The pairbond in the titi monkey (Callicebus moloch): intrinsic versus extrinsic contributions of the pairmates

Aspects of a monogamous relationship can be inferred by observing reactions of mated individuals to unfamiliar conspecifics. The present study examined the behaviours shown by male and female titi monkeys (Callicebus moloch) toward an opposite-sex stranger, and the effect of their pairmate's absence or presence on these encounters. Behaviours within unfamiliar heterosexual pairs showed superficial similarities to behaviours of mated pairs. Although there were few affiliative behaviours between unfamiliar individuals, animals were often in spatial proximity and even performed sexual behaviour. The visual presence of a pairmate clearly affected encounters between unfamiliar heterosexual pairs in several respects. The presence of a male pairmate had a much stronger influence on all behavioural measures compared to the presence of a female pairmate. Possible functional aspects of these results are discussed.     

Sexual dimorphism in responses to unfamiliar intruders in the tamarin, Saguinus oedipus

Aspects of social structure in group-living species can be inferred by observing the responses of individuals to unfamiliar animals. This study examined the responses of mated pairs of cotton-top tamarins (Saguinus oedipus oedipus) to presentation of either unfamiliar conspecifics or members of a related tamarin species, the saddle-back tamarin (Saguinus fuscicollis fuscicollis). Male and female responses to intruders differed: resident males threatened, displayed piloerection, approached, and attacked intruders, especially males, while resident females showed increases in suprapubic scentmarking in the presence of intruders. Both males and females discriminated between the species of intruders, exhibiting more threats, scent-marking, piloerection, and approaches in the presence of conspecific intruders. There are pronounced sex differences in the signals and behaviour patterns that are elicited in an aggressive or territorial encounter with unfamiliar conspecifics in this monogamous primate.     

Sex Discrimination via Anal Gland Secretion in a Territorial Monogamous Mammal

Monogamy in mammals is relatively unusual, only occurring in 3–5% and to an even lesser degree in rodents. Monogamy exists in two forms, facultative which evolved due to female dispersion and obligate when male care is needed for offspring survival. Most monogamous rodents use scent marking as a form of territorial defence to obtain exclusive access to vital resources. Intrasexual competition occurs in many species to maintain pair bonds and also to signal presence within a territory. In this study, we tested the hypothesis that resident obligate monogamous Eurasian beaver (Castor fiber) can discriminate between the sexes when investigating anal gland secretions (AGS) from unknown (stranger) mated pairs. We predicted that, due to intrasexual competition, dominant territorial male and female beavers will display a stronger response to AGS of same‐sex conspecifics. Territorial intrusion by mated pair strangers was simulated by the formation of experimental scent mounds (ESM) with AGS. Our results showed that both sexes (1) displayed a stronger response to the male AGS in sniffing duration, (2) physically responded for longer durations towards male AGS and (3) overmarked male AGS more frequently. We infer that obligate monogamous mammals can determine the sexual identity of intruding conspecifics of a mated pair via AGS and that intruding males may pose more of a threat to resident males via intrasexual competition and resident females due to the long‐term costs, such as infanticide and abortion, of a new dominant male.     

Developmental changes in responsiveness to parents and unfamiliar adults in a monogamous monkey (Callicebus moloch)

Titi monkeys (Callicebus moloch) are monogamous New World primates that are characteristically found in family-type groups consisting of a mated adult pair and one or two young. The factors maintaining the small size of these groups are not known. Based on observations of free-ranging and captive families, parental aggression toward older offspring seems unlikely to play a significant role. Maturing individuals themselves, however, could undergo behavioral changes that weaken ties to their natal group. These might include waning of affiliative relations with parents, or subtle forms of aversion. Independent of such changes, increasing interest in unfamiliar conspecifics could be a factor. We examined these possibilities in the present study by assessing changes in social behavior and social preferences from initial ambulatory independence (6 months) through reproductive maturity (24 months) in a combined cross-sectional/longitudinal study of 21 captive titi monkeys living with their parents. Responses to both parents and to an unfamiliar adult heterosexual pair, a single unfamiliar adult male, and a single unfamiliar adult female were observed when subjects were given a choice between parents and strangers presented simultaneously or as the only social incentive. Social stimuli were at opposite ends of a 16.8-m-long test corridor. Subjects could move freely about the corridor for 5 min with each configuration of social stimuli. They stayed closer to parents than to strangers at all ages. Responsiveness to strangers increased with age and suggested growing ambivalence, particularly toward the male stranger. As they approached 24 months of age, male subjects showed a dramatic increase in the frequency and intensity of agonistic behaviors toward male strangers, behaviors that were rarely directed toward female strangers or parents. Waning of attraction to parents may be less important in dispersal from the natal group than changing reactions to strangers.     

Behavioral and cardiophysiological responses of common marmosets (Callithrix jacchus) to social and environmental changes

Under captive conditions common marmosets (Callithrix jacchus) show socially monogamous propensities. Male and female form a social bond as characterized by signs of behavioral arousal during separation of the pairmates, high levels of affiliative interactions between pairmates and agonistic responses towards strange conspecifics. In the present study behavioral and cardiophysiological responses of mated individuals of common marmosets were recorded while the animals were in an unfamiliar environment (1) alone, (2) with the pairmate, or (3) with an opposite-sexed stranger. Pairmates of 6 established pairs were tested in 3 replicates yielding a total of 36 trials per experiment. A trial was divided into three 10-min segments (baseline; unfamiliar environment; reunion). Behavioral responses were videotaped with a remote controlled camera system installed within the cage. Systolic (SBP) and diastolic blood pressure (DBP), and heart rate (HR) as well as locomotor activity (ACT) were recorded telemtrically through peritoneally implanted transmitters. The individuals’ responses measured while in an unfamiliar environment was only reduced by the pairmate, but not by an opposite-sexed stranger. No affiliative behaviors occurred between strange conspecifics, whereas aggressive and sexual behaviors were observed. During reunion with the pairmate individuals recovered physiologically. The present study shows that an individualized pair bond exists between pairmates of common marmosets. Further, it becomes evident that establishing a social bond with the pairmate is important for maintaining physiological homeostasis.     

An experimental investigation of the pair bond in the callitrichid monkey,Saguinus labiatus

The strength and specificity of attraction between mated pairs of red-bellied tamarins (Saguinus labiatus) were tested in the laboratory. Test individuals were placed in a choice situation in which they could indicate their preference, by proximity and quality of behavior measures, to either their pair mate in an adjoining cage or an alternative in a second adjoining cage (same-sex animal, opposite-sex animal, or an empty cage). The test animals showed a significant preference to be in visual contact and proximity with their pair mates instead of the alternative when it was an animal of the same sex as the test individual or an empty cage. However, when the choice was between their pair mate and an animal of the opposite sex, no preference for their pair mate was apparent. No sex differences were found. It is concluded that attraction to a pair mate is not sufficient to maintain a pair bond, and when pairs ofS. labiatus breed monogamously, the pair relationship is likely to be maintained, at least in part, through aggression between same-sex individuals.     

Social facilitation of agonistic responses to strangers in pairs of saddle back tamarins (Saguinus fuscicollis)

The effect of the presence of a familiar social partner on the interactions of saddle back tamarins with unfamiliar conspecifics was studied. Fifteen adult male-female pairs, of which six were composed of a castrated male and an intact female, served as subjects. All subject pairs were given two social encounters during which both mates met a strange male and two encounters during which they met a strange female. In addition, all subjects were given four encounters during which they met the same strangers while their own pair mates were absent. As a group, the subjects showed higher intensities of injurious aggression and of agonistic displays when they met strangers in the presence of their own pair mates. Females and castrated males, as subgroups, showed significant increases in most agonistic responses when they met strangers in the presence of their pair mates. Intact males, however, did not.     

Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics

In socially monogamous species, mate‐guarding could be a reproductive strategy that benefits both males and females, especially when males contribute to parental care. By actively guarding mates, males may reduce their chances of being cuckolded, whereas females that mate‐guard may reduce the likelihood that their mates will desert them or acquire additional mates, and hence limit or reduce paternal care of offspring. Owl monkeys (Aotus spp.) are socially monogamous with biparental care of young and, hence, potential beneficiaries of mate‐guarding. We presented mated pairs of captive owl monkeys (A. nancymaae) with unfamiliar male and female conspecifics, to determine if either member of the pair exhibits intraspecific aggression toward an intruder or stays close to its mate, behaviors indicative of mate‐guarding. Male mates were more responsible for the maintenance of close proximity between mates than females. Male mates also exhibited elevated levels of behavior that signify arousal when presented with a male conspecific. These responses by mated male owl monkeys are consistent with patterns that may help prevent cuckoldry. Am. J. Primatol. 72:942–950, 2010. © 2010 Wiley‐Liss, Inc.     

Social patterns of food sharing in monogamous owl monkeys

Captive owl monkeys (Aotus nancymaae, A. azarai) share food frequently within both families and pairs. In this study food sharing was observed in seven mated pairs and four families (i.e., four mated pairs and their offspring). Patterns of food sharing were examined with respect to age class, sex, and the presence or absence of dependent offspring. Within families, most food transfers were from adult males to developing offspring. Adult males and females transferred food to their mates in caged pairs as well as in family units. Food interactions between adults are as likely to result in food transfers as those between adults and offspring. This pattern of food sharing between mates in a monogamous species may serve both nutritional and social functions that differ from those in polygamous species.     

A comparison of scent marking between a monogamous and promiscuous species of peromyscus: pair bonded males do not advertise to novel females

Scent marking can provide behavioral and physiological information including territory ownership and mate advertisement. It is unknown how mating status and pair cohabitation influence marking by males from different social systems. We compared the highly territorial and monogamous California mouse (Peromyscus californicus) to the less territorial and promiscuous white-footed mouse (P. leucopus). Single and mated males of both species were assigned to one of the following arenas lined with filter paper: control (unscented arena), male scented (previously scent-marked by a male conspecific), or females present (containing females in small cages). As expected, the territorial P. californicus scent marked and overmarked an unfamiliar male conspecific's scent marks more frequently than P. leucopus. Species differences in responses to novel females were also found based on mating status. The presence of unfamiliar females failed to induce changes in scent marking in pair bonded P. californicus even though virgin males increased marking behavior. Pair bonding appears to reduce male advertisement for novel females. This is in contrast to P. leucopus males that continue to advertise regardless of mating status. Our data suggest that communication through scent-marking can diverge significantly between species based on mating system and that there are physiological mechanisms that can inhibit responsiveness of males to female cues.     

Mating behavior and sex change of the anemonefish,Amphiprion clarkii,in the temperate waters of southern Japan

Synopsis In the main habitat of the anemonefishes Amphiprion, their movements between host sea anemones are generally restricted because of the low population density of hosts and high predation pressures. On the contrary, movements of A. clarkii between hosts were usual in the present study area (temperate waters of southern Japan), where host anemones are abundant. The general social unit of the anemonefishes is an isolated group consisting of a monogamous breeding pair and a varying number of nonbreeders. In the present study area, however, monogamous pairs established territories almost contiguous to others and nonbreeders had home ranges on the outskirts of the pairs' territories. The high host population density allows A. clarkii to move between hosts for searching for mates and acquiring additional mates. Most pair bonds lasted for more than 6 months, but 13% of the pairs separated because of migration of a mate to another territory. Bigamy occasionally originated from a penetration into a territory of a breeder by a mated neighbor of the opposite sex after the former's mate loss. Among 18 males who had lost their mates, only 3 changed sex and others re-paired with immigrant females, migrated to unmated females' territories or invaded pairs' territories. In the present study area, sex change to female is not the best way for an unmated male to increase his future reproductive success because of a loss of time spent on sex change and an opportunity to re-pair with new mates larger than himself, but is adaptively maintained as the best of a bad situation for the unmated male.     

Serum cortisol concentrations of single-housed and isosexually pair-housed adult rhesus macaques

Possible social distress was evaluated in 20 adult rhesus macaques housed in compatible isosexual pairs (5 female pairs, 5 male pairs) for the purpose of social environmental enrichment. Serum cortisol concentrations of paired animals were compared with serum cortisol concentrations of individually housed adult rhesus macaques of both sexes (5 females, 5 males). In both sexes, cortisol concentrations of paired animals (means 10 females = 19.5 +/- 2.9 micrograms/dl; means 10 males = 17.5 +/- 4.6 micrograms/dl) showed no significant difference (p always greater than 0.1) with those of single animals (means 5 females = 20.5 +/- 2.1 micrograms/dl; means 5 males = 15.9 +/- 2.6 micrograms/dl). Both in male and in female pairs, dominant partners had cortisol concentrations that were equivalent to those of their subordinate counterparts. It was concluded that neither female nor male adult rhesus macaques experience more distress when sharing a cage with a compatible partner of the same sex than when living alone.     

Etude des interactions sociales entre male et femelle chez la Genette (Genetta genetta L.): Relations entre marquage olfactif et agression

Study on Social Interactions between Male and Female Genets (Genetta genetta L.): Relations between Scent Marking and Aggression The aim of this work was to study the relations between marking behaviour and aggression in genets (Genetta genetta L.). Observations on social interactions were made on a socially stable pair and during encounters between unfamiliar pairs. In the first case, there appeared to be a relationship between marking activity in the male and aggression. During aggression periods, marking with the ano-urogenital region increased in the male and decreased in the female. Another striking variation concerned flank rubbing and hindleg rubbing. In both male and female these marking frequencies increased significantly during aggression periods and flank rubbing was modified by visual cues. Data recorded during encounters between unfamiliar pairs (one male being introduced in a female's cage) showed that agonistic behaviours were released through visual cues in females and olfactory cues in males. The same changes in marking frequencies were observed. These results also showed that ano-urogenital marking was inhibited in females during aggression periods. The adaptative significance of these phenomena is discussed.     

Experimental field studies of Asian ape social systems

The Asian apes, orangutans and gibbons, possess unusual social systems among anthropoid primates. Social groups of gibbons consist of mated adult pairs and their offspring; mature orangutans are primarily solitary. Recent experimental field research has begun to yield insights into the behavioral mechanisms employed by these animals to maintain their characteristic patterns of social dispersion. While spatial separation between female orangutans appears to be maintained passively, aggression, which is manifest during direct encounters and long-distance vocal interactions, mediates male asociality. Male-male aggression is the result of intense intrasexual competition occurring between animals for mating access to females. To reduce intrasexual competition, male orangutans have adopted alternative mating tactics. In contrast to female orangutans, female gibbons show marked agonistic tendencies toward conspecifics. Female territoriality contributes to preventing males from becoming polygynous. Male gibbons, restricted to monogamous relationships, attempt to ensure their paternity through intrasexual aggression. These observations suggest that the spatial dispersion of females constrains male mating options in both species. However, variations between orangutan and gibbon social systems can be understood as consequences of the temporal dispersion of sexually receptive females. The temporal clumping of females, due to relatively high operational sex ratios, limits the ability of male gibbons to acquire multiple mates. Conversely, an extremely low operational sex ratio in orangutans creates a strong selection pressure for intrasexual competition and polygamous mating. These considerations provide a novel framework for interpreting the social systems of the African apes.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.

     

Plasticity in the mating system of the longnose filefish,Oxymonacanthus longirostris, in relation to mate availability

The mating system of the longnose filefish,Oxymonacanthus longirostris, was examined on coral reefs of Okinawa, Japan. This species has been shown previously to be monogamous. Fish were usually found swimming together in heterosexual pairs with the male and female sharing the same feeding territory. However, both monogamous and polygynous (bigamous) males were found in the present study. Polygynous males, which were larger than monogamous males, visited and stayed several minutes in turn with each female within the territories. Although most males were monogamous in the early breeding season, over 20% of males mated polygynously in the late breeding season. The adult sex ratio in the former was unbiased, but became slightly female-biased toward the end of the breeding season because of the higher disappearance rate of males. The higher disappearance rate may be due mainly to a higher mortality rate of males resulting from a greater deterioration of physical condition during the breeding season. Thus, the mating system varied with the change of the adult sex ratio. Plasticity in the mating system of this species may be the outcome of male mating tactic depending on local mate availability.     

Social Reversal of Sex‐Biased Aggression and Dominance in a Biparental Cichlid Fish (Julidochromis marlieri)

In biparental species, aggression, dominance, and parental care are typically sexually dimorphic. While behavioral dimorphism is often strongly linked to gonadal sex, the environment—either social or ecological—may also influence sex‐biased behavior. In the biparental cichlid fish Julidochromis marlieri, the typical social environment for breeding pairs consists of large females paired with smaller males. While both sexes are capable of providing territory defense and parental care, the larger female provides the majority of defense for the pair, while the smaller male remains in the nest guarding their offspring. We examine the contributions of sex and relative mate size to these sex‐biased behaviors in monogamous J. marlieri pairs. Both female‐larger and male‐larger pairs were formed in the laboratory and were observed for territorial aggression (against conspecifics and heterospecifics), dominance, and parental care. In female‐larger pairs, territorial aggression and intra‐pair dominance were female‐biased, while in male‐larger pairs this bias was reversed. For both pairing types, the presence of an intruder amplified sex differences in territorial aggression, with the larger fish always attacking with greater frequency than its mate. Though less robust, there was evidence for plasticity of sex‐bias for some egg care related behaviors in the inverse direction. Our study suggests that relative mate size strongly influences the sex bias of aggression and dominance in J. marlieri and that this aspect of the social environment can override the influence of gonadal sex on an individual's behavior. The remarkable plasticity of this species makes Julidochromis an exciting model that could be used to address the relationship between proximate and ultimate mechanisms of behavioral plasticity.     

Polyandry enhances offspring viability with survival costs to mothers only when mating exclusively with virgin males in Drosophila melanogaster

A prominent hypothesis for polyandry says that male–male competitive drivers induce males to coerce already‐mated females to copulate, suggesting that females are more likely to be harassed in the presence of multiple males. This early sociobiological idea of male competitive drive seemed to explain why sperm‐storing females mate multiply. Here, we describe an experiment eliminating all opportunities for male–male behavioral competition, while varying females’ opportunities to mate or not with the same male many times, or with many other males only one time each. We limited each female subject's exposure to no more than one male per day over her entire lifespan starting at the age at which copulations usually commence. We tested a priori predictions about relative lifespan and daily components of RS of female Drosophila melanogaster in experimental social situations producing lifelong virgins, once‐mated females, lifelong monogamous, and lifelong polyandrous females, using a matched‐treatments design. Results included that (1) a single copulation enhanced female survival compared to survival of lifelong virgins, (2) multiple copulations enhanced the number of offspring for both monogamous and polyandrous females, (3) compared to females in lifelong monogamy, polyandrous females paired daily with a novel, age‐matched experienced male produced offspring of enhanced viability, and (4) female survival was unchallenged when monogamous and polyandrous females could re‐mate with age‐ and experienced‐matched males. (5) Polyandrous females daily paired with novel virgin males had significantly reduced lifespans compared to polyandrous females with novel, age‐matched, and experienced males. (6) Polyandrous mating enhanced offspring viability and thereby weakened support for the random mating hypothesis for female multiple mating. Analyzes of nonequivalence of variances revealed opportunities for within‐sex selection among females. Results support the idea that females able to avoid constraints on their behavior from simultaneous exposure to multiple males can affect both RS and survival of females and offspring.     

Social relationships and social structure of the mound-building mouse (<Emphasis Type="Italic">Mus spicilegus</Emphasis>) in intraspecific cage groups

The social relationships of Mus spicilegus were studied in intraspecific cage groups for a month during the reproductive period to clarify the role of intraspecific aggressiveness in shaping social structure and in reproduction. The mound-building mice were captured from a wild population in northern Bulgaria. A total of 13 groups, 5 male, 4 female, and 4 male–female groups, were tested. Each group consisted of five unfamiliar adults. The experiments were carried out in 100×100-cm glass cages. The patterns of behaviour and the dominant–subordinate structure within each group were investigated. A dominance index for every individual in the group was calculated. During the period of establishment of the hierarchical structure in the groups a high level of aggressiveness was registered among individuals. About half of the subdominants and subordinates were found dead, with or without obvious marks of injury. Male–male interactions were more aggressive compared to these of females. Dominant–subordinate relationships between individuals of the same sex were observed in the mixed groups. A link between dominance rank and reproduction was established. The dominant male and the dominant female formed a pair and started to breed. Based on these findings it can be assumed that the aggressiveness of M. spicilegus is an adaptation to its life in the fields, where dominance is likely to be an essential factor in individual reproductive success. It is likely that the successful rearing of offspring in natural populations, which are exposed to strong biotic and abiotic impact, necessitates the existence of monogamous relationships. Communicated by P. Gama Mota     

Testosterone Manipulation of Male Attractiveness has no Detectable Effect on Female Home-Range Size and Behavior During the Fertile Period

Female dark‐eyed juncos (Junco hyemalis) are socially monogamous, but they engage in extra‐pair copulations (EPCs). We examined spatial activity and behavior of female juncos during their fertile period to determine whether they engaged in tactics likely to facilitate EPCs and whether any such tactics varied with the attractiveness of their social mates. We manipulated the attractiveness of social mates by implanting experimental males with tubes containing testosterone (T‐males) and control males with empty tubes (C‐males). Previous findings in free‐living juncos showed that females mated to C‐males were more likely to produce extra‐pair young than females mated to T‐males. We radio‐tracked 13 females (eight C‐mated, five T‐mated) for an average of 15 h each over 3 d during their fertile periods. We predicted that C‐mated females, to compensate for the induced relative unattractiveness of their social mates, would foray from their territories to seek EPCs and as a result would have larger home ranges than T‐mated females. Females of both treatment groups made extra‐territorial forays, some of considerable distances, but we observed no EPCs during forays. Further, neighboring T‐ and C‐males frequently made incursions into the home ranges of T‐ and C‐mated females but we saw no EPCs during these incursions. Our ability to detect statistical differences was limited by sample size, but given that constraint, we found no detectable difference in female home‐range size in relation to the treatment of their mates, nor did other female behavior differ according to male treatment. Male behavior was significantly affected by testosterone treatment. C‐males guarded their mates more closely than did T‐males. We conclude that female juncos make extra‐territorial movements during their fertile period without regard to male attractiveness (testosterone treatment), but we found no evidence that these function as a special tactic to gain EPCs.