Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): Ground nests,parking, and biparental guarding

Over a 4 month period, systematic and ad libitum observations were conducted on two adult female black-and-white ruffed lemurs (Varecia variegata variegata) and their infants in a 3.5 ha forest enclosure. The females were mother and daughter, members of a family group that had been semifree-ranging for 2 years and 3 months at the time of the births. One to two weeks before parturition, the females independently constructed nests, in which they kept their infants during the first few weeks following parturition. The older mother, cage-reared herself, prepared at least one nest. Her daughter, who has lived in the forest since late juvenescence, prepared at least four. Two to three weeks after parturition, the mothers moved their infants high into trees. During periods of maternal absence, the infants were often alone, and they rarely or never moved, vocalized, or groomed themselves. The mothers often kept their infants together after nests were no longer used. Each infant nursed freely from both lactating females. The infants were carried orally only by their mothers and were never transported by clinging to the pelage of any group members. Previously, researchers suggested that ruffed lemurs build nests for care of infants high up in trees. The present observations, however, suggest that two major modes of neonate care in Varecia exist: serial use of multiple ground nests and “parking” of infants high in trees. Advance preparation of several nest sites, relative lack of large predators, alternate maternal and paternal guarding of infants, infant immobility during absence of mother, and rapid infant development make this tactic of care for neonates plausible.     

The nature and frequency of agonism in free-ranging and semi-free-ranging brown lemurs,Eulemur fulvus

Agonistic behaviour was studied in three groups each of free-ranging and semi-free-ranging brown lemurs (Eulemur fulvus) at Berenty, Madagascar and the Duke University Primate Center (DUPC) respectively. The purpose of the study was to answer questions arising from the work of other researchers regarding the frequency and intensity of agonism in this species. Authors of field studies generally concluded that agonism was rare and mild, whereas those who had studied semi-free-ranging or captive animals at the DUPC reported intense agonism during the peaks of the mating and birth seasons, with sometimes fatal wounding occurring among captive animals. I recorded 30 agonistic behaviours or “signals” which I grouped into seven general categories — cuffs, other physical contact, threats, chases, third party intervention, unprovoked submissive signals, and reciprocal aggression. The seven categories represent the types of signals which initiated or otherwise defined agonistic interactions, regardless of whether or not there was a submissive response to aggression. The relative percentages of all agonism constituted by the seven categories were not found to be significantly different between study sites. Agonistic signals were also classified as either subtle or obvious, a classification which crosscut the seven categories. At both study sites, the majority of agonistic signals initiating or defining interactions were subtle. Rates of agonism for the Berenty groups, studied during the birth season only, were significantly lower than those for the DUPC groups during the birth season, possibly due to (1) easier observation conditions at the DUPC, and (2) the impossibility of successful emigration at the DUPC, which might have resulted in social stresses translating into higher rates of agonism. In only one DUPC group was there significant variation in rates of agonism between seasons. I found agonistic behaviour to be mild, at both study sites, in the senses of subtlety of both aggressive and submissive signals, unlikelihood of response to aggression, and virtual absence of wounding; and I noted that serious wounding during other studies at the DUPC involved animals captive in caged runs. Comparing rates of the study groups with rates reported in other research for brown lemurs, other lemuriform species, and some New and Old World anthropoid species, I concluded thatE. fulvus agonism was in fact not rare except in comparison to baboons and macaques.     

A comparative study of breeding seasonality and litter size in eleven taxa of captive lemurs (Lemur andVarecia)

Breeding records of 11 taxa of captive lemurs housed at the Duke University Primate Center (DUPC), North Carolina, were analyzed for differences in the timing of births, for the relationship between breeding season and photoperiod, and for differences in litter size. At DUPC there are significant differences in the timing of births among certain taxa, including differences among some subspecies of Lemur fulvus.However, changes in latitude result in changes in the timing of the breeding season. Lemurs moved to higher latitudes mate at lower light-dark ratios than on Madagascar. The data presented here are consistent with the following model: a photoperiodic cue initiating reproductive activity, presumably a light-dark threshold, precedes the actual mating season by approximately 2 months, with an intervening period of physiological and social preparation. On Madagascar, selection may have favored births that coincide with the end of dry seasons and the beginning of wet seasons, which results in lactation and weaning during times of resource abundance. Taxa from the north and east have the highest mean litter sizes; those from the west have the lowest.     

Baby-transfer and other interactions between its mother and grandmother in a captive social group of lowland gorillas

This report describes the responses of an experienced gorilla mother to inappropriate maternal behavior displayed by her young adult daughter toward a newborn baby and repeated acts of baby-transfer between these two females in a captive social group of lowland gorillas (Gorilla g. gorilla). The quality of infant care by the young adult daughter clearly improved during the first 4 days after birth, and this improvement was at least partly based on her mothers encouragement. Thus, the mothers activities can be considered scaffolding for her daughter with regard to maternal infant care.     

Troop fission in wild ring-tailed lemurs (Lemur catta) at Berenty, Madagascar

A detailed fission process in a wild ring-tailed lemur (Lemur catta) troop was observed at Berenty Reserve, Madagascar. The troop fission occurred as follows: 1) During the birth season in 2000, two adult females (mother and daughter) were evicted as a result of "targeted aggression" (i.e., intense and persistent aggressive behavior toward particular individuals). 2) Two adult and three immature females in the same kin group as the evicted females spontaneously immigrated into the new group. 3) A male immigrated into the new group 1.5 months later. 4) The new troop successfully established its own home range. This report exemplifies three characteristics of troop fission in ring-tailed lemurs. First, targeted aggression initiated the fission process. Second, the troop females divided along matrilineal lines. Finally, no male played a specific role in the fission process.     

Social Behaviour of the Carpenter Bee Xylocopa pubescens (Spinola)

The development of about 20 relatively small nests of Xylocopa pubescens was studied. After the first offspring had become adult, these nests reached a social stage in which there was only one egg-layer per nest. Freshly emerged (teneral) adults eat a lot of food, collected by a forager, before they fly out of the nest. This food appears to be of major importance to these bees in that it makes them fully agile. It seems therefore, that part of the food needed for the development of a young bee is not given at the larval stage, via the beebread, but at the teneral adult stage. As a result of this, a necessary overlap of generations is accomplished. Besides, less pollen has to be collected for the provision of a brood cell, so more cells can be constructed within a short period of time. There is a high degree of nest competition. Many nests were taken over by conspecific individuals (or by females of X. sulcatipes) that were searching for nesting sites within the study area. However, although more than 50% of the solitary nests were taken over sooner or later, strangers hardly ever intruded into social nests, with more than one adult. This illustrates how important it is for a reproducing female to tolerate the presence of nestmates which guard the nest in her absence. Although in most cases the foundress of a nest proceeded to produce new brood in the presence of her offspring, it happened that a daughter took over reproduction from her mother. In two of these cases, it could be observed that a mother started a new nest elsewhere after having been thrown out by her own daughter. At least in these cases, nest competition between mother and daughter started long before the mother had reached the end of her reproductive capacities. Since nesting possibilities are scarce, it seems a logical strategy to stay in the maternal nest and wait for a chance to become the egg-layer if the mother dies or if she loses her dominance. The occurrence of several social interactions among nestmates is discussed: — trophallaxis was observed often, not only under ‘forced’ conditions, but also as a form of ‘voluntary’ feeding; — nestmates were observed to groom each other.     

Observations on reproduction,hormones, copulatory behavior,and neonatal mortality in captive Lemur mongoz (Mongoose lemur)

This study examines correlates of reproduction in Lemur mongoz, an endangered prosimian primate with a history of poor captive reproduction. Male testicular growth and regression were quantified via testicular indices (TI). Although TIs could be used to predict male breeding condition, they were not indicators of ability to sire offspring. Serum estradiol (E₂) and progesterone (P) concentrations, along with vaginal cytology, were used to monitor female reproductive cyclicity. E₂ and P profiles showed no abnormalities. An elevation of E₂ with low P, approximately one estrous cycle length (31.4 days) prior to the onset of fertile cycles, was consistent with the phenomenon of ‘pseudoestrus’ observed in other lemur species. The copulatory pattern, consisting of thrusting, multiple intromissions, single or multiple ejaculations, and no copulatory lock, was more complex than expected for an animal with a supposedly monogamous mating system. The preference for natural arboreal substrata during copulation suggests that enclosure furnishings may influence copulatory behavior. A 30% neonatal mortality rate tempered recent success in breeding L. mongoz at the Duke University Primate Center (DUPC). Although infant sex and parity of the mother were not predictive of neonatal mortality, mother's natal status was, with captive-born females having a 67% infant mortality rate, compared with 15% in wild-caught females. Based on these observations, a number of factors, including housing, behavior, and photoperiod, may be relevant to successful captive propagation of L. mongoz. © 1992 Wiley-Liss, Inc.     

Avian nest predation by a semi-captive collared lemur (Lemur fulvus collaris)

A lemur (Lemur fulvus collaris) in a semi-captive group of six animals at the Duke University Primate Center (DUPC) was observed eating an egg from the nest of a mourning dove (Zenaida macroura). The manner in which the animal had been foraging prior to this incident, and the fact that wild birds at the DUPC frequently direct antipredator behaviors, such as mobbing toward thisL. f. collaris group, suggest that nest predation is part of normal foraging behavior in these animals.     

Reproductive activity of ruffed lemurs (Varecia variegata variegata) in a Madagascar rain forest

Mating activity was observed during four breeding seasons in two groups of black and white ruffed lemurs (Varecia variegata variegata) living in lowland rain forest on Nosy Mangabe island, Madagascar. The onset of the May-July breeding season was signalled by behavioral changes in adult males. Males made forays outside their usual home ranges, were more aggressive to other males, and performed appetitive and other sex-specific behaviors more frequently. Females showed receptive and proceptive behaviors during a 1-2 day behavioral estrus. Ruffed lemurs mated monogamously, polyandrously, and polygynously. These observations do not support previous assertions that they live only in monogamous families. Limited evidence suggests females exercised mate choice and may have preferred familiar males. © 1993 Wiley-Liss, Inc.     

Third-party grooming in a captive chimpanzee group

Social grooming is ubiquitous among the captive chimpanzees at Chester Zoo. Seven individuals were chosen here for a study of third-party social dynamics. The grooming decisions of five adult males were analysed, but only insofar as they directed attention to a mother–daughter pair. Uniquely, the daughter was an unpopular and physically disabled subadult whose congenital motor impairments prevented her from grooming others effectively. The impetus for this study was the observation that some males increased their grooming towards the disabled daughter during days when the mother had a tumescent anogenital swelling (sexually attractive to males) compared to days when the mother was not tumescent (less attractive). Apparently, males were grooming the daughter with no possibility of payback (because the daughter could never “return the favour”). A “grooming rate” (avg. grooming time/hour) was calculated that showed the grooming efforts of all five males towards both mother and daughter. These rates were compared on days when (1) the mother’s anogenital swelling was tumescent, and (2) days when the swelling was not tumescent. Each male showed a different pattern of behaviour. Two males groomed the daughter significantly more when the mother was tumescent. Results for all males were graphed against the quality of the social relationship between each male and the mother. Apparently, only males that had a weaker relationship to the mother groomed the daughter more when the mother was tumescent. This pattern did not exist for males with a stronger relationship to the mother. Possibly, the insecure males were using the disabled daughter as a way to curry favour with the attractive mother. If this is confirmed, then this type of triadic situation is a possible setting for indirect reciprocity to occur.     

Dominance relations in captive groups of adult and juvenile arctic blue foxes (Alopex lagopus)

Dominance relationships were studied in captive Arctic blue fox (Alopex lagopus) groups comprising adults (four males, five females) and juveniles (four males, five females). The results showed that Arctic blue foxes easily formed a social organization with an observable hierarchy, in which adults typically dominated over juveniles. Within the same age group, males usually dominated over females. Dominance correlated most significantly with body weight in autumn, but later that correlation decreased. Urine marking activity was very low during autumn and early winter, but increased significantly prior to and during the breeding season when aggressive encounters were also most pronounced. In addition to several adults, the social status of some juveniles was high at breeding time. Altogether 7 out of 11 females (63.6%) whelped, but the survival rate of litters was low and kits of only two adult females survived (18.2%). It can be concluded that hierarchical development and reproduction in Arctic blue fox groups are markedly influenced by dominance relationships.     

Juveniles Outrank Higher-Born Females in Groups of Long-Tailed Macaques with Minimal Kinship

In a typical matrilineal or nepotistic hierarchy a mother's rank sets both her daughter's lowest rank (above lower-born females), and her daughter's highest rank (below the mother and higher-born females). Long-tailed macaques (Macaca fascicularis) form typical matrilineal dominance orders. We report a variant of this system that we observed in 4 groups of captive long-tailed macaques characterized by an unusual kinship structure. Each group was composed of the smallest possible matrilineages (mother-offspring pairs), the mothers being unrelated to each other. In each group, juveniles ranked above all the females subordinate to their mother, as this is the case in a typical matrilineal hierarchy, but a majority of juveniles of both sexes outranked their own mothers and/or several higher-born females and their offspring. Adult females resisted the juveniles and were 2.5 times heavier than the latter. The patterning of interventions in conflicts suggests that this unusual ranking pattern resulted from the existence of bridging alliances between the juveniles and individuals ranking above the juveniles' targets. The results indicate that the sole presence of the mother is sufficient for a daughter to outrank the females subordinate to her mother, but it is not sufficient to prevent the daughter from ascending the rank order. Our data suggest that in the absence of extensive alliances among kin, which normally stabilize the rank order, juveniles were able to benefit from infrequent, opportunistic interventions by high-ranking nonkin individuals.     

Seasonal influence on reproduction in chimpanzees of gombe national park

Although wild chimpanzees are not seasonal breeders, there are seasonal effects on several aspects of chimpanzee reproduction. I examined the seasonal incidence of anogenital swelling in cyclic, pregnant, and acyclic female chimpanzees in Gombe National Park, May 1975–April 1992, and surveyed important reproductive events to determine whether there is a seasonal effect. I analyzed data by season (wet vs. dry) and seasonal quarter;early dry season = May–July;late dry = August–October;early wet = November–January;late wet = February–April. When data for the 17 years are combined, the percentage of females in each reproductive state remains consistent throughout the year. In a given month, 30–35% of subjects were in the cyclic category, 11–15% were pregnant, and 54–61% were acyclic. Cyclic females showed full swelling more often during the late dry season. Pregnant females exhibited anogenital swelling more often during the late dry and early wet seasons. Acyclic females also exhibited a seasonal effect with more anogenital swelling during the late dry season. There is no seasonal difference in frequency of live births (dry, 20;wet, 23). However, the timing of conception showed a seasonal effect (dry, 32;wet, 16). Consistent with earlier reports, the onset of postpartum cycles is highly seasonal;30 occurred during dry season, 9 during wet season. The occurrence of first full swellings for young females is also concentrated in the late dry season. It appears that the dry season is a time of great change for Gombe chimpanzee reproductive physiology. Previous studies indicated that seasonal changes in food availability play a role in increasing group size during the dry season and social contact between females can enhance cyclicity. Accordingly, I suggest that seasonal changes in diet may play a role, either directly (food content) or indirectly (social contact), to alter reproductive physiology.     

Juvenile social play and yearling behavior and reproductive success in female Belding’s ground squirrels

Benefits of play behavior have been described for individuals during the juvenile period; however, it is less clear whether benefits of juvenile play commonly extend beyond the period of juvenile development. I evaluated possible associations between juvenile social play and yearling maternal territorial behavior and reproductive success in female Belding’s ground squirrels (Urocitellus beldingi). Higher rates of juvenile social play were associated with greater intensity of territorial aggressive and vigilant behavior during gestation but not later phases of the yearling reproductive cycle, suggesting that both juvenile play and later experience may influence maternal territorial behavior in yearling females. Juvenile social play was also a reliable predictor of whether a yearling female successfully weaned a litter, raising the possibility that juvenile play behavior influences yearling reproductive success via effects on maternal territorial behavior in female U. beldingi. Other factors were also related to reproductive success in yearling females. Body mass at the beginning of the yearling reproductive period was not correlated with juvenile social play but was associated with the likelihood of successfully weaning a litter. Yearling females whose mother was still alive were more likely to wean a litter than those whose mother was not alive. Mothers and yearling daughters tended to have maternal territories near each other, and mothers with a surviving yearling daughter expressed aggressive behavior at elevated rates and directed aggression toward intruders on the daughter’s territory. Overall, results of the study suggest that juvenile social play is among the variables that influence maternal territorial behavior and reproductive success in yearling female U. beldingi, and are consistent with the idea that juvenile play has benefits beyond the juvenile period for female U. beldingi.     

Vigilance behavior during the birth and lactation season in naturally occurring ring-tailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

I examined the vigilance behavior of adult males and females in two groups of ring-tailed lemurs(Lemur catta)during the birth and lactation season at the Beza-Mahafaly Reserve, southwestern Madagascar. I found no sex difference with respect to the rates of overall vigilance, rates of vigilance toward a potential predator or unfamiliar sound, or rates of vigilance toward conspecifics from other social groups, nor were there sex differences in the percentage of time spent vigilant in any of the above categories. Higher-ranking females were vigilant significantly more often toward predators or potential predators than lower-ranking females were. I detected no relationship between vigilance behavior and dominance rank among adult males. The alpha female in each group exhibited significantly more vigilance behavior than all other members of her group. It was predicted that males should exhibit more vigilance behavior than females do, particularly during the birth and lactation season, when predator pressure is high, if they are benefiting females in this respect. I discuss the results in the context of this prediction and in terms of how ring-tailed lemur males benefit females, and why they may be tolerated in social groups.     

Intra- and Inter-seasonal Variation in the Socio-Spatial Behavior of Adult Male Collared Lizards, Crotaphytus collaris (Reptilia, Crotaphytidae)

When individuals maintain strong inter‐seasonal philopatry to the same territories, males may be able to re‐establish territory occupancy without intense intra‐sexual aggression, and instead spend more time courting females early in the reproductive season. Furthermore, when some males have prior experience defending the same territories, it may be necessary for young males to exhibit higher levels of aggression because they are establishing a territory for the first time. We tested these hypotheses by examining within‐season (1992 and 1997) temporal variation in the social behavior of adult male collared lizards of known age and prior territorial experience in a population where inter‐season philopatry to territories is high. Contrary to expectations, the frequency of aggression exhibited by males with and without prior territorial experience did not differ. The frequency of intra‐sexual aggression was higher in 1992 than in 1997, perhaps because male competitors were more abundant in 1992. Although there was an interactive effect of year, male display and patrol were low at the beginning of the reproductive season in Apr. and May, reached peaks during midseason in June, and then decreased as reproduction ended in July. The size of territories showed a similar pattern, with males defending larger areas in June. Our data support the philopatry hypothesis in that the establishment of territories occurred without high levels of aggression early in the season, perhaps because territory boundaries have been well defined by high rates of patrol and advertisement during the middle of the previous season. Inter‐sexual interactions were most frequent in June rather than at the beginning of the reproductive season. Adult females are producing their second clutches and yearling females are producing their first clutches in June. The high rate of inter‐sexual encounters in June supports the hypothesis that males allocate more time to courtship when females are receptive because there are more reproductively active females at this time. The temporal pattern of activities in adult Crotaphytus collaris appears to function as a compromise between competing intra‐ and inter‐sexual social demands on males, allowing males to maximize mating opportunities as well as maintain future access to productive territories.     

Group changing in free-ranging male rhesus monkeys

Group changing behavior of maleMacaca mulatta was studied over a six-year period at the rhesus monkey colony on two coastal islands at La Parguera, Puerto Rico. Males first left their natal group at a mean age of 47 months and became solitary for the first time at a mean age of 64 months; all had left their natal groups by seven years of age. Age, mating season, sex ratios of adult males and females in the social bands, and geographical barriers all had significant effects on the group shifting. Population size, rank of mother or being an orphan did not significantly affect the changing process. Two factors, age (size) and seniority in the group, were important in determining a male's rank in his new group.     

Aggression with mixed age-sex groups of bolivian squirrel monkeys following single animal introductions and new group formations

The social organization of the Bolivian squirrel monkey (Saimiri boliviensis boliviensis) is thought to be sexually segregated, with males and females forming separate social groups during the nonbreeding season. To investigate the influence of this social order on patterns of aggression, controlled single animal introductions within established groups and establishment of new groups were studied in a systematic manner. Behavioral observations were made using an all-occurrences technique to sample all agonistic interactions. In study I, 4 animals of each age-sex class (adult males and females, juvenile males and females) were introduced one at a time into 4 different social groups composed of 1 adult male and 8 to 10 adult females. Behavioral observations were made prior to and after the introductions. Newly introduced adult males received significantly more contact aggression than other age classes. Only the adult females increased aggression after the introduction of new animals. In study II, new social groups were formed and behavioral observations were made following formation. One group was formed from 7 pairs of familiar females and an unfamiliar adult male. This group had a high frequency of aggression during the first half hour, with contact aggression rising to peaks at 3 and 5 h. The second group consisted of 10 familiar females, 2 pairs of familiar females and an unfamiliar male. There was a significant peak in contact aggression 3 h into the observation.     

Effects of size and sex on the courting success and foraging behaviour of Embiotoca jacksoni

To test life-history theory that body size and sex should influence how animals allocate time to foraging versus reproductive activities, we measured the effects of size and sex on courting success and foraging behaviour of black surfperch Embiotoca jacksoni off Santa Catalina Island, southern California. Observations of focal fish were made while snorkelling, during which the length of each fish (estimated to the nearest cm), total duration of courting encounters and foraging rates were recorded. We made observations during and outside the mating season. Courtship occurred only between pairs and its duration increased with the size of both the male and female. Although males would court females that were smaller or larger than themselves, pairs that were closely matched in size had long courting sessions, whereas those that differed considerably in size courted only briefly. Small fish foraged more than larger fish, both during and outside the mating season. Males and females foraged at similar rates outside of the mating season, but during the mating season males reduced their foraging rates to less than half that seen outside of the mating season, whereas females continued to forage at the same rate. This decrease in foraging rate of males during the mating season was seen in all sizes of males but was proportionally greatest in the largest males. These observations indicate that males trade off time spent on foraging for time spent courting during the mating season, whereas females do not.