Demography of Lemur catta at Berenty Reserve,Madagascar: Effects of Troop Size,Habitat and Rainfall

We censused Lemur catta within a 1 km² study area at Berenty Reserve, Madagascar, during the September–October birth season for 19 years between 1963 and 2000, a total of 290 troop counts (266 with age and sex). The non-infant population was 155 in 1972–5, fell to 105 in 1985, and rose to a maximum of 282 in 1997, while troops increased from 12 in 1972–1985 up to 25 in 1998–2000. Local density varies between habitat types from 1 per ha to ca. 6 per ha. Troops fission at ca. 15–25 individuals, or 6–10 females. Adult sex ratio has no apparent correlation with fissions, birth rate or survival. Birth rate falls steeply with number of adult females, from 80–100% in 2-female troops to about 50% in 8–10 female troops. The penalty for large troop size is greater in the dense, rich areas, but nonetheless troops there are also larger. One-year-survival does not vary with troop size, and is lower in the sparse, dry zone. Troop size is too large for optimal birth rate, but fissioning to much lower size might make troops too small for optimal adult survival, given the intense intertroop competition. This reflects Sibley's (1983) conjecture that troop sizes may not reach stable optima. Rainfall per lemur-year (beginning Oct 1) varied from 265 to 894 mm. Drought followed by rain can eliminate >90% of a cohort, especially in the dryest zone. Possibly this results from fruit failure in years following drought. It is unknown whether food supplementation of some Berenty troops is dangerous for the forest, or helpful for an isolated and vulnerable ring-tailed lemur population.     

Daytime deliveries observed for the ring-tailed lemurs of the berenty reserve, Madagascar

In the Berenty Reserve, Southern Madagascar, of the 16 deliveries recorded for ring-tailed lemurs from 1995 and 1997, 10 cases occurred during daytime hours (07:00 – 16:59). Four mothers lost contact with their troop members during parturition, but were able to rejoin them after about one hour. No attack from the individuals of the neighboring groups or predators on the mothers or their newborn infants was observed, whereas, other females of the mother’s own troop attacked them after delivery in two cases. Such daytime delivery may have originated from the circadian rhythm of the species’ nocturnal ancestors, who might have given birth during the daytime. This pattern may now be a non-adaptive feature, in agreement with the “evolutionary disequilibrium hypothesis (EVDH).”     

The social development of free-ranging infantLemur catta at Berenty reserve,Madagascar

The social development of 11 free-ranging infantLemur catta was examined over the first 16 weeks of the infants' lives. By 16 weeks, infants still occasionally suckled and were carried dorsally, but on the whole, they were independent of their mothers. Sex or mother's rank was not found to affect frequency or type of play behavior. Mother's rank had no effect on frequency of maternal rejections, from the nipple or from riding, but female infants were rejected slightly more frequently than males were. Mothers tended to reject infants more severely and more frequently from dorsal riding than from the nipple. Sex and rank differences were not found with respect to behaviors determined as measures of independence; however, lower-ranking infants engaged in significantly more dependent behaviors than higher-ranking young did. It may be necessary for the infant of a low-ranking mother to maintain closer proximity to its mother for a longer period of time during infancy because such infants may be subject to abuse by higher-ranking group members and, furthermore, may not be as readily rescued in a stressful or dangerous situation as a higher-ranking infant. Sex was not found to be a factor in terms of measures of dependence. The lack of sex differences in developmental behaviors in this species may be related to female dominance, as well as to the fact that, as adults, both sexes engage in aggressive territorial behavirs.     

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.     

Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty,Madagascar

The mating behavior of ring-tailed lemurs at Berenty, Madagascar, was observed in April 1982. Although Troop A included five adult females, only two were observed to mate. The mating period covered two consecutive days, April 24 and 25. Each female was receptive for about 4 hr. Data from 47 copulations, of which 38 were with ejaculation, suggest that to be the first mating partner is of importance for male ring-tailed lemurs. Previously it has been suggested that male dominance is of little significance in determining mating partners. In this investigation it was observed that the second most dominant male MK was always the first mating partner. Only after several ejaculations and resultant fatigue did he lose possession of the female to lower ranking males, and the first ranking male was not seen to copulate with either female at any time. These results suggest that a male's mating success is partly, but not completely correlated with his dominance rank, and that other factors, including his length of residence in the group and female choice, also determine patterns of mating.     

Maternal responses to dead and dying infants in wild troops of ring-tailed lemurs at the Berenty Reserve,Madagascar

We describe responses of seven mothers and other troop members to dead and dying infants in several troops of ring-tailed lemurs(Lemur catta) at the Berenty Reserve, Madagascar. In contrast to mothers in simian species, ring-tailed lemur mothers rarely carried their dying, immobile or dead infants. However, they sniffed, licked, and touched them even after they had died. While the dying infants were still peeping, their mothers remained near them, and 15 to 76 min after the infants ceased to peep, they were left by their mothers. Six of the seven mothers returned to their dead infants several times within the first few hours after they had left them. All seven mothers gave repeated calls, such as “mew” and “pyaa,” when they were separated from either their dead infants or other troop members or both. Thus, each mother exhibited some form of maternal behavior toward her dead infant for hours after its death. These results indicate that there may not be a great gap in terms of maternal affection between simian and prosimian mothers. We also discuss visuospatial memory ability in ring-tailed lemurs and the causes of the infants’ deaths.     

Sniffing Behavior in Lemur catta: Seasonality, Sex, and Rank

We analyzed the role of direct olfactory investigation in relation to seasonality, sex, and female rank via of a longitudinal study on 16 adult ring-tailed lemurs living in two groups at the Pistoia Zoo (Tuscany, Italy). The observations took place from May 1997 to March 1999 and lasted >1,500 h. Males were olfactorily more active than females except for skin licking, which also appeared to be associated with affiliative behaviors. Both sexes had peak frequency of direct olfactory monitoring during the reproductive season; contrarily, skin licking showed apparently random fluctuations. There is a significant positive correlation between rank and sniffing genitals performed by females on other females and a significant negative correlation between rank and sniffing genitals received: high-ranking females are mostly actors, while low-ranking females are mostly receivers. The continuous follow-up of the reproductive conditions of potential competitors suggests that sniffing genitals might play a role in female reproductive strategies.     

Social Relationships Among Ring-Tailed Lemurs (Lemur catta) in Two Free-Ranging Troops at Berenty Reserve, Madagascar

We observed two free-ranging troops of ring-tailed lemurs at the Berenty Reserve, Madagascar. Kinship affinities in these troops are known only for mothers and their offspring 4 years of age. We attempted to quantify social relationships. Almost all agonistic interactions were dyadic, and triadic agonistic interactions, such as alliances, were very rare. Dominance hierarchies in both sexes in the two troops were not linear. As in cercopithecine monkeys, mothers were dominant over their adult daughters. However, the daughters were not ranked immediately below their mothers. Close proximity and social grooming occurred more frequently between closely related females, such as mother–daughter and sister–sister dyads, than between unrelated females. Frequent-proximity relations also occurred between adult males that had emigrated from another troop and entered the present troop together, even though they did not rank closely to one another. Subordinates were likely to groom and to greet dominants more frequently than vice versa. During group encounters, particular females were involved in agonistic interactions with animals of other troops, regardless of dominance rank. Adult males, regardless of their dominance rank, but not adult females, constantly tried to drive solitary males away.     

Copulatory Plug Displacement Evidences Sperm Competition in Lemur catta

Male displacement of copulatory (sperm) plugs from female vaginas provides further evidence for sperm competition in ring-tailed lemurs (Lemur catta), a gregarious prosimian species with a multimale, multifemale mating system. During two mating seasons, I studied two groups of free-ranging ring-tailed lemurs on St. Catherines Island, GA, USA. I observed 22 mating pairs in which males achieved penile intromission. Copulatory plug displacement by males occurred in 9 cases. Plugs were displaced during copulation by male penes upon withdrawl following deep vaginal thrusting. In every case of copulatory plug displacement, the male displacing a plug mated to ejaculation with the estrous female. In a mating system in which females typically mate with more than one male during estrous, often in succession, copulatory plug displacement may function to disrupt or preclude other males' successful insemination of estrous females. The effects of sperm plug displacement on paternity in Lemur catta are unknown, as no study had heretofore documented copulatory plug displacement in this species. The first-male mating advantage suggested for Lemur catta should be re-evaluated where mating order is known, and copulatory plug displacement during mating, or lack thereof, is identified. Because there is a tendency for first-mating males to mate-guard for longer periods of time in Lemur catta, the latency period between the first mate's ejaculation and that of subsequent mates may be an important determinant of male fertilization success.     

Feeding behavior ofLemur catta andLemur fulvus

The feeding behavior of two sympatric species of lemurs, Lemur cattaand Lemur fulvus,was studied in an enclosure simulating a natural habitat at the Duke University Primate Center. L. fulvusspent less time feeding during the day than L. catta.But the former species ate more fruit and had longer feeding bouts on preferred food items than L. catta.They also had a shorter food passage time than L. cattaand their choice of resting places was more influenced by food distribution. Furthermore, the two lemur species ate parts of different plant species and showed different reactions to chemical plant components. According to these results, L. fulvusis a more conservative feeder than L. catta.These interspecific differences in feeding behavior may be one of a number of differences that allow the two species to coexist. In allopatry, however, L. fulvusmay also adopt feeding patterns similar to those of L. catta.But L. cattawas never found to change its feeding strategies in different areas. It may be this option of L. fulvusto adopt different feeding strategies in different situations that allows this species to have the widest range of all Malagasy lemurs. Duke University Primate Center Publication No. 259.     

Microhabitat Variation and Its Effects on Dietary Composition and Intragroup Feeding Interactions Between Adult Female <Emphasis Type="Italic">Lemur catta</Emphasis> During the Dry Season at Beza Mahafaly Special Reserve,Southwestern Madagascar

We compared diets and female feeding agonism in 2 groups of ring-tailed lemurs living in markedly diverse microhabitats in and near the Beza Mahafaly Reserve, Madagascar during mid-to-late gestation periods and height of the dry season to test predictions concerning differences in resource availability, preferred foods, female rank, and degree and frequency of feeding agonism in relation to usurpability and monopolization of food resources. Quadrat sampling in disturbed forest habitat revealed a greater number of plant species than in the gallery forest home range area, but females in both groups consumed nearly equal numbers of actual food plant species. Higher-ranking females in disturbed forest consumed human food scraps from the researchers camp significantly more often than low-ranking females did, while there was no rank effect for consumption of any food type between females in the gallery forest group. Higher rates of female feeding agonism in both groups occurred around usurpable fruit and leaves, as well as over monopolizable human food scraps in the disturbed forest group. There is no association between degree of agonism and food type in either group, and rate of feeding agonism is similar for both groups. The most highly contested food items came in large packages and were high in nutrients: beneficial foods for gestating females in the height of dry season in southwestern Madagascar.     

Antipredator behavior in troops of free-rangingLemur catta at Beza Mahafaly special reserve,Madagascar

Observations of antipredator behavior in two troops of free-rangingLemur catta were made during a 13-month study ofL., catta feeding ecology. Both responses to and frequency of encounters with other species were recorded. Ringtailed lemur antipredator calls differentiated between terrestrial and avian predators. L. catta responded to the Madagascar harrier hawk (Polyboroides radiatus) and the Madagascar buzzard (Buteo brachypterus) in a specific manner that differed from their reaction to the other bird of prey in the reserve, the Black kite (Milvus migrants) and to potential mammalian and reptilian predators. Encounters with avian predators peaked during the birth season and when infants were being weaned. These periods coincide with previously observed nesting periods for the Harrier hawk and the buzzard, and with times when their offspring are fledged. Both were periods whenL. catta infants might have been especially vulnerable to prédation.     

Grooming and touching behaviour in captive ring-tailed lemurs (Lemur catta L.)

The distribution of grooming and touching behaviours was recorded in a group of captive ring-tailed lemurs. Grooming was found to be performed chiefly by older, higher ranking animals; touching (i.e., “reach out and touch” behaviour) was directed primarily by younger, low ranking animals to older, high ranking individuals. It is suggested that such touching is a submissive gesture in this species.     

Reproductive Strategies in Lemur catta: Balance Among Sending,Receiving, and Countermarking Scent Signals

Our goal is to go deep into behavioral olfactory strategies possibly used by ring-tailed lemurs in reproductive competition and to shed some light on the function of female scent marks deposited outside the breeding season. We followed 16 captive adults at the Pistoia Zoo (Tuscany, Italy) for > 1,500 h from May 1997 to March 1999. Male direct and indirect olfactory investigation on females showed complementary distributions, the former peaking during the breeding and the latter during the birth season. Males are thus able to monitor female reproductive conditions throughout the whole year. During the birth season there was an increase of female genital marking. The olfactory advertisement probably guarantees that the extremely brief estrus does not remain unnoticed and allows male intrasexual competition a long period to operate. Male indirect olfactory monitoring and countermarking on female signals peaked during the birth season, which suggests that male intrasexual competition is achieved both by getting female chemical messages and by concealing them from other males. Female countermarking on other female genital marks peaked during the breeding season. High-ranking females had higher frequencies of countermarking than those of low-ranking females, which suggests that the advantage of obliterating scent signals of other females is greater than the disadvantage of revealing one's own reproductive condition.     

The acquisition process of a novel behavior pattern in a group of ring-tailed lemurs (Lemur catta)

The process of acquisition and propagation of a novel behavior pattern in a group of 18Lemur catta was examined. Six of eight animals that acquired the new habit were infants or juveniles. Adult males did not take up the new behavior pattern. Effects of rank and kinship on the aquisition process were not obvious.     

Discrimination by male ring-tailed Lemurs (Lemur catta) between the scent marks of male and those of female conspecifics

Olfaction plays an important role in the social communication of all prosimians. (The experiment reported in this paper forms part of an intensive chemobehavioral study of olfaction in Lemur catta (ring-tailed lemur) being carried out in this laboratory.) Five male Lemur cattawere tested on their behavioral responses to paired scent stimuli. Responses measured were (1) total investigation time, (2) arm-marking, (3) ABO/BO rubbing, and (4) flehmen. Males showed a strong discrimination between the scent stimuli,giving higher levels of response to female scent on measures 1, 3, and 4. This response suggests an olfactory-related preference by males for female scent under controlled conditions. This preference may be a consequence of the females’ dominance over males and the brevity of estrus in L. catta,both of which would favor such choice behavior.     

Troop Histories and Range Inertia of Lemur catta at Berenty,Madagascar: A 33-year Perspective

Lemur catta troops in a 1-km ² study area at Berenty Reserve have maintained fidelity to core areas since Budnitz and Dainis' study of 1972–1973, and for two troops possibly since 1963. Population in 1 km ² fluctuated from 155 to 105 to 282 individuals (excluding infants), and the number of troops increased from 12 to 21. Most troops retain the same core areas from year to year (170 observed troop-years). Ten troops derived from known fissions have settled in parts of their parent troop range or an adjacent neighbor's range. Five more troops may derive from similar matrilocal fissioning, inferred from behavior and ranging patterns. One has remained unchanged. Five have unknown parentage, in the ranges of four previously censused troops. Once a fissioned troop completely replaced another, one troop permanently extended its range, three times females joined a different troop, once a female remained nomadic for two years without stable home range. No fissioned troop has been seen to leapfrog others: to settle discontiuously from its parent. Intertroop antagonism may reflect benefits of long-term core area control.     

Drinking from tails: Social learning of a novel behaviour in a group of ring-tailed lemurs (Lemur catta)

Several examples have been documented of novel behaviours which have apparently arisen spontaneously in primate groups and then spread through the group by learning. Here we describe the first recorded instance of such an acquired behaviour in a prosimian. The behaviour, consisting of immersing the tail in water and then drinking from the wet tail, was observed in a group of semi free-ranging ring-tailed lemurs (Lemur catta). Seventeen of 28 animals showed the behaviour, including adult males. Several animals which did not show the behaviour were observed watching and sometimes sharing the wet tail of animals who did. Several incomplete sequences, notably of non-stimulus directed elements, were also seen in non-performers. It is likely that stimulus enhancement is the mechanism of spread of this behaviour through the group, although the presence of the incomplete sequences suggests that imitation is also a possibility.     

Development of Olfactory Behavior in Captive Ring-Tailed Lemurs (Lemur catta)

We conducted a long-term research project (1996–1999) on developmental aspects of olfactory behavior in ring-tailed lemurs to document the ontogenetic sequence of olfactory behavior, including the possible presence of sexual differences, and the maturation of scent-marking. The subjects were a group of 18 lemurs housed in the Pistoia Zoo (Tuscany, Italy), which we observed during 1,735 h via all-occurrences sampling, scan-animal sampling and ad libitum sampling methods. We determined the time sequence of olfactory exploration and of scent-marking patterns, and investigated sexual differences in timing and frequency. We also followed the development of scent-marking through the juvenile and adolescent phases taking into account the two aspects of motor control and of the acquisition of social competence. On the whole, we found that olfactory investigation appears and matures earlier than scent-marking. Moreover, olfactory investigation of conspecifics appeared later than substrate exploration, and seemed to follow a sequence of increasing level of acceptance by the receiver. Social play is very important for the maturation of the gestural component of scent-marking. The olfactory behavioral pattern appeared to mature during the juvenile and adolescent phases. Although sexual maturation had obvious influence on the development of olfactory behavior, the onset of scent-marking patterns was only partially parallel to sexual maturation.     

A preliminary study of kinship and social organization in a semi-free-ranging group ofLemur catta

From long-term studies of a number of anthropoid species, many investigators have shown that kinship affinities affect social relationships. Factors such as proximity, social grooming, dominance rank, and mating patterns have been shown to be related to kinship. In this paper, we report the results of a preliminary study of the social organization of a group of prosimians (Lemur catta) in which individuals were identified and kinship affinities were known. We found that close matrilineal kin preferred to groom one another and to remain in close proximity more than did nonkin and distantly related animals. Furthermore, no copulations were observed within matrilines. These results are similar to those found in a number of species of anthropoids. This research was conducted on a semi-free-ranging group at the Duke University Primate Facility, Durham, North Carolina.