Animal Learning & Behavior 1976. Vol. 4 (lA). 77-83 Male-female associations in the domestic

WILLIAM W. JACOBS University ofChicago, Chicago, Illinois 60637

Male courtship of nonreceptive females and male-male agonistic encounters were monitored daily for eight heterosexual groups of guinea pigs. Typically, one male (the associating male) accounted for much more courtship of a given female during her pregnancy than did any of the other males. Associating males were high ranking but were not always the group's normal alpha male. Nonalpha associating males invariably ranked higher on the day of the female's litter and postpartum estrus than their modal daily rank during her pregnancy. In 10 of the 18 cases, a nonalpha associating male took over the alpha position on the day of the litter. The courtship of females by associating males was found to differ from that by nonassociating males in that associating males displayed circling, rumping, swaying, and pursuit in a significantly higher percentage of the total number of courtship bouts.

The long history and importance of the domestic tion situation - when the receptive female is placed cavy ( porcellus) as a laboratory has led to with the male. The occurrence of these behaviors when the use of the term "guinea pig" in reference to experi­ no receptive females are present has received two explan­ mental subjects in general. Despite the animal's familiar­ ations. Males who court nonreceptive females have been ity, its behavior in social groups and the structure of thought to be either (1) searching for receptive females these groups are poorly known. This lack of knowledge by trial and error (Avery, 1925; Loeb & Lathrop, 1914; is due in large part to the absence of quantitative data Louttit, 1927), or (2) inexperienced and low-ranked from long-term observational studies in the literature. animals, that in time or with a better social situation Previous observational studies concur in the observa­ would restrict their attentions to receptive females tion that a dominance order is formed among adult (King, 1956; Kunkel & Kunkel, 1964). Recent reports males when two or more are housed together (Jacobs, have suggested that the number of courtship bouts Beauchamp, & Hess, 1971; King, 1956; Kunkel & performed by males in a group is positively correlated Kunkel, 1964; Rood, 1969, 1972). The absence of clear­ with the position in the dominance order (Beauchamp, clear-cut rank-order relationships among domestic guinea Jacobs, & Hess, 1971; Rood, 1972). pig females has been noted in these papers, but Rood This paper presents a detailed report of long-term, (1969, 1972) indicates that female rank orders are daily quantitative observations of the social behavior of formed by the wild Cavia aperea. Guarding of receptive domestic guinea pigs in heterosexual groups. The results females by alpha males and instances of the alpha male's show that the courtship of nonreceptive females is a inability to completely eliminate copulating by other normal aspect of guinea pig social behavior. In addition, males have been noted (Kunkel & Kunkel, 1964; Rood, the formation fo male-female associations and the 1972). Rood shows, however, that the alpha male is effects of these associations upon the male dominance usually the first to copulate with the female he has order are described. Finally, the possible functional guarded, and is sometimes the only male to do so. significance of the male-female association is discussed. Gilmore, (1952) suggested that wild cavy males-might collect females in harems, but Rood (1972) concluded METHOD that matings are promiscuous and that permanent social bonds are not formed. Animals The topographies of the male guinea pig's courtship Guinea pigs observed in the social groups reported here were and/or sexual behaviors have been described many times descendants of heterogeneous stock obtained from an animal breeder in 1967, plus additional heterogeneous stock added from (e.g., Avery, 1925; Louttit, 1927; Young & Grunt, time to time. Within the breeding colony, males were moved 1951). The inheritance of these behaviors has been from cage to cage to reduce inbreeding. Animals selected for studied (Jakway, 1959) and the effects ofearly isolation membership in the social groups spent at least their first month on male sexual behavior have been reported (e.g., Gerall, of life with other animals of both sexes. Fully grown adult males 1963; Harper, 1968; Valenstein, Riss, & Young, 1955). were about 1100 g, nonpregnant females about 900 g. Animals under 25 days of age are considered to be "young." Generally the behaviors were recorded only in a copula- Females are called "adults" at 25 days of age. Males are called This work was supported in part by the U. S. Public Health "subadults" at 25 days and adults at about 80 days. The defini­ Services Grant 5 ROI MH 00076 to Dr. E.H. Hess, Department tion of adulthood is a functional one, based on the attainment of of Psychology, University of Chicago. The author was supported fertility, which in the female (Kunkel & Kunkel, 1964) is at a by University Unendowed and USPHS fellowships. The author wishes to thank Dr. Hess for support and instruction and Dr. considerably younger age than in the male (Freund, 1960; G. K. Beauchamp, Dr. John Rogers and Dr. R. L. Doty for Webster & Young, 1951). constructive comments on earlier drafts of this paper. Requests for reprints should be sent to Dr. William W. Jacobs, Monell Groups Chemical Senses Center, University of Pennsylvania, 3500 Eight heterosexual groups were studied. Group compositions Market St., Philadelphia, Pennsylvania 19104. and observation times are summarized in Table 1. Most groups

77 78 JACOBS

Table I Compositions of and Observation Programs for Groups Studied Group IA II III IlIA IV V VA Composition Adult and juvenile males 10-15 5-7 1 1-2 3-4 4-5 2 10 Adult females 6-11 2-8 2-3 3 2-3 2-13 4-{j 9-12 Observation program Months studied 6.5 4 3 1.5 1.5 11.5 3.5 3 Hours observed 264 132 119 13 25 189 101 66 Observation Daily Daily Daily Irreg. Daily Daily Daily Daily Length of observation period (h) Mean (variable period) 1.34 1.16 .33 Duration (fixed period) 1.5 .5 .5 1.0 .75

were observed daily over periods of several months. Changes in which would have brought the animal into contact with a second group composition occurred over time as young animals matured animal and moved quickly off in a new direction, the encounter and as animals died. Groups including the letter "A" in their was termed an "avoid." Such encounters were very rare. Decided identification were formed entirely from animals of the group of encounters were classed as threats, chases (including chase-bites), the same Romal numeral and their offspring. Ten adult and bites (without chase), or avoids according to the behavior juvenile males were removed from Group I before the Group IA displayed by the winning animal. Standoffs were stand-threat study was begun. Group IV was formed by combining the three (Rood, 1972) bouts which were not followed by a threat, chase, adult males and two females of Group IlIA with an adult male or bite delivered by one of the principals. The classes and beha­ and two females. In Group IV, the number of adult and juvenile viors are described in detail by Jacobs (1973). Encounters were males was limited to 5 by culling young males at 25 days of age. determined as beginning with the onset of the first agonistic In Group VA, the number of adult and juvenile males was behavior between the two participants and as ending when similarly limited to 10 and the number of adult females was not agonistic behavior ceased for several seconds or when an encoun­ permitted to expand beyond 12. ter between one of the participants and another animal Groups I, lA, II, V, and VA were housed indoors in tile commenced. floored enclosures. The enclosure used for Groups I and IA was Animals were ranked according to the identities of the trapezoidally shaped with a floor area of 14.2 rn". Groups II, V, animals from whom they won encounters and to whom they and VA were kept in an enclosure which could be divided into lost. A linear hierarchy was usually formed, although dominance two pens by placing a board over a small doorway in the central triangles were occasionally seen. Following each day's observa­ partition. Group V originated as two one-male, three-female tions, a ranking of males was made from the results of the groups; the board was removed from the doorway after 1% encounters recorded. Daily ranking was necessary because of months of study. Group VA occupied the entire enclosure day-to-day shifts in rank position (see below). Pairs of males not throughout the study. This enclosure was 12.7 m2 in floor area. involved in a decided encounter on a given day were ranked Groups III, IlIA, and IV were housed outdoors. Groups III according to the outcome of their last observed decided encoun­ and IlIA were kept in a 53.0 m 2 open pen. The animals fed on ter and the results of their encounters with other males. plants growing in the enclosure in addition to the commercial Courtship Encounters. Bouts of courtship by males were guinea pig diet provided all groups. Group IV was housed in a recorded for all groups. A courtship encounter was considered to cement-floored enclosure (11.7 m2 in area) constructed within a begin with the male's first showing of a courtship behavior to­ large outdoor cage (30.2 m2 in area). Heat was provided in ward the female and to end with cessation of courtship activity winter for this group by two lamps placed inside a 1.2 m 2 for several seconds. For Groups lA, II, III, IlIA, IV, V, and VA, rectangular shelter. individual behaviors included in the sequence were recorded each Daily observation periods were of variable durations for time they appeared. Unless otherwise noted the behaviors scored Groups I, lA, and III, and of fixed durations for Groups II here follow Louttit (1927). They include: Licking (and sniffing (90 min), IlIA (30 min), IV (30 min), V (60 min), and VA or nibbling target animal's anogenital region), pursuit, nosing (or (45 min). nibbling fur), rumbling (or purring), swaying, circling, jumping Procedures over female, rumping, rump attempt (Jacobs, 1973), kissing, Location of Animals. For indoor groups (I, lA, II, V, and nibbling (or biting) ear, chin-rump-follow (Rood, 1972), perineal VA), the location ofeach animal was noted at regular time inter­ drag (Kunkel & Kunkel, 1964) during courtship (mark), supra­ vals during the observation periods. The interval between records caudal rub (Jacobs, 1973), mounting, disoriented (atypical, head was 30 min for Groups I and lA, 10 min for Group II, and or side orientation) mounts, pelvic thrusts (pelvic movements), 15 min for Groups V and VA. intromission (copulatory strokes) and ejaculation. Agonistic Encounters. Results of decided agonistic encount­ Recording procedures. Behaviors were scored by hand using ers - those in which winner or loser could be identified - among an abbreviation method. The first letters of the names or the adult and subadult males were scored for all groups containing identifying numbers of the participating animals were noted more than one male. Standoffs (see below) between males were followed by the intensity score of the encounter and a coded recorded for all multi-male groups except Group I. The partici­ description of the behaviors occurring during the encounter. The pating animals were noted for all encounters and the winner and abbreviation method enables the observer to record the behavior­ loser were recorded for decided encounters. A loser was deter­ al sequence quickly without removing his gaze from the animals. mined when an animal moved on all four feet away from a By restricting attention to agonistic and courtship encount­ second animal (the winner) which quickly turned its head or ers, it was possible to obtain an estimate of the performances extended its snout toward the first animal without moving on all of all males in the group a! the same time. Comparisons of four feet (threat), moved on all four feet toward the first animal this sampling procedure with results obtained for Groups IV and (chase), and/or abruptly contacted the first animal with the V using focal animal sampling of one adult male at a time snout (bite). If a male abruptly altered a course of progression revealed no difference in the male hierarchy or in rank in overall MALE-FEMALE ASSOCIATIONS IN THE DOMESTIC GUINEA PIG 79 courtship output among adult males (Jacobs, in prep.) When time permitted for Groups II, III, IlIA, and IV, female-female and male-female interactions were also scored. 2 RESULTS

!: Male-Female Association ~ All males in all groups observed courted nonreceptive 5::I females. However, the courtship ofnonreceptive females 0 U was not evenly distributed among the adult males in any ... multimale (3+) group. 0 III In Group I, a significant positive rank order correla­ tion (rho = 0.94, N = 10, P < ,01) was found between § rank position and total number of courtship bouts. Significance in this measure was also found for the five-male portion of Group IV (rho = +1.00, N = 5, 60 P < .02) and for Group VA (rho = +.90, N = 10, p < .02), but not for Group IA (rho =+.10, N =5, N.S.) or for the four-male portion of Group IV (rho =+.80, N = 4, N. S.). Although significance was reached for Group VA, 24% more bouts of courtship were perform­ 30 60 ed by males occupying the 3rd rank position than by DAYS OF GESTATION alpha-ranked males. Consideration of the courting directed to individual Figure 2. Cumulative courtship of female B during her fourth pregnancy by the five males of Group IV. The associating male females revealed a strong tendency for one male to was S. The litter was born 10/S/72. direct many more bouts of courtship toward a given female than did any other male. The greater frequency twice as often during her gestation as any of the other of courtship of the female by this male was generally males, that male was called "the associating male." apparent throughout her gestation periods. Less For the 41 litters (involving 26 different females) in frequently, two or three males directed nearly equal and Groups I, lA, IV, and VA for which data were collected high numbers of courtship bouts toward a female during for at least the last 26 days prepartum, the ratio of her pregnancy while the remaining males seldom courted courtship by the most frequent courter to the next most the female. If one male courted the female more than frequent courter ranged from 1.04 to 16.90. For 31 gestations, the ratio was better than 2: 1 and for 22 it was above 3: 1. In four cases in which the ratio of highest courter to second-highest was less that 2.0: 1, 240 the relationship was termed an association because only one male was frequently courting the target female during the last 12 days of gestation. Therefore, an associating male was determined for 35 of the 41 gesta­ .. UTn• tions discussed here. For 27 of the 41 litters, animals i DAY III ..• were observed throughout gestation . s c Steady domination by one male of the courtship of ...U females was seen throughout the gestation periods of 0 females in 27 of the 41 cases. Two such cases are ..III depicted in Figures 1 and 2. These two Group IV ::I i females littered 11 days apart, but each was in associa­ tion with a different male. An increase in the total rate of courtship of females toward the end of gestation is usually seen (Beauchamp, Jacobs, & Hess, 1971). In Group IV, more full length (65-69 days) gestations (11) were observed in their entirety than in any of the other groups. For the purposes of analysis, these periods were 30 60 divided into 17 four-day intervals counting backward DAYS OF GESTATION from the last observation before parturition. In 9 cases, the rate of courtship of the pregnant female was higher Figure I. Cumulative courtship of female E during her first pregnancy by the five males of Group IV. The associating male during the period immediately preceding parturition was C. The litter was born 9/24/72. than during any other interval. A significant association 80 JACOBS

Table 2 the study of Group I (Table 2). The tendency for Social Affinity Scores (3!23/7o-5!25!70) and Times frequent spatial proximity between associating male and Courting Females During Pregnancy by First female was most pronounced during the last 7-14 days Eight Males in Group I Hierarchy preceding the birth of the litter. This tendency was fre­ Social Affinity (Courtship) quently absent during the first eight weeks of gestation. Male Females 16 95 69 59 Ranking of Malesand Changes in Rank As the ranks ofmales fluctuated somewhat, it became 68 .221 (10) .215 (7) .372 (101)* .372 (5) 2 .464 (169) .127 (4) .112 (5) .266 (28) necessary to apply the term "normal alpha male" to the 31 .135 (9) .291 (48) .138 (10) .181 (3) animal that dominated the male hierarchy on most days 22 .063 (4) .089 (12) .074 (6) .128 (3) for an extended period oftime. An associating male was 19 .045 (I) .063 (3) .064 (12) .089 (4) considered to have been the normal alpha male if he 93 .050 (10) .044 (13) .058 (29) .080 (I) 89 .081 (I) .089 (I) .064 (9) .089 (4) occupied the alpha position for at least 60% of the 44 .063 (6) .101 (18) .048 (14) .097 (3) female's gestation days, including at least 7 ofher last 14 days of pregnancy. The modal daily rank during the "Italics indicate associated pairs. female's pregnancy was determined for the leading courter during the gestation. A litter day rank was between periods and courtship rates was demonstrated determined for these males from the results of male-male with the Friedman test (xf = 42.30; 16 df, p < .001). agonistic encounters on the last observation prior to the Comparisons among rank sums for different periods, female's receptivity. The post litter day rank for these using the methods described by Hollander and Wolfe animals was determined to be their modal rank for the (1973) revealed that the period immediately preceding first 12 days postpartum. parturition was significantly different from 10 of the Males that formed associations with females were remaining 16 periods (p values ranging from .05 to usually among the higher-ranked males in their colonies. .001). There were no significant differences among the For groups with 10 or more adult males (I and VA), 16 other periods. Some of this late gestation courtship during the gestation period, the modal daily ranks of increase arose as some of the nonassociating males associating males and males involved in two- or three­ abruptly began courting pregannt females just before male suitorships ranged from alpha to eighth, but in all term. but two cases the leading courter at the time of the litter Members of a male-female association are frequently came from among the top four males. For five-male found together at resting places and feeding areas and groups, all associating males came from the top two are often seen moving around together, usually with males in the hierarchy. male following female. This tendency becomes most In groups with 10 or more adult and subadult males, pronounced as parturition approaches. For example, the associating male was more likely to have been a social affmity scores, which represent the percentage of nonalpha male during the period of the female's gesta­ total location observations that two animals were found tion than in 4-5 male groups. In 14 of 21 litters in together (in the same place at the same time), were groups with 10 (+) males (Groups I and VA), the associa­ highest between the associating male and the female in ting male was not the normal alpha male. However, the three of four litters dropped during the first third of associating male was not the normal alpha in only 5 of Table 3 Associating Males and Their Ranks in Four Multirnale Groups Group I Group IA Group IV Group VA Total Number of litters 13 4 15* 8 40 Associating male alpha on litter day 11 3 15 3 32 Associating male not alpha on litter day 2 1 0 5 8 Associating Male is Normal Alpha Male Instances 4 3 12 3 22 Remains alpha on litter day 4 3 12 3 22 Not alpha on litter day 0 0 0 0 0 Falls in rank after litter day 1 0 2 I 4 Associating Male is Not the Normal Alpha Male Instances 9 I 3* 5 18 Alpha on litter day 7 0 3 0** 10 Not alpha on litter day 2 I 0 5 8 Litter day rank higher than gestation rank 9 1 3 5 18 Litter day rank lower than gestation rank 0 0 0 0 0 Associating male falls in rank after litter day 5 1 2 3 11 Associating male goes up in rank after litter day 1 0 0 0 1 "One Group IV litter not included due to the mISSIng of the observation period on the day of the litter. **One nonalpha associating male was part of a dominance triangle at the top of the hierarchy on the litter day. MALE-FEMALE ASSOCIATIONS IN THE DOMESTIC GUINEA PIG 81

20 instances in 4-5 male groups (lA, IV). Thus, there is a Table 4 significant association between the size of the male pop­ Endurance of Associations Over Successive Pregnancies ulation and the likelihood that the associating male is Litter Associating the normal alpha male (X2 = 6.43, df= I, P < .01). Female Number Male Associating males became more aggressive as parturi­ Group I tion and the post-partum estrus approached. The associ­ 39 1 68 ating males' (and leading courters') ranks on litter day 39 2 68 were compared to these males' modal daily ranks during 20 1* 19 the gestation period. If the associating male was not the 20 2 44,22** 20 3 44 group's normal alpha male, he often took over the alpha 57 1 31 position on the litter day (Table 3). In the four two- or 57 2 31 three-male suitorships in which none of the males 50 1 68 involved was the normal alpha male, none achieved alpha 50 2 68 status on litter day. Even when no takeover occurred, Group IA the associating male (or leading courter) moved up in the 43 1* 77,15** hierarchy. At parturition, none of these males was 4~ 2 15,77** ranked lower than or even equal to his modal rank Group IV during the gestation period. However, normally subalpha D 4* S D 5 S associating males and leading courters often fell in rank D 6 S soon after the litter day. In four instances, a normal D 7 S alpha associating male fell in rank after the litter. In D 8 S three of these cases, the male failed to regain the normal D 9 S position for the remainder of the study. B 1 S,V** B 2 S B 3 S Duration of Associations B 4 S Male-female associations tend to endure through E 1 C successive pregnancies (Table 4). In 14 of the 16 cases of E 2 C observation of successive litters by a female within the Group VA same social group, the associating male or leading 129 3* 211 courter (if a single associating male was not identifiable) 129 4 211 during the succeeding gestation had been the associating "These females were not observed for the requisite 26 days male or leading courter during the previous pregnancy pre-partum for these litters. Identity of associating male was (p < .012, two-tailed binomial test). An association . obvious for all cases except Female 43. between two animals which was first detected in **Two-male suitorships. First male listed is leading courter. Group IlIA endured for more than 13 months and definition he directs more bouts of courtship to his survived the transfer of the animals to Group IV. Other female during her gestation. It is possible, however, that associations survived successive pregnancies. Occasion­ the relative amount of courtship directed to the female ally, however, the male of an apparent associating pair by the various males of a group is involved in the esta­ was replaced by another male. These replacements were blishment and maintenance of an association with that marked either by intense fighting between the two males female. It may also be that only some ofthe courtship or by a cessation of interest in the female by one of the behavior patterns are important in this respect. males, followed somewhat later by increased interest by When compared with the courtship of his female by the second male. Of 8 such apparent replacements, two the other males in the group, the associating male's occurred during the female's first pregnancy, two bouts of courtship of his female were more likely to between successive pregnancies observed to parturition include certain elements and less likely to include others. (Table 4), and four with multiparous females for which a Table 5 summarizes these comparisons for the fourteen subsequent parturition was not observed due to cessa­ gestations from Group IV for which data were collected tion of the study (3) or death of the female (1). daily for all or nearly all (53 or more days) of the gesta­ tion period. The percentage of total bouts of courtship Courtship Behavior Directed to Pregnant Females including at least one performance of a behavior pattern The most frequently observed behaviors of the was the measure used. This percentage for the associa­ broadly defined courtship series are rumble-sway, lick, ting male was compared to the percentage pooled pursuit, fur nibble, circle, rump, kiss, and mark (perineal across the other males. (pooling was required as a means drag during a courtship sequence). Associating males of reducing error because the numbers of courtship tend to account for more performances of these acts bouts for some of the nonassociating males were than do the remaining males. That the associating male extremely low.) In Group IV, pursuit, jump-over, mark, dominates in these behaviors is not surprising since by sway, circle, and rumping were performed by the associ- 82 JACOBS

Table 5 Comparisons Between Associating Males and Other Males in Group IV in Percentage of Courtship Bouts in Which Various Courtship Patterns Were Performed (Based on 14 Gestations)

Number of Associ­ Mean Rank of ations in Which Associating Comparison of Associating p Behavior Behavior Seen Male * Male to Others* Value] Licking 14 3.64 4+ 10­ .180 Pursuit 14 1.79 12+ 2­ .012 Nosing 14 2.64 8+ 6­ .790 Nibbling Ear 12 2.71 3+ 9­ .146 Chin-Rump-Follow 14 1.71 9+ 5- .424 Kiss 14 4.29 0+ 14­ .00012 Jump-Over 6 1.00 6+ 0­ .031 Mark 14 1.64 12+ 2­ .012 Sway 14 1.50 13+ I­ .002 Circle 14 1.50 13+ I­ .002 Rumping 14 1.71 13+ 1­ .002 Rumping Attempt 14 2.00 11+ 3­ .058 Atypical Mount 14 1.86 10+ 4­ .180 Side Mount 8 1.25 6+ 2­ .290 Head Mount 7 2.43 3+ 4­ 1.000 Full Mount 11 1.55 8+ 3­ .226 Thrust 9 1.44 7+ 2- .180 "In percentage bouts including behavior tSign test, two-tailed ating male in a higher percentage of his courtship bouts other investigators. If quantitative records were not in a significant number of cases. Kiss was least likely to taken daily over periods of several months, associations be performed in a given bout by the associating male. formed may have gone undetected. Rood (I972) Similar comparisons of the chief courter with the observed cavy groups for short periods oftime at widely pooled values for other males were made for the eight spaced intervals. If the number of males were low and gestations of Group VA. The trends found with the environment simple, an established alpha male might Group IV for circle and rump were again seen (8+, 0­ be able to chase other males away from all females most for circle, p =.008; 7+, 1- for rumping, p =.070), but of the time. An observer might conclude that the alpha the values for pursuit (6+, 2-) and sway (5+, 3-) did male takes all females by virtue of rank alone (see not significantly favor the associating male or leading Kunkel & Kunkel, 1964; Rood, 1972). If the groups courter. were not observed daily for several months or if daily Interruption of Courtship quantitative records were not maintained, observations Courting males are sometimes attacked by other (such as have been made by King, 1956; Kunkel & males. This interruption of courtship may serve to Kunkel, 1964; and Rood, 1972) that nonalpha males reduce the courtship of the attacked animal, and may court young animals more frequently than does the account for the significant rank correlations seen in alpha male might be taken as support that domination some groups between social rank and courtship bouts and frustration alone can explain the ways in which performed. It is possible that selective interruption of animals court and are courted. However, the courtship other males' courtship of an associating male's females of young females appears to be related to the formation would account for the reduced attention paid to the of associations (Jacobs, 1973; in prep.), and the normal female by these other males. alpha male may account for much of this attention in Data were collected for Group IV on this question. In some cases. this group, one male (S) associated with two females for Despite situational and observational problem, associ­ a total of eight pregnancies, and another (C) associated ations probably were formed in the groups studied by with five females during six gestations. Both males were other authors. Kunkel and Kunkel (I964) reported rank more likely to interrupt the courtship of females with changes among four males in a group but did not corre­ whom they associated than that of other females late them with changes in females' reproductive states. (x 2 = 144.55, 1 df, P < .0001 for S; X2 = 86.94, 1 df, King (1956) presented data indicating that certain males p < .0001 for C). were often found with certain females. Rood (I972) reported a rank change which was clearly associated with the receptivity ofa young female in a group of C aperea DISCUSSION XC porcellus hybrids. As associations were not noted, the significance of this apparent case of recruitment of a Male-female associations were found in all multimale young female by a nonalpha male was not elaborated groups observed, but they have not been reported by upon. MALE-FEMALE ASSOCIATIONS IN THE DOMESTIC GUINEA PIG 83

The association appears to be a basic unit of the attention that these males pay to the associating male's sociology of the domestic guinea pig. The influence that females. As associating males are typically higher-ranked male-female relationships may exert upon the genetic than the "average" non associating male, the urine smell makeup of future generations is not known, but because on the female plus the interruption of courtship may the associating male does seem to inhibit the mating also serve to reduce the performance of visually conspic­ activities of other males with "his" female (Jacobs, uous (pursuit, rumping, rumble-sway, mounting), 1973), it is likely that the associating male biases the auditorily conspicuous (rumble), and olfactorally genotype of the next litter in favor of his own alleles in conspicuous (rumping, marking, rumble-sway) courtship a significant number of cases. patterns by the nonassociating males. The male rank changes associated with postpartum The material reported here indicates that the social receptivity and occasionally with cyclic estrus have not organization of the guinea pig is more complex than been reported before for guinea pigs (with the exception previously thought, and that changes in the alpha posi­ of Rood's one case). I have not found for other species tion in the male hierarchy may occur as the result of reports of male rank changes on the day of the litter male-female associations. Several hypotheses have been which are predictable on the basis of male courtship of advanced regarding role of courtship and agonistic beha­ specific females during pregnancy. viors in establishing and maintaining the association. It is The observation in this study that the same male believed that this work has more sharply defmed the tends to associate with a female over successive pregnan­ questions to be asked in future research efforts concern­ cies suggests that Rood's (1972) conclusion that ing the social behavior of this species. permanent social bonds are not formed by Caviinae was premature for the domestic cavy. In preliminary manipu­ REFERENCES lation tests, associations persisted following the combi­ Avery, G. T. Notes on reproduction in guinea pigs. Journal of nation of two groups and after removal of the female Psychology, 1925, 5, 373-396. Beauchamp, G. K. Attraction of male guinea pigs to conspecific from the group for one week. urine. Physiology and Behavior, 1973, 10, 589-594. The role of the female in the establishment and Beauchamp, G. K., Jacobs, W. W., & Hess, E. H. Male sexual behavior in a colony of domestic guinea pigs. American maintenance of the association is not fully established. Zoologist, 1971, 11, 618. (Abstract) Observations of females following their associating males Freund, M. Development of semen production in the guinea pig. Federal Proceedings, 1960, 19, 371. about after courtship or after the group has been Gerall, A. A. An exploratory study of the effect of social isola­ disturbed suggest that the female's role is not entirely tion variables on the sexual behavior of male guinea pigs. Animal Behaviour, 1963, 11, 274-281. passive. Gilmore, R. M. Fauna and ethnozoology of South America. Handbook of South American Indians, 1952, 6, 345-464. Circling and rumping were found in a higher percent­ (U.S. Bureau of American Ethnology, Bulletin 143.) age of the associating male's bouts of courtship than in Harper, L. V. The effects of isolation from birth on the social behavior of guinea pigs at adulthood. Animal Behaviour, that of other males in both groups for which such data 1968, 16, 58-64. were analyzed. In one of the groups, the associating Hollander, M., & Wolfe, D. A. Nonparametrie statistical meth­ ods. New York: Wiley, 1973. male's courtship was also more likely to include pursuit, Jacobs, W. W. Social behavior of the domestic guinea pig: The anal drag (marking), and swaying. The functions of male-female association. Unpublished doctoral dissertation, University of Chicago, 1973. these behaviors are not thoroughly understood; however, Jacobs, W. W., Beauchamp, G. K., & Hess, E. H. Male rank-order in a colony of domestic guinea pigs (Cavia porcetlusy. Ameri­ the rumble-sway display appears to be attractive to can Zoologist, 1971, 11, 635. (Abstract) females. Males are sometimes able to induce females to Jakway, J. S. Inheritance of patterns of mating behaviour in the male guinea pig. Animal Behaviour, 1959, 7, 159-162. follow them across open spaces by performing a rumble­ King, J. A. Social relations of the guinea pig living under semi­ sway before embarking. The rumble-sway and circling natural conditions. Ecology, 1956, 37, 221-228. Kunkel, P., & Kunkel, I. Beitrage zur Ethologie des Hausmeer­ appear to immobilize females to a degree and thus may schweinchens Cavia aperea f. poreel/us (L.). Zeitschrift fur facilitate accurate enurination when the male rumps the Tierpsychologie, 1964, 21, 602·641. Loeb, L., & Lathrop, A. E. C. Correlation between the cyclic female. changes in the uterus and the ovaries in the guinea-pig. As the rumble-sway may be thought of as assisting in Biological Bulletin, 1914, 27,1-44. Louttit, C. M. Reproductive behavior of the guinea pig. I. The the male-female aspects of the association, rumping (and normal mating behavior. Journal of Comparative Psychology, possibly supracaudal rub and marking by perineal drag) 1927,7,247-263. Rood, J. P. Observations on the ecology and behavior of Micro­ may contribute to the male-male aspects. The presence cavia. and Cavia. Acta Zoologica Lilloana, 1969, 24, 111-114. of male urine on a female may make her a less attractive Rood, J. P. Ecological and behavioral comparisons of three courtship target by making the female smell male-like. genera of Argentine cavies. Animal Behaviour Monographs, 1972,5,1-83. As male guinea pigs are able to discriininate one male's Valenstein, E. S., Riss, W., & Young, W. C. Experimental and urine from another's (Beauchamp, 1973), the urine genetic factors in the organization of sexual behavior in the male guinea pig. Journal of Comparative and Physiological marked female may also be a less attractive courtship Psychology, 1955,44,492-500. Webster, R. C., & Young, W. C. Adolescent sterility in the male target because nonassociating males are "reminded" of guinea pig. "'ertility and Sterility, 1951, 2, 175-181. the associating male whenever they inspect the female. Young, W. C. & Grunt, J. A. The pattern and measurement of sexual behavior in the male guinea pig. Journal of Compara­ Such a factor would tend to act in concert with the tive and Physiological Psychology. 1951, 44, 492-500. associating male's interruption of courtship of his (Received for publication April 23, 1975. females by other males to reduce the amount of Revision accepted August 16. 1975.)