Duke University Primate Center Research Articles

Sex Ratio at Birth and Age-Reversed Dominance among Female Varecia

Analysis of 283 offspring born at the Duke University Primate Center show that young female ruffed lemurs, Varecia variegata, produce significantly more daughters, whereas old mothers produce more sons than expected. Data are compared to 3 hypotheses for sex ratio bias: the Trivers-Willard hypothesis which predicts that dominant females produce more males, the local resource competition (LRC) hypothesis which predicts that subordinate females produce more males, and the local resource enhancement (LRE) extension of the LRC hypothesis that females produce the sex that provides later cooperative benefits. In the case of Varecia, this may include alloparenting or cooperative breeding. The results are more consistent with the LRC model. However, observations of 8 mother-daughter relationships show that female dominance rank in free-ranging Varecia groups is age reversed, with daughters aggressively outranking their mothers. Daughters born into the group were not beneficial as future supporters in within-group intermatriline competition as assumed by the LRE model, or as subordinate alloparents, cooperative breeders or aids in territorial defense. Both sex ratio and ranking observations are consistent, however, with the hypothesis that mothers produce daughters when they are young and able to invade elsewhere and sons as they age and are less able to do so. This is supported by a single observation of a mother dispersing which resulted in her daughter inheriting the natal territory. These data are supportive of the LRE model with female alliances and cooperative breeding among dispersed females.

Paternal Care in Propithecus verreauxi coquereli

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.

Kinematics of bipedalism in Propithecus verreauxi

AbstractBipedalism is rare in primates and has evolved in two distantly related groups: hominoids and indrids. Although copious data are available on the mechanics of bipedal locomotion in hominoids and vertical clinging and leaping (VCL) in indrids, no research has addressed the unique mode of bipedal locomotion exhibited by select indrid primates. Propithecus verreauxi is a highly specialized indrid vertical clinger and leaper that uses a peculiar form of bipedalism on the ground. The objectives of this study were to describe the bipedal gait of Propithecus, to assess the influence of VCL specializations on the kinematic patterns and propulsion mechanisms used by Propithecus during bipedalism, and to compare Propithecus bipedalism with the bipedal gaits of other primates capable of using bipedalism. Video was collected of five adult P. verreauxi moving bipedally in a seminatural setting at the Duke University Primate Center. Duty factor, footfall patterns, joint angles and center of mass movement were quantified in the sagittal plane for 73 steps. Propithecus uses a bipedal gallop, a gait unique to Propithecus. The kinematic similarities (e.g. large hip and knee angular excursions and preparatory countermovements) between bipedal galloping and VCL lead us to suggest that Propithecus takes advantage of specializations for VCL to conserve energy during bipedal galloping. Propithecus also walks bipedally at slower speeds. When Propithecus walks, it utilizes a relatively compliant gait similar to that of other primate facultative bipeds (Pan, Hylobates). During bipedal walking, energy conservation may be sacrificed for increased balance and reduced joint loads.

Semantic Differences in Sifaka (Propithecus verreauxi)Alarm Calls: A Reflection of Genetic or Cultural Variants?

AbstractIn this study, we compared the usage of alarm calls and anti‐predator strategies between a captive and a wild lemur population. The wild lemur population was studied earlier in Western Madagascar (Fichtel & Kappeler 2002). The captive population was studied in outdoor enclosures of the Duke University Primate Center. Alarm calls and anti‐predator behavior were elicited by conducting experiments with both vocal and visual dummies. We scored the subjects’ immediate behavioral responses, including alarm calls, from video recordings made during the experiments. In principle, both populations have a mixed alarm call system with functionally referential alarm calls for aerial predators and general alarm calls for terrestrial and aerial predators and for situations associated with high arousal, such as group encounters. Although wild and captive sifakas exhibit the same alarm call system and use the same alarm call types, we discovered striking differences in the usage and perception of some of the alarm calls. We argue that these differences indicate either an evolutionary drift in the meaning of these calls or reflect cultural variation. The latter possibility is consistent with our understanding of the ontogeny of call usage and comprehension.

Retrospective evaluation of the incidence and severity of hemosiderosis in a large captive lemur population

Significant concern has been generated about the susceptibility of captive lemurs to iron storage disease, which has led some researchers to propose husbandry changes regarding dietary iron. In the current study we sought to determine the history, severity, and prevalence of iron storage disease within a large captive lemur population. Iron concentration and hemosiderin accumulation in a target organ, the liver, were assessed in necropsy specimens from 15 different species (n=153) of lemurs over a 12-yr period at the Duke University Primate Center. Banked liver tissue was used to quantify liver iron concentration (LIC) via neutron activation analysis (NAA). Prussian blue staining was used to accentuate the presence of liver iron for evaluation using an established scoring system. Of the 153 reports examined, 49 (32%) of the animals were considered positive for the presence of hemosiderin in the liver, lymph node, duodenum, and kidney, with 36 of the 49 (73%) showing deposition of iron in the liver. Total iron scores (TIS) ranged from 0.3+/-0.3 in Lemur catta to 33.3+/-1.7 in Cheirogaleus medius. The mean LIC ranged from 209+/-1.4 microg/g wet weight in L. catta to 2957+/-414 microg/g in C. medius. Management practices may have contributed to some of the results observed in this study. Although evidence of excess iron deposition in the liver was present across several species studied, the levels were not as pervasive as previously reported in other captive lemur populations. Hemochromatosis was not observed, and excess iron was not related to the cause of death in any of the animals studied. The current findings suggest that iron overload in lemurs may be more complex than was previously believed.

Patterns of participation and free riding in territorial conflicts among ringtailed lemurs (Lemur catta)

Cooperation in animal social groups may be limited by the threat of “free riding,” the potential for individuals to reap the benefits of other individuals’ actions without paying their share of the costs. Here we investigate the factors that influence individual contributions to group-level benefits by studying individual participation in territorial defense among female ringtailed lemurs (Lemur catta). To control for potentially confounding factors, particularly group size, we studied two semi-free-ranging groups at the Duke University Primate Center. First, we used a combination of experimental and observational methods to investigate the costs and benefits of territorial defense for individual lemurs. We found three indications of costs: physical contact occurred during inter-group encounters, participation in territorial defense was negatively correlated with ambient temperature, and rates of self-directed behaviors increased during encounters. Benefits were more difficult to quantify, but observational and experimental tests suggested that individuals shared the gains of territorial defense by foraging in defended territories. Thus, during experiments in which one of the groups was prevented from defending its territory, the free-ranging group made more frequent incursions into the other group’s territory. Second, we examined variation in participation in territorial defense. Individuals varied significantly in their rates of aggression and genital marking during inter-group encounters. The extensive variation documented among individuals was partially accounted for by dominance rank, kinship and patterns of parental care. However, we found no evidence to suggest that participation was enforced through punishment (policing) or exchange of benefits involving grooming. In conclusion, this study provides further insights into cooperative behavior in mammalian social groups by revealing how the costs and benefits of territoriality influence patterns of individual participation in the context of shared (collective) goods.

The potential effects of sex, posture and living condition on lateralized behaviors in ring-tailed lemurs (Lemur catta)

This research explores the effects of posture, sex, and living condition on hand and side preferences of semi-free-ranging, adult ring-tailed lemurs (Lemur catta) housed at the Duke University Primate Center in Durham, NC. Data were collected on 11 adult individuals (five females and six males) during normal daily activities over a ten-week period from May–July 2001. Variables analyzed in this study include unimanual behaviors (i.e., reach, hold, and limb used to start locomotion) and other potentially lateralized behaviors that do not involve handuse (i.e., whole-body turning and tail position). The data were analyzed to investigate potential individual and population level side biases for each behavior; potential sex biases in side preference for each behavior; and for ‘reach’, potential effects of posture (sitting, tripedal stance, or bipedal stance) on individual hand preferences. Additionally, to investigate potential effects of living condition on lateral biases, the data from this study were compared to data collected on the same individual Lemurs living under more restrictive living conditions during the previous year. Largely, as predicted based on available literature, we found that there was a significant sex difference across all hand-use categories and for whole-body turning, and that posture was a significant factor in the expression of hand preference for reaching. Contrary to previous research, the effect of living condition on lateral preferences was minimal, and no side preferences were found at the population level for any of the behaviors analyzed.

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 of E. m. flavifrons, our data strongly suggest that this subspecies can be characterized as female dominant.

Lateral bending of the lumbar spine during quadrupedalism in strepsirhines

Much research has been devoted to spinal kinematics of nonmammalian vertebrates, while comparatively little is known about the locomotor role of spinal movements in mammals, especially primates. This study, conducted at the Duke University Primate Center, examines the function of lateral spinal bending during quadrupedal walking among a diverse sample of strepsirhines. The taxa studied include Loris tardigradus (1), Nycticebus coucang (1), N. pygmaeus (1),Cheirogaleus medius (2), Varecia variegata (2), Eulemur fulvus (2), and a total sample size of 261 strides. Lateral bending varies among the taxa with respect to both magnitude and effects of velocity, and does not appear to be correlated with body size. In addition, the timing of lateral bending during a stride appears to differ from that reported for other (nonmammalian) tetrapods. On average, maximum lateral flexion occurs just after ipsilateral foot touchdown, which may be functionally associated with touchdown of the contralateral forelimb during diagonal sequence gait. For some of the taxa, lateral flexion coincides more closely with foot touchdown as velocity increases, suggesting a functional role in increasing hindlimb stride length. Both of these timing patterns contrast with those reported for lizards. Finally, although lorids as a group have been described as having a “sinuous” gait, this study shows more pronounced lateral flexion in Nycticebus than in Loris.

Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta.

The objective of this project was to better define the similarities and differences in gastrointestinal morphology present in lemur species. Measurements of the gastrointestinal tract of lemurs were obtained at necropsy from the captive population at Duke University Primate Center. Measurements of body length and weight, as well as gastrointestinal length, were recorded from five prosimian species: Propithecus tattersalli, Propithecus verreauxi, Varecia variegata, Hapalemur griseus, and Lemur catta. Photographs and measurements were used to obtain illustrations. Preliminary results suggest differences in gastrointestinal morphology among lemur species that coincide with differences in diet. Distinct sacculations in either the cecum or the colon were present for H. griseus, L. catta, P. verreauxi, and P. tattersalli, but not for V. variegata. The Propithecus specimens possessed a much greater ratio of gastrointestinal length to body length than the other three species. A short, blunt cecum and a shortened and sacculated colon were unique characteristics of the H. griseus specimens. These differences correlate well with a dietary shift from consumption of large amounts of structural plant cell wall (Propithecus sp.) to consumption of variable or moderate amounts (H. griseus, L. catta, and V. variegata). They also suggest that captive groups would benefit from further diet refinement in captivity.

Group histories and offspring sex ratios in ringtailed lemurs ( Lemur catta )

Birth sex ratios were examined for ringtailed lemurs (Lemur catta) at the Duke University Primate Center. This population provides a long-term database of births under a variety of demographic and management conditions, including two semi-freeranging groups between which males transfer freely and females defend stable territorial boundaries. We examined three hypotheses usually considered in studies of primate sex ratio bias. The Trivers-Willard hypothesis predicts that dominant females produce males, local resource competition at the population level (LRC-population) predicts that the dispersing sex (males) will be overproduced in dense populations, and local resource competition among individuals (LRC-individual) predicts that dominant females overproduce the philopatric sex (females). We also examined a fourth hypothesis, local resource enhancement (LRE), which is usually subsumed under LRC-individual in studies of primate sex ratio evolution. LRE predicts that under certain conditions, females will produce the sex that provides later cooperative benefits, such as alliance support for within- or between-group competition. Our data provide support for LRE: females overproduce daughters given prospects of new group formation, either through group fission or threatened expulsion of young mothers. Behavioral data from Duke and also wild populations show that daughters serve mothers as important allies in this context and LRE effects also have been documented in other mammals that experience similar group histories. Nonsignificant trends in the data supported the LRC-population hypothesis, and we suggest that LRC interacts with LRE to explain offspring sex ratios in ringtailed lemurs.

Description of the gastrointestinal tract of five lemur species:Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus,andLemur catta

The objective of this project was to better define the similarities and differences in gastrointestinal morphology present in lemur species. Measurements of the gastrointestinal tract of lemurs were obtained at necropsy from the captive population at Duke University Primate Center. Measurements of body length and weight, as well as gastrointestinal length, were recorded from five prosimian species: Propithecus tattersalli, Propithecus verreauxi, Varecia variegata, Hapalemur griseus, and Lemur catta. Photographs and measurements were used to obtain illustrations. Preliminary results suggest differences in gastrointestinal morphology among lemur species that coincide with differences in diet. Distinct sacculations in either the cecum or the colon were present for H. griseus, L. catta, P. verreauxi, and P. tattersalli, but not for V. variegata. The Propithecus specimens possessed a much greater ratio of gastrointestinal length to body length than the other three species. A short, blunt cecum and a shortened and sacculated colon were unique characteristics of the H. griseus specimens. These differences correlate well with a dietary shift from consumption of large amounts of structural plant cell wall (Propithecus sp.) to consumption of variable or moderate amounts (H. griseus, L. catta, and V. variegata). They also suggest that captive groups would benefit from further diet refinement in captivity.

Infant killing, wounding and predation in Eulemur and Lemur

Infant killing by primates is highly controversial. Sexual selection of infanticidal males has been disputed, especially for seasonally breeding species, in which death of an infant does not advance conception of the next infant. We report attacks, infants found wounded, and predation in seasonally breeding Eulemur and Lemur at Berenty, Beza Mahafaly and Duke University Primate Center, and review cases seen elsewhere. Observed attacks leading to wounds or death conservatively total twelve by extratroop males, two by troop males, and seven by troop females. Eulemur are occasional vertebrate predators, whose prey includes infant Lemur catta. Wounds inflicted by lemurs are usually abdominal canine slashes or bites to the head, with rare eating, a pattern distinct from carnivore and raptor kills. Infant killing as inferred from corpses is more frequent than previously thought, but still rare. Adaptive advantages of killing plausibly include eliminating resource competitors of females, and sexual selection on males.

The socioecology of the ringtailed lemur: Thirty-five years of research

Linnaeus' original scientific description of Lemur catta, the ringtailed lemur, was based on a living animal brought to England in 1749. Although there were many brief descriptions of wild ringtailed lemurs, it was not until Jolly wrote her now classic book, Lemur Behavior, that we had our first detailed description of the natural history of these beautiful animals (Fig. 1). Since then, long-term field studies, mainly from two study sites in Madagascar, Berenty and Beza Mahafaly (Fig. 2), as well as studies on forest-living groups in captivity at the Duke University Primate Center in Durham, North Carolina, have greatly expanded our knowledge of the ecology and behavior of this species (Table 1, Box 1). Thirty-five years of research on this species at these various sites indicates that Lemur catta is proving to be every bit as complex in its behavior as are many anthropoid primates. This very complexity has been reflected in the current controversies and questions concerning the ecology and behavior of this species.

Management of the Grey gentle or Eastern lesser bamboo lemur Hapaletnur griseus griseus at Duke University Primate Center, Durham

Since 1970 Duke University Primate Center, Durham. has maintained Grey gentle lemurs Hapalemur griseus griseus. This paper gives an overview of the status of Hapalemur spp in captivity and provides an introduction to their conservation status and natural history in Madagascar. Husbandry techniques developed at the Primate Center, with emphasis on the special needs of ♀♀ and infants, are discussed. Scent marking, vocalizations. ♀ dominance, breeding. infant development and hand‐rearing are described. Information on natural‐habitat enclosures. diet and health concerns is also given.

Body weights of wild and captive lemurs

The mean body weight of a species is often used as a summary measure of size in evolutionary and functional studies. Additionally, body weight is often used to assess the health of captive animals. Contrasts of the captive and wild body weights of a species can be used to examine the effects of captivity on the species. We provide an analysis of adult body weight in nine taxa of Malagasy lemurs. We compare weights of wild and captive lemurs and provide analyses of relationships between captive weight variation and management actions. Body weights are derived from a number of sources, the majority from the Duke University Primate Center (DUPC) capture and husbandry records. Captive animals are, on average, heavier than wild conspecifics. However, the difference is significant in only three taxa (Hapalemur griseus griseus, Eulemur coronatus, E. macaco flavifrons). Based on a retrospective analysis of DUPC records, we assess patterns of adult weight relative to caging conditions and evaluate changes in mean weight over a period of approximately 20 years. Cage type appears to have no effect on body weight. Mean weight has decreased for some taxa housed at the DUPC over time. We calculate a weight-based criterion for identifying obese animals and demonstrate that obesity is not currently a prevalent condition in DUPC lemurs. Examinations of the physiological correlates of excessive weight, and especially relationships between weight and reproductive success, await further analysis. These analyses need to be based, in part, on reliable measures of body weight. We suggest that systematic weighing of wild and captive animals is important for further examinations of the overall health of captive animals as well as for studies ranging in scope from evolutionary to clinical. Zoo Biol 16:17–30, 1997. © 1997 Wiley-Liss, Inc.

Phylogenetic Affinities Among the Extant Malagasy Lemurs (Lemuriformes) Based on Morphology and Behavior

The difficulty in achieving a consensus on the phylogenetic relationships of lemuriform primates has been due largely to the lack of a lemur fossil record and to the lack of an appropriate outgroup that would facilitate polarization of character states. Recent findings allow us to polarize some of the bony characters, but to a large extent this problem still remains. In the past, phylogenetic analyses have focused on specialized character sets such as dentition or basicranial traits, or they have employed differential weighting schemes to a more variable set of characters. In the analysis presented here, I combined all relevant characters available in the literature into one data set but restricted my selection to those traits having discontinuous states and for which no contradictory coding schemes were published. I reduced the assumptions in this analysis by removing most external weighting and ordering effects on these data sets. The available data from the literature were supplemented with data from my own observations at the Duke University Primate Center. Data were collected for 25 characters and 20 taxa and were submitted to a cladistic analysis. Some important findings from this study include support for (1) a sister-group relationship between Lepilemur and the Indridae, (2) a sister-group relationship between the Lemuridae (except Varecia) and the Indridae/Lepilemur clade, (3) a monophyletic genus Eulemur, and (4) the exclusion of Varecia from the Lemuridae.

Dental microwear and microstructure in early oligocene primates from the Fayum, Egypt: implications for diet.

Textbook descriptions usually portray the Fayum anthropoideans as frugivores, with Parapithecus grangeri including a folivorous component in its diet and Apidium a component of hard-object feeding. Recent work with modern mammals has shown that analyses of both dental microwear and dental microstructure may yield insights into diet and tooth use. The purpose of this study was to combine these two techniques to gain a better perspective on the paleobiology of the Fayum higher primates. Dental microwear analyses involved the use of high resolution epoxy casts of Aegyptopithecus, Parapithecus, and Apidium housed in the Duke University Primate Center. Scanning electron micrographs were taken at x500, and all microwear features in each micrograph were digitized. For microstructure analyses, molar teeth were sectioned in a variety of planes, lightly etched, and photographed in the SEM. Results of the dental microwear analyses indicate that the three Fayum anthropoideans all clustered with modern primate frugivores but that there were also significant differences between Aegyptopithecus and the other two Fayum genera. By contrast, dental microstructure analyses showed important differences between Apidium and the other two genera. The reason for these differences probably lies in a combination of body size and dietary differences, with Aegyptopithecus occasionally feeding on hard objects and Apidium maximizing wear resistance through a unique emphasis of radial (rather than decussating) enamel.

The nature and frequency of agonism in free-ranging and semi-free-ranging brown lemurs,Eulemur fulvus

Agonistic behaviour was studied in three groups each of free-ranging and semi-free-ranging brown lemurs (Eulemur fulvus) at Berenty, Madagascar and the Duke University Primate Center (DUPC) respectively. The purpose of the study was to answer questions arising from the work of other researchers regarding the frequency and intensity of agonism in this species. Authors of field studies generally concluded that agonism was rare and mild, whereas those who had studied semi-free-ranging or captive animals at the DUPC reported intense agonism during the peaks of the mating and birth seasons, with sometimes fatal wounding occurring among captive animals. I recorded 30 agonistic behaviours or “signals” which I grouped into seven general categories — cuffs, other physical contact, threats, chases, third party intervention, unprovoked submissive signals, and reciprocal aggression. The seven categories represent the types of signals which initiated or otherwise defined agonistic interactions, regardless of whether or not there was a submissive response to aggression. The relative percentages of all agonism constituted by the seven categories were not found to be significantly different between study sites. Agonistic signals were also classified as either subtle or obvious, a classification which crosscut the seven categories. At both study sites, the majority of agonistic signals initiating or defining interactions were subtle. Rates of agonism for the Berenty groups, studied during the birth season only, were significantly lower than those for the DUPC groups during the birth season, possibly due to (1) easier observation conditions at the DUPC, and (2) the impossibility of successful emigration at the DUPC, which might have resulted in social stresses translating into higher rates of agonism. In only one DUPC group was there significant variation in rates of agonism between seasons. I found agonistic behaviour to be mild, at both study sites, in the senses of subtlety of both aggressive and submissive signals, unlikelihood of response to aggression, and virtual absence of wounding; and I noted that serious wounding during other studies at the DUPC involved animals captive in caged runs. Comparing rates of the study groups with rates reported in other research for brown lemurs, other lemuriform species, and some New and Old World anthropoid species, I concluded thatE. fulvus agonism was in fact not rare except in comparison to baboons and macaques.

Deciduous dentition of the aye aye, Daubentonia madagascariensis.

Until the 1980s all interpretations of the deciduous dental formulae of the unusual and endangered prosimian primate Daubentonia madagascariensis were based on a publication more than 125 years old [Peters, 1866a]. Rather than being based on original material all later interpretations were exclusively derived from Peters' figures and descriptions. A relatively recent attempt by Luckett and Maier [1986] to establish the true milk dentition of the aye aye was based on histological evaluation of a late aye aye fetus from the collection of W.W. Hubrecht that was chemically preserved at least 80 years earlier. The death of a newborn aye aye at the Duke University Primate Center in 1992 finally made the following new evaluation of the D. madagascariensis deciduous tooth formula possible. Using X-rays and dissection, it here is demonstrated that aye ayes have one incisor, one canine, and two premolars in both the upper and in the lower milk dentition. Therefore the deciduous dental formula of Daubentonia madagascariensis should read: $${{\hbox{1i}\cdot\hbox{1c}\cdot\hbox{2p}} \over{\hbox{1i}\cdot\hbox{1c}\cdot\hbox{2p}}}.$$ © 1996 Wiley-Liss, Inc.