Reproductive Behavior of Female Propithecus verreauxi at Beza Mahafaly,Madagascar

Prosimian and anthropoid females are generally thought to have divergent reproductive patterns, characterized by circumscribed and situation-dependent receptivity. This dichotomy underpins the traditional view that nonreproductive mating serves a social function in anthropoid females, distinguishing them from prosimians which, like most other mammals, mate only when conception is most probable. Circumscribed estrous cycles differ from anthropoid menstrual cycles by the presence of menstruation, and greater flexibility in timing and longer duration of receptivity in the latter. The degree to which sexual behavior is tightly synchronized to periovulatory events in Propithecus verreauxi was assessed via the behavioral, hormonal, and social correlates of reproduction in a free-ranging population. I collected data from two social groups before and during the 1990–1991 and 1991–1992 breeding seasons at Beza Mahafaly, Madagascar. I also conducted 644 focal-animal hours and collected 485 fecal samples from five marked females in the Vaovao and Vavy Masiaka social groups. Estrus was behaviorally characterized by 0.5–96-h periods of receptivity when females were motivated and willing to mate, the latter not always coincident with periovulatory events. Females exhibited age- and rank-related asynchronous receptivity, and in some cases, periovulatory synchrony within groups. Sifaka were not pair-bonded. Most females mated with multiple males, temporally ordering partners based on male residence and age. Mating was limited by male mate-guarding and sexual aggression by males, female mate competition, and aversions to mating with certain partners. It was facilitated by surreptitious copulations, positive mate choice, and the availability of non-resident mating partners.     

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.     

Reproduction in free-ranging male Propithecus verreauxi: The hormonal correlates of mating and aggression

Endocrine studies of captive strepsirrhine primates suggest that physical environment and social factors mediate inter-individual variations in testicular function and serum testosterone (sT) in males. While these studies have made major contributions to our understanding of the individual proximate mechanisms influencing androgen activity in male strepsirrhines, none have investigated how these mechanisms work coincidentally in free-ranging populations. In this study we used fecal steroid analysis to examine androgen-behavior interactions associated with reproduction in free-ranging male Propithecus verreauxi. Behavioral and hormone data were collected from two social groups during the 1990–91 and 1991–92 breeding seasons at Beza Mahafaly, Madagascar. Solid phase and radioimmunoassay techniques were used to quantify testosterone (T) in 105 desiccated fecal samples collected weekly from seven males. Results suggest that 1) solid phase extraction and radioimmunoassay techniques were reliable and accurate methods for quantifying T in sifaka feces; 2) fecal T (fT) elevations spanned a minimum of 4 months, peak levels occurring 1 month prior to the January onset of the breeding season; 3) fecal T concentrations were influenced by developmental factors and, among mature males, social factors associated with rank, intergroup aggression, and group instability. Am J Phys Anthropol 105:137–151, 1998. © 1998 Wiley-Liss, Inc.     

Application of fecal steroid techniques to the reproductive endocrinology of female verreaux's Sifaka (Propithecus verreauxi)

Solid phase extraction, high performance liquid chromatography, and radioimmunoassay were used to test the validity of fecal steroid analysis for assessing ovarian function in sifaka (Propithecus verreauxi). Daily fecal samples were collected over a 4 month period from two cycling female sifaka, and single samples were collected from females during normal gestation and males while housed at the Duke University Primate Center. Tests of radioimmunoassay validity indicated that solid phase extraction and microradioimmunoassay techniques were reliable and accurate methods for quantifying ovarian steroids in sifaka feces. The progesterone (P₄) antibody specifically quantitated only P₄, while several estrogen metabolites made small contributions to immunoreactive measures of estradiol (E₂). A 1:10 dilution reduced these contributions to 3–15% of the estimated E₂ concentration. Although the spectral data suggested that E₂ was not the major metabolite present, it accounted for the majority of the immunoreactivity at normal assay dilutions. Fecal profiles of immunoreactive E₂ and P₄ in the conceptive female resembled serum profiles of other strepsirhines. E₂ and P₄ were elevated at the end of the conceptive cycle and were more markedly increased in late pregnancy in the two pregnant females. Mating behavior and indices of sexual interest were observed in conjunction with E₂ peaks, although not all peaks were accompanied by observations of sexual behavior. © 1995 Wiley-Liss, Inc.     

Characterization of seven microsatellite marker loci in a genus of Malagasy lemurs (Propithecus)

The sifakas (genus Propithecus) are large, diurnal, lemurs endemic to the island of Madagascar. Throughout the island, lemur species are particularly vulnerable to extinction due to relatively small geographical ranges (Martin 2000). Thus, understanding the taxonomy of these highly endangered primates is essential for taking appropriate conservation action. For this study we collected tissue samples from 68 wild sifakas representing various Propithecus species. Genomic DNA was isolated and polymerase chain reaction (PCR) amplification was carried out. We describe seven microsatellites found to be polymorphic and useful for analysis of the population genetics of sifakas.     

Characterization of 21 microsatellites developed from Propithecus deckeni deckeni

Decken's sifaka (Propithecus deckeni deckeni) is found between the Mahavavy and Manambolo Rivers, in western Madagascar. Twenty‐one polymorphic nuclear microsatellite loci were isolated from genomic DNA derived from a P. d. deckeni, from Tsingy de Bemaraha National Park. Population genetic parameters were estimated on 10 individuals each, sampled from Tsingy de Bemaraha National Park and Tsiombikibo Classified Forests. Significant null alleles were detected in seven loci which were dropped before population genetic parameters were re‐estimated and compared to the full marker suite.     

Characterization of 20 microsatellite marker loci in Coquerel's sifaka (Propithecus coquereli)

The Coquerel's sifaka (Propithecus coquereli) is one of the species of Propithecus, living in the dry forest of northwest Madagascar. This species is endangered due to the loss and fragmentation of its natural habitat, consequential of deforestation. Twenty nuclear microsatellite loci were isolated from genomic DNA derived from a free ranging Coquerel's sifaka from the Mariarano Classified Forest, Madagascar. Population genetic parameters were estimated as baseline values from samples collected in that forest.     

Birth season glucocorticoids are related to the presence of infants in sifaka (Propithecus verreauxi)

The responses of plural breeding mammals to environmental stressors are little understood in free-ranging populations, but recent studies of singular breeders suggest that ecological factors and social milieu influence the variable physiological stress responses observed among individuals. Our previous studies examining faecal glucocorticoid (fGC)–behaviour interactions in plural breeding male sifaka (Propithecus verreauxi) show that fGC elevations coincide with specific dispersal events, particularly the eviction of subordinates by resident alpha males. This study examined the utility of fGC assays for assessing the stress responses of male sifaka to demographic changes in the population during the birth season. Analyses were based on 889 faecal samples collected over five birth seasons from 124 adult males residing in 55 different groups at Beza Mahafaly, Madagascar. Results show that fGC levels in males are unrelated to age, residence, group stability or rank, but are significantly and positively correlated with the presence of infants, annual elevations in weekly mean fGC concentrations in males paralleling increasing numbers of infants born annually in the population. These data are the first to show that in seasonal plural breeding species such as sifaka, elevated fGC in males reflects specific events related to reproduction rather than states or social context during the birth season.     

Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux's sifakas (Propithecus verreauxi verreauxi)

The production of vocalizations in nonhuman primates is predominantly innate, whereas learning influences the usage and comprehension of vocalizations. In this study, I examined the development of alarm call recognition in free-ranging infant Verreaux's sifakas. Specifically, I investigated their ability to recognize conspecific alarm calls as well as those of sympatric redfronted lemurs (Eulemur fulvus rufus) in Kirindy forest, western Madagascar. Both species have functionally referential alarm calls for aerial predators and give general alarm calls for both aerial and general predators and also other kinds of threats, such as intergroup encounters with conspecifics. I conducted playback experiments with members of two birth cohorts (nine and ten individuals) to determine the age at which infant Verreaux's sifakas discriminate between conspecific alarm calls, heterospecific alarm calls, and non-alarm vocalizations (parrot song). Most 3-4 months old infants fled toward adults after hearing any playback stimuli, whereas 4-5-month-old infants did so only after presentation of alarm calls. Moreover, all infants of these age classes showed a longer latency to flee after the parrot song indicating their emerging ability to discriminate between alarm calls and non-alarm stimuli. At an age of about 6 months, infants switched from fleeing toward adults to performing adult-like escape responses after presentation of conspecific and heterospecific alarm calls. Thus, the ability to discriminate between alarm from non-alarm stimuli precedes the appearance of adult-like responses. The transition to adult-like escape behavior was coincident with the physical independence of infants from their mothers.     

Characterization of 13 microsatellite marker loci in Verreaux's sifaka (Propithecus verreauxi)

The Verreaux's sifaka (Propithecus verreauxi) is one of the species of Propithecus, living in the dry forest of southwest Madagascar. This species is endangered due to the loss and fragmentation of its natural habitat, a consequence of deforestation. Thirteen novel nuclear microsatellite loci were isolated and characterized in three populations of Verreaux's sifaka. The marker suite proved informative with an average of 8.9 alleles per locus and observed heterozygosity across the three populations of 0.675.     

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.     

Characterization of 21 microsatellite marker loci in the silky sifaka (Propithecus candidus)

The silky sifaka, Propithecus candidus, considered one of the rarest and most endangered primates in the world, exists in only a few fragmented forests in northeastern Madagascar. This species faces increasing pressures as a direct result from loss of habitat in the form of tavy (slash and burn agriculture), illegal logging and mining along with hunting for subsistence, even within protected areas. We report a marker suite of 21 loci developed from genomic DNA from a silky sifaka collected in 2003 from Anjanaharibe-Sud Special Reserve. Polymorphism of each locus evaluated in 18 individuals pooled from Marojejy National Park and Anjanaharibe-Sud Special Reserve. The number of observed alleles per locus ranges from 2 to 7. The observed and expected heterozygosity were 0.389–0.889 and 0.322–0.789, respectively. The information revealed in this study will provide useful tools for further study of the social structure and population dynamics of the silky sifaka to facilitate conservation management in the imminent future.     

Paternal Care in <Emphasis Type="Italic">Propithecus verreauxi coquereli</Emphasis>

Alloparental behavior is documented for several anthropoid primates, but few researchers have investigated the extent or variability of such behavior in prosimians. We report results from a study of male-infant interactions in 2 groups of Coquerel’s sifaka (Propithecus verreauxi coquereli) at the Duke University Primate Center (DUPC). Both groups contained 1 adult pair, 2 juveniles, and a newborn. The adult males exhibited paternal behavior toward their offspring in the form of grooming and holding the infant, though males differed in the amount of time they spent engaged in these activities. Group differences in the proximity maintained between the infants’ parents suggest that the relationship between adult males and females may help account for the variation. The presence of juveniles appeared to diminish paternal behavior in the group exhibiting a higher overall rate of male-infant interaction.     

Sex differences in scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

In this study we compared the scent-marking rates of females with those of males. Specifically, we examined the ability of season, dominance status, and natal status to explain the frequency of scent marking in female sifakas living wild in Ranomafana National Park, Madagascar, and compared the results with those published for males [Pochron et al., American Journal of Primatology, in press]. We also sought to determine whether vulnerability to infanticide affects marking frequency in adults of either sex, and whether female reproductive status affects female marking behavior. We found that males marked at twice the rate of females, and like males, females in single-female groups marked at the highest rates. Dominant females and non-natal females marked at higher rates than did subordinate females and natal females, a pattern also seen in males. This suggests that scent marks may convey important information about status. Neither females nor males varied their marking frequency with the presence of vulnerable infants. Females did not alter marking frequency with reproductive state, and like males, they marked at higher rates in the period prior to the mating season than they did in the mating season itself. This implies that females may use scent marks more for intrasexual aggression or territoriality than for mate attraction.     

Spatial variation in density and total size estimates in fragmented primate populations: the golden‐crowned sifaka (Propithecus tattersalli)

The golden‐crowned sifaka (Propithecus tattersalli) is an endangered lemur species found only in the Daraina region, a very restricted area in north‐eastern Madagascar. Its forest habitat is highly fragmented and expected to suffer from significant changes in the near future. The species is poorly known and only one census study, carried out in 2000, has ever been published. It is thus crucial to update the conservation status of the golden‐crowned sifaka before major anthropogenic environmental changes take place. Using the line‐transect approach, we estimated the species density in the main forest fragments located in both the peripheral and central parts of the distribution range, including both protected and unprotected areas. In parallel, we tried to determine whether an edge effect could be detected by comparing densities at different distances from the forest edges. We found important variation of sifaka densities among forest fragments. The total species abundance is thus difficult to determine, but we estimated that it is likely to be over 18,000, two to three times higher than previously thought. However, our data also suggested that most P. tattersalli live in forests located in the central part of the distribution range and that the estimated densities in the central part were high (>80 individuals/km²). Two forest fragments, found to host a large part of the total population, are currently outside the managed area and their incorporation to the managed area is strongly recommended. Lastly, as expected for a folivorous and not heavily hunted species, our results are consistent with the hypothesis that this species does not experience a clear edge effect, at least during the first half of the dry season. This could be due to a high resiliency to habitat fragmentation or to the fact that fragmentation has been going on for some time. Am. J. Primatol. 72:72–80, 2010. © 2009 Wiley‐Liss, Inc.     

Characterization of twenty-one microsatellites developed from <Emphasis Type="Italic">Propithecus diadema</Emphasis>

Diademed sifaka (Propithecus diadema) distributed throughout Madagascar’s eastern rain forests from the Mangoro and Onive Rivers north to the Mananara River. Twenty-one polymorphic nuclear microsatellite loci were isolated from genomic DNA derived from a P. diadema, from Mantadia National Park. Population genetic parameters were estimated on 10 individuals each, sampled from Mantadia National Park and Maromizaha Unprotected Forest. Allele sizes ranged from 4 to 14 and observed heterozygosities ranged from 0.200 to 0.900 per locus. This marker suite will be informative in further population genetic studies.     

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.     

Characterization of 20 microsatellites developed from <Emphasis Type="Italic">Propithecus deckeni coronatus</Emphasis> with cross-amplification in <Emphasis Type="Italic">Propithecus deckeni deckeni</Emphasis>

The crowned sifaka (Propithecus deckeni coronatus) is found between the Mahavavy the Betsiboka Rivers in either Anjahamena or Antrema Classified Forest. The crowned sifaka is endangered due to the loss and fragmentation of its natural habitat by deforestation. Twenty polymorphic nuclear microsatellite loci were isolated from genomic DNA derived from a P. d. coronatus from Anjahamena, Madagascar. Population genetic parameters were estimated on 10 individuals sampled from Anjahamena, Madagascar, to determine marker utility and preliminary baseline values to study the species’ genetic diversity and phylogeography. In a cross-amplification test, each marker in the suite was informative in P. d. deckeni.