Population ecology of the ring-tailed lemur, Lemur catta, and the white sifaka, Propithecus verreauxi verreauxi, at Berenty, Madagascar, 1981

The diurnal lemurs Propithecus verreauxi verreauxi and Lemur catta at Berenty in southern Madagascar, have been studied for the last 30 years. The August 1981 census indicates that the population size of L. catta remains stable at 150 adults but that P. v. verreauxi troops have become fragmented and scattered and the population is apparently increasing. Eight different vegetation types were classified within the reserve and their influence on the distribution of L. catta and P. v. verreauxi investigated. Behavioural data obtained shows the niche separation between these two, potentially competitive, sympatric lemurs.     

Tradition in Lemur catta Behavior at Berenty Reserve,Madagascar

Lemur catta Troop D at Berenty Reserve has been studied intermittently for 35 years. During 90 hours of continuous sampling in August 1998, I observed and mapped troop movement and scent marking. I compared these observations with data from June, 1975. The core of Troop D1's 1998 home range is the same as for Troop D in 1975. Sixty-two percent of Troop D1's time in 1998 was spent in the 1975 home range, and 52% of their scent marks were placed in that 1975 home range. The remainder of their time was spent in an extension of their home range, which is now an area of confrontation with an adjacent troop. They used the same sleeping trees in the 2 years, and all of the 1998 scent marks deposited in the 1975 home range were placed in the same locations marked in 1975. The similarities in their use of space in 1975 and 1998 were remarkable.     

A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar

Chemical deterioration of teeth is common among modern humans, and has been suggested for some extinct primates. Dental erosion caused by acidic foods may also obscure microwear signals of mechanical food properties. Ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar, display frequent severe tooth wear and subsequent tooth loss. In contrast, sympatric Verreaux's sifaka display far less tooth wear and infrequent tooth loss, despite both species regularly consuming acidic tamarind fruit. We investigated the potential impact of dietary acidity on tooth wear, collecting data on salivary pH from both species, as well as salivary pH from ring-tailed lemurs at Tsimanampesotse National Park, Madagascar. We also collected salivary pH data from ring-tailed lemurs at the Indianapolis Zoo, none of which had eaten for at least 12 hr before data collection. Mean salivary pH for the BMSR ring-tailed lemurs (8.098, n=41, SD=0.550) was significantly more alkaline than Verreaux's sifaka (7.481, n=26, SD=0.458). The mean salivary pH of BMSR (8.098) and Tsimanampesotse (8.080, n=25, SD=0.746) ring-tailed lemurs did not differ significantly. Salivary pH for the Indianapolis Zoo sample (8.125, n=16, SD=0.289) did not differ significantly from either the BMSR or Tsimanampesotse ring-tailed lemurs, but was significantly more alkaline than the BMSR Verreaux's sifaka sample. Regardless of the time between feeding and collection of pH data (from several minutes to nearly 1 hr), salivary pH for each wild lemur was above the "critical" pH of 5.5, below which enamel demineralization occurs. Thus, the high pH of lemur saliva suggests a strong buffering capacity, indicating the impact of acidic foods on dental wear is short-lived, likely having a limited effect. However, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. These data also suggest that salivary pH varies between lemur species, corresponding to broad dietary categories.     

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.     

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.     

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.     

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.     

Effects of spatial proximity and alliances on dominance relations among female ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar

In the present study, we describe a change in the dominance rank of the top-ranking female in a wild troop of ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. After the top-ranking female fell to the bottom-ranking position, she was able to outrank a low-ranking female with the support of her adult daughter or an unrelated high-ranking female. These results indicate that, as in cercopithecine monkeys such as macaques and baboons, close proximity and alliances influence dominance relations among adult females in a wild troop of ring-tailed lemurs.     

Influence of Dry Season and Food Quality and Quantity on Behavior and Feeding Strategy of Propithecus verreauxi in Kirindy, Madagascar

According to optimal foraging theory, herbivores can base food choice mainly on the quality or the quantity of food, or both. Among herbivorous primates, folivorous lemurs living in the highly seasonal environment of Madagascar have to cope with the shortage of high-quality food during the dry season, at least in deciduous forests. We studied (Verreaux's sifaka) in Kirindy, western Madagascar, to understand the influence of dry season and food quality and quantity on behavioral patterns and feeding strategy (qualitative vs. quantitative dietary choice) of a folivorous lemur in a deciduous forest. We followed 7 groups (4 groups/period; 3 individuals/group/month) during 4 periods of the year (wet season: February–March; early/middle/late dry season: May–June; July–September; October–November). We collected samples of plants eaten and examined behavioral and feeding patterns, considering food quality (macronutrients, proteins/fibers ratio, and tannins) and abundance. We found 1) a significant reduction of home range, core area, and daily path length from the wet to the dry season, possibly related to dietary change and 2) a daily period of inactivity in the dry season for energy conservation. Regarding the feeding strategy, Kirindy sifakas showed 1) high variation and selection in choosing food items and 2) a dietary choice based mainly on quality: Kirindy sifakas fed on plant species/families independently from their abundance and tannins represented a feeding deterrent during the dry season. Overall, behavioral and dietary adaptations allow Kirindy sifakas to overcome the shortage of high-quality food in the lean period.     

Demography, range use, and behavior in black lemurs (Eulemur macaco macaco) at Ampasikely, northwest Madagascar

We studied a black lemur population over a 2-year period (1992-1993) and 8 years later (2000) in a 50-ha secondary forest in northwest Madagascar. All of the animals were marked to investigate population dynamics and seasonal variation in ranging and behavior, and new data on black lemurs were obtained. Our data on demographic characteristics were expanded to include other forest sites and contrasted with those collected in other Eulemur macaco macaco field studies, in relation to human activity and the presence of introduced and cultivated plant species. Density is affected by deforestation and hunting. Group size and home range depend on the composition of the forest and probably food patches. Sex ratio at birth varies according to the number of females per group, a result that fits the local resource competition model. Groups are multimale-multifemale, and adult females form the core of the groups. Reproductive parameters indicate sharply defined seasonal breeding, a high female reproductive rate, and birth synchrony. Changes in group composition reveal male and female juvenile dispersal, male transfer between groups at the time of mating, and adult female transfer and group fission when groups exceed a critical size. At mating and birth, intergroup agonistic encounters occurred at home-range boundaries, and larger groups were dominant over smaller groups. Patterns of intragroup interactions suggest that males compete for access to groups of females during the mating season, and that females may compete for food resources during the birth season. Our study also reports female social dominance and lack of sexual weight dimorphism in this species.     

Coat condition of ringtailed lemurs,Lemur catta at Berenty Reserve,Madagascar: I. differences by age,sex, density and tourism, 1996–2006

An index of coat condition can be a non‐invasive tool for tracking health and stress at population level. Coat condition in ringtailed lemurs, Lemur catta, was recorded during September–November birth seasons of 1996, 1997, 1999, and 2001–2006 at Berenty Reserve, Madagascar. Condition was scored on a scale from 0: full, fluffy coat with guard hairs present, to 5: half or more of body hairless. Adult males did not differ overall from adult females. Coats were worse in adults than in 2‐year‐old subadults; 1‐year‐old juveniles were intermediate. Mothers and adult males lost coat condition as the season progressed: non‐mother females maintained condition. Years 1999–2002 scored better coats than either 1996–1997 or 2003–2006. Lemurs in high population density areas had worse coats than in natural forest, but tourist presence had less effect than density. Monitoring coat condition in an apparently healthy population reveals differences between population segments, and in a forest fragment with limited immigration or emigration it can track progressive changes, correcting impressions of progressive improvement or degradation over time. Above all it gives a baseline for response to climate changes or eventual pathology. Am. J. Primatol. 71:191–198, 2009. © 2008 Wiley‐Liss, Inc.     

Coat condition of ringtailed lemurs,Lemur catta,at Berenty Reserve,Madagascar: II. Coat and tail alopecia associated with Leucaena leucocepahala, 2001–2006

Fur condition in wild ringtailed lemurs, Lemur catta, was recorded during September–November birth seasons 2001–2006 at Berenty Reserve, Madagascar. Body coat condition was scored on a scale from BS 0: full, smooth coat with guard hairs, to BS5: half or more of back and limbs hairless. Tail condition was scored from TS 0: full, to TS 5: half or more hairless. Where troop core areas included stands of Leucaena leucocephala, alopecia was dramatically more frequent than in similar areas without leucaena, including many animals with score BS5 or TS5, “bald lemur syndrome.” Female coats were worse than males,' possibly related to female dominance and access to this preferred food. Tails in non‐leucaena‐feeding females tend to remain full, even if coats deteriorate, but with leucaena‐feeding female tails are highly correlated with coat condition and equally bare. Coat and tail condition in L. catta reflected not only the dietary toxin but individual differences as well as differences between adjacent troops that may result from territorially mediated access to the environment. Leucaena contains the non‐protein amino acid mimosine, a known cause of alopecia, wasting, and organ damage in livestock, although the effects are usually reversible. This is the first case of its effect in wildlife. Leucaena is an agroforestry tree introduced throughout the tropics. In high dietary concentrations leucaena might potentially affect any browsing mammal. Am. J. Primatol. 71:199–205, 2009. © 2008 Wiley‐Liss, Inc.     

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.     

Assessment of organochlorine pesticides and metals in ring‐tailed lemurs (Lemur catta) at Beza Mahafaly Special Reserve,Madagascar

Like most of Madagascar's endemic primates, ring‐tailed lemurs (Lemur catta) face a number of threats to their survival. Although habitat loss is of greatest concern, other anthropogenic factors including environmental contamination may also affect lemur health and survival. In this study, we examined ring‐tailed lemurs from the Beza Mahafaly Special Reserve (BMSR), southern Madagascar for exposure to organochlorine (OC) pesticides and metals and examined differences in contaminant concentrations between sexes and among age groups, troops, and habitats. A total of 14 pesticides and 13 metals was detected in lemur blood (24 individuals) and hair (65 individuals) samples, respectively. p,p′‐DDT, heptachlor, aldrin, heptachlor epoxide, endrin aldehyde, and endrin were among the most prevalent pesticides detected. Surprisingly, the persistent metabolite of p,p′‐DDT, p,p′‐DDE, was not detected. The most commonly detected metals were aluminum, zinc, boron, phosphorus, silicon, and copper, whereas metals considered more hazardous to wildlife (e.g. arsenic, cadmium, lead, selenium, vanadium) were not found above detection limits. Overall, concentrations of OC pesticides and metals were low and similar to those considered to be background concentrations in other studies examining the ecotoxicology of wild mammals. Few inter‐sex, ‐age, ‐troop, and ‐habitat differences in contaminant concentrations were observed, suggesting a uniform distribution of contaminants within the reserve. Several statistically significant relationships between lemur body size and contaminant concentrations were observed, but owing to the lack of supportive data regarding contaminant exposure in wild primates, the biological significance of these findings remains uncertain. Results of this study document exposure of ring‐tailed lemurs at BMSR to multiple OC pesticides and metals and provide essential baseline data for future health and toxicological evaluations of lemurs and other wild primates, especially those in regions with expanding agricultural and mining operations. Am. J. Primatol. 71:998–1010, 2009. © 2009 Wiley‐Liss, Inc.     

Demographic and life-history patterns in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly Reserve,Madagascar: a 15-year perspective

Over 15 field seasons (1987-2001), we collected census and life-history data on a population of individually identified ring-tailed lemurs at the Beza Mahafaly Reserve, Madagascar. No significant difference was found in population size over the study period, though a marked decline in the population occurred following a 2-year drought. The population rebounded rapidly after the immediate postdrought period. There was nearly a complete replacement of individuals over the study period. Average group size is 11.5 animals, and adult male to female sex ratio is 0.92. Most females reproduce annually, and the average fecundity rate is 84.3%. The greatest variability in fecundity is found among old females. We suggest that ring-tailed lemur females follow an "income breeding" strategy, i.e., females use maximum resources during reproduction rather than relying on fat stores, as do "capital breeders." Infant mortality to 1 year of age in a nondrought year is 52%, higher than infant mortality in small to medium-sized anthropoids. The oldest known female was 18 years old in 2001. We suggest that 18-20 years may represent the maximum life-span for wild ring-tailed lemurs. Because males regularly emigrate from the population, we have no data regarding male life-span; however, there is some indication that males do not survive as long as females. Group fission has occurred three times: twice from one parent group living in the driest area of the reserve, with the most dispersed food resources. We suggest that the reproductive strategy that has evolved in this species, wherein females reproduce early in life and annually until old age, is a response to the unusual climate and environmental conditions under which Lemur catta has evolved.     

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.