Possible Infanticidal Event of an Aye-Aye (Daubentonia madagascariensis) in Torotorofotsy, Madagascar.

Infanticide occurs in an array of mammalian species, especially primates. Most infanticidal events occur in polygynous societies, though they sometimes happen in nongregarious populations. We witnessed a possible infanticidal event of a 3-month-old male aye-aye, a species that exhibits a dispersed multimale social system, in Torotorofotsy, Madagascar. Though firsthand killing of the infant was not observed, physical injuries to the infant, vocalizations of the adult female, and her subsequent chase of the adult male aye-aye strongly indicates infanticide. If true, this would be the first recorded incident of an infanticidal event in a noyau primate. The evidence for three different explanations of infanticide is evaluated.

Female Power: A New Framework for Understanding "Female Dominance" in Lemurs.

Female dominance is often associated with lemurs. However, consensus does not exist among primatologists on how to define, measure, or explain female dominance. This review explores the utility of applying a broader concept of power to understanding lemur intersexual relationships. In this framework, power is defined as arising from an asymmetry in a dyadic relationship and can be divided into 2 types: dominance and leverage. Intersexual asymmetries based upon females having superior fighting ability are considered female dominance. However, economic power also exists, and females with resource-based power exhibit female leverage. Additionally, power has 4 characteristics (base, means, amount, and scope) that describe the precise nature of observed phenomena. This article utilizes the 4 characteristics outlined in the power framework to review the existing "female dominance" literature for lemurs and highlights the value of adopting both an expanded concept of power and a more precise language. By placing the multiple phenomena currently labeled under the single term "female dominance" within the power framework, much of the confusion disappears. Thus, not only is the debate reframed, facilitating endeavors to find evolutionary explanations, but the uniqueness of female power in lemurs can be determined empirically rather than by definition.

Intra-specific variation in social organization of Strepsirrhines.

Strepsirrhines, that is, lemurs, galagos, and lorises, are considered basal primates, making them important to understand the evolution of primate sociality. Apart from some lemurs, they are nocturnal and solitary living, though the view of their sociality nature has changed with field studies being completed. We conducted a review of the primary literature about the social organization (group composition) of strepsirrhines, with the aim to determine whether intra-specific variation in social organization (IVSO) occurs and to determine how many species are pair-living, group-living, or solitary living. We found data in 83 peer-reviewed studies for 43 of the 132 strepsirrhine species and compared our results using two databases on social systems of mammals published in 2011 and 2013. While it is often assumed that primates show relatively fixed social organizations, we found that 60.5% of species for which data exist have IVSO. We found only 7% of the species to be truly solitary living (with 34.9% additional species to be sometimes solitary living), which is in contrast to the other databases, which had reported 60.9% and 37.7% of species to be solitary. We further explored group compositions by designating "functional groups" (e.g., foraging, breeding, and infant care groups). While functional groups might explain IVSO within a single species, this was not consistent over species with IVSO, such that IVSO was poorly explained by functional groups. Our study supports the view that most strepsirrhines are social (58.1% of species with another 34.9% of species sometimes living in pairs or groups) and show complex and often variable social organizations; reinforcing the assumption that the ancestor of all primates was social and not solitary.

Why aye-ayes see blue.

The capacity for cone-mediated color vision varies among nocturnal primates. Some species are colorblind, having lost the functionality of their short-wavelength-sensitive-1 (SWS1) opsin pigment gene. In other species, such as the aye-aye (Daubentonia madagascariensis), the SWS1 gene remains intact. Recent studies focused on aye-ayes indicate that this gene has been maintained by natural selection and that the pigment has a peak sensitivity (lambda(max)) of 406 nm, which is -20 nm closer to the ultraviolet region of the spectrum than in most primates. The functional significance behind the retention and unusual lambda(max) of this opsin pigment is unknown, and it is perplexing given that all mammals are presumed to be colorblind in the dark. Here we comment on this puzzle and discuss recent findings on the color vision intensity thresholds of terrestrial vertebrates with comparable optics to aye-ayes. We draw attention to the twilight activities of aye-ayes and report that twilight is enriched in short-wavelength (bluish) light. We also show that the intensity of twilight and full moonlight is probably sufficient to support cone-mediated color vision. We speculate that the intact SWS1 opsin pigment gene of aye-ayes is a crepuscular adaptation and we report on the blueness of potential visual targets, such as scent marks and the brilliant blue arils of Ravenala madagascariensis.

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis).

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair-living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio-collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair-living anthropoid primates. Findings support the hypothesis that social relations in pair-living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode.

Grooming patterns in Verreaux's sifaka.

Lemur grooming has received very little attention in the literature. Nevertheless, allogrooming in lemurs has been suggested to be fundamentally different from the grooming of anthropoids. One reason is that lemurs generally rely on oral rather than manual grooming. Lemur allogrooming has also been suggested to serve less of a social function than has been attributed to anthropoid grooming. I analyzed the allogrooming behaviors of 29 Verreaux's sifaka (Propithecus verreauxi) living in five social groups in the Kirindy Forest of Madagascar. Based upon 1,586 observation hours, I found that sifaka, like anthropoids, spend very little time mutual grooming (2+/-3%). Half of all allogrooming involved parts of the body that could have been easily groomed by the recipient, such as the limbs. Even though ectoparasite loads are expected to be greater during the rainy season, allogrooming did not increase during the rainy season. Allogrooming rates were influenced by both rank and sex, and increased by 50-100% during the mating season. The results of this study suggest that allogrooming in Verreaux's sifaka plays an important social function, even though it is performed with a toothcomb.

Design, delivery and perception of condition-dependent chemical signals in strepsirrhine primates: implications for human olfactory communication.

The study of human chemical communication benefits from comparative perspectives that relate humans, conceptually and empirically, to other primates. All major primate groups rely on intraspecific chemosignals, but strepsirrhines present the greatest diversity and specialization, providing a rich framework for examining design, delivery and perception. Strepsirrhines actively scent mark, possess a functional vomeronasal organ, investigate scents via olfactory and gustatory means, and are exquisitely sensitive to chemically encoded messages. Variation in delivery, scent mixing and multimodality alters signal detection, longevity and intended audience. Based on an integrative, 19-species review, the main scent source used (excretory versus glandular) differentiates nocturnal from diurnal or cathemeral species, reflecting differing socioecological demands and evolutionary trajectories. Condition-dependent signals reflect immutable (species, sex, identity, genetic diversity, immunity and kinship) and transient (health, social status, reproductive state and breeding history) traits, consistent with socio-reproductive functions. Sex reversals in glandular elaboration, marking rates or chemical richness in female-dominant species implicate sexual selection of olfactory ornaments in both sexes. Whereas some compounds may be endogenously produced and modified (e.g. via hormones), microbial analyses of different odorants support the fermentation hypothesis of bacterial contribution. The intimate contexts of information transfer and varied functions provide important parallels applicable to olfactory communication in humans. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Use of social network models to understand play partner choice strategies in three primate species.

Although play is seen in many species, its evolutionary function is still largely unknown. Several relevant, proposed hypotheses (such as the training for the unexpected, self-assessment, social skills, and dominance hierarchy hypotheses) make predictions about how animals should optimally choose their play partners based on their familiarity or other demographic variables. We used a social network approach to analyze focal sample data on brown capuchins (Cebus apella), hamadryas baboons (Papio hamadryas), and diademed sifaka (Propithecus diadema) to understand how these species choose their play partners with respect to demographic variables. Using exponential random graph models (ERGMs), we found that sifaka and capuchins generally tended to play with animals who were similar to them. The baboons were only sensitive to age differences in the formation of strong play relationships. Our data most strongly support the training for the unexpected hypothesis, as according to predictions all species preferred to play with animals who were their close social partners, decreasing the possibility of cheating during play. Through the first application (to our knowledge) of ERGMs to primate behavior, we were able to compare the effects of many demographic variables on the complex, interdependent social structure of primates. Applying this tool to additional groups and species will provide further insight into evolutionary mechanisms of play behavior across taxa.

Intergroup relations and home range use in Verreaux's sifaka (Propithecus verreauxi).

Relationships between neighboring groups feature prominently in socioecological theory, but few empirical studies have focused on the effects of neighbors on the behavior of primates. Interactions between neighboring groups are most conspicuous during intergroup encounters, but the likelihood of encounters with neighbors can also affect ranging and activity patterns indirectly, and, as a result, behavioral patterns in areas of exclusive use may differ from those in overlap areas of adjacent home ranges. The aim of this study was to examine intergroup relations and spatial variation in home range use in Verreaux's sifaka (Propithecus verreauxi) during the annual mating season. Based on 230 hr of focal animal data collected from ten members of five adjacent groups, we found that behavioral patterns and patterns of resource utilization were not markedly different between areas of exclusive use and overlap areas of adjacent home ranges. Group cohesion tended to be higher in overlap than in core areas, but the proportion of time spent resting and foraging did not differ between these two areas. However, dominant males exhibited a higher scent-marking rate in overlap areas. Observations during intergroup encounters revealed that chases between males occurred frequently, whereas fights involving physical contact were not observed. We also found that the intergroup dominance hierarchy depended on the relative group size or the number of males in each group, with groups of lower dominance rank exhibiting a tendency to sleep proportionally more often in their core areas. The results of this study suggest that in primate species with a moderate level of intergroup aggression, such as Verreaux's sifaka, the possibility of encountering neighbors in areas of home range overlap does not exert strong influence on their behavior and resource utilization.

Diurnal distribution of loud calls in sympatric wild indris (Indri indri) and ruffed lemurs (Varecia variegata): implications for call functions.

We carried out a short study on the diurnal call distribution of two sympatric lemurs in the Réserve Naturelle Intégrale Zahamena (eastern Madagascar). Whereas indris (Indri) song bouts were clearly concentrated in the early morning hours, the roar/shriek choruses of ruffed lemurs (Varecia) exhibited a much more even distribution throughout the day. These differences in distribution pattern support earlier claims that indri song bouts are more likely to serve territorial functions, whereas ruffed lemur loud calls may serve both spacing and/or alarm call functions.

Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)?

In contrast to most anthropoid primates, sifakas (Propithecus verreauxi), like many group-living lemurs, exhibit a number of features that deviate from predictions of sexual selection theory. Despite a promiscuous mating system, they lack sexual dimorphism, suggesting that physical combat plays only a minor role in intrasexual competition for receptive females. In this study, we investigated the hypothesis that socioendocrinological mechanisms contribute to suppression of reproductive function of subordinate males. For that purpose, 10 male sifakas from five social groups were observed for 669 focal animal hours for 4 months, including the mating season, in Western Madagascar. Concomitantly 315 fecal samples of these animals were collected and the concentration of immunoreactive testosterone was quantified hy enzymeimmunoassay procedures. Clear dominance relationships existed among coresident males. Testosterone levels of dominant males were significantly higher than those of subordinates during, as well as outside, the mating season. Additionally, the increase in testosterone levels prior to the mating season was more pronounced for dominant than for subordinate males. These findings are in accordance with the hypothesis of suppression of sexual function of subordinate males, probably providing dominant males with ani advantage in sperm competition. If reproductive success is mainly determined by this nonagonistic form of intrasexual competition, the results of this study contribute an important piece to the puzzle of lacking sexual dimorphism in P. verreauxi.

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.

Importance of cooperation and affiliation in the evolution of primate sociality.

The idea that competition and aggression are central to an understanding of the origins of group-living and sociality among human and nonhuman primates is the dominant theory in primatology today. Using this paradigm, researchers have focused their attention on competitive and aggressive behaviors, and have tended to overlook the importance of cooperative and affiliative behaviors. However, cooperative and affiliative behaviors are considerably more common than agonistic behaviors in all primate species. The current paradigm often fails to explain the context, function, and social tactics underlying affiliative and agonistic behavior. Here, we present data on a basic question of primate sociality: how much time do diurnal, group-living primates spend in social behavior, and how much of this time is affiliative and agonistic? These data are derived from a survey of 81 studies, including 28 genera and 60 species. We find that group-living prosimians, New World monkeys, Old World monkeys, and apes usually devote less than 10% of their activity budget to active social interactions. Further, rates of agonistic behaviors are extremely low, normally less than 1% of the activity budget. If the cost to the actors of affiliative behavior is low even if the rewards are low or extremely variable, we should expect affiliation and cooperation to be frequent. This is especially true under conditions in which individuals benefit from the collective environment of living in stable social groups.

Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs.

The aim of this review is to summarize newly available information on lemur social systems, to contrast it with the social organization of other primates and to relate it to existing models of primate social evolution. Because of their evolutionary history, the primates of Madagascar constitute a natural experiment in social evolution. During millions of years of isolation, they converged with other primates only in the most fundamental way in the evolution of solitary, pair-living and group-living species, but deviate in several respects within these basic categories of social organization. Solitary lemurs remain poorly studied, but their social organization appears to be broadly similar to that of other solitary primates, even though the unexpected lack of sexual dimorphism may indicate that similar types of social organization can give rise to different mating systems. The determinants of a solitary lifestyle remain elusive. Pair-living lemurs show striking convergences with other monogamous primates in several behavioural traits, but also deviate in that the majority of species are at least partly nocturnal and do not exhibit direct paternal care of dependent young. Group-living lemurs have not evolved single-male groups, male-bonded and multi-level societies, and polyandrous groups may also be lacking. Female philopatry is common, but female bonds are generally weakly developed and eviction of females from natal groups is not unusual. Group-living lemurs also differ from anthropoids in that their groups have even adult sex ratios, smaller average size and may split up on a seasonal basis. Feeding competition, predation risk and reproductive competition can not fully explain these unusual aspects of lemur social organization. It has therefore been suggested that the social consequences of the risk of infanticide and of recent changes in activity may be ultimately responsible for these idiosyncracies of group-living lemurs, an explanation largely supported by the available evidence. Thus, social factors and fundamental life-history traits, in addition to ecological factors, contribute importantly to variation in social systems among lemurs, and possibly other primates. However, neither the diversity of lemur social systems, nor the evolutionary forces and mechanisms operating in these and other primates are yet fully understood.

Pair-bonding, female aggression and the evolution of lemur societies.

Lemur societies have been described as convergent with those of anthropoids, including Papio-like female-bonded multi-male groups. Recent research, however, shows at least 5 pair-bonded species among the Lemuridae and Indriidae. Three more, Eulemur mongoz, Eulemur fulvus and Varecia variegata, have societies combining aspects of pairing with aspects of troop life. The best-known female-bonded societies, those of Lemur catta, Propithecus diadema edwardsi and Propithecus verreauxi, may be assemblages of mother-daughter dyads, capable of high aggression towards other females, but derived from more solitary female ancestors, perhaps also living as pairs. The internal structure of such lemur groups differs from the more extensive kin groups of catarrhines. This in turn may relate to the lemurs' level of social intelligence and to lemur female dominance over males.

Milk composition reflects pattern of maternal care in prosimian primates.

Hypothesized relationships between milk composition and life history traits were examined by analyzing mid-lactation milks of seven lemurs (Eulemur fulvus, E. macaco, E. rubriventer, E. mongoz, Varecia variegata, Hapalemur griseus, Lemur catta), three bushbabies (Otolemur crassicaudatus, O. garnettii, Galago moholi), and two lorises (Nycticebus coucang, Loris tardigradus); partial data were also obtained for the lemuroid Cheirogaleus medius. There were no significant differences in milk composition among species within either Eulemur or Otolemur, but the four genera for which multiple samples were available (Eulemur, Varecia, Otolemur, and Nycticebus) exhibited large composition differences. Eulemur milk was, on average, very dilute (9.9% dry matter) and low in energy (0.49 kcal/g). These milks contained 0.9% fat, 1.2% protein, and 8.4% carbohydrate on a fresh weight basis. Protein energy comprised only about 15% of total milk energy. Varecia had significantly higher dry matter (13.5%), fat (3.2%), protein (4.2%), gross energy (0.80 kcal/g), and protein energy:total energy ratio (28%) than Eulemur. Milks of the lorisoid genera Otolemur and Nycticebus were very similar, and both had significantly higher dry matter (18.3, 16.3%), fat (7.6, 7.0%), and gross energy concentration (1.27, 1.13 kcal/g) than either lemuroid genus. Otolemur milk was higher in protein than Nycticebus milk. We conclude that lorises, bushbabies, and perhaps cheirogaleids produce relatively rich, energy-dense milks in comparison with anthropoid primates. However, dilute milks appear to be uniformly found among species of Eulemur and perhaps in Lemur catta. The milk of Varecia (and perhaps Hapalemur) is intermediate in composition. Differences in milk composition among prosimians may be related to differences in maternal care: prosimians that carry their young during lactation produce more dilute milks than do species which leave their young unattended for prolonged periods. When looking at primates as a whole, however, the picture somewhat less clear, since the milks of some "parkers" like Varecia do closely resemble those of large anthropoid primates who carry their young.

Preliminary observations on hand preference for tapping, digit-feeding and food-holding in captive aye-ayes (Daubentonia madagascariensis).

Aye-ayes possess highly adapted hands, using their specialized third digits to investigate potential food sources by tapping and the third or fourth digits to transfer food to the mouth. Observations were conducted on 11 captive aye-ayes (10 wild-caught; 1 captive-bred) following presentation of food or novel objects, and hand use for holding, tapping and digit-feeding was scored. Eight of the individuals showed significant hand preferences for one or more of the 3 measures, although there was no consistent pattern. These preliminary results are compared to those from other lemur species.

Tool use, aye-ayes, and sensorimotor intelligence.

Humans, chimpanzees, capuchins and aye-ayes all display an unusually high degree of encephalization and diverse omnivorous extractive foraging. It has been suggested that the high degree of encephalization in aye-ayes may be the result of their diverse, omnivorous extractive foraging behaviors. In combination with certain forms of tool use, omnivorous extractive foraging has been hypothesized to be linked to higher levels of sensorimotor intelligence (stages 5 or 6). Although free-ranging aye-ayes have not been observed to use tools directly in the context of their extractive foraging activities, they have recently been reported to use lianas as tools in a manner that independently suggests that they may possess stage 5 or 6 sensorimotor intelligence. Although other primate species which display diverse, omnivorous extractive foraging have been tested for sensorimotor intelligence, aye-ayes have not. We report a test of captive aye-ayes' comprehension of tool use in a situation designed to simulate natural conditions. The results support the view that aye-ayes do not achieve stage 6 comprehension of tool use, but rather may use trial-and-error learning to develop tool-use behaviors. Other theories for aye-aye encephalization are considered.

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.

Reciprocal recognition of sifaka ( Propithecus verreauxi verreauxi) and redfronted lemur ( Eulemur fulvus rufus) alarm calls.

Redfronted lemurs ( Eulemur fulvus rufus) and Verreaux's sifakas ( Propithecus verreauxi verreauxi) occur sympatrically in western Madagascar. Both species exhibit a so-called mixed alarm call system with functionally referential alarm calls for raptors and general alarm calls for carnivores and raptors. General alarm calls also occur in other contexts associated with high arousal, such as inter-group encounters. Field playback experiments were conducted to investigate whether interspecific recognition of alarm calls occurs in both species, even though the two species rarely interact. In a crossed design, redfronted lemur and sifaka alarm calls were broadcast to individuals of both species, using the alarm call of chacma baboons ( Papio cynocephalus) as a control. Both species responded with appropriate escape strategies and alarm calls after playbacks of heterospecific aerial alarm calls. Similarly, they reacted appropriately to playbacks of heterospecific general alarm calls. Playbacks of baboon alarm calls elicited no specific responses in either lemur species, indicating that an understanding of interspecific alarm calls caused the responses and not alarm calls in general. Thus, the two lemur species have an understanding of each other's aerial as well as general alarm calls, suggesting that even in species that do not form mutualistic associations and rarely interact, common predator pressure has been sufficient for the development of heterospecific call recognition.