Callithrix Kuhli) During the 80 Days from the Initial Day of Pairing

American Journal of Primatology 36185-200 (1995)

Development of Heterosexual Relationships in Wied’s Black Tufted-Ear Marmosets (Callithrix kuhh]

COLLEEN M. SCHAFFNER’, REBECCA E. SHEPHERD’, CRISTINA V. SANTOS’.’, AND JEFFREY A. FRENCH’ ‘Callitrichid Research Facility, Department of Psychology, University of Nebraska at Omaha;‘Departmento Psicologia Exoerimental, Universidade de Sdo Paulo, Sdo Paulo, Brazil In tamarins and marmosets, long-term stable sociosexual relationships are formed between heterosexual adults, but these “monogamous” relationships are often formed in groups that contain multiple adults of both sexes. The patterning of interactions during pair formation may therefore be shaped by this demographic profile. We evaluated the development of sociosexual relationships in six captive pairs of Wied’s black tufted-ear marmosets (Callithrix kuhli) during the 80 days from the initial day of pairing. Social behavior, sexual behavior and activity profiles were recorded. Social behaviors, including allogrooming, grooming solicitation, and intragroup monitoring calls, increased across the four 20-day time blocks. Males were more responsible than females for maintaining intrapair proximity during the first 40 days of pairing. Females and males were equally responsible for intrapair proximity maintenance after this time. The highest rates of sexual behavior, including copulation and proceptive open mouth displays, occurred upon pairing and then decreased non-significantly over time. The results indicate that sexual relationships in callitrichid primates are not dependent on the prior existence of a social relationship between males and females. Higher rates of copulation, greater male responsibility for proximity maintenance, and male initiative in sexual interactions early in pairing are consistent with a male reproductive strategy in which male-male competition may be common. 0 1995 Wiley-Liss, Inc.

Key words: Callithrix kuhli, heterosexual social relationships, development, sexual behavior, callitrichids

INTRODUCTION Sociosexual relationships in non-human primates vary along a continuum ranging from the short-term opportunistic consortships and matings of the chim- panzee (Pantroglodytes) [Nishida & Hiraiwa-Hasegawa, 1987; Tutin, 19791 to the long-term bonds found in gibbons and siamangs [e.g., Hylobates; Leighton, 19871.

Received for publication February 24, 1994; revision accepted September 21, 1994. Address reprint requests to Colleen M. Schaffner, Psychology Department, University of Nebraska at Omaha, Omaha NE, 68182.

0 1995 Wiley-Liss, Inc. 186 / Schaffner et al. The dynamics of these relationships, and the proximate mechanisms that are responsible for their establishment, maintenance, and regulation, are also likely to vary widely among species. Callitrichid primates (tamarins and marmosets) have been described as cooperative breeders [Goldizen, 1987; Price & Evans, 19911. The most conspicuous and predictable long-term sociosexual relationship within a com- munally breeding group is between the breeding adult male and female. In callitrichids, the social bond between adult males and females is characterized by a high rate of affiliative behavior that includes frequent grooming, close spatial proximity, and sexual interactions [Kleiman, 19771. In addition to high rates of affiliative behavior, heterosexual callitrichid pairs often cooperate in a coordinated fashion to defend their territory [Garber, 19881 and share in the rearing of the offspring [Tardif et al., 19931. Collectively, these factors suggest that the long-term sociosexual relationship between breeding adults is a crucial one within callitrichid groups. Like cooperatively breeding species in other taxa [e.g., Mongolian gerbils, Meriones unguiculatus; Agren et al., 1989; French, 1994; Splendid fairy-wrens, Malurus splendens, Russell & Rowley, 19931, the existence of a strong social relationship between the dominant male and female in callitrichid primate groups does not necessarily imply an exclusive sexual relationship between the pairmates. Social affiliation and copulatory behavior with individuals outside of a single breeding unit have been reported in callitrichid species in both field and captive settings [Inglett et al., 1990; Price & McGrew, 1991; Rothe & Koenig, 1991; Goldi- Zen, 1987; Baker et al., 1993; Garber et al., 19931. The potential independence of social and sexual interactions suggests that the proximate mechanisms that un- derlie these two aspects of intrapair relationships are not identical. Recent research has explored the development and maintenance of heterosexual relationships in marmosets and tamarins by evaluating temporal variations in the expression of social and sexual behavior between adult males and females. The maintenance of social relationships has been assessed by monitoring patterns of social interactions in stable and well-established social groups. These studies have revealed that affiliative social interactions, such as allogrooming and approaches to the partner, occur at stable rates over long periods of time and across multiple breeding cycles [e.g., Kleiman, 1977; Savage et al., 1988; Stribley et al., 19871. While some variation in patterns of affiliative behavior as a function of reproductive status of the female has been reported [e.g., Kendrick & Dixson, 1983; Price, 19921, the magnitude of this variation is small relative to the overall consistent patterns of affiliation. Thus, a stable pattern of affiliative social interaction ap- pears to be a correlate of the long-term maintenance of relationships between breeding adult males and females. The development of social relationships between heterosexual adults in callitrichid primates has been assessed via systematic observations of social interactions during the early stages of pairing. Significant changes in both the quality and the quantity of social interactions have been reported in a number of species. Female golden-lion tamarins (Leontopithicus rosalia) were more responsible for terminating bouts of close social proximity in well-established pairs than in animals paired for less than 12 weeks [Ruiz, 19901. Higher rates of mounting and males sniffing females occurred in newly-paired lion tamarins than occurred in well-established pairs [Kleiman, 19771. Cotton-top tamarin (Saguinus oedipus) females showed a similar profile: females in newly-formed pairs spent more time in contact, allogroomed and huddled with their mate than did females from well- established pairs. Furthermore, male cotton-top tamarins were more likely than females to initiate contact, bouts of allogrooming, and engage in social sniffing in Relationship Development in Marmosets / 187 newly-formed pairs. In well-established pairs, these sex differences were no longer observed. Copulations, but not male sniffs, were also more likely to occur in new pairs than in well-established pairs [Savage et al., 19881. In the common marmoset (Cullithrixjucchus) the highest levels of sexual activity, vocalizing, and affiliative behaviors were reported during the first week of pairing [Evans & Poole, 19831. Rates of both social and sexual behavior declined in subsequent weeks. In addition, males followed females more than females followed males. In the golden-lion tamarin, however, males approached females more often than females approached males in both newly-formed and well-established pairs [Ruiz, 19903. Cumulatively, these findings demonstrate that levels of both sexual and social interactions are higher in newly-formed pairs of callitrichids than in long-term pairs. These interaction patterns then decline over the duration of the relationship. Taken as a whole, then, the results suggest that social and sexual relationship formation follow a similar time course and may reflect a single developmental process. In the present study, we examined the temporal dynamics of the development of sociosexual relationships between adult male and female Wied’s black tufted-ear marmosets (Cullithrix kuhli). We addressed several specific questions: first, we wondered if the occurrance of sexual behavior was concurrent with, or was distinct from, the expression of affiliative social relationships [cf. Kleiman, 19771. In addition, we explored whether individuals who successfully produced offspring shortly after pairing would differ in the development of sociosexual relationships compared to unsuccessfully breeding pairs. In common marmosets, the social profile of pairs who conceived shortly after pairing did not differ from that of pairs who failed to conceive after pairing [Evans & Poole, 19831. Second, we examined female activity profiles to determine whether they changed during the development of the sociosexual relationship. Third, we examined bouts of sexual activity between pairmates to determine the form and frequency of behaviors that were involved in the coordination of sexual interactions. Last, we evaluated overall sex differences in the expression of social and sexual behaviors. METHODS Subjects Six male-female pairs of Wied’s black tufted-ear marmosets (Callithrix kuhli) served as subjects for the study. CulEithrix kuhli, distributed in the coastal forests of southern Bahia in Brazil, is recognized by Hershkovitz 119771 as Callithrix jucchus penicillutu. Recent taxonomies, however, have argued for species-level status for this form [Santos et al., 1987; Mittermeier et al., 19881. All animals were captive born to parents who were one or two generations removed from wild-born stock. The marmosets had previously been housed at the Centro de Primatalogia do Rio de Janeiro in the Federal Republic of Brazil. All of the marmosets had remained in their natal family groups for at least one subsequent set of offspring, and hence, had experience as sibling helpers. None of the marmosets had been previously paired with an unrelated partner of the opposite sex, and all females were nulliparous at the time the study began. The maximum interrelatedness between pairs was r = 0.25. At the time of pairing, males were an average of 3.7 years of age (range: 1.5 to 7.0 yrs.) and females were an average of 4.0 years of age (range: 2.0 to 8.0 yrs.). Three additional pairs were monitored to supplement observations on the detailed behavioral characteristics of sexual interactions (e.g. the role of open-mouth display in coordinating sexual interactions between pairmates), but since records were not complete from the onset of pairing, data from these pairs were not used to evaluate the development of social and sexual relationships. The supplemental animals had been paired for 5 months prior to observations and the 188 I Schaffner et al. females averaged of 2.7 years of age (range: 2.0 to 3.0 yrs.) and males averaged 3.5 years of age (range: 2.0-4.5 yrs.). The animals were housed at the Callitrichid Research Facility at the Univer- sity of Nebraska at Omaha. Pairs were maintained within large enclosures mea- suring either 1.2 X 0.9 x 2.4 m or 1.6 x 0.9 x 2.4 m. The enclosures were equipped with natural branches, a nesting tube, and wood shavings that covered the floor. The groups were visually isolated from each other but had olfactory and auditory contact with other groups. The animals were fed a varied diet two times per day. The morning feeding consisted of Hill’s brand Marmoset Diet (Topeka, KS), cereal, raisin bread soaked in milk, vegetable mash, a vitamin supplement, and one of the following proteins: tuna, egg, peanut butter, or cheese. The after- noon feeding consisted of diced apples, oranges, bananas, and grapes. Water was provided ad libitum to all groups. Lighting was controlled automatically and was set for a 12:12 hour onloff cycle with light phase beginning at 0700 hours. Procedures Pairs were selected to minimize inbreeding coefficients. Four of the breeding pairs were introduced simultaneously to new cages while, for two of the pairs, the males were introduced into the home cage of the female. Observations commenced on the first day of pairing. Observers familiar to the marmosets collected data while sitting quietly in the colony room. Pairs were observed between 0900 hours and 1500 hours for 30 minutes approximately every other day. Observations for newly-formed pairs spanned a minimum of 80 calendar days. There was an average of 9.7 observations per 20-day block (minimum average = 7.33, maximum = 12.33). Records of behavior were entered into a Tandy TRS-102 portable lap-top computer. Three observers collected observational data; inter-observer reliability was determined by dividing the total number of observations on which each potential pair of observers agreed by the total number of observations. Reliability was at least 89% for all possible pairs of observers. The ethogram for the black tufted-ear marmoset was derived from our own preliminary observations and from the ethogram developed by Stevenson and Poole [1976] for the common marmoset. We recorded all occurrences of the com- municative, social, and sexual behaviors listed in Table I. In addition, we used instantaneous sampling every 30 seconds to record the proximity of pairmates (greater than or less than arm’s length, or approximately 10 cm), and the female’s predominant activity [Altmann, 19741. Analyses Previous studies have revealed significant changes in rates of social and sexual behavior during the first eight to twelve weeks of pairing in callitrichid primates [Evans & Poole, 1983; Savage et al., 19881. Therefore, we evaluated changes in the patterning of social and sexual behavior by collapsing observation periods into four 20-day blocks. A two-factor mixed ANOVA (Time x Sex) was used to assess any significant changes in patterns of sociosexual behavior over these 20- day blocks, and to assess significant differences in the mean frequencies of behavior patterns between sexes. A one-way within factor ANOVA (time) was performed for sex-typical patterns (e.g., mounting by males). We also employed ANOVA to determine if differences existed between the behavior of pairs in which the female become pregnant during the 80-day study period (n = 21, and pairs in which the females did not become pregnant during this time (n = 4) over the 20-day time blocks. Fisher’s test of least significant difference was used for post-hoc comparisons in the event of a significant omnibus F statistic. Relationship Development in Marmosets I 189

TABLE I. Ethomam for the Black Tufted-Ear Marmoset Behavior pattern Definitions Behaviors Scored for Instantaneous Scan Samples for Females Sitting/Resting Animal is stationary on any substrate, either lying with rear feet folded under body or sitting. Sprawling Animal lies on substrate with the ventral surface from the breastbone to the pubic region against the surface, commonly observed with one or both rear feet dangling. Autogroom Animal manipulates its own fur with hands or mouth. Locomotion Animal is moving about the cage, e.g.; running, walking. Forage Animal actively searches for food, most often observed when animal is on the floor of the cage and manipulating bedding with hands, also scored when animal is on floor and on rear legs with head facing the cage floor and head moves back and forth (often observed with hand perched to manipulate bedding). Eat Animal has food item in mouth or hand and is actively masticating. Nest t u b e Scored when animal is within the nesting tube and specific activity is obscured from the observer. Social Scored when animal is actively engaged in any form of social activity with their mate (e.g., allogrooming, copulating). Huddle Animal is in sitting or resting position in contact with its mate. Other Scored when animal is engaged in a non-defined activity, (e.g., dangling from the cage wire by the rear feet). Social Behaviors Scored for both Males and Females Genital display Animal raises tail to expose genital region while simultaneously looking back over its shoulder at the directed target. Scentmark Includes suprapubic, when the animal drags pubic area across a substrate, often with both rear legs dangling, or anogenital when animal sits still and rubs the anal region on a substrate. Branch sniff/lick Animal touches nose to substrate or licks substrate, commonly observed immediately after another animal has scentmarked at the target site. Long calls A series of three to seven ‘phee’ vocalizations. Contact calls Includes twitters, a louder descending vocalization that is approximately four syllables in length, and trills that are soft whirring vocalizations. Approach Animal moves to within 10 centimeters of partner and remains there for at least three seconds. Leave Animal moves away from partner, more than 10 centimeters. Allogroom Scored when one animal manipulates the pelage of the other by parting the hair with its hands and removing particles with the mouth or hands. Grooming Scored when animal presents head, back or other body part to other. solicit Food transfer Included any passive food sharing, in which one animal permitted other to take food item or offered food item to other. Sexual Behavior Scored for both Males and Females Open-mouth A rhythmic opening and closing of the mouth that occurs as one individual display approaches another in the context of sexual behavior or is emitted during the act of an attempted mount, mount or copulation. Genital sniff When one individual places nose and face in the anogenital region of the partner. Sexual Behavior Scored for Males Attempted Male places one or two arms on the back of the female, no thrusting or mount intromission is observed. Mount Male grasps female’s back with both arms followed by intromission and thrusting. Copulation Same as mount with the exception that the male licks its penis following the act. 190 / Schaffner et al. The Hinde index [Hinde & Atkinson, 19701 was used to determine whether males or females exhibited greater responsibility for maintaining contact and proximity, and whether these trends changed during the 80 days from pairing. For each trial, the proportion of bouts of social proximity that were terminated by the female was subtracted from the proportion of bouts of proximity that the female initiated. The value of the resulting index was positive if females assumed greater responsibility for maintaining proximity and a negative value resulted if males assumed a greater role in maintaining proximity. The Hinde Index scores were then averaged for each 20-day block, and changes over the four blocks were analyzed by a one-way repeated measures ANOVA. We closely evaluated behavior records on days in which sexual interactions occurred. We were particularly interested in sex differences in the initiation of interactions that ultimately led to sexual activity and the role of open-mouth display (OMD) in coordinating these interactions. OMD is a rhythmic opening and closing of the mouth that resembles the gross motor pattern of proceptive tongue flicking in the common marmoset [Stevenson & Poole, 1976; Kendrick & Dixson, 19831. A one-sample, two-tailed t-test was used to determine if there was a significant departure from equal responsibility for “approaches” and “leaves” by males and females during sexual encounters. A two-factor ANOVA was used to determine if a difference existed in the proportion of interactions that terminated at either attempted mount, mount or copulation, and whether OMD was emitted, by either animal, prior to the encounter. RESULTS Temporal Variation in Sociosexual Behavior Social behavior. There were significant changes in the patterning of social behavior across the 80 days of pairing. Allogrooming differed significantly across time blocks (F[3,30] = 4.02, P < 0.025) with higher rates of allogrooming occurring during the last time block relative to the first three time blocks (P < 0.05, Fig. la). Changes in rates of grooming solicitation tended to follow the pattern observed in allogrooming, with significant increases throughout the 80 days of pairing (F[3,301 = 3.22, P < 0.05; Fig. lb). Like allogrooming, grooming solicitation was significantly higher during the last time block relative to the first two time blocks (P < 0.05). Intragroup contact calls (twitters and trills; Fig. lc) showed a significant increase over time (F[3,301 = 3.56, P < 0.051, however, there were no significant pairwise comparisons. The following behaviors did not vary significantly across the four time blocks: scentmarking (F[3,301 = 1.74); genital display (F[3,30] = 1.43); long call (F[3,30] = 0.74); and genital sniffing (F[3,15] = 0.46). Activity profiles for females were examined to determine if there were any differences in the distribution of activity across the 80 days of pairing. We found that the number of instantaneous samples in which females were engaged in social behavior increased significantly over time (F[3,151 = 3.74, P < 0.05). For each observation session, there were a potential of 61 intervals in which females could be scored as engaging in social behavior. We found that females were engaged in social behavior on significantly more intervals during the fourth time block (5.8 ? 2.6) relative to the first (3.3 1.9) and third time (3.5 * 1.6) blocks (P < 0.05). Sexual behavior. Changes in rates of sexual behavior followed a different timecourse than changes in social behavior in newly-formed pairs (Fig. 2). Signif- icant differences were identified over time for OMD (F[3,30] = 4.48, P < 0.025). Post-hoc comparisons indicated that OMD occurred significantly more often during the first time block relative to the last three time blocks (P < 0.05, Fig. 2a). Rates of attempted mount, mount and copulation were summed into a composite score, Relationship Development in Marmosets / 191

1.8

a Male 1.6 0 Female

1.4

1.2

1.o

0.8

0.6

0.4

0.2

0.0 2.4

2.0

1.6

1.2

0.8

0.4

0.0

T 6 4 L1-/ 2

0 0 20 40 60 80 Days Afler Pairing

Fig. 1. Mean frequencies (2 s.e.m.) of social behavior per 30 minute trial across four 20-day blocks after pairing: (a) allogrooming; (b)grooming solicitation; (el intergroup monitoring calls. 192 / Schaffner et al.

a Male 0 Fernalc .-6 I 0.8 0 & a [I] I 0.6 0 x c 2 0- S' 0.4 LL mc I 0.2

0.0 D 6 b 8 0.4 fn

c2. .z 0.3 -8 m X (I) R 0.2 m

?0 c ._ 5 0.1 eQ a

0.0 I I I I 20 40 60 80 Days After Pairing

Fig. 2. The mean proportion (+ s.e.m.) of open-mouth display (OMD) (a) are presented over the four 20-day blocks for males and females and the proportion of days (2s.e.m.) that sexual activity was scored it comprised a composite score of male sexual behavior that included attempted mounts, mounts and copulations (b).

and although rates were considerably higher during the first 20 days (0.69 5 0.52) than during all other time blocks (0.15 5 0.07), there was considerable variability among pairs in rates of copulation and differences across time were not significant (F[3,15] = 1.36). In order to minimize individual variation in rates of copulation, we analyzed the proportion of days during each time block in which sexual interactions (OMDs, attempted mounts, mounts, and copulation) occurred in each pair (Fig. 2b). Sexual interactions between partners tended to occur on a higher proportion of days shortly after pairing than at later times (F[3,15] = 2.48, P = 0.10). Rates of genital sniffs performed by males did not change significantly over time (F[3,15] = 0.46). Relationship Development in Marmosets / 193 Proximity Regulation. The mean frequency of male approaches was significantly greater than the mean frequency of female approaches (F[1,10] = 5.19, P < 0.05). However, there were no significant differences across the four time blocks (F[3,30] = 0.79, Fig. 3a). Females and males displayed equal responsibility for leaving (Fig. 3b). A two-factor mixed ANOVA yielded no difference between the two sexes (F[1,10] = 0.065), or across time blocks (F[3,301 = 1.92). Scores on the Hinde Index changed significantly over time (F[3,151 = 5.43, P < 0.01). Index scores were significantly lower during the first two time blocks relative to the last two time blocks, as indicated by pairwise comparisons (P < 0.05). During the first two time blocks the Hinde Index was negative, indicating that males were more responsible for maintaining proximity than females, whereas in the latter two time blocks, index values were closer to zero indicating that males and females had equal roles in maintaining proximity (Fig. 3c). Social and Sexual Profiles in Successful and Unsuccessful Breeding Pairs We compared the expression of social and sexual behavior in pairs with females that became pregnant during the study period (n = 21, with pairs in which the female did not conceive during the study period (n = 4). There were no differences in rates of social or sexual behaviors between successful and unsuccessful breeding pairs: allogrooming (F[1,11] = 0.13); grooming solicitation (F[1,111 = 0.00); OMD (F[1,111 = 0.00); intragroup contact calls (F[1,111 = 0.55); genital display (F[1,111 = 1.54); attempted mounts (F[1,51 = 0.70); mounts (F[1,51 = 0.88); and scentmarking (F[1,111 = 0.53). Sexual Behavior and Proximity Maintenance During Sexual Encounters Fifty-five separate bouts of sexual activity were recorded for seven pairs. A bout was considered to be any series of sexual behaviors in which two or more sexual acts (an individual sexual behavior) were scored. Typical bouts were preceded by OMDs, followed by a male approaching the female and executing two or more attempted mounts, mounts, or copulations. Twenty-one of the bouts terminated with an attempted mount, 28 terminated with a mount, and six interactions were considered full copulations. The presence or absence of OMDs prior to the sexual interaction was associated with variations in the terminal behavior of a bout of sexual activity (Fig. 4). A significant interaction was obtained for proportion of sexual bouts that terminated in either an attempted mount, mount or copulation, and whether the sexual interaction was preceded or not by an OMD (F[2,12] = 5.29, P < 0.05). Subsequent analyses revealed that incomplete sexual encounters, attempted mounts, and mounts were more likely to occur in the absence than in the presence of OMD (attempted mounts: P < 0.05; mounts: P < 0.011, and successful sexual encounters were more likely to occur than attempted mounts and mounts when OMD preceded a sexual bout than when it did not (P < 0.05). For all sexual interactions, whether preceded by an OMD or not, we found that males were more likely to initiate proximity than females. Across pairs, males tended to approach females more frequently prior to sexual interactions than the reverse (75.0 12.0% of the interactions; t[6] = 2.01, P = 0.09). Males terminated proximity after interactions (57 2 0.13% of the time; t161 = 0.52, P = 0.62). DISCUSSION We examined temporal variations in the patterning of sexual behavior and social behavior in newly-formed heterosexual pairs of black tufted-ear marmosets 194 I Schaffner et al.

12 ._e Male a z 0 Female 0 "9 kl a v) r 06 2 Q 2 53 r

K b z._ m09 L n $6 t 1a c :3 2

0 0.06

X 0.00 U = -0.06 U ._ I -0.12

-0.18

-0.24 20 40 60 80 Days Afler Pairing

Fig, 3. Maintenance of proximity for males and females over the four 20-day blocks are presented. Mean number of approaches (* s.e.m.1 (a),and mean number of leaves (* s.e.m.1 (b),and Hinde Index (c) values are presented. See text for derivation of the Hinde Index.

and found a distinct time course for the emergence of sexual interactions among pairmates from the emergence of a social relationship. Social behavior, including allogrooming and grooming solicitation, as well as intergroup contact calls increased over time. Activity budget analyses revealed a corresponding increase in the time females allocated to social behavior throughout the period of pairing. On the other hand, behaviors related to sexual activity were highest during the first 20 days of pairing and decreased over time. Males were more responsible for maintaining proximity than females during the first two time blocks and initiated contact more frequently than females did prior to bouts of sexual activity. We could not identify differences in the form or rate of expression of social or sexual behavior between unsuccessful and successful breeders, and there was no difference in the Relationship Development in Marmosets / 195

I I - 0.20 0NoOMD =OMD u) ._0 5 2 0.16

I C - m3 - i 0.12 r C .- r 0.08 a c f 0.04

0.00 copulation t mount Point of Bout TerminationI Fig. 4. Percent of sexual activity (? s.e.m.); attempted mounts, mounts and copulations, that occurred in the presence and the absence of OMD. form or rate of expression of behavior across the sexes, with the exception of higher rates of genital sniffing by males. Higher rates of copulatory behavior tended to occur during the first 20 days relative to later time blocks in black tufted-ear marmosets. Higher rates of sexual behavior have also been reported in newly-formed versus well-established pairs of common marmosets, golden-lion tamarins and cotton-top tamarins [Evans, 1984; Kleiman, 1977; Savage et al., 1988; Stribley et al., 19871. For common marmosets, the highest rates of copulatory behavior were recorded during the first week of pairing [Evans & Poole, 19831. In addition to examining changes in the frequency of sexual behavior over time, we also compared the temporal variation of sexual behavior between successful and unsuccessful breeding pairs. We found that unsuccessful breeders, those that did not conceive during the study period, showed the same pattern as pairs who conceived offspring during the 80 days of the study: rates of sexual interactions in both tended to decrease over time. One might argue that if sexual behavior was related specifically to the female’s fertility status, then unsuccessful breeding pairs should show higher levels of sexual behavior across the 80 day observation period. On the other hand, if one of the members of the pair was infertile, then it could be argued that rates of sexual behavior should be lower in unsuccessful breeders. However, the fact that the patterns are the same in successful and unsuccessful breeders suggests that cues other than fertility status (e.g. social or temporal ones) are important regulators of reproductive behavior in marmosets. Unlike sexual behavior, rates of affiliative social behavior were initially low and increased during the 80 days of pairing. Increases were recorded for allogrooming, intragroup contact calls, and grooming solicitation. In the common marmoset, similar increases in allogrooming were identified from weeks two through 196 / Schaffner et al. five, and six through 10, relative to week one [Evans & Poole, 19831. Common marmosets exhibited an overall decrease in rates of vocalizing as pairs became well-established [Evans & Poole, 1983; Evans, 19841. In cotton-top tamarins and common marmosets, higher rates of allogrooming were identified in newly-formed relative to well-established breeding pairs [Evans, 1984; Savage et al., 19881. Dif- ferences across studies in rates of social and sexual behavior during relationship formation may be due to methodological differences among studies. In the present case, we examined how behavior changes across relatively small time blocks (i.e., 20 days). Previous studies that examined newly-formed pairs of callitrichids col- lapsed data across a larger time period during pair formation [12 weeks in golden- lion tamarins, Kleiman, 1977; Ruiz, 1990; Stribley et al., 1987; eight weeks in cotton-top tamarins, Savage et al., 19881 and contrasted behavioral patterns during these long time blocks with patterns in well-established pairs (pairs who had resided together greater than 12 months). Our approach, and that of Evans and Poole 119831, focused on changes within the initial weeks of pairing. Comparisons of interaction patterns over large time blocks may mask more subtle changes that occur during the early stages of pair formation. Thus, while the broader patterns of change that occur in social and sexual behavior in callitrichid primates consist of decreases in both social and sexual behavior over the first 12 months of pairing, these behavioral systems follow a different timecourse during the first weeks of pairing. Rates of sexual behavior are initially high relative to later time periods, while the incidence of social behavior rises throughout the first weeks of pairing. Our examination of the detailed behavioral correlates of sexual interactions between pairmates identified a proceptive display: OMD. OMDs occurred significantly more often prior to sexual activity that terminated in complete copulations and occurred much less often prior to sexual interactions that terminated in either attempted mount or mounts. Proceptive displays have been described previously for the common marmoset, and are associated with the coordination of reproductive behavior between partners. Tongue flicking occurred significantly more often around the time of ovulation [Kendrick & Dixson, 19831, and treatment of ovariectomized common marmosets with estradiol-17p facilitated tongue flicking behavior immediately prior to mounting by the male [Dixson, 1986; 19871. Ovariec- tomized common marmosets were significantly less likely to refuse mounts and emitted significantly more proceptive tongue flicks when treated with estradiol- 17p, indicating that tongue flicks may reflect a motivation on the part of females to engage in sexual activity [Kendrick & Dixson, 19851. Our findings suggest that OMDs in black tufted-ear marmosets serve a similar function to lipsmacking or tongue flicking in the common marmoset, since successful sexual interactions were not likely to occur in the absence of OMDs. Thus, OMDs may signal a motivation on the part of an animal to engage in sexual activity, as well as coordinating bouts of sexual activity between partners, at least early in pair formation. Well- established pairs show lower rates of OMD and sexual interactions. In these pairs, sexual interactions may be initiated or coordinated by other signals [e.g., olfactory cues, Ziegler et al., 19931. Our data suggest that social relationships between adult male and female marmosets are contingent upon the patterning of social interactions over time, but that sexual interactions are not. This conclusion is supported by two additional sets of findings. The first comes from studies of social preference, in which individuals are given the opportunity to interact with unfamiliar opposite-sexed animals in the presence and absence of their long-standing mates. These studies reveal a tendency, in animals who are already members of an existing breeding Relationship Development in Marmosets / 197 pair, to express social andlor sexual affiliation with extra-pair individuals [common marmosets: Evans, 1983; Sutcliffe & Poole, 1984; saddleback tamarins: Epple, 1990; golden-lion tamarins: Inglett et al., 1990; Inglett, 1993; red-bellied tamarins, S. labiatus, Buchanan-Smith & Jordan, 19921. The second set of findings is the increased incidence of reported departures from monogamy in callitrichid primates. Sexual activity and conceptions in individuals outside of the dominant “breeding” pair all occur with some regularity in callitrichids [e.g., Rothe & Koenig, 1991; Price & McGrew, 1991; Dietz & Baker, 19933. Indeed, recent field studies indicate that multiple males within a group copulate with the breeding femaleb), both during and outside the period of maximal fertility [Goldizen, 1987; Garber et al., 1993; Baker et al., 19931. One would expect, therefore, some manifestation of competition among males for fertiliza- tions. In lion tamarins, dominant males monopolize access to the female during periods of maximal fertility, and subordinate male copulations occur when it is unlikely that conception will occur [Baker et al., 19931. In saddleback tamarins [S. fuscicollis; Goldizen, 19871 and moustached tamarins [S. mystax; Garber et al., 19931, relationships among males are neutral or nonaggressive, even during times of heightened sexual activity. High rates of copulation and male responsibility for initiating proximity and contact with the female may, therefore, represent an alternative competitive strategy among males for enhancing the likelihood of sir- ing offspring [cf. Harcourt, 19813. It would be of interest, in this light, to compare the ontogenetic pattern of sexual behavior after pairing in groups that consist of a single male and female (as in the present study) with groups that contain multiple males [Epple, 1975; Kleiman, 19781. To the extent that high rates of sexual activity and male initiative in proximity maintenance during the initial stages of pairing reflect a competitive strategy by the male, then these patterns should remain high and not diminish in multimale groups compared with groups containing single males. Social relationships between male and female callitrichids primates may be critical for cooperative rearing, joint defense of territories, group foraging, and coordinated antipredator activities within social groups [Caine, 19931. The evidence presented here supports the notion that social bonds are not formed in- stantly, but develop over the initial weeks of pairing in callitrichids. In contrast, sexual interactions are not contingent upon the existence of social relationships among partners, nor do they appear to be an emergent property of social relationships in black tufted-ear marmosets. CONCLUSIONS 1. During the initial 80 days of pairing, heterosexual pairs of black tufted-ear marmosets exhibited varying rates of sexual behavior and social behavior. Sexual behavior was highest during the initial time block and then decreased, non-significantly, over the four time blocks. Social behavior increased over the course of observations, peaking during the last time block. 2. There were changes in the dynamics of proximity maintenance over the first 80 days of pairing. Males maintained proximity and approached their mate more often than females during the first 40 days of pairing. During the second 40 days of pairing, males and females were equally responsible for proximity maintenance. 3. Detailed examination of sexual behavior identified an open-mouth display (OMD) that may serve a proceptive function. Sexual interactions that were preceded by OMDs were more likely to end in ejaculation than sexual interactions that did not include OMDs. These conspicuous facial displays occurred significantly more often during the first 20 days of pairing relative to later time periods. 198 / Schaffner et al. 4. The distinct temporal patterning of sexual behavior and social behavior suggests that the development of a sexual relationship between partners is not dependent on the existence of a social relationship between partners. In addition, high rates of sexual activity, male initiative for proximity maintenance, and a tendency for males to initiate interactions that lead to copulatory activity, are consistent with a male reproductive strategy in which competition among males may be common. ACKNOWLEDGMENTS This study was supported in part by grants from the National Science Foun- dation (BNS 90-00094, IBN 92-09528 and OSR-92-55225) and by the Rhoden Bi- ological Fellowship, University of Nebraska at Omaha to C.M.S. We thank Marnie Miller for assistance with data collection, the Henry Doorly Zoo and Dr. Corrine Brown for excellent veterinary support, and D. Hightower and B. Oldenhuis for their dedication to the care and maintenance of the marmosets. Dr. Pissinatti and A.F. Coimbra-Filho of the Centro de Primatologia do Rio de Janeiro in Brazil provided assistance in the development of our colony of Callithrix kuhli in North America. The animals in our colony consist of captive-born animals legally im- ported into the United States under the guidance of IBAMA and the U. S. Fish and Wildlife Service. We thank M. Platt, B. Inglett, and T. Dethlefs for consultation and commentary on the manuscript, as well as, the anonymous reviewers for their suggestions. 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