of odour signals in wild rabbits, Oryctolagus cuniculus. Acta zool. fenn., 171, 71-75.

Rasa, A. E. 1973. Marking behaviour and its social significance in the African dwarf mongoose, Helogale undulata rufula. Z. Tierpsychol., 32, 293-318.

Rottmann, O. & Bieniek, J. 1982. Beziehungen zwischen Umwelteinfliissen, Brunsterscheinungen und der Ovar- reaktion beim Kaninchen. Z. Versuchstierk., 24, 202-205.

Siegel, S. 1969. Nonparametric Statistics for the Behavioral Sciences. New York: McGraw Hill.

Soares, M. J. & Diamond, M. 1982. Pregnancy and chin marking in the rabbit, Oryctolagus cun&ulus. Anita. Behav., 30, 941-943.

Thiessen, D. & Rice, M. 1976. Mammalian scent gland marking and social behavior. Psychol. Bull., 83, 505-539.

Wales, N. A. M. & Ebling, F. J. 1971. The control of the apocrine glands of the rabbit by steroid hormones. J. Endocrinol., 51, 763-770.

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Spontaneous and odour-induced chin marking in domestic female rabbits