The roaring of southern brown howler monkeys (Alouatta guariba clamitans) as a mechanism of active defence of borders

Our study aimed to understand the function(s) of roars of southern brown howler monkeys (Alouatta guariba clamitans). The study group called almost exclusively on its range borders and preferentially on early mornings, but with no dawn peak. Intergroup encounters were associated with 88% of all sessions. Predation deterrence and regulation of access to mating partners do not seem compatible with our findings, but more work is needed to reject the latter hypothesis. Their roars seem to be related to intergroup spacing, but through an active defence of borders, instead of mutual avoidance or regular advertisement of occupancy, as proposed for other howler monkey species.     

Spatial and Diurnal Distribution of Loud Calling in Black Howlers (Alouatta pigra)

Loud calling, i.e., howling, is the single most distinctive behavioral attribute of the social system of howler monkeys (Alouatta spp.), yet no general consensus has been established regarding its function. During a 16-mo study, we investigated the degree to which howling bouts varied in duration and spatial and temporal patterns across different social contexts in three groups of black howlers (Alouatta pigra) at Palenque National Park, Mexico, to assess how howling functions in intergroup spacing. We recorded 359 howling bouts, of which 42% were spontaneous with no apparent cause, 28% followed nearby howling without visual contact with the caller(s), 25% were during intergroup encounters, and 5% were during encounters with solitary individuals. The mean duration of howling bouts was 14.8 ± SE 0.6 min. During encounters with neighboring groups or solitary individuals howling bouts lasted significantly longer than spontaneous and reply calls. Spontaneous and reply howling showed a bimodal pattern with a marked concentration around dawn and a second increase of howling in the afternoon. In contrast, howling during encounters with neighboring groups or solitary individuals occurred randomly throughout the day. In addition, howling, irrespective of the context in which it was given, occurred throughout the groups’ home ranges without concentrations in the heavily used core areas or borders of the home ranges. Our findings suggest that loud calling in black howlers functions principally in regularly announcing the occupancy of an area, and is concentrated in the morning when sound propagation is optimal.     

Patterns of range use,range defense,and intergroup spacing in moustached tamarin monkeys (Saguinus mystax)

In this paper we examine patterns of group spacing and habitat utilization in neighboring groups of marked free-ranging moustached tamarin monkeys (Saguinus mystax) inhabiting Padre Isla, a small island in the Amazon Basin of northeastern Peru, and describe the set of behavioral mechanisms used by tamarins to maintain the spatial isolation and social integrity of individual groups. Specifically, we address a series of questions regarding the importance of resource defense, mate defense, and territorial defense in intergroup interactions. From June through November 1990, we recorded 67 intergroup interactions involving members of our two main study groups. These interactions occurred at a rate of .14/observation hour and were of two general types. Vocal battles averaged 18 min in duration and were characterized by a series of high frequency, short syllable, long calls that were exchanged between groups separated by distances of greater than 25 m. Aggressive encounters averaged 26 min in duration and involved visual contact, alarm calls, scent marking, and sequences of chases and retreats. Intergroup confrontations did not cluster around the perimeter of a group's home range, and there was no evidence that moustached tamarins patrolled range borders. Our data indicate that 35% of aggressive encounters occurred in the vicinity of major feeding trees. Priority access to these sites is likely to have an important influence on tamarin foraging success. Mate defense and the exploration of new breeding opportunities also appear to be important functions of intergroup conflicts. Not only did the frequency of aggressive encounters increase during breeding periods, but three-fourths of all observed copulations occurred during or within 30 min of an encounter. Given the high degree of reproductive competition reported among tamarin females and the time and energy group members devote to intergroup aggression, maintaining access to a stable home range and the resources contained within that range appear to be critical functions of moustached tamarin social interactions.     

Causes of Intraspecific Aggression in Alouatta palliata mexicana: Evidence from Injuries,Demography, and Habitat

Although howlers have been traditionally considered to be pacific, showing one of the lowest rates of aggression among primates, new evidence is emerging to question this image. We present data on injuries in Mexican mantled howlers (Alouatta palliata mexicana) in relation to different sociecological parameters. We censused howler populations in 19 forest fragments over a 17-mo period in the Los Tuxtlas Region, southern Veracruz, Mexico. We conducted detailed observations of scars, torn lips, broken fingers, mutilated tails and other visible injuries. We also collected data on the demography, biogeography and vegetation of each fragment in order to relate injury data to them. We censused 333 howlers, of which we exhaustively observed 254 for injuries. Four resident adult females (n = 108) and 29 adult resident males (n = 76) had injuries, while none of the solitary males (n=16), solitary females (n=1), juveniles (n=23) and infants (n=30) had them. We discuss possible interpretative scenarios for the distribution of injuries. Although some results suggest that food resource concentration may determine intergroup agonistic encounters, we propose that physical injury is primarily associated with male-male agonistic encounters during takeovers, and consequently it could indicate migration among troops.     

Increased Frequency of Intergroup Encounters in Wild Bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>) Around the Yearly Peak in Fruit Abundance at Wamba

Intergroup interactions in primates vary from nonagonistic to severely aggressive. Food resources and fertile females cause intergroup aggression when groups defend resources and mates from other groups. Peaceful intermingling during intergroup encounters is rare but has been reported in several primates, including bonobos (Pan paniscus). Although intergroup encounters in bonobos occur at both nonprovisioned and provisioned sites, provisioning may be one factor responsible for frequent intergroup encounters. We studied intergroup encounters between one bonobo group (PE) and its neighboring groups, one semihabituated and two habituated groups, under nonprovisioned conditions in 2010–2015 at Wamba, Democratic Republic of Congo. We examined whether fruit abundance and females with sexual swellings influenced encounter frequency. PE group encountered the other groups on 7.1 days (mean, range: 0–19) per month. Up to four different groups met simultaneously at one location. Encounter frequency was highest around the yearly peak in fruit abundance, suggesting that reduced food competition is linked to increased encounter frequency. During periods of relatively low fruit abundance, the probability of an encounter was higher when a higher number of adult females with maximum sexual swellings were present, suggesting that the attractiveness of females with sexual swellings promoted group encounters during periods of relatively low fruit abundance. These findings suggest that both competition for food and the availability of females with sexual swellings influence encounter frequency in bonobos.     

Intergroup encounters in wild white-faced capuchins (Cebus capucinus)

Wrangham (1980) hypothesized that knowledge of the nature of intergroup encounters is crucial to understanding primate social relationships and social organization. I studied a single social group of wild white-faced capuchins over a period of 26 months and observed 44 encounters between social groups during 3703 hr of observation. All intergroup encounters consisted of predominantly hostile social interactions. However, nonaggressive interactions between males of different social groups occurred in a few cases. Adult males were the sole participants in 39 encounters and the primary participants in all 44 encounters. The alpha male was the most frequent participant. High-ranking females participated aggressively in five encounters, and low-ranking females never participated. There was no stable intergroup dominance hierarchy. I hypothesize that the need for male-male cooperation in intergroup aggression is an important factor influencing the quality of intragroup male-male relationships. Behavior during intergroup encounters is consistent with the idea that intergroup behavior is related to male reproductive strategies, but inconsistent with the idea that intergroup aggression is related to female defense of resources. The possibility that males are “hired guns” (Wrangham, 1980) cannot be ruled out.     

Sociality in Callithrix penicillata: II. Individual Strategies During Intergroup Encounters

In social animals, intergroup interactions, whether through agonistic and competitive behaviors or affiliative ones, can influence important parameters such as home range, territory sizes, and access to resources, which may directly affect both female and male fitness. We studied the intergroup interaction patterns of a wild group of black-tufted-ear marmosets (Callithrix penicillata) in central Brazil. Agonistic interactions occurred at low frequencies during intergroup encounters. The marmosets directed agonistic interactions without physical aggression primarily against same-sex individuals, suggesting that male and female aggression patterns are shaped by their sexual interests. However, females of the focal group also directed agonistic behavior toward extragroup males that attempted copulation. The marmosets appeared to use intergroup encounters to gather information about possible partners and extragroup reproductive opportunities. Intergroup sexual interactions occurred mainly in the form of copulations or attempted copulations by all adults, with the exception of the dominant female. Our results suggest that a possible reproductive strategy used by males is to attempt fertilization of extragroup females. Adult males copulated with the same extragroup female during several opportunities, which suggests sperm competition or the establishment of social bonds with neighboring females.     

Intergroup Relationships in Western Black-and-White Colobus, <Emphasis Type="Italic">Colobus polykomos polykomos</Emphasis>

We investigated patterns of intergroup relationships in western black-and-white colobus, Colobus polykomos, in Taï National Park, Côte d'Ivoire, between 1993 and 1999. They live in one-male multifemale units, and demonstrate male dispersal and occasional dispersal by females. Solitary males and all-male bands are absent or very rare. Our aim was to investigate the function of female and male aggression during intergroup interactions. The species is particularly interesting because, in contrast to predictions from socioecological models, female aggression occurs during intergroup interactions in combination with female dispersal. Home ranges of neighboring groups overlapped considerably and groups lacked an area of exclusive access. Intergroup interactions occurred once every 6.6 observation days. Encounters were either peaceful (12%), or involved displays and threats (25%) or chases and fights (63%). Females interacted in 74% and males in 98% of aggressive intergroup encounters. We found little to no indication that male and female aggression correlated with the presence of food, importance of a location, or presence of infants or receptive females. However, females were more often aggressive during the months when the group depended strongly on seeds from Pentaclethra macrophylla. We also observed forays by males to other groups. Forays occurred on average once every 20 observation days. In 75% of the forays, the intruding male chased members of the target group. In 25% of the forays 1–3 females joined their male but females never attacked the target group. Our main study group was the target of such forays significantly more often when young infants were present in the group than when not. We conclude that female aggression between groups was related to food procurement and that male forays might be related to infanticide.     

Neighbor effects in marmosets: social contagion of agonism and affiliation in captive Callithrix jacchus

Researchers have demonstrated the neighbor effect for affiliative and agonistic neighbor vocalizations in captive chimpanzees. We extend the investigation of the neighbor effect to New World monkeys, Callithrix jacchus. We collected data on vocalizations and behaviors of 31 focal individuals and concurrent neighbor vocalization within three behavioral categories: intragroup and intergroup aggression and intragroup affiliation. We investigated whether there was an influence of neighbor vocalizations on focal behavior within the same behavioral category. For data analysis we used approximate randomization of paired‐sample t‐tests. We found that marmosets performed intergroup aggressive behavior (bristle, anogenital present for neighbor loud shrill only) for significantly longer, and emitted significantly more intergroup agonistic vocalizations (twitter, loud shrill), at a high frequency of intergroup agonistic neighbor vocalizations (twitter, loud shrill) than at low. The marmosets were also significantly more likely to engage in bristle behavior immediately after hearing a neighbor intergroup aggressive call (twitter, loud shrill) than directly beforehand. High neighbor intragroup agonistic calls (chatter) were associated with significantly longer spent in related behavior (composite of: attack, chase, steal food). Affiliative behaviors (share food, grooming invite) were engaged in by marmosets for significantly longer at higher frequencies of affiliative neighbor chirp calls than at low. Marmosets were also significantly more likely to perform food sharing and active affiliative contact immediately after rather than before hearing a neighbor chirp call. Our findings suggest that neighbor vocalizations influence marmoset behavior through social contagion and indicate that the neighbor effect for affiliation and aggression generalizes to the marmoset. Am. J. Primatol. 72:549–558, 2010. © 2010 Wiley‐Liss, Inc.     

Sex Differences in the Song of <Emphasis Type="Italic">Indri indri</Emphasis>

In some primate species, males and females within a social group emit loud calls in a coordinated manner or chorus. Indri indri emits a very conspicuous loud call that elicits the loud calls of neighboring groups. Previous investigations have hypothesized that the main functions of the indri chorus are related to territorial announcement, intergroup avoidance, and group cohesion. We investigated sex differences in indri song. We recorded and analysed songs given by 10 different groups over 160 d. Overall singing duration did not vary between the sexes. However, males emitted significantly fewer but longer notes. Adult males and females of each group participated in the song with sex-specific repertoires. Females had a song repertoire of 8 note types; males shared all of their 6 notes with females. Apart from the initial roars, in all note types shared by both sexes, male notes were significantly longer than female ones, whereas variations in frequency parameters differed according to the note type. These findings suggest that indri song may provide cues to conspecifics, such as group size and sex composition, which could influence interactions between groups.     

Aspects of Male Competition in <Emphasis Type="Italic">Colobus vellerosus</Emphasis>: Preliminary Data on Male and Female Loud Calling,and Infant Deaths After a Takeover

Male Colobus vellerosus are the main participants in intergroup encounters, and lead incursions in neighboring groups during which they attack infants. Extragroup copulations, all-male groups, and male takeover occur in the species. Here, we provide additional information on behaviors associated with male reproductive competition in Colobus vellerosus. We examined 1 resident male loud calling and participation in intergroup encounters in relation to a takeover. We also report a second case of takeover that led to the death of the former resident male and the death of 2 male infants, presumably as a result of aggression from the all-male group. The new resident male wounded the third infant of the group, which apparently died after its mother abandoned it. During the period characterized by the attacks on the infant and after its disappearance, females initiated and participated in loud call bouts with the new resident male. We examine the possible functions of female loud calling, and suggest that in this context, it might force the resident male to call along to indicate his presence.     

Intergroup encounters in wild moor macaques (<Emphasis Type="Italic">Macaca maurus</Emphasis>)

We studied intergroup encounters among moor macaques at the Karaenta Nature Reserve, South Sulawesi, Indonesia. Group B has been observed on the basis of individual identification since 1988. We analyzed 85 encounters between members of Group B and members of neighboring groups from September 1990 to November 1998. The average frequency of intergroup encounters was 0.035/hour. Neither the presence of females in estrus nor rainfall had an effect on encounter frequency. Behaviors of moor macaques during intergroup encounters differed from those of Japanese macaques. In moor macaques, no intergroup interactions with body contact were observed during encounters, and females never directed aggression toward members of different groups. The present study did not confirm the prediction of the model ofvan Schaik (1989). Extension of the existing models is required to explain the difference in female dominance styles among macaques by socioecological factors.     

Interspecific Infanticide and Infant‐Directed Aggression by Spider Monkeys (Ateles hybridus) in a Fragmented Forest in Colombia

Interspecific aggression amongst nonhuman primates is rarely observed and has been mostly related to scenarios of resource competition. Interspecific infanticide is even rarer, and both the ultimate and proximate socio‐ecological factors explaining this behavior are still unclear. We report two cases of interspecific infanticide and five cases of interspecific infant‐directed aggression occurring in a well‐habituated primate community living in a fragmented landscape in Colombia. All cases were initiated by male brown spider monkeys (Ateles hybridus) and were directed toward infants of either red howler monkeys (Alouatta seniculus: n = 6 cases) or white‐fronted capuchins (Cebus albifrons: n = 1 case). One individual, a subadult spider monkey male, was involved in all but one case of interspecific infanticide or aggression. Other adult spider monkeys participated in interspecific aggression that did not escalate into potentially lethal encounters. We suggest that competition for food resources and space in a primate community living in high population densities and restricted to a forest fragment of ca. 65 ha might partly be driving the observed patterns of interspecific aggression. On the other hand, the fact that all but one case of interspecific infanticide and aggression involved the only subadult male spider monkey suggests this behavior might either be pathological or constitute a particular case of redirected aggression. Even if the underlying principles behind interspecific aggression and infanticide are poorly understood, they represent an important factor influencing the demographic trends of the primate community at this study site. Am. J. Primatol. 74:990‐997, 2012. © 2012 Wiley Periodicals, Inc.     

Intergroup calls of male pig-tailed langurs (Simias concolor)

Pig-tailed langurs (Simias concolor) were observed in the Pagai Islands and in Siberut. They lived in 1-male groups containing from one to five or more females plus their young. Adult males produced loud vocalizations of the sortGautier andGautier (1977) called “type 1 loud calls.” The pig-tailed langur's type 1 loud call (TOLC) was a series of 2 to 25 nasal barks, the loudest of which could be heard for 500 m or more in the rain forest. Exchange of TOLC's between males was the only frequent intergroup interaction. Fifty-one percent of TOLC's were emitted spontaneously, 33% occurred in response to TOLC's of other males, 13% to falling trees, 4% in response to thunder, and 1% during a fight between males of different groups. Although TOLC's occurred throughout the day, they exhibited a bimodal distribution, with a peak of calling early in the morning, and another in late afternoon. Tape-recorded TOLC's played back in the field stimulated males hearing them to emit TOLC's of their own. Barks in experimentally-elicited TOLC's were delivered at a faster rate than barks in other TOLC's were. While TOLC's mediate intergroup communication among males, field playback experiments are needed to truly elucidate their functions.     

Loud calls of adult male red howling monkeys (Alouatta seniculus)

Loud calls of adult male red howlers (Alouatta seniculus) inhabiting a deciduous and semideciduous open woodland site in Venezuela were recorded opportunistically and categorized by ear and sonographically as barks and roars. Five to six different bark syllables were identified as occurring singly or in sequences of doublets and triplets. In barks, spectral energy was concentrated in bands at 350-400 Hz, 900-1,100 Hz, 1,800-2,200 Hz and 3,000-3,500 Hz, but not all higher bands were present in each syllable. Roars appeared sonographically like prolonged barks composed of a pulsated preface, a long legato climax and a brief, fractionated and at times pulsated coda; each part varied internally to the ear and in acoustic structure. All loud calls were of the noisy type (nonharmonic energy over a broad frequency range). Acoustic characteristics of the calls are interpreted in terms of the subserving vocal tract anatomy. I compare loud calls of red howlers with those of mantled (A. palliata) and black (A. caraya) howlers.     

Sex differences in leadership during group movement in mantled howler monkeys (Alouatta palliata)

Benefits of group life depend in large part on whether animals remain cohesive, which often requires collective decisions about where and when to move. During a group movement, the leader may be considered as the individual occupying the vanguard position of the group progression, when its movement evokes following by other group members. In nondespotic societies, individuals with greater incentives to move frequently are leaders. During 15 months of observations (1,712 contact hours), we investigated two mantled howler monkey (Alouatta palliata) groups at La Flor de Catemaco (Los Tuxtlas, Mexico) to examine whether sex and female reproductive state influenced leadership likelihood in two contexts: movements toward feeding trees; movements associated with loud calls, a group-defense behavior used by males of this genus. Females led and occupied forward positions during group movements toward feeding trees more often than adult males. Adult females led these movements more frequently when they were gestating than when they were lactating or cycling. There were no differences between sexes in the leadership of group movements associated with loud calls. Leadership by gestating females is perhaps the result of their higher nutritional/energetic needs when compared with cycling females, and of their greater mobility when compared with lactating females carrying dependent offspring. Female leadership during movements toward feeding trees may be a mechanism to optimize access to food resources in mantled howler monkeys.     

Consequences of lethal intragroup aggression and alpha male replacement on intergroup relations and home range use in tufted capuchin monkeys (Cebus apella nigritus)

In conflicts between primate groups, the resource-holding potential (RHP) of competitors is frequently related to group size or male group size, which can remain relatively constant for long periods of time, promoting stable intergroup dominance relationships. Demographic changes in neighboring groups, however, could introduce uncertainty into existing relationships. Among tufted capuchin monkeys (Cebus apella nigritus), dominant male replacement is a relatively infrequent demographic event that can have a profound effect on both the composition and size of the social group. Here, we report such a case and the consequences for home range use and intergroup aggression. Between June 2008 and August 2010, we periodically followed two neighboring groups (Macuco and Rita) in Iguazú National Park, recording daily paths (N = 143) and encounters between the groups (N = 28). We describe the events leading to a change in the male dominance hierarchy in the larger group (Macuco), which resulted in the death or dispersal of all adult males, followed by the succession of a young adult male to the dominant position. This takeover event reduced the numerical advantage in number of males between the two groups, although the ratio of total group sizes remained nearly constant. Following this shift in numerical asymmetry, the degree of escalation of intergroup aggression increased, and we observed reversals in the former intergroup dominance relationship. These changes in behavior during intergroup encounters were associated with changes in the use of overlapping areas. In the 6 months following the takeover, the area of home range overlap doubled, and the formerly dominant group's area of exclusive access was reduced by half. These results suggest that RHPin tufted capuchin monkeys is related to male group size. Furthermore, they highlight the importance of considering rare demographic events in attempts to understand the dynamics of aggression between primate groups.     

Individual participation in intergroup contests is mediated by numerical assessment strategies in black howler and tufted capuchin monkeys

Asymmetries in resource-holding potential between opposing groups frequently determine outcomes of intergroup contests. Since both numerical superiority and high intergroup dominance rank may confer competitive advantages, group members should benefit from assessing the relative strength of rivals prior to engaging in defensive displays. However, differences in individual assessment may emerge when cost–benefit trade-offs differ among group members. We examine the influence of numerical superiority and intergroup dominance relationships on individual participation in intergroup encounters in black howler monkeys (Alouatta pigra) and tufted capuchin monkeys (Sapajus nigritus). Black howlers responded with longer vocal displays during encounters with neighbours with an equal number of resident males, while tufted capuchins increased their participation with increasing relative male group size. Within each species, males and females responded similarly to varying numerical odds, suggesting that despite pay-off asymmetries between males and females, both sexes were similarly influenced by numerical asymmetries in deciding to participate in collective group defence. Whereas the outcome of contests among tufted capuchins was determined by relative male group size, reflected in a pronounced intergroup dominance hierarchy, the absence of dominance relationships among black howler groups may have provoked prolonged vocal displays in order to assess rival groups with matching competitive abilities.     

Intergroup loud calls,range size,and spacing in Callicebus torquatus

Observations are reported on the response of a free-ranging group of Callicebus torquatus to recordings of loud intergroup calls. When the recording consisted of the call of a solo adult male, the group fled from the recording. When the recording consisted of the adult male and female duetting together, the group remained in place and called back to the recording. These results contrast with previously described vocal and spatial responses of C. moloch and suggest that range size influences the mechanisms that regulate between-group spacing. The consequence of intergroup loud calls in C. moloch is to define and reinforce the location of boundaries, whereas in C. torquatus, homologous calls maintain spacing between groups.     

Lethal intergroup aggression by chimpanzees in Kibale National Park, Uganda

Chimpanzees (Pan troglodytes) have hostile intergroup relations throughout most or all of their geographic range. Hostilities include aggressive encounters between members of neighboring communities during foraging and during patrols in which members of one community search for neighbors near territory boundaries. Attacks on neighbors involve coalitions of adult males, and are sometimes fatal. Targets include members of all age/sex classes, but the risk of lethal intergroup coalitionary aggression is highest for adult males and infants, and lowest for sexually swollen females. The best-supported adaptive explanation for such behavior is that fission-fusion sociality allows opportunities for low-cost attacks that, when successful, enhance the food supply for members of the attackers' community, improve survivorship, and increase female fertility. We add to the database on intergroup coalitionary aggression in chimpanzees by describing three fatal attacks on adult males, plus a fourth attack on an adult male and an attack on a juvenile that were almost certainly fatal. Observers saw four of these attacks and inferred the fifth from forensic and behavioral evidence. The attackers were males in two habituated, unprovisioned communities (Ngogo and Kanyawara) in Kibale National Park, Uganda. We also summarize data on other intercommunity attacks at Ngogo. Our observations are consistent with the "imbalance of power" hypothesis [Manson & Wrangham, Current Anthropology 32:369-390, 1991] and support the argument that lethal coalitionary intergroup aggression by male chimpanzees is part of an evolved behavioral strategy.