Urine marking in populations of wild house mice Mus domesticus Rutty. II. Communication between females

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1 Anim. Behav., 1990, 40, Urine marking in populations of wild house mice Mus domesticus Rutty. II. Communication between females JANE L. HURST Animal Behaviour Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD, U.K. Abstract. Several hypotheses were proposed for the function of urine mark communication between female house mice; predicted responses of females towards urine marks were then compared with those observed within eight captive territorial family groups. The responses of individual resident females in four classes (breeding and non-breeding adults, subadults and juveniles) were measured towards familiar resident, familiar neighbour and unfamiliar urine from breeding and subadult females, and towards a clean patch of substrate, introduced into their family-marked territory. Strong counter-marking of breeding female urine by resident breeding females especially on neighbour urine, prolonged investigation of familiar and unfamiliar urine by subadult females, and the specific attraction of resident females to neighbour female urine, support the proposal that urine marking plays an important role in communication between females. Responses were consistent with the hypothesis that females mark at high frequency to advertise their dominant breeding status to other females. The importance of such communication for the social modulation of individual breeding status within female social groups is discussed. The behavioural responses of captive house mice towards female urine marks encountered in their home area suggest that urine marking could be an important mode of communication between females (Hurst 1989). Breeding females living in isolated family groups counter-mark urine from unfamiliar breeding females and resident subadult females particularly strongly, while young females closely investigate urine from both familiar resident and unfamiliar females. In this paper I examine the potential functions of urine marking for communication between females within socially organized mouse populations. The social organization of female mice is more complex and variable than the simple territorial dominance found among males (see Hurst 1990a). Nonetheless, social interactions determine individual spatial range and reproductive success, and I have found highly significant differences in social behaviour between females classified according to their range and breeding status (Hurst 1987a). Several females usually share the same range and nest sites in established populations, ranging over one or several male territories (e.g. Reimer & Petras 1967; Lloyd 1975; Hurst 1987a). Females within a group may be closely related (Crowcroft & Rowe 1963; Lidicker 1976; Pennycuik et al. 1986) though previously unfamiliar females will also form social groups (Crowcroft & Rowe 1963; Baker 1981). Breeding females, distinguished from non-breeding females by their higher frequencies of social interaction and aggression (Hurst 1987a), often help to defend their shared range from intruding neighbours and unfamiliar mice of both sexes, though to a much lesser extent than aggressive territorial males (Crowcroft & Rowe 1963; Reimer & Petras 1967; Rowe & Redfern 1969; Hurst 1987a). Some non-breeding females are tolerated within the group without being attacked, and share the same range and nest sites as breeding females (Hurst 1987a). Other non-breeding females are attacked by both dominant breeding females and territorial males, and are restricted to less preferred areas along with the subordinate males (Lloyd 1975; Hurst 1987a). However, some subordinate females persist in breeding and using defended nest sites despite attacks from the dominant residents (Hurst 1987a). Female urine contains olfactory cues that influence the reproductive physiology of other females. Prolonged exposure to olfactory cues in the urine of familiar adult or grouped females inhibits maturation and oestrous cycling in young females (see review by Brown 1985). Older dominant females continue to breed even in crowded populations (e.g. Terman 1965; Lloyd & Christian /90/ $03.00/ The Association for the Study of Animal Behaviour 223

2 224 Animal Behaviour, 40, ; Hurst 1987a; see also Massey 1986) while removal of these breeding females results in earlier maturation and breeding of young females (Delong 1978). In contrast, puberty is accelerated by urine from a previously unfamiliar pregnant or lactating female when young females are not crowded in dense groups (Drickamer 1979, 1982; Drickamer & Hoover 1982). HYPOTHESES AND PREDICTIONS Communication between female house mice is essential both for territory defence against intruding females and for modulation of breeding status within social groups. Urine marking could play several roles in such communication, and each hypothesis proposed below predicts a different set of responses when females encounter particular urine marks. (1) Females may deposit marks to advertise territory defence to intruders. Female marking and behaviour towards marks should be similar to that predicted for male territory defence (Hurst 1990a). Aggressive breeding females should investigate and strongly counter-mark urine from nonresident females encountered within their territory, especially urine from other dominant females, while showing comparatively little interest in the urine of fellow group members. Non-aggressive females (breeding or non-breeding) should not urine mark and may avoid the marks of nonresident aggressively dominant females. Note that advertisement of dominance over all other mice in the territory, proposed for territorial males, is not appropriate for females: several dominant breeding females frequently share the same range and they are rarely agonistic towards their fellow group members (see above). (2) Females may mark to advertise their dominant breeding status, providing cues to influence the reproductive physiology of other resident females. Cooperative communal nursing by pairs of familiar breeding females can increase their individual reproductive success (Saylor & Salmon 1971; Konig 1989) but, in crowded nest sites, nestling mortality is a major hazard (e.g. Southwick 1955; Rowe et al. 1964; Delong 1978). It has been suggested that females that have a low probability of raising their offspring in crowded nest sites benefit by delaying reproduction, especially if their delay promotes the survival of offspring from closely related dominant breeding females which are better able to raise young (Brown 1985; Vandenbergh & Coppola 1986; Hurst 1989). Further, females whose puberty is delayed by urine cues from other females, or are older when they first conceive, produce more young per litter and have a longer reproductive lifespan under laboratory conditions than those with earlier puberty (Drickamer 1988). This hypothesis thus predicts that breeding females will deposit marks investigated by young non-breeding females to assess local conditions. Breeding females should ensure that their own marks predominate around their home area, counter-marking the urine of other breeding females regardless of their own aggressive status or social relationship with the urine donor. Puberty is delayed and oestrus suppressed by prolonged exposure to the familiar odours of specific individuals (see Brown 1985), so females should be more sensitive to urine from familiar neighbours than to unfamiliar odours, and young females should avoid prolonged exposure to urine marks of non-group members. (3) Females may mark to provide a pool of information concerning the individual identity and breeding status of all group members. Both breeding and non-breeding females should deposit marks, and counter-mark urine from non-resident females. Differential breeding status would then depend on differential sensitivity of individual members to the mixed cues of the entire group. In contrast to the previous hypothesis, non-breeding females will also deposit cues that might suppress the breeding status of their fellow residents. (4) Females may deposit marks for orientation and group cohesion. Females may not mark to communicate breeding status or aggressive dominance to other females, though cues deposited for orientation could have secondary reproductive primer effects and would be available to allow non-resident mice to orient away from a defended territory. However, if marks are not deposited to communicate with other females, female urine stimuli should not be counter-marked more strongly than any other novel stimulus. METHODS The methods were identical to those in the previous paper dealing with the responses of male mice to male urine stimuli encountered within their home

3 Hurst: Communication between female mice 225 territory (Hurst 1990a), except that the subjects were the female mice in each of the eight families, and urine test stimuli were collected from individual breeding adult and non-breeding subadult females. One of the eight founding females died prior to this experiment when she was accidentally trapped in a nestbox, but the other seven breeding adults were all pregnant and/or lactating during tests. The 13 female offspring born in the first litters within each family were adult ( days old) but showed few signs of sexual behaviour and were designated non-breeding adult females. None produced young during the test period, though three were seen mating with their father, one of them producing young 10 days after the end of the tests. There was no evidence of any sexual activity from the 13 subadult (49-75 days old) or 14 juvenile females (21-48 days old) born in the second and third litters until well after the end of this experiment. I thus measured the responses of 47 females in four classes (breeding adult, non-breeding adult, subadult and juveniles) towards breeding adult and subadult urine from females in the same family (resident urine), from females in the neighbouring family (neighbour urine) and from females in an unfamiliar family (unfamiliar urine). I again tested subjects individually by introducing floor tiles marked artificially with test urine into an isolated area of their family-marked home enclosure for 3 min. For the family without a breeding adult female, urine from a non-breeding adult was substituted (affecting six of 47 resident, and two of 47 neighbour breeding female urine trials). The responses of females to non-social novelty (a clean water-marked tile) and a control test, in which established marks on the tiled substrate were disrupted without introducing any odours, were also measured for each subject according to the same methods detailed previously for males. Behaviour towards each introduced test tile was compared both with behaviour towards surrounding home area tiles during the same trial, and with behaviour on an equivalent home area tile during the control trial, using Wilcoxon matched-pair tests. Counter-marking (the number of marks deposited on the test tile) was compared with counter-marking on control tiles only. Differences in behaviour between age classes were examined using analysis of variance and Duncan's multiple range tests on logarithmically transformed data. Spearman rank correlations tested for any relationship between counter-marking and investigation or time spent in contact with each test tile; this test also showed that there was no significant habituation in any response with successive trials. Social Organization RESULTS Females persistently invaded the neighbouring territory during periods of access, despite frequent attacks and chases by every resident dominant male (see Hurst 1990b). During invasion, intruders continuously investigated the substrate and frequently entered nestboxes, though rarely stopped to feed or drink. Non-breeding adult females invaded at almost every opportunity, rarely hesitated when entering the neighbouring territory, and frequently spent much time there, while subadult females were much less likely to invade and often failed to approach the doorway between territories (Table I). Dominant breeding adult females that fought with neighbouring females (see below) were often cautious when entering the neighbouring territory, while other breeding females entered without hesitation. The aggressive and investigatory interactions between different dyads of females when they had access to the neighbouring territory are shown in Tables II and III, respectively. Only one instance of aggression was recorded between females of the same family, while the social relationship between neighbouring females varied between pairs of families. Two pairs of breeding adult females were highly aggressive towards each other fighting for up to 30 s when they met, though no serious injuries were sustained. Aggressive interactions between neighbours were mostly initiated by the resident breeding female, though 24% of attacks were initiated by the invading neighbour. These aggressive breeding females investigated but rarely attacked non-breeding adult or subadult neighbours (or juveniles that invaded during later periods), and there were high frequencies of investigation but little aggression between the other two sets of neighbours. Thus if females deposit marks to advertise their defence of their territory, only the four aggressive breeding females should strongly counter-mark introduced female odours; non-aggressive females and tolerated intruders should not respond strongly to neighbour marks.

4 226 Animal Behaviour, 40, 2 Table I. Percentage (.~'+_ se) of females that invaded the neighbouring territory and their preferred location during eight periods when mice had access to the neighbouring territory before olfactory testing began Female class Breeding Non-breeding adults adults Subadults N Entry to neighbouring territory* No hesitation 65.7 _ Cautious 28.6 _ _+ 3.4 No entry 5.4_ Major percentage of time Resident territory 57.1 _ _ Neighbouring territory 10.7 _ _ _ 2.9 Both territories _+3-4 *Entries excluding those occurring during social interactions (border fights, chases or following). Table II. Aggression by females towards other females in the same or neighbouring family Female class Breeding adults Non-breeding adults Subadults Family Neighbour Family Neighbour Family Neighbour Breeding adult females (49) (12) Non-breeding adult females (1) Subadult females (2) (5) (4) Aggression from mice in each row towards mice in each column when mice had access to the neighbouring territory before olfactory testing began. Total frequencies (in parentheses) are divided by the number of mouse dyads that could interact in that category to give the aggression per dyad. For example, six breeding females were able to interact with a neighbour breeding female, thus 49 interactions between six dyads gives 8,17 aggressive interactions per dyad. Location of interaction is not taken into account. Female Responses to Female Urine Females investigated all introduced stimuli significantly more than surrounding or control tiles, and marked all introduced stimuli significantly more than control tiles (marking was not measured on surrounding tiles), as found during similar tests within isolated family groups (Hurst 1989). However, some female urine stimuli generated very strong responses from particular classes of mice, especially urine from neighbour females, indicating that female marking was not simply a response to novelty in their olfactory environment but might have a communicatory function. These responses are examined below. Marking All high frequency counter-marking responses were due to breeding adult females. Non-breeding adult, subadult and juvenile females deposited low frequencies of marks on all types of introduced

5 Hurst." Communication between female mice 227 Table IlL Investigation by females of other females in the same or neighbouring family Female class Breeding adults Non-breeding adults Subadults Family Neighbour Family Neighbour Family Neighbour Breeding adult '62 females (26) (9) (31) (2) (8) Non-breeding adult females (16) (29) (6) (30) (5) (6) Subadult females (1) (11) (4) (8) (2) (5) Investigation from mice in each row towards mice in each column, expressed as frequencies per dyad of each type, with total frequencies in parentheses (see Table II for full explanation). Location of interaction is not taken into account. (o) (b) E Q. IOC C ~ 4 O 5 50 r / C W BF SF 2 I C W BF SF Tesf odour Figure 2. Marking rates (~'_+ SE) of breeding adult females while in contact with test odours from resident (O), unfamiliar ([]) and neighbour (11) donors. C" control; W: water-marked clean substrate; BF: breeding female urine; SF: subadult female urine. Test odour Figure 1. Frequency of marks (~'_+ se) deposited by breeding and non-breeding (adult, subadult, and juvenile) females on test odours from resident ([]), unfamiliar ([]) and neighbour (9 donors. C: control; W: water-marked clean substrate; BF: breeding female urine; SF: subadult female urine. (a) Non-breeding females; (b) breeding females. stimuli, counter-marking urine from breeding adult females slightly more than subadult urine or clean water-marked tiles (Fig. 1). Females never marked control tiles, and rarely marked clean tiles either. In isolated groups the non-social novelty of a clean tile generated significant marking from both breeding and young female mice (Hurst 1989). Breeding females with social experience of neighbours now marked strongly in response to neighbour female urine, especially from breeding adult neighbours, as well as counter-marking urine from unfamiliar breeding females (Fig. 1); breeding females deposited significantly more marks than non-breeding classes on these three types of urine stimuli (Duncan's multiple range tests, P<0"05). Urine from resident subadult daughters, which stimulated comparatively high mark frequencies from breeding females before territory formation, was hardly marked at all. Taking into account differences in the amount of time spent on each test tile, some breeding females marked at much higher rates on neighbour breeding female urine than on any other stimulus (Fig. 2). This strong response

6 228 Animal Behaviour, 40, 2 Table IV. Initial attraction of females to neighbour female urine marks Adult neighbour urine Subadult neighbour urine % Attracted* Pt % Attracted* P'~ Breeding adults Non-breeding adults Subadults Juveniles ' 101 All females "017 *Percentage of females that first visited the test tile more quickly than their mean delay to the surrounding home area tiles during the same trial. twilcoxon test of delay to first visit versus the mean delay to first visit to the surrounding home area tiles. was not related to the agonistic social relationships between some females: both aggressive and nonaggressive females deposited high frequencies of marks. Breeding females visited the strongly countermarked subadult neighbour urine and unfamiliar breeding female urine stimuli significantly more frequently than surrounding or control tiles (Wilcoxon tests, P < 0'05). As one would expect, the number of marks deposited tended to increase with the amount of time they spent in contact with neighbour subadult female urine though this was not quite significant (rs=0.694, P=0-084); marking was not significantly related to time in contact with unfamiliar breeding female urine (rs=0.519, P= 0-232). In contrast, the amount of time breeding females spent on neighbour breeding female urine was correlated very significantly but negatively with their counter-marking response: females that counter-marked strongly spent very little time in contact with this test tile (rs= , P=0.004). This accounts for the very high mark rates of some breeding females shown in Fig. 2. Young females showed the opposite response to neighbour breeding female urine: more marks were deposited by juvenile (r,=0"732, P=0"004) and subadult females (r~ = 0.508, P= 0"076) the longer they were on the tile. Their low frequency marking was not correlated with time on any other test stimuli suggesting that only urine from breeding neighbours continued to stimulate a counter-marking response after their initial contact with the test tile. Attraction and Investigation When first released into the test area, females did not avoid female neighbour urine but many were initially attracted, both to breeding adult and subadult neighbour stimuli (Table IV). While subadult females were not attracted, breeding females showed a particularly strong attraction to neighbouring breeding female marks. However, the attraction was one of initial investigation only, as there were no significant differences in the amount of time any females then spent in contact with neighbour breeding female urine compared with surrounding tiles. This urine type stimulated the shortest investigatory responses of all introduced stimuli when female classes were combined (Table V; see also Fig. 3), though two breeding females did stop to investigate for more than 2 s. All resident breeding females thus responded strongly to urine from neighbour breeding females: attracted to the urine from a distance, they either counter-marked and spent little time in contact with the urine, or investigated but deposited very few marks. This difference in response did not correspond to the agonistic relationship between particular neighbours, or to their reproductive status when tested (three females were pregnant and four were feeding young nestlings). Urine from subadult neighbours generated more consistent investigation from all females. Breeding females showed no apparent interest in resident urine stimuli but young females tended to be attracted, especially subadult females which investigated familiar urine from their resident mother at length (Fig. 3; Table V). Subadult females also spent significantly longer on their mother's urine (Wilcoxon test, P=0.039) and on subadult resident urine (P = 0.039) than on control tiles due to increases in both investigatory and non-investigatory behaviour.

7 Hurst: Communication between female mice 229 Table V. The significance of Wilcoxon one-tailed tests for the data given in Fig. 3 on the investigation of test odours compared with that of surrounding tiles and control tiles (in parentheses) Female class Breeding Non-breeding All adult adult Subadult Juvenile females N Control * rqs * Ns ** Clean substrate * (rqs) **(**) ** (*) Ns (*) ***(***) Breeding female urine Resident Ns(r~s) rqs (*) **(**) Ns (*) ***(***) Unfamiliar NS(NS) * (*) **(**) * (*) ***(***) Neighbour r~s(ns) Ns (*) **(~qs) r~s(ns) ** (*) Subadult female urine Resident r,rs(ns) Ns (*) * (Ns) * (*) *** (*) Unfamiliar NS(rqS) NS (*) * (*) NS(NS) ** (*) Neighbour * (NS) * (*) * (NS) * (lqs) ***(***) *P <0.05; **P<0.01; ***P< Young females also showed much interest in urine from unfamiliar breeding females. Subadult females spent significantly longer in contact with this tile (P= compared to surrounding tiles) due to their extensive investigation of the urine (Fig. 3); their non-investigatory behaviour was correspondingly reduced (P=0.033 compared to surrounding tiles). Investigation of unfamiliar subadult urine by all but juvenile females (Fig. 3; Table V) similarly resulted in a significant reduction in non-investigatory behaviour by all females on these tiles (P = compared to surrounding tiles). DISCUSSION Strong counter-marking of breeding female urine by resident breeding females, prolonged investigation of particular urine stimuli by non-breeding females, and attraction specifically to urine marks from neighbour females, strongly support the proposal (Hurst 1989) that female urine marking plays an important role in communication between female mice. Comparison of these responses with those predicted by the likely functions of such communication further suggest that females mark at a high frequency to advertise their dominant breeding status to other females. Marking by non-breeding females was consistent with the low frequency mark response of all mice to any change in their familiar olfactory background, a response that allows them to detect novel changes in their social and physical environment (Hurst 1987b, 1989). Marking by breeding females in these territorially organized groups was stronger and more specific. The specific counter-marking of neighbour and unfamiliar urine (especially from other breeding females), together with the lack of marking by non-breeding females, were predicted by two different hypotheses: dominant breeding females mark to advertise either territory defence or their dominant breeding status. Not all breeding females defended their territory from invading neighbours, however, confirming the wide variation in agonistic behaviour previously found among breeding females (Hurst 1987a); female marking responses were not related to observed aggression. Non-aggressive breeding females thus were not marking to advertise defence of their territory to female neighbours, which they appeared to accept as members of the same social group (note that neighbours were not previously familiar though were caught from the same population and could have been related). By itself this does not rule out the possibility that resident breeding females marked to advertise defence to other potential intruders that they would not tolerate within their territory. However, this hypothesis still does not explain (1) the stronger response to urine of tolerated neighbours (group members) than to unfamiliar urine, (2) the extensive investigation of breeding female urine by young females that were in no immediate danger of attack from the urine

8 230 Animal Behaviour, 40, 2 v g_ (a) (b) (d) C W BF SF Test odour Figure 3. Female investigation (.~_+ se) of test odours from resident ([]), unfamiliar ([]) and neighbour (9 donors. C: control; W: water-marked clean substrate; BF: breeding female urine; SF: subadult female urine. The significance of each response is given in Table V. (a) Juveniles; (b) subadults; (c) non-breeding adults; (d) breeding adults. donors, or (3) the initial attraction of females to neighbour urine. Females appeared to mark to advertise their breeding rather than their agonistic status. The counter-marking behaviour of resident breeding females would ensure that their own urine marks also predominated in any area where there was a local concentration of breeding female marks. As only one female in each family was breeding, responses to urine from other resident breeding females could not be tested, buttheir responses to tolerated neighbours suggest that females would similarly counter-mark urine of fellow group members. Could females be advertising their breeding status to males rather than to other females, counter-marking urine from potential mate competitors? This hypothesis does not explain the subsequent avoidance of neighbour urine after heavy counter-marking, the counter-marking of urine from neighbour but not resident or unfamiliar subadult females, or the prolonged investigation of female urine by subadult females. Breeding females also failed to counter-mark strongly in response to their mate's urine marks, though this would be predicted if females marked only for intersexual communication (see Hurst 1989 and the third paper in this series). The modulation of female breeding status according to female density when food is not limited (e.g. Lloyd & Christian 1969; Ryan & Schwarze 1977; Pennycuik et al. 1986) requires communication between those females. Breeding status is not inhibited through aggression from other females or from males, as most non-breeding females are subjected to very infrequent attack (Hurst 1987a, present study). However, urine cues deposited by breeding females could provide an assessment of the density and individual identities of females breeding in the marked area. I predicted that young or subordinate females, which have the most to gain from a delay in reproduction (see Hypotheses and Predictions), would investigate such marks to assess local breeding conditions. Correspondingly, familiar resident and unfamiliar breeding female urine provoked prolonged investigation from subadult females. However, if females are to Use such cues to determine their own reproductive status, they must be able to distinguish between the cues of resident and non-resident females (otherwise invading females could cheat and deposit cues to inhibit resident females from breeding). Brown (1985) has reviewed the multiplicity of laboratory studies that show that primer cues in female urine can have strong inhibitory effects on the puberty of young females and on the oestrous cycling of adults, depending on the physiological status and social experience of both urine donor and recipient. Although little is yet known about the operation of such cues in socially organized mouse populations, Massey & Vandenbergh (1980) have demonstrated that puberty-inhibiting cues are produced by feral female mice when populations are dense. Established breeding females, however, are not generally inhibited from reproducing except

9 Hurst: Communication between female mice 231 when populations are severely overcrowded (e.g. Crowcroft & Rowe 1957; Lloyd & Christian 1969; Lidicker 1976). Counter-marking may help to protect breeding females from the inhibitory cues of other females by ensuring that their own marks always predominate in their environment. Adult or grouped female odours on cage bedding are effective cues for delaying puberty (Drickamer 1979, 1981) and, to a lesser extent, suppressing oestrus among adults (Champlin 1971), though all of these inhibitory effects require prolonged exposure to stimuli from the same individual female(s) over at least several days (Brown 1985). Thus primer cues in the urine marks of unfamiliar females could influence reproductive physiology only if encountered repeatedly over several days. The counter-marking responses of all resident mice will rapidly dilute the cues, while reinstatement of the familiar background marking should forestall further investigation (see Hurst 1989). Investigation of unfamiliar urine should not, therefore, expose females to inhibitory cues, while the prolonged investigation of unfamiliar female urine found among young but not among adult mice in this study may allow them to recognize odours from the same donor in future, should new females persistently mark the area. However, the odours of familiar non-resident neighbours would have the same inhibitory effects as familiar resident odours. This could then explain the strong counter-marking and avoidance response of resident breeding females towards neighbour urine marks, the relatively short investigation of neighbour urine by all residents after initial attraction (to counter-mark), and persistent counter-marking ofneighbour urine by nonbreeding females. Subadult females, in particular, discriminated in their investigation of urine from familiar resident or neighbour breeding females, and subadults did not even show an initial attraction to neighbour urine. It is not yet known whether such specific investigation, avoidance and countermarking of substrate urine marks are important components in the actions of reproductive primer cues in mouse populations; so far laboratory experiments have only involved either direct nasal application or close confinement of subjects with odour cues that are repeatedly replenished. Less counter-marking on subadult than breeding female urine marks suggests that non-breeding female marks are less important than marks from breeding females for inter-female communication; the low frequency mark responses of all non- breeding females were consistent with marking in response to any novel odours described previously (Hurst 1989). The artificial introduction of a local concentration of subadult marks in these tests may have induced a strong investigatory response partly because of the novelty of this stimulus. It must be noted, however, that breeding females in isolated family groups (Hurst 1989) counter-mark and avoid marks from familiar subadult residents while they counter-mark and investigate unfamiliar subadult marks. ACKNOWLEDGMENTS This work was supported by a Postdoctoral Research Fellowship and research grant from the Science and Engineering Research Council. REFERENCES Baker, A. E. M. 198 I. Gene flow in house mice: behaviour in a population cage. Behav. Ecol. Sociobiol., 8, Brown, R. E The rodents I: effects of odours on reproductive physiology (primer effects). In: Social Odours in Mammals. Vol. 1 (Ed. by R. E. Brown & D. W. Macdonald), pp Oxford: Clarendon Press. Champlin, A. K Suppression of oestrus in grouped mice: the effects of various densities and the possible nature of the stimulus. J. Reprod. Fert., 27, Crowcroft, P. & Rowe, F. P The growth of confined colonies of the wild house mouse (Mus musculus L.). Proc. zool. Soc. Lond., 129, Crowcroft, P. & Rowe, F. P Social organization and territorial behaviour in the wild house mouse (Mus museulus L.). Proc. zool. Soe. Lond., 140, Delong, K. T The effect of the manipulation of social structure on reproduction in house mice. Ecology, 59, Drickamer, L. C Acceleration and delay of first estrus in wild Mus musculus. J. Mammal., 60, Drickamer, L. C Acceleration and delay of sexual maturation in female house mice previously selected for early and late first vaginal oestrus. J. Reprod. Fert., 63, Drickamer, L. C Acceleration and delay of the first vaginal oestrus in female mice by urinary chemosignals: dose levels and mixing urine treatment sources. Anita. Behav., 30, Driekamer, L. C Long-term effects of accelerated or delayed sexual maturation on reproductive output in wild female mice (Mus musculus). J. Reprod. Fert., 83, Drickamer, L. C. & Hoover, J. E Effects of urine from pregnant and lactating female house mice on sexual maturation of juvenile females. Devl Psychobiol., 12,

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