Ecological Correlates to Lemur Community Structure in Southeast Madagascar

The Fandriana-Marolambo forest corridor is one of the largest (ca. 250,000 ha) and least explored tracts of unprotected forest in southeast Madagascar. Although published range maps show continuous distributions for many lemurs throughout the region, there are few data on lemur community structure in the corridor. We aimed to determine lemur community structure, with its ecological correlates (altitude, agriculture, selective logging, and hunting), in the Fandriana-Marolambo forest corridor. We surveyed 7 sites and sighted 4 nocturnal taxa (Avahi laniger, Cheirogaleus major, Lepilemur mustelinus, and Microcebus rufus) and 6 diurnal taxa (Eulemur rubriventer, E. fulvus rufus, E. f. fulvus, Propithecus diadema edwardsi, Hapalemur griseus griseus, and Varecia variegata variegata). Composition of the lemur community was broadly similar to that of nearby protected areas (Ranomafana and Mantadia National Parks). However, we sighted no Hapalemur aureus, H. simus, or Indri indri, and observed Propithecus diadema edwardsi and Varecia variegata variegata at only 1 site each. We sighted an apparent hybrid form of Eulemur fulvus fulvus and E. f. rufus that may represent a new hybrid zone for lemurs. After testing for spatial autocorrelation, lemur diversity correlates negatively with altitude and agricultural intensity. Though the Government of Madagascar is assessing the corridor as a new national park, we suggest conservation plans for local lemurs are complicated by population isolation and lack of data on minimum viable size of the proposed protected area.     

Effect of habitat structure on positional behavior and support use in three species of lemur

This study compares locomotor and postural behavior and substrate use of three species of lemur, the diademed sifaka (Propithecus diadema edwardsi), the brown lemur (Eulemur fulvus rufus), and the red-bellied lemur (Eulemur rubriventer) at two different localities within Ranomafana National Park. The object of the study is to see if there are quantitative differences in the behavior of the lemurs or their choice of substrates in forests that have different structural attributes. Analysis of the physical characteristics of the habitat demonstrates that compared to the Talatakely area, the forest at Vatoharanana has a higher proportion of larger, taller trees. The behavior of the lemurs also differs in the two areas: all species leap less and climb and move quadrupedally more at Vatoharanana. All species use small size supports less frequently at Vatoharanana, choosing insted medium size supports (all three species) or tiny supports (Propithecus andE. fulvus) found in tree crowns and terminal branches. The lemurs prefer (i.e. use more often than would be expected based on abundance) large trees at both sites. At Vatoharanana however, they are more frequently observed higher in trees and in taller trees with greater trunk breadth. The differences in locomotor behavior are in part due to the fact that at Vatoharanana, more bouts are collected during feeding and foraging than during travel. The relationship between this difference in activity pattern and the structural differerences in the two forests, however, is not clear. This study points out the need for longer term field studies of positional behavior and substrate use that incorporate the variety of forest types the subject species inhabit.     

The influence of social organisation on leadership in brown lemurs (Eulemur fulvus fulvus) in a controlled environment

Studies on leadership during group movements in several lemur species showed that females were responsible for the travelling choices concerning time and direction. Interestingly, in these species females are dominant over males. We investigated the influence of social organisation upon leadership processes by studying a lemur species in which social organisation is characterized by the absence of female dominance: the brown lemur (Eulemur fulvus fulvus). The study was conducted on a semi-free ranging group of 11 individuals and the analysis performed on 69 group movements showed that all the individuals could initiate a group movement. In 34 cases, the whole group moved. There was no significant difference in the number of start attempts or in the number of group members involved from one initiator to another. Moreover, there was no effect of sex or age of the initiator on the number of individuals following it or on the speed of the joining process. Therefore, the leadership observed is widely distributed to all group members. These results support the hypothesis of an influence of social organisation upon the decision-making processes but still remain to be studied in a more relevant ecological context.     

Seasonal variation in positional behavior of malagasy lemurs

I describe the positional behavior of four species of Malagasy lemur (Propithecus diadema, Eulemur fulvus rufus, Eulemur rubriventer,and Varecia variegata)at two times of year at Ranomafana National Park,Madagascar. There were significant seasonal differences in locomotor behavior in all species except P. diademaAmong the lemurids, leaping was more frequent and quadrupedism less frequent in the dry season. Only E. rubriventerexhibited seasonal differences in posture, and there were few seasonal differences in support use. The observed differences in positional behavior were not the result of differences in activity budget or in microhabitat use attributable to seasonal variation in resource use.     

Infanticide in Propithecus diadema edwardsi: An Evaluation of the Sexual Selection Hypothesis

Infanticide might be described as a reproductive strategy employed by anthropoid primate males when they immigrate into new groups. But infanticide has rarely been observed in wild prosimian primates. For the Malagasy lemurs this may reflect one or more of the following: strict breeding seasons; relative monomorphism in canine tooth and body size; small group sizes; male–female dominance relations; and male–female dyads within groups. We addressed the following questions: Do prosimian males commit infanticide in circumstances similar to those in which anthropoids do? and Is there any reproductive advantage for a highly seasonal breeder to commit infanticide? To help answer these questions, we describe the death of a 24-hr-old infant male Propithecus diadema edwardsi from wounds received during a fight between his mother, her adult daughter, and a newly immigrant male. Interbirth intervals between surviving offspring are 2 years for Propithecus diadema edwardsi; therefore, a male could dramatically shorten the time between reproductive windows by killing an infant. Whether this tactic would be favored by sexual selection cannot be addressed until more information has been collected on the length of interbirth interval due to infanticide relative to that of infant death by other causes; how social factors such as stability of breeding relationships affect long-term male reproductive success; how effective female counterstrategies are to prevent infanticide and/or whether they choose to mate with males that commit infanticide; and how often males that kill infants subsequently sire infants, particularly in groups that contain a resident male.     

Special relationships instead of female dominance for redfronted lemurs,Eulemur fulvus rufus

Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale–multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male–female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male–female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male–female affiliations illuminated developmental and functional aspects of male–female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male–female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male–female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate. Am. J. Primatol. 43:239–258, 1997. © 1997 Wiley-Liss, Inc.     

Paternity Determination in Two Groups of Eulemur fulvus mayottensis: Implications for Understanding Mating Strategies

We used random amplified polymorphic DNA (RAPD) to determine paternity in two groups of brown lemurs (Eulemur fulvus mayottensis). We analyzed the results in relation to behavioral data on observed copulations, dominance relationships among adult males, and female behavior. The association between paternity determination and behavioral sampling shows that paternity determination is a crucial tool for understanding the mating strategies and reproductive success in the studied species. In brown lemurs, dominance relationships between males are correlated with reproductive success, but male social dominance could be altered by female choice as suggested by the ability of subordinate males to sire offspring in the presence of a dominant male.     

Adult Male Scent-Marking in Lemur catta and Eulemur fulvus rufus

Scent-marking and olfactory communication are used extensively by prosimians and can provide spatial and temporal records of group movement and behavior. We compare rates of male scent-marking in relation to reproductive seasons, male dominance rank, and habitat use in two related prosimians: Lemur catta and Eulemur fulvus rufus. We collected scent-marking data on adult male Lemur catta at Beza-Mahafaly Reserve (dry forest), and on Eulemur fulvus rufus at Ranomafana National Park (rainforest), Madagascar. In Lemur, rates of overall scent-marking differed significantly by reproductive season, with higher rates occurring in mating and lactation/migration periods, whereas in Eulemur, reproductive season did not appear to affect scent-marking rates. Dominance rank of male Lemur catta did not affect rates of scent-marking. Among male Eulemur fulvus, dominance relations were not apparent; however, 2 of the 5 focal males scent-marked somewhat more frequently during the mating season and also experienced greater mating success. In Lemur catta, higher rates of scent-marking in the mating season may relate to indirect reproductive competition during a period of high aggression, while such mating competition was not as marked in Eulemur fulvus. Furthermore, higher rates of marking in resident male Lemur catta during male migration may correlate with vigilance toward immigrating males. Greater overall scent-marking rates in ring-tailed lemurs may relate to extensive intergroup home range overlap and no area of exclusive use, whereas the red-fronted lemur groups tended to forage in areas of their home range where little-to-no intergroup overlap occurred.     

Morphological Variation in Populations of <Emphasis Type="Italic">Eulemur albocollaris</Emphasis> and <Emphasis Type="Italic">E. fulvus rufus</Emphasis>

Sexual dimorphism in body size and canine weaponry is commonly associated with high levels of male-male competition. When group living species do not rely heavily on male-male competition for access to females, sperm competition may represent a viable alternative strategy. Unlike most haplorhine primates, lemurs are typically monomorphic in body weight and canine height. We assessed variability of body mass dimorphism and canine size dimorphism in brown lemurs using morphometric data from 3 populations in southeastern Madagascar: Eulemur fulvus rufus, E. albocollaris, and hybrids of the species. We found significant male-biased canine dimorphism in E. albocollaris in conjunction with body-size monomorphism. We observed similar patterns in the hybrids, but E. fulvus rufus exhibited significant female-biased size dimorphism and canine monomorphism. Testes volume was relatively high across study populations. Thus, sperm competition appears to be strong in brown lemurs. E. albocollaris males combine sperm competition with large canines, but not higher body mass, indicating a difference in sexual strategy from most lemurs. Patterns of body mass and canine size dimorphism are not uniform across brown lemur populations, indicating that future work on these populations can explicitly test models that predict relationships between size dimorphism and various types of competition.     

Leading ladies: leadership of group movements in a pair-living, co-dominant, monomorphic primate across reproductive stages and fruit availability seasons

For gregarious species, individuals must maintain cohesion while minimizing the costs of coordinated travel. Leaders of group movements potentially influence energy expenditure, energy intake, and predation risk for individuals in the group, which can have important fitness consequences. Models of pair-living species predict that energetic asymmetries lead to an emergent leader, with those in greater need leading. We investigated sex differences in leadership in pairs of red-bellied lemurs, Eulemur rubriventer, a monomorphic species with bisexual dispersal and no discernible hierarchy, to determine whether higher energetic requirements by adult females lead to female leadership. We collected leadership data in Ranomafana National Park, Madagascar on six groups of habituated E. rubriventer for 13 consecutive months between 2004-2005. To determine whether females led group movements more than males, we examined the difference in leadership frequencies of progressions in adult males and adult females within each group (n = 1,346 progressions). We further investigated the behavioral context (i.e. travel followed by feeding or not) and seasonal contexts (fruit availability, reproduction) of leadership. Group leadership was distributed, with different individuals leading the group at different times. However, females led significantly more than males, a pattern which was consistent in both feeding and non-feeding contexts and throughout all fruiting seasons and reproductive stages. While disparities in energetic status among the sexes may impact leadership in this species, leadership did not differ with changes in food availability or reproductive stage, and thus we were unable to determine whether female leadership might be related to changes in energetic status. Females may have higher energetic needs than males at all times, not merely seasonally, or female leadership may be unrelated to immediate energetic need. Rather, female leadership may be a legacy of female dominance not currently expressed in other contexts.     

Female dominance in blue-eyed black lemurs(Eulemur macaco flavifrons)

Female dominance is unusual among mammals and has been described in detail for only a handful of species. Here we present data on the frequency and outcome of dominance interactions in seven semi-free ranging and captive groups of blue-eyed black lemurs (Eulemur macaco flavifrons) housed at the Duke University Primate Center. We collected over 260 hours of focal data during which all occurrences of dominant-subordinate interactions were recorded. We collected data outside the typical breeding and birthing seasons for this species, thus eliminating possible confounding factors and increased aggression associated with these periods. We found that females were dominant over males in all seven groups, with females winning 99% of all dominance interactions.E. m. flavifrons used aggressive dominance (e.g. chase, cuff, bite) in 81% of all interactions, with the remainder of interactions being decided using social dominance (e.g. deference in the form of supplants or cowers). Older females were dominant over younger females in two out of three multi-female groups (in each case, younger females were daughters), and younger males (sons of the dominant female) received less aggression from females than did older males (n = 2 groups). Caging and group size appear to play a minimal role in the expression of female dominance. While confirmation must await further observations on free-ranging groups ofE. m. flavifrons, our data strongly suggest that this subspecies can be characterized as female dominant.     

Costs and benefits of multi-male associations in redfronted lemurs (Eulemur fulvus rufus)

The evolution of group-living has fascinated but also puzzled researchers from the inception of behavioural ecology. We use a simple optimality approach to examine some of the costs and benefits of group-living in redfronted lemurs (Eulemur fulvus rufus). We show that dominant males profit from accepting subordinates within their groups, as the latter significantly decrease the likelihood that the group is taken over by intruders. This benefit is large enough to outweigh the costs of reproductive competition and may constitute the driving force behind the evolution of multi-male associations in this species.     

Direct and Indirect Impacts of Raptor Predation on Lemurs in Southeastern Madagascar

I calculated rates of predation by 2 species of diurnal raptors, Polyboroides radiatus and Accipiter henstii, on the lemur community of Ranomafana National Park, Madagascar from 2700 h of observation and 470 prey deliveries at 7 nests of each hawk species. The 2 hawks consumed 7 of 12 lemurs found in the park region, with a body mass of 63–3500 g and including diurnal and nocturnal species of all group sizes. Calculations of predation rates indicate that raptor predation is a significant cause of mortality for lemur populations relative to other causes. Minimum rates of predation by Polyboroides radiatus and Accipiter henstii on Microcebus rufus, Cheirogaleus major, Avahi laniger, Hapalemur griseus, Eulemur fulvus rufus, Eulemur rubriventer, and Varecia variegata resulted in the raptors removing of 1–21% of the population per yr, similar to other rates of predation on primates documented in the literature. Modeling of lemur populations under varying levels of raptor predation pressure that I calculated found that one may attribute 3–17% of adult, juvenile, and infant mortality for nocturnal lemurs and 2–66% of adult, juvenile, and infant mortality for diurnal lemurs to diurnal raptor predation. Raptor predation may significantly depress intrinsic growth rates and carrying capacity of Avahi laniger, Hapalemur griseus, Eulemur fulvus rufus, Eulemur rubriventer, and Varecia variegata owing to their low fecundities, long life spans, and long age to sexual maturation. Nocturnal lemurs may best avoid predation by diurnal raptors by exhibiting a solitary lifestyle and cryptic antipredator tactics, whereas, diurnal lemurs benefit less by increasing group size than by using specific antipredator tactics.     

Patterns of female dominance in Propithecus diadema edwardsi of Ranomafana National Park, Madagascar

Many lemur species are characterized by some form of female dominance, ranging from female feeding priority to complete female dominance, although this is a rare trait in primates and other mammals. The status of the Milne-Edwards' sifaka (Propithecus diadema edwardsi), a diurnal lemur, is ambiguous. Some short-term studies have found little or no aggression. The aim of the current, long-term study was to quantify the intersexual-dominance patterns of this sifaka. The distribution, outcome, and context of aggressive interactions were studied in four groups of wild sifakas. The majority of intersexual aggressive interactions were decided, with the loser expressing submissive behavior. Intersexual aggressive interactions occurred in all social contexts, and within all social contexts the females won the vast majority (92.7-96.0%) of aggressive interactions. While aggression rates were low (0.22/hr), this evidence suggests female dominance. We propose that female dominance exists because it provides a fitness advantage to both males and females.     

Does agonistic dominance imply feeding priority in lemurs? a study in Eulemur fulvus mayottensis

We studied agonistic dominance and priority of access to a limited drinking resource in two captive groups of Eulemur fulvus mayottensis.Gender is not systematically related to agonistic dominance or to drinking priority. The dominance hierarchy obtained in the drinking competition test is correlated with the baseline hierarchy in the absence of induced competition, but not with drinking priority. We analyze results within the framework of recent dicussions on female dominance in Malagasy prosimians.     

Rates of Agonism by Diurnal Lemuroids: Implications for Female Social Relationships

Sterck and colleagues (Behaviour 134:749–774, 1997) focused attention on the evolutionary ecology of female social relationships within and between groups and proposed a model that distinguishes 4 categories of female relationships, which correspond to particular types of intra- and intergroup competition. They emphasized literature on haplorhines in their model because of numerous, detailed studies conducted on a range of species in the wild; in contrast, strepsirrhines such as the lemuroids are poorly represented. We evaluate more closely their classification of lemuroids as Dispersal-Egalitarian using a greater number of species of Lemur, Eulemur, Varecia, Hapalemur, Indri, and Propithecus. For the focal species we found that female philopatry occurs rarely, agonistic rates are relatively low, female dominance hierarchies are not stable and do not exist year-round, and intra- and intergroup female-female competition is infrequent. Therefore, our results support the suggestion that a majority of lemuroid taxa we surveyed correspond to the Dispersal-Egalitarian category with 2 probable exceptions: Lemur catta and Propithecus edwardsi. Because female Lemur catta are philopatric, have year-round dominance hierarchies with female matrilines, exhibit the highest rates of agonism in studied lemuroids, and have frequent intra- and intergroup female-female competition, it would seem that they more closely correspond to the category Resident-Nepotistic. However, maternal Lemur catta rarely support their offspring in agonistic contests and matrilineal rank is not inherited, which leads us to state that the species does not fit into any existing category that explains the nature of female social relationships. The relationships of female Propithecus edwardsi are also a challenge to categorize under the current model because some of their characteristics —typical female dispersal and low agonistic rates— fall into the Dispersal-Egalitarian category, yet other behaviors —intense targeted aggression and stable and year-round female dominance hierarchies— do not.     

Coordination of Group Movements in Wild Red-fronted Lemurs (<Emphasis Type="Italic">Eulemur rufifrons</Emphasis>): Processes and Influence of Ecological and Reproductive Seasonality

Group-living species have to coordinate collective actions to maintain cohesion. In primates, spatial movements represent a meaningful model to study group coordination processes across different socio-ecological contexts. We studied 4 groups of red-fronted lemurs (Eulemur rufifrons) in Kirindy Forest, Madagascar, between 2008 and 2010 across different ecological and reproductive seasons. We collected data on ranging patterns using GPS collars and observational data on different predefined parameters of group movements, including initiation, leadership, followership, overtaking events, termination, and travel distances. Cohesion of these relatively small, egalitarian lemur groups was high year-round, but daily path length and home range size varied considerably between ecological seasons, presumably due to long-distance migrations of some groups at the beginning of the rainy season. Individuals of different age and sex classes successfully initiated group movements. However, stable female leadership prevailed year-round, irrespective of ecological and reproductive season, which might be due to higher or more specific energetic requirements of reproduction. In contrast to lemur species with a more despotic social structure, female red-fronted lemurs did not recruit more followers than males. Adult leaders recruited more followers than subadult ones. Further, recruitment success was higher during the peak of the dry season, when predation risk appeared to be higher. Distances of single group movements did not depend on the initiator’s sex and age or on ecological seasons. Our results provide new insights into seasonal variability of coordination processes and the role of social dominance in lemur group movements, thereby contributing to a comparative perspective from a primate radiation that evolved group living independently of anthropoids.     

Craniodental Characters in the Taxonomy of Propithecus

The indriid genus Propithecus comprises the sifakas, medium-sized lemurs endemic to the forests of Madagascar. Traditionally, scientists divided the genus into only 2 or 3 species —Propithecus diadema, P. verreauxi, and, since 1988, P. tattersalli— with 4 or 5 subspecies in each of the first 2 taxa, but recent authors have suggested that many more distinct species should be recognized. We draw from quantitative and qualitative studies of craniodental traits to evaluate further the phenetic distinctiveness and taxonomic status of each named form of Propithecus. We recognize 9–10 species in the genus. The 4 or 5 species of the Propithecus diadema group —P. diadema, P. candidus, P. perrieri, P. edwardsi, and perhaps P. holomelas, if distinct— share several derived features, including large average body size and a mandible specialized for rotational chewing, and clearly comprise a closely related complex. The 5 species of the Propithecus verreauxi group —P. verreauxi, P. coquereli, P. deckenii, P. coronatus, P. tattersalli— are each highly distinctive morphologically and likely do not comprise a monophyletic group. In particular, we point out the highly distinctive cranial features of Propithecus coronatus, which researchers have traditionally largely overlooked.     

Dietary and Feeding Differences Between Sympatric Propithecus diadema diadema and Indri indri

We analyzed the dietary profiles and feeding behaviors of Propithecus diadema diadema and Indri indri in a community of animals that reside in midaltitude rain forest within Madagascar's Mantadia National Park. Propithecus diadema diadema ate a diverse mixture of fruits, seeds, flowers and young leaves, while the bulk of the diet of Indri indri consisted of young leaves, which resulted in significantly higher levels of fat and water-soluble carbohydrates in foods eaten by Propithecus diadema diadema. Fiber values of items eaten are high (54% NDF) for both species, though not significantly different between them. The preference for immature foliage by Indri indri suggests that their overall intake of fiber is greater than that of Propithecus diadema diadema, which had a high proportion of non-leaf material in their diet. We propose that differences in gut morphology between the two indriids contribute to their disparate diets. Levels of secondary compounds were high in certain food items, but overall they are also not significantly different between the two indriid diets. Propithecus diadema diadema exhibited a strong preference for 2 alkaloid-containing seed species, while no food of Indri indri contained alkaloids. In addition, Propithecus diadema diadema consumed a higher diversity of plant species on a daily/yearly basis, exhibited more feeding bouts on a daily basis, and their feeding bouts (on young leaves, fruit and flowers) are significantly shorter in duration than those of Indri indri. Furthermore, Propithecus diadema diadema had twice the number of geophagic episodes of Indri indri.     

Effects of size and sex on the social organization of reef-associated hogfishes,Bodianus spp.

Synopsis Three species of wrasses (Labridae) were examined in the field to determine the relative importance of size and sex in structuring social organization. The Spanish hogfish, Bodianus rufus, was characterized by stable dominance hierarchies that were linearly organized according to sex and relative size. Males were the largest and most-dominant individuals within discrete social groups of females (harems) whose dominance increased with body size. Dominance rank also increased with body size among both males and females of the Mexican hogfish, B. diplotaenia. Most encounters occurred between the sexes and males were clearly dominant over females. The vieja, B. eclancheri, differed from the other congeners since social interactions were not strongly patterned by either relative body size or sex. Hogfish dominance relationships appear to develop according to the manner in which males compete for females, including the formation of harems in permanent territories with single-male pairspawns (B. rufus), defense of temporary reproductive territories with single-male pairspawns (B. diplotaenia) or maximizing sperm production in multi-male group spawns (B. eclancheri).