Social System of <Emphasis Type="Italic">Microcebus berthae</Emphasis>, the World’s Smallest Primate

Our goal was to provide a first characterization of the social system of pygmy mouse lemurs (Microcebus berthae), the worlds smallest primate species. During a 4-mo field study of 12 females and 27 males, we combined capture-recapture and morphometric data with detailed behavioral observations of individually marked subjects and genetic paternity analyses of a population in Kirindy Forest, western Madagascar. We describe the social organization of Microcebus berthae as a solitary forager living in an individualized neighborhood system characterized by extensive intra- and intersexual home range overlap of adult individuals within a male-biased population. Male and female pygmy mouse lemurs inhabited home ranges (males: 4.9 ha; females: 2.5 ha) that are more than twice as large as those of sympatric Microcebus murinus. On average, pygmy mouse lemurs of both sexes spent about half of the days sleeping alone. Preliminary analysis of genetic population structure suggests female philopatry and male dispersal. Sleeping associations of variable composition that consisted not preferentially of close relatives and proximity during part of the nightly activity contributed together with regular social interactions to the maintenance of a social network. The spatial distribution pattern of adult males and females, the absence of sexual size dimorphism, relatively large male testicular volume and moderate female estrous synchrony suggest a promiscuous mating system with a high potential for scramble competition. In general, there are many similarities between the social system of Microcebus berthae and those of other Microcebus spp. However, striking differences with sympatric gray mouse lemurs (Microcebus murinus) in female home range size, dispersion and sleeping behavior indicate the existence of species-specific socioecological adaptations in closely related species occupying very similar ecological niches.     

Defining the Low End of Primate Social Complexity: The Social Organization of the Nocturnal White-Footed Sportive Lemur (Lepilemur leucopus)

Whereas other species of sportive lemurs (genus Lepilemur) have been described as living in dispersed pairs, which are characterized by spatial overlap but a lack of affinity or affiliation between one adult male and female, existing reports on the social organization of the white-footed sportive lemur (Lepilemur leucopus) are conflicting, describing them as either living in dispersed one-male multifemale systems or pairs. We conducted this study in the spiny forest of Berenty Reserve, southern Madagascar, to clarify the social organization and to characterize the level of social complexity of this species. We combined 1530 h of radio-telemetry and behavioral observations over a period of 1 yr to describe the spatiotemporal stability, size, and interindividual overlap of individual home ranges as well as interindividual cohesiveness. Results revealed low intra- and high intersexual home range overlap. Although most of the social units identified consisted of dispersed pairs (N = 5), males were associated with two adult females in two cases. Furthermore, members of a social unit were never observed to groom each other or to share a daytime sleeping site, and Hutchinson’s and Doncaster’s dynamic interaction tests indicated active avoidance between pair partners. Low cohesiveness together with extremely low rates of social interactions therefore arguably places Lepilemur leucopus at the low end of primate social complexity.     

Spatiotemporal distribution of individuals as an indicator for the social system of Lepilemur sahamalaza

Primate social systems are highly diverse, complicating the classification of particularly elusive species that are difficult to observe. The spatial distribution of individuals over time is a critica lindicator for the social organization and long‐term studies are important to establish patterns of social interactions. In recent years, species of the cryptic, nocturnal sportive lemurs of the genus Lepilemur were found to live in pairs in which a single male and a single female share and defend a mutual home range. The present study aimed to forward research into this underrepresented genus by determining the social organization and structure of the Sahamalaza sportive lemur, L. sahamalaza. We collected 773.15 hr of behavioral and GPS data during a period of 10 months (between 2015 and 2016) on 14 individuals: eight females and six males. There was no evidence of pair‐specific home range use as intra‐ and intersexual home range overlap was high. No pattern of social interactions between focal individuals could be distinguished despite high range overlap. Individuals met and interacted infrequently, resulting in an interaction rate of 0.32 interactions/hr. Sleeping associations between adult individuals were never observed. While both sexes had access to multiple potential mating partners, range sizes or ranging distances did not increase in mating periods. Overall, the social system of Sahamalaza sportive lemurs exhibits aspects of a solitary social organization and structure with potential for the polygamous mating system. These findings underline the importance of detailed social ecology studies that can provide the basis for understanding potential environmental influences on social system variability of closely related species.     

Sleeping and Ranging Behavior of the Sambirano Mouse Lemur, <Emphasis Type="Italic">Microcebus sambiranensis</Emphasis>

Primates require secure sleeping sites for periods of rest, but despite their importance, the characteristics of desired sleeping sites are poorly known. Here we investigated the sleeping ecology of a radio-collared population of the Sambirano mouse lemur, Microcebus sambiranensis, during the nonreproductive season in the Anabohazo forest, northwestern Madagascar. We also investigated their ranging behavior and examined the spatial distribution of sleeping sites within the home ranges of the collared individuals. We took measurements of the sleeping tree’s physical characteristics and recorded the number of collared individuals using each sleeping site. We found that M. sambiranensis generally use foliage sleeping sites more frequently than tree holes and individuals slept more frequently in densely foliated trees than in sparsely foliated trees, often alone. We observed no significant differences in home range size or nightly travel distance between males and females; however, home ranges were smaller than those described for other mouse lemur species. Finally, we found that M. sambiranensis sleep peripherally and forage centrally within their home ranges, a behavior not previously described for mouse lemurs. Our results indicate profound differences in the social organization between M. sambiranensis and other mouse lemur species described in the literature, suggesting species-specificity in mouse lemur ecology. Understanding the sleeping ecology and ranging behavior of mouse lemurs is of great importance to their conservation, as these data facilitate the planning of long-term reforestation, habitat management, and population assessment.     

Biology of <Emphasis Type="Italic">Cheirogaleus major</Emphasis> in a Littoral Rain Forest in Southeast Madagascar

Greater dwarf lemurs (Cheirogaleus major) are small nocturnal primates from the rain forests of eastern Madagascar. I investigated a population of Cheirogaleus major in a littoral rain forest of Southeast Madagascar during 2 rainy seasons to supplement the sparse information available for the species. I collected data on morphology, group composition, sleeping behavior, home range, and social organization via mark/recapture, radio telemetry, and focal individual observations. I identified 2 presumed family groups, and my data from radiotracking revealed a monogamous social organization. In each group, I found an adult pair and its presumed offspring sharing home ranges and sleeping sites together. I also observed gregarious behavior of group members during their nocturnal activity. I found no difference in body measurements between sexes, but body mass and tail circumference increased significantly from November to February, indicating a fatting period before hibernating.     

Out of Sight but Not Out of Mind? Behavioral Coordination in Red-Tailed Sportive Lemurs (<Emphasis Type="Italic">Lepilemur ruficaudatus</Emphasis>)

Many animals are organized into social groups and have to synchronize their activities to maintain group cohesion. Although activity budgets, habitat constraints, and group properties may impact on behavioural synchrony, little is known regarding how members of a group reach a consensus on the timing of activities such as foraging bouts. Game theory predicts that pair partners should synchronize their activities when there is an advantage of foraging together. As a result of this synchronization, differences in the energetic reserves of the two players develop spontaneously and the individual with lower reserves emerges as a pacemaker of the synchrony. Here, we studied the behavioral synchrony of pair-living, nocturnal, red-tailed sportive lemurs (Lepilemur ruficaudatus). We observed 8 pairs continuously for ≥1 annual reproductive cycle in Kirindy Forest, Western Madagascar. During focal observations, one observer followed the female of a pair and, simultaneously, another observer followed the male. We recorded the location and behavioral state of the focal individual every 5 min via instantaneous sampling. Although behavioral synchrony of pair partners appeared to be due mainly to endogenous activity patterns, they actively synchronized when they were in visual contact (<10 m). Nevertheless, red-tailed sportive lemurs benefit from synchronizing their activity only for 15% of the time, when they are close together. The lack of an early warning system for predators and weak support for benefits via social information transfer in combination with energetic constraints may explain why red-tailed sportive lemurs do not spend more time together and thus reap the benefits of behavioral synchrony.     

Use of space and home range characteristics of Lepilemur mittermeieri,an endangered sportive lemur endemic to the Ampasindava peninsula,north‐west Madagascar

Lepilemur mittermeieri, a little‐studied sportive lemur of north‐west Madagascar, endemic to the Ampasindava Peninsula, faces habitat loss through forest degradation and rapid fragmentation. Understanding its habitat requirement is the first step toward preservation of this threatened forest‐dependent species. In this study, we gathered data on the use of space and home range characteristics of L. mittermeieri. We studied individuals from early March to the end of June 2015 and 2016, in three sites of the Ampasindava peninsula. We radio‐tracked 15 individuals to obtain detailed information on the size and location of home ranges (around 450 hr of tracking). Direct observation and morphometric measurements provided additional data sets. Both kernel density estimation (KDE) and minimum convex polygon (MCP) methods yielded similar home range sizes (an average of 2.01 ha with KDE method and 1.96 ha with MCP method). We did not find differences in home range size between males and females, with respect to forest type or proximity to the forest edge. Home ranges overlapped and individuals showed low levels of territoriality. We highlighted a sexually‐dimorphic trait: males have longer upper canine than females. Our results constitute the first set of ecological information on Lepilemur mittermeieri and could be the basis for a conservation strategy for this endangered species with a very small distribution area.     

Territorial behavior of the plethodontid salamander Plethodon kentucki: influence of habitat structure and population density

To investigate the possible influence of variation in ecological and demographic factors on the spatial organization of the terrestrial plethodontid salamander Plethodon kentucki, I conducted a 3-year capture-recapture study and determined home-range characteristics and spatial relationships of individuals at two field sites that differed in predominant cover type and population density. Home ranges of adults were fixed and the home ranges of same-sex adult neighbors were mostly exclusive. The spatial arrangement of adult home ranges exhibited overall regularity or regularity within aggregations, whereas the distribution of juvenile home ranges was usually random. Analysis of nearest-neighbor sex indicated a positive intersexual association of adult home ranges. Removal studies provided evidence for defense of adult home ranges only at the high-density site. The distribution of home ranges was influenced by the presence of cover objects, but there was no significant relationship between adult body size and percent of home-range area with cover. Males overlapped the home ranges of gravid females significantly more often than those of non-gravid females, indicating that the distribution of gravid females had a strong influence on the distribution of male home ranges. In laboratory tests, increased male-male aggression during the breeding season suggests that males may compete for access to mates. At the high-density site, larger males may have benefited by having greater reproductive success than smaller males because they were more dominant and their home ranges overlapped a greater number of gravid-female home ranges. My results indicate that habitat structure and population density may influence the spatial organization and mating system of P. kentucki. Received: 26 May 1997 / Accepted: 9 October 1997     

The Effects of Climate Seasonality on Behavior and Sleeping Site Choice in Sahamalaza Sportive Lemurs, <Emphasis Type="Italic">Lepilemur sahamalaza</Emphasis>

Temperature, rainfall, and resource availability may vary greatly within a single year in primate habitats. Many primate species show behavioral and physiological adaptations to this environmental seasonality, including changes to their diets and activity. Sahamalaza sportive lemurs (Lepilemur sahamalaza) inhabit the northwest of Madagascar and have been studied only during the dry, colder period of the year. We investigated potential effects of climate seasonality on this species by collecting behavioral data between October 2015 and August 2016, encompassing both the warmer wet and the colder dry seasons. We collected 773.15 hours of behavioral data on 14 individual sportive lemurs to investigate year-round activity budgets, ranging behavior, and sleeping site locations. Additionally we recorded temperature and rainfall data at our study site to describe the environmental conditions during the study period. The study individuals significantly decreased their time spent traveling and increased their time spent resting in the dry season compared to the wet season. Although home range size and path lengths did not differ over the study period, sleeping locations were significantly different between seasons as the lemurs focused on more confined areas in colder periods. Overall, the results indicate that Sahamalaza sportive lemur behavior varies with season, in line with reports for other primates.     

Habitat Utilization of Three Sympatric Cheirogaleid Lemur Species in a Littoral Rain Forest of Southeastern Madagascar

I compared the habitat utilization in 3 sympatric species of Cheirogaleidae (Microcebus murinus [81 g], Cheirogaleus medius [183 g] and Cheirogaleus major [362 g]) in a littoral rain forest in southeastern Madagascar during 3 rainy seasons. Females of promiscuous Microcebus murinus had small home ranges and the males had large overlapping home ranges. Home ranges of family groups of monogamous Cheirogaleus medius and C. major overlapped extensively. Home ranges of all 3 species overlapped completely in the study area but home range sizes differed among species and correlate positively with body masses. Male Microcebus murinus slept in open vegetation (79%) and alone (71%), whereas female M. murinus and family group members of Cheirogaleus spp. preferred communal sleeping in tree holes. There are significant interspecific differences in the choice of sleeping sites: smaller lemurs chose smaller trees and used more sleeping sites than larger lemurs did. Species also differed significantly in the vertical dimension of forest utilization: Cheirogaleus major used the upper part of the trees, C. medius used the middle parts, and Microcebus murinus used the understory during nocturnal activities. The 3 species differed mainly in vertical habitat utilization and showed vertical stratification.     

Determinants of Pair‐Living in Red‐Tailed Sportive Lemurs (Lepilemur ruficaudatus)

Pair‐living and a monogamous mating strategy are rare and theoretically unexpected among mammals. Nevertheless, about 10% of primate species exhibit such a social system, which is difficult to explain in the absence of paternal care. In this study, we investigated the two major hypotheses proposed to explain the evolution of monogamy in mammals, the female defence hypothesis (FDH) and the resource defence hypothesis (RDH), in red‐tailed sportive lemurs (Lepilemur ruficaudatus), a nocturnal primate from Madagascar. We analysed behavioural data from eight male–female pairs collected during a 24‐mo field study to illuminate the determinants of pair‐living in this species. Male and female L. ruficaudatus were found to live in dispersed pairs, which are characterised by low cohesion and low encounter rates within a common home range. Social interactions between pair partners were mainly agonistic and characterised by a complete absence of affiliative interactions – body contact was only observed during mating. During the short annual mating season, males exhibited elevated levels of aggression towards mates, as well as extensive mate guarding and increased locomotor activity. In addition, males were exclusively responsible for the maintenance of proximity between pair partners during this period, and they defended their territories against neighbouring males but not against females. Together, these results point towards the importance of female defence in explaining pair‐living in L. ruficaudatus. We discuss the spatial and temporal distribution of receptive females in relation to the female defence strategies of males and suggest possible costs that prevent male red‐tailed sportive lemurs from defending more than one female.     

Social organization and space use in California voles: seasonal,sexual, and age-specific strategies

We intensively monitored space use and movement in Microtus californicus over a 2-year period that included 1 year of high density (maximum 618/ha) and one of low (minimum 5/ha); historically this population has exhibited cycles of 2 or 4 years. Adults of both sexes dispersed at the start of the breeding season, culminating in the establishment of intrasexually exclusive territories. In females, these territories persisted throughout life, except that many young females recruiting during the breeding season established contiguous, overlapping, or adjacent home ranges with their mothers. This female philopatry explains the conclusion of previous workers that females of this species are non-territorial. In the dry (non-breeding) season, females had smaller ranges that often overlapped and were clustered. Adult males moved breeding territories at a modal interval of 6 weeks; this is consistent with their avoidance of inbreeding with philopatric daughters. Ranges overlapped 1–4 adult females at any one time, and a cohort of 7 long-lived males overlapped an average of 16.4 females during their tenure on the grid. The period of maximum overlap with adult females varied among individual males, and did not correlate with the time of maximum body weight. Ranges of males in the dry season overlapped extensively, with persistent associations among some individuals. In the lowdensity year, ranges of some adults failed to overlap intersexually. Juvenile males dispersed gradually between 3 and 13 weeks of age (half before 9 weeks), with some leaving after reaching sexual maturity; a few remained philopatric. Of juvenile females, 47% remained philopatric with the rest disappearing before 9 weeks of age. New understanding of vole social behavior, dispersal, and space use is achieved by focusing on the seasonal dynamics of spatial relationships among individuals with respect to age, sex, and relatedness.     

Space use in the root vole: basic patterns and variability

Home range characteristics and spatial organization of the root vole Microtus oeconomus were assessed by radio-tracking The aim of this paper is to test the assumption that each microtine species employs a certain modal spatial system around which there is considerable flexibility In the studied population the basic modes of spatial organization were female territoriality and male use of overlapping home ranges Female territories were significantly smaller and less diversified in size than male ranges The size of male home ranges was positively correlated with body mass Each female territory was overlapped by several male ranges, larger male ranges usually overlapped more female territories The above spatial organization suggests that the prevailing mating system in the root vole is promiscuity, and larger males have an access to more receptive females than have small-sized males
Departures from these basic modes were found among young mature females from summer cohort, forming clusters even at low density, and occasionally among females in locally crowded habitat patches, where they held overlapping home ranges A single male usually monopolized such a cluster, excluding other males from the area used by the females     

The Round-Eared Sengi and the Evolution of Social Monogamy: Factors that Constrain Males to Live with a Single Female

Animal dispersion in space and time results from environmental pressures, and affects the outcome of a species' social organization. When females are solitary, males may either roam or be pair-living. We studied possible environmental influences affecting the social organization of the round-eared sengi ( Macroscelides proboscideus ) in a semi-desert in South Africa, using trapping and radio-tracking across 2.5 yr. Adult sex ratios did not deviate from 1:1 and we found no indication of sexual dimorphism in body mass. Females maintained exclusive areas, which had little overlap (<4%) with neighbouring females (NF), and males overlapped predominately only with the home range of single females. Generally, inter- and intra-sexual overlap with neighbouring individuals was low (3–6%) for both sexes, indicating territoriality and pair-living. Pairs were perennial and territories were maintained year-round. However, males generally maintained much larger areas than females, which were sensitive to population density. Male space use appeared to be primarily limited by the presence of neighbouring males. Female home ranges were smaller-sized despite changes in population density, possibly for energetic efficiency. Some paired males attempted to take over widowed females, but shifted back to their original home range following the intrusion of an un-paired male. We conclude that social monogamy is the predominant social organization in round-eared sengis in a semi-desert that may have resulted from females living solitarily in small exclusive territories, balanced sex ratios, and from a low variation of body mass between males.     

Seasonality in Reproduction of <Emphasis Type="Italic">Lepilemur edwardsi</Emphasis>

Sportive lemurs are threatened species in the IUCN Red Data Book. However, quantitative information on their reproduction, urgently required for conservation, has been lacking. We collected first data on reproductive activity of Milne-Edwards’ sportive lemurs in a population inhabiting the dry deciduous forest of the Ankarafantsika National Park in northwestern Madagascar during 1998, 2001, and 2003. The species showed a seasonal reproduction. The main mating season extended from May to June, as indicated by the presence of males with high testes volumes and estrus females. In the mating and early postmating season and in the postparturition season, sexes did not differ in body mass. Females had a significantly higher body mass than males in August and November, indicating pregnancy, which together with the presence of small infants in October and November implies that gravidity in females lasted for about 4–5 mo. All litters consisted of singletons. Individuals with body mass at the lower limit of the population either did not develop measurable testes volumes (males) or were not in estrus (females). They were probably juveniles from the previous birth season that achieved sexual maturity not before their second year after birth. The first data on reproduction suggest a low reproduction rate for Lepilemur edwardsi and a request for a higher conservation status than previously attributed and the need for further management strategies.     

Life history traits and parental care in Lepilemur ruficaudatus

In this study we investigated the importance of biparental care for the evolution and/or maintenance of pair-living in red-tailed sportive lemurs (Lepilemur ruficaudatus), a nocturnal folivorous lemur. Between 2000 and 2005, we collected data on life history traits from a total of 14 radio-collared pairs of adults and their offspring in Kirindy forest, western Madagascar. Predation rate varied between years with a minimum of 0% and a maximum of 40% per year. Patterns of parental care were quantified during simultaneous focal observations of both pair-partners in 2003 and 2004. Mating activity was limited to the months of May and June, as indicated by conspicuous changes of vulval morphology and male mate guarding behavior. After a gestation length of about 5 months, which is much longer than expected for a lemur of this body mass, single infants were born in November. Lactation lasted for about 50 days. Apart from lactation, females provided infant care by warming, grooming and transporting infants orally. Infants were parked in dense vegetation while females foraged. Males were seen only rarely in proximity to infants and we found no evidence for direct infant care provided by social fathers. We conclude that the necessity of direct infant care cannot explain the evolution and/or maintenance of pair-living in Lepilemur ruficaudatus.     

Group Size, Home Range Use, and Seasonal Variation in the Ecology of Eulemur mongoz

We collected data during a 10-month study carried out on the mongoose lemur, Eulemur mongoz, at Anjamena in northwestern Madagascar, which provide baseline information on seasonal variation in the ecology, home range use and some aspects of the behavior of two neighboring groups. We monitored group size of nine groups in the study area and assessed them for seasonal variation. We present additional information collected during short-term surveys in other areas before and during the study for comparison. The study groups were small family units, and changes in group size were limited to births and emigrations of sexually mature progeny. In spite of clear seasonal changes in climate and vegetation, there is no variation in grouping patterns, so it is not possible to correlate variation in group size with seasonal variation of ecological variables. Comparison with ecological data from other field studies on lemurids reveals differences in food resource distribution in western forests versus other types of Malagasy forest. This distribution of food resources may predict home range size in mixed frugivorous–folivorous lemurs. Small home ranges, mainly in the West, could be correlated with a uniform distribution of food resources. Finally, we suggest that the dry season in the West may not present frugivorous–folivorous lemurs with major problems in finding an adequate food supply. This is supported by the lack of seasonal differences in ranging behavior of mongoose lemurs.     

Intraspecific Variation in Home Range Overlap with Habitat Quality: A Comparison among Brown Bear Populations

We developed a conceptual model of spatial organization in vertebrates based upon changes in home range overlap with habitat quality. We tested the model using estimates of annual home ranges of adult females and densities for 30 populations of brown bears (Ursus arctos) in North America. We used seasonality as a surrogate of habitat quality, measured as the coefficient of variation among monthly actual evapotranspiration values for areas in which study populations were located. We calculated home range overlap for each population as the product of the average home range size for adult females and the estimated population density of adult females. Home range size varied positively with seasonality; however, home range overlap varied with seasonality in a nonlinear manner. Areas of low and high seasonality supported brown bears with considerable home range overlap, but areas of moderate seasonality supported brown bears with low home range overlap. These results are consistent with behavioural theory predicting a nonlinear relationship between food availability and territoriality.     

Spatial structuring and dispersal in a high density population of the California vole Microtus californicus

Space use patterns of California voles are described from intensive live-trapping data obtained during the late breeding season in a peak density year. Operational sex ratios were strongly female biased. Breeding males had mutually exclusive home ranges that overlapped the home ranges of one to several females. The average male home range was larger than the average female home range and tended to encompass female home ranges in their entirety. Breeding females had home ranges that often overlapped extensively with the home ranges of other breeding females. The degree of overlap, however, tended to be either very high or very low, indicating that groups of females may act territorially among themselves. Family groups that may include members of sequential litters formed at high density. Males on experimental removal grids had larger home ranges than males on the high density grids and some became wanderers while most females had home ranges comparable to those on the high density grids.
Dispersers onto low density grids were not a random sample of the high density population; large breeding adults and small juveniles were under-represented. No sex differences in dispersal were noted. Immigration into the high density populations was probably negligible.     

Avoiding predators at night: antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus)

Although about one-third of all primate species are nocturnal, their antipredator behavior has rarely been studied directly. Crypsis and a solitary lifestyle have traditionally been considered to be the main adaptive antipredator strategies of nocturnal primates. However, a number of recent studies have revealed that nocturnal primates are not as cryptic and solitary as previously suggested. Thus, the antipredator strategies available for diurnal primates that rely on early detection and warning of approaching predators may also be available to nocturnal species. In order to shed additional light on the antipredator strategies of nocturnal primates, I studied pair-living red-tailed sportive lemurs (Lepilemur ruficaudatus) in Western Madagascar. In an experimental field study I exposed adult sportive lemurs that lived in pairs and had offspring to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own mobbing calls (barks) given in response to disturbances at their tree holes. I documented the subjects' immediate behavioral responses, including alarm calls, during the first minute following a playback. The sportive lemurs did not give alarm calls in response to predator call playbacks or to playbacks with barks. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two classes of predators, suggesting that the corresponding vocalizations were correctly categorized. In response to barks, they scanned the ground and fled. Because barks do not indicate any specific threats, they are presumably general alarm calls. Thus, sportive lemurs do not rely on early warning of acoustically simulated predators; rather, they show adaptive escape strategies and use general alarm calls that are primarily directed toward the predator but may also serve to warn kin and pair-partners.