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.     

Demography of Propithecus verreauxi at Beza Mahafaly,Madagascar: Sex ratio,survival, and fertility, 1984–1988

Eighty-five sifakas (Propithecus verreauxi) have been captured, marked, released, and monitored between September 1984 and August 1988 at the Beza Mahafaly Special Reserve in southwest Madagascar. Estimates are presented of the age and sex structure of this population and of age-specific fertility and survival. Using data from this and other studies, it is shown that sifaka tertiary sex ratios do not depart significantly from 50:50, but that they do differ significantly from those of haplorhine primates, which have strongly female-biased tertiary sex ratios. Two demographic mechanisms that could give rise to this distinction are considered: 1) intermittently male-biased birth cohorts among sifakas and 2) different patterns of survivorship in haplorhines and sifakas.     

Ecogeographic size variations in Sifakas: a test of the resource seasonality and resource quality hypotheses

Ecogeographic size variations have been documented in some but not all sifakas. Few morphometric or body weight data have been available for two critically endangered subspecies of diademed sifakas: Perrier's sifakas (Propithecus diadema perrieri) and silky sifakas (Propithecus diadema candidus). The objectives of our study were to determine size variations in sifakas and if these variations are related to resource quality and/or resource seasonality. P. d. perrieri and P. d. candidus were captured, weighed, and measured in northern Madagascar. Body weights and morphometrics were compared with other subspecies of diademed sifakas and indris (Indri indri). Differences in body weights and morphometrics between taxa are particularly pronounced for P. d. perrieri compared to P. d. diadema, P. d. edwardsi, and I. indri. Most morphometrics varied in comparisons between P. d. candidus and the other Indriidae (P. d. diadema, P. d. edwardsi, and I. indri). Average body size in sifakas is positively correlated with annual rainfall and negatively correlated with length of dry season. Sifaka body size is not correlated with protein-to-fiber ratios. Thus, size variations in sifakas are related to resource seasonality rather than resource quality. The relationships between the temporal availability of food resources and sifaka body size reflect complex and regionally varying causalities. Detailed, longitudinal information on the ecological factors underlying food selection and nutrient requirements in sifakas are needed to determine the relationship between ecogeographic variables and body size in sifakas.     

Relative growth of the limbs and trunk in sifakas: Heterochronic,ecological, and functional considerations

Limb, trunk, and body weight measurements were obtained for growth series of Milne-Edwards's diademed sifaka, Propithecus diadema edwardsi, and the golden-crowned sifaka, Propithecus tattersalli. Similar measures were obtained also for primarily adults of two subspecies of the western sifaka: Propithecus verreauxi coquereli, Coquerel's sifaka, and Propithecus verreauxi verreauxi, Verreaux's sifaka. Ontogenetic series for the larger-bodied P. d. edwardsi and the smaller-bodied P. tattersalli were compared to evaluate whether species-level differences in body proportions result from the differential extension of common patterns of relative growth. In bivariate plots, both subspecies of P. verreauxi were included to examine whether these taxa also lie along a growth trajectory common to all sifakas. Analyses of the data indicate that postcranial proportions for sifakas are ontogenetically scaled, much as demonstrated previously with cranial dimensions for all three species (Ravosa, 1992). As such, P. d. edwardsi apparently develops larger overall size primarily by growing at a faster rate, but not for a longer duration of time, than P. tattersalli and P. verreauxi; this is similar to results based on cranial data. A consideration of Malagasy lemur ecology suggests that regional differences in forage quality and resource availability have strongly influenced the evolutionary development of body-size variation in sifakas. On one hand, the rainforest environment of P. d. edwardsi imposes greater selective pressures for larger body size than the dry-forest environment of P. tattersalli and P. v. coquereli, or the semi-arid climate of P. v. verreauxi. On the other hand, as progressively smaller-bodied adult sifakas are located in the east, west, and northwest, this apparently supports suggestions that adult body size is set by dry-season constraints on food quality and distribution (i. e., smaller taxa are located in more seasonal habitats such as the west and northeast). Moreover, the fact that body-size differentiation occurs primarily via differences in growth rate is also due apparently to differences in resource seasonality (and juvenile mortality risk in turn) between the eastern rainforest and the more temperate northeast and west. Most scaling coefficients for both arm and leg growth range from slight negative allometry to slight positive allometry. Given the low intermembral index for sifakas, which is also an adaptation for propulsive hindlimb-dominated jumping, this suggests that differences in adult limb proportions are largely set prenatally rather than being achieved via higher rates of postnatal hindlimb growth. Our analyses further indicate that the larger-bodied P. d. edwardsi has a higher adult intermembral index than P. tattersalli and P. verreauxi, thus supporting the allometric argument regarding the interspecific scaling of limb proportions in arboreal primates which employ vertical postures (Cartmill, 1974,1985; Jungers, 1978, 1985). Lastly, additional analyses indicate that P. d. edwardsi exhibits significant sexual dimorphism where adult females are larger than adult males in about one-third of all adult comparisons, whereas P. tattersalli exhibits significant sexual dimorphism in about one-fifth of all adult comparisons. Among western sifakas, adult P. v. coquereli exhibit significant sex dimorphism in about one-third of all comparisons, whereas adult P. v. uerreauxi show no significant differences between the sexes. Given that all taxa are ontogenetically scaled, this suggests that sexual dimorphism develops via such processes as well. Interestingly, our data indicate that sex dimorphism is allometric, with larger-bodied taxa like P. d. edwardsi being more dimorphic.     

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.     

Functional and evolutionary significance of the recruitment and firing patterns of the jaw adductors during chewing in Verreaux's sifaka (Propithecus verreauxi)

Jaw-muscle electromyographic (EMG) patterns indicate that compared with thick-tailed galagos and ring-tailed lemurs, anthropoids recruit more relative EMG from their balancing-side deep masseter, and that this muscle peaks late in the power stroke. These recruitment and firing patterns in anthropoids are thought to cause the mandibular symphysis to wishbone (lateral transverse bending), resulting in relatively high symphyseal stresses. We test the hypothesis that living strepsirrhines with robust, partially fused symphyses have muscle recruitment and firing patterns more similar to anthropoids, unlike those strepsirrhines with highly mobile unfused symphyses. Electromyographic (EMG) activity of the superficial and deep masseter, anterior and posterior temporalis, and medial pterygoid muscles were recorded in four dentally adult Verreaux's sifakas (Propithecus verreauxi). As predicted, we find that sifaka motor patterns are more similar to anthropoids. For example, among sifakas, recruitment levels of the balancing-side (b-s) deep masseter are high, and the b-s deep masseter fires late during the power stroke. As adult sifakas often exhibit nearly complete symphyseal fusion, these data support the hypothesis that the evolution of symphyseal fusion in primates is functionally linked to wishboning. Furthermore, these data provide compelling evidence for the convergent evolution of the wishboning motor patterns in anthropoids and sifakas.     

Volatile components of lemur scent secretions vary throughout the year

Olfactory signals can communicate a wide variety of information and are very important in many mammalian species. However, little is known about the olfactory communication of primates. This study used gas chromatography to examine the volatile components of the anogenital gland secretions of wild Milne-Edward's sifaka, Propithecus edwardsi (Primates, Indriidae) (n = 17), captured in Ranomafana National Park, Madagascar. We compared scent swabs of animals and examined differences between social group, age class, sex, and season. The only identified differences in the volatiles were between swabs from the different seasons; all other categories were statistically indistinguishable.     

Lemur habitat and dental senescence in Ranomafana National Park, Madagascar

Not only can teeth provide clues about diet, but they also can be indicators of habitat quality. Conspecific groups living in different habitats with different kinds of foods may exhibit different rates of dental attrition because their teeth are less well adapted to some foods than to others. Ecological disequilibrium describes the situation in which animals live in habitats to which they are relatively poorly adapted. We test whether dental senescence, the wear-related decrease in dental functionality that is associated with decreased survival of infants born to older Propithecus edwardsi females, can be explained by ecological disequilibrium. Specifically, we compare the rates of dental wear in sifaka groups living in nearby habitats that differ in the degree of anthropogenically induced disturbance. We hypothesize that sifakas living in disturbed areas have an unusual rate of tooth wear compared to those living in a more pristine area, and that dental senescence is a consequence of an atypically high wear rate in a degraded habitat. To test whether habitat quality affects tooth wear more generally, we compare rates of use-wear in two subsets of Microcebus rufus living in either relatively undisturbed or disturbed habitats. Contrary to our predictions, we did not detect different rates of tooth wear in disturbed versus undisturbed habitats for either species and consider that reproductively detrimental dental senescence in P. edwardsi females is unlikely to be a pathological consequence of ecological disequilibrium.     

Interspecific Responses of Ringtailed Lemurs to Playback of Antipredator Alarm Calls Given by Verreaux's Sifakas

The ringtailed lemur, Lemur catta, and Verreaux's sifaka, Propithecus verreauxi verreauxi, are diurnal prosimians living sympatrically in Madagascar. Species-specific alarm calls emitted by each of these two species in response to aerial and terrestrial predators differ acoustically. Behavioural responses of ringtailed lemurs evoked by playbacks of conspecific alarm calls differ when the vocalizations were produced in response to aerial predators as opposed to terrestrial predators. We conducted playback experiments on two populations of ringtailed lemurs, using two types of sifaka alarm calls. One population consisted of free-ranging groups which lived sympatrically with sifakas, the other was a colony group which had no contact with sifakas. The results illustrate that the former group of lemurs can perceive what type of predators the sifaka calls refer to, whereas the latter group was not able to recognize the difference in the calls.     

Forest access restores foraging and ranging behavior in captive sifakas

Captive wildlife benefit from ecologically informed management strategies that promote natural behaviors. The Duke Lemur Center has pioneered husbandry programs rooted in species' ecology for a diversity of lemurs, including housing social groups in multiacre forest enclosures. We systematically document the foraging and ranging patterns of Coquerel's sifakas (Propithecus coquereli) living in these forest enclosures. Coquerel's sifakas are seasonal frugo-folivores that exhibit striking feeding flexibility in the wild. They are also one of the few members of the Indriidae family to persist in captivity. During all-day follows in the spring and summer of 2 consecutive years, we tracked the behavior of 14 sifakas in six forest enclosures. The sifakas' ranging and foraging patterns reflected those of wild sifakas in western Madagascar: On average, DLC sifakas occupied 3-day home ranges of 1.2 ha, traveled 473 m/day, and spent 26% of their time foraging for wild foodstuffs. The sifakas foraged most for young and mature leaves, fruits, nuts, and flowers from 39 plant species, especially red maple (Acer rubrum), tulip poplar (Liriodendron tulipifera), black locust (Robinia pseudoacacia), grapevine (Vitis rotundifolia), hickory (Carya spp.), and white oak (Quercus alba). Foraging patterns varied across seasons, enclosure areas, and groups, potentially reflecting differences in phenology, microhabitats, and individual preferences. While demonstrating that captive-bred primates express wild-like behaviors under ecologically relevant conditions, our results underscore the feeding flexibility of the Coquerel's sifaka. Captive wildlife exhibiting the range of species-specific behaviors are key resources for ecological research and might be best suited for future reintroductions.     

Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates

Among primates, catarrhines (Old World monkeys and apes) andcertain platyrrhines (New World monkeys) possess trichromaticcolor vision, which might confer important evolutionary advantages,particularly during foraging. Recently, a polymorphism has beenshown to shift the spectral sensitivity of the X-linked opsinprotein in certain strepsirrhines (e.g., Malagasy lemurs); however,its behavioral significance remains unknown. We assign genotypesat the X-linked variant to 45 lemurs, representing 4 species,and test if the genetic capacity for trichromacy impacts foragingperformance, particularly under green camouflage conditionsin which red detection can be advantageous. We confirm polymorphismat the critical site in sifakas and ruffed lemurs and fail tofind this polymorphism in collared lemurs and ring-tailed lemurs.We show that this polymorphism may be linked to "behavioraltrichromacy" in heterozygous ruffed lemurs but find no comparableevidence in a single heterozygous sifaka. Despite their putativedichromatic vision, female collared lemurs were surprisinglyefficient at retrieving both red and green food items undercamouflage conditions. Thus, species-specific feeding ecologiesmay be as important as trichromacy in influencing foraging behavior.Although the lemur opsin polymorphism produced measurable behavioraleffects in at least one species, the ruffed lemur, these effectswere modest, consistent with the modest shift in spectral sensitivity.Additionally, the magnitude of these effects varied across individualsof the same genotype, emphasizing the need for combined geneticand behavioral studies of trichromatic vision. We conclude thattrichromacy may be only one of several routes toward increasedforaging efficiency in visually complex environments.     

Mass change, environmental variability and female fertility in wild Propithecus verreauxi

Accurate estimates of mass and size are important in a wide range of research questions in population and evolutionary biology, and yet such data are still rare for wild primates. This study presents detailed longitudinal data from a large population of wild indriids, and demonstrates links between fluctuations in body mass, environmental cycles, and reproduction. Understanding these links is a necessary step toward explaining the function and evolution of distinctive features of lemur biology and behavior.During the first 12 years of an ongoing study of the sifaka, Propithecus verreauxi verreauxi, at Beza Mahafaly in southwest Madagascar, 320 animals were captured and weighed throughout the year. Adult males and females exhibit seasonal cycles of mass loss, with females losing significantly more mass than males. In 2 drought years this pattern was especially pronounced. Compared to lighter females, females who were heavier at the time of the mating season were more likely to give birth in the following birth season. By showing (1) seasonally greater mass loss in reproductive females compared to males, particularly in drought years, (2) a close link between female mass and fertility, and (3) an uncoupling of the periods of highest body mass and of gestation and lactation, these results suggest that energy acquisition and storage are critically important in the life history strategies of female sifaka, and that "capital breeding" may be a feature of sifaka reproductive strategies.     

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.     

Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi)

Studies in anthropoid primates and other mammals suggest that reproductive season, rank, reproductive skew, aggression received, and social support are the major factors influencing glucocorticoid output. In which way these are also affecting adrenal function in lemurid primates has been studied rarely. Here, we examine the influence of reproductive season and rank on glucocorticoid output in male sifakas (Propithecus verreauxi), a species characterized by high breeding seasonality, a hierarchy among males and extreme reproductive skew towards dominant males. We established a fecal assay for non-invasively monitoring adrenal activity and collected 315 fecal samples during the reproductive and birth season from 10 male sifakas living in 5 groups in Western Madagascar. We found a significant effect of season on glucocorticoid output, with males exhibiting higher fecal glucocorticoid levels during the reproductive compared to the birth season in conjunction with an increase in overall aggression rates during the former period. Moreover, our data indicate a significant effect of rank on adrenocortical activity with dominant males exhibiting higher glucocorticoid levels than subordinate males in the reproductive season. However, dominant males did not differ significantly in rates of initiated or received aggression and rates of affiliative behavior from subordinates but showed significantly lower rates of submission. Given their highly formalized dominance relationships, we conclude that higher glucocorticoid output in dominant males during the 4-month reproductive season is likely related to higher energetic demands necessary to cope with the challenges of male reproduction rather than to physical demands of increased fighting frequency to maintain dominance status. High rank in sifakas may thus carry high costs, which, however, may be outweighed by monopolization of almost all paternities. In sum, our data generally support the findings on the relationship between environmental and social factors and glucocorticoid output found in non-lemurid primates.     

Fitness and extra-group reproduction in male Verreaux's sifaka: An analysis of reproductive success from 1989-1999

Adult males in social groups often compete with other male group members for access to adult females. In some primate species, males also seek mating opportunities in neighboring social groups. Such extra-group fertilizations (EGFs) provide an additional source of variation in male fitness. This additional component of fitness provided by EGFs must be incorporated into analyses that investigate sources of variation in male lifetime reproductive success. In this study, a model is analyzed in which male fitness over a 10-year sample period is decomposed into additive and multiplicative variance and covariance components. The data come from an ongoing study of a wild population of Verreaux's sifaka (Propithecus verreauxi verreauxi) located at Beza Mahafaly Special Reserve, Southwest Madagascar. Paternity and demographic data for 134 males are used to decompose male fitness into the following three multiplicative components: reproductive lifespan during sample period, fertility, and offspring survival. These multiplicative components are estimated for males reproducing within their resident groups plus (i.e., the additive portion) for males reproducing in neighboring social groups. The analysis shows that variation in fertility makes the largest contribution to variation in total fitness, followed by variation in amount of time spent in sample period (which is a proxy of total reproductive lifespan) and variation in offspring survival. EGFs contribute an important source of variation to male fitness, and numerous factors enhance the opportunities for EGFs in male sifaka. These include female choice, a high degree of home range overlap, and a limited mating season.     

Patterns of male scent-marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

Scent-marking behavior has been well documented in many primate species. Three common functions attributed to scent-marking in males of multi-male/multi-female lemur species include: 1) advertisement of individual identity, 2) territorial defense, and 3) reproductive suppression. We examined the average number of scent-marks per hour exhibited daily by adult male sifakas (Propithecus edwardsi) and found that patterns of scent-marking changed with season, natal status, and dominance status. Males in single-male groups scent-marked at the highest rate, followed by dominant males, males of equal status, and subordinate males. Non-natal males generally scent-marked at higher rates than natal males, and adult males living in a natal group without a parent marked at higher rates than males living with a parent. All males scent-marked at higher rates in the migration season compared to the other seasons. These patterns were consistent with territorial defense and advertisement to females, and the suggestion that these chemical signals impart information concerning status. Since scent-marking behavior tracked seasons and varied with both dominance and natal status, it may serve multiple functions in males.     

Dietary patterns in Perrier's sifakas (Propithecus diadema perrieri): a preliminary study

Some lemur species range into only one habitat type, whereas others range into a variety of habitats. Because plant community structure can differ between habitats, dietary patterns may vary for conspecific groups of primates that range into more than one type of habitat. The goal of our study was to determine how habitat variation influences dietary patterns in Perrier's sifakas (Propithecus diadema perrieri) that range into both dry and riparian forests in northern Madagascar. We collected 542 hr of data on the behavior and diet of two groups of P.d. perrieri from 7 June to 4 August 1998 at Camp Antobiratsy in Analamera Special Reserve, Madagascar. We computed indices of dietary diversity for each group and dietary/plant species similarity between groups. P.d. perrieri in group 1 fed predominantly in dry forest (72.7% of feeding records, n=660), whereas those in group 2 fed most often in riparian forest (73.7% of feeding records, n=666). The index of dietary similarity (0.986) was significantly higher than the index of plant species similarity (0.767). Although the P.d. perrieri in the two study groups fed predominantly in different forest habitats, they ate similar food items in very comparable proportions (but not from the same plant species). However, based on habitat availability measures, neither group fed where they were expected to feed.     

Systematics and body size: implications for feeding adaptations in New World monkeys.

The relationship between body size and feeding ecology is well established for primates. It is argued that the evolutionary history of modern New World monkeys and, in particular, the path to attainment of current body size is significant in understanding the similarities and differences between dietary strategies and other ecological parameters of similar-sized monkeys. Current interpretations of New World monkey evolutionary relationships are reviewed. Based on a synthesis of available body weights and the assumption that the earliest New World monkeys weighed close to 1 kg, similar to modern Aotus and Callicebus, predicted patterns of body size change in each lineage are given. Restrictions on directions of body size change in primates are discussed, and it is shown that "Stanley's Rule" offers a good explanation for differing body size ranges in New and Old World anthropoids. Predicted ecological correlates to body size drawn from the mammalian literature are offered and tested using data on New World monkeys, which show some concurrence and several interesting departures from predicted patterns. Sexual dimorphism in body weight of New World monkey species is reviewed, based on the new summary of body weight data given.     

Are Kirindy sifaka capital or income breeders? It depends

The capital and income breeding framework has only recently been used to explain variation in female reproductive strategies in primates. The application of this framework to primates and other mammals with long reproductive cycles has not been consistent. We evaluated data on Verreaux's sifaka (Propithecus verreauxi verreauxi) in the Kirindy Forest of western Madagascar to determine whether they are capital or income breeders. We found that Verreaux's sifaka can be classified as either capital or income breeders, depending on how these concepts are operationalized. These conflicting findings highlight why the capital/income framework is currently problematic and must be standardized if it is to be a useful framework for primatologists.