Characterization of new microsatellite loci for the ring‐tailed lemur (Lemur catta)

In this report we describe the development and characterization of six dinucleotide microsatellite loci for the ring‐tailed lemur (Lemur catta). The new markers were isolated from the genomic DNA of L. catta and all loci were found to be polymorphic when evaluated by genotyping a minimum of 34 individuals. Mendelian inheritance of each locus was verified using four families of captive ring‐tailed lemurs. The loci presented will facilitate the genetic survey of free‐ranging L. catta, enabling study of their social organization and mating patterns.     

Reproduction in the crowned lemur (Lemur coronatus) in captivity

Four pairs of captive crowned lemurs (Lemur coronatus) were studied during their annual breeding season in order to obtain baseline data on their reproductive biology for comparison with other Lemur species and to enhance their captive breeding success. Vaginal smears, testicular measurements, and records of the Duke University Primate Center provided the presented data. During a single breeding season, females cycled an average of three times, with an average cycle length of 34 days. Cycles were detected between November and March. Vaginal estrus and copulations were limited to one day per cycle. After 125 days of gestation females gave birth to one or two young. Both sexes attained sexual maturity at an age of about 20 months. Mean male testis size peaked in late December; at the same time, three of the females experienced their first estrus. Based on all available data, there was a significant positive correlation between cycle length and gestation length in the genus Lemur.     

Cathemerality in the mongoose lemur, Eulemur mongoz

Results of a 10 month study of the mongoose lemur (Eulemur mongoz) at Anjamena are presented. The activity pattern is documented in detail for both wet and dry seasons based on observations conducted over the entire 24 h period. E. mongoz was found to be cathemeral throughout the year but exhibited shifts towards more diurnal activity in the wet season and more nocturnal activity in the dry season. The cathemeral activity pattern in the mongoose lemur appears to be coordinated with sunrise, sunset, and day length and modulated by an inhibitory effect of low nocturnal light intensity in the forest during the wet season, resulting in mainly diurnal activity. Temperature and rainfall may also influence the activity pattern. Few advantages to food-related behavior appear to derive from this activity pattern, although resource accessibility may be enhanced by nocturnal behavior in the dry season, leading to reduction in interspecific competition. Cathemerality may also represent a behavioral thermoregulatory mechanism allowing the mongoose lemur to conserve energy by being active during the cool nights of the dry season. In addition, nocturnal behavior in the dry season probably allows avoidance of predation by raptors at the time of year when least protection is afforded by vegetation.     

Isolation of 10 microsatellite markers for mongoose lemurs (Eulemur mongoz)

We present here 10 new microsatellite markers for the mongoose lemur (Eulemur mongoz), nine of which were isolated from E. mongoz and one from Lemur catta. At least 60 individuals were genotyped for each of the 10 loci. Mendelian inheritance at each locus was tested by genotyping five captive families with known pedigrees. All loci were polymorphic and demonstrated simple Mendelian inheritance. The microsatellite markers presented here will be useful for genetic surveys of wild E. mongoz, to gain insights into the genetic background of the captive population, and to aid in the conservation of the species’ genetic diversity.     

Successful care and propagation of the endangered amargosa vole (Microtus californicus scirpensis) in captivity

The Amargosa vole (Microtus californicus scirpensis) is a highlyendangered rodent endemic to a small stretch of the California portion of the Amargosa River basin in Inyo County's Mojave Desert. Although the Amargosa vole has survived in this naturally fragmented ecosystem for thousands of years, recent habitat degradation due to land development, water drainage, and marsh exploitation has further isolated the species and reduced its available habitat. As part of a conservation effort to preserve the species, a captive breeding population was established in 2014 to serve as an insurance colony and as a source of individuals to release into the wild as restored habitat becomes available. As this is the only captive colony for this species, there is little published information about appropriate care and husbandry for the Amargosa vole. Here we provide information about behavior, diet, reproduction, drug sensitivities, and diseases that affect successful captive care. We also provide recommendations for housing and disease management to preserve natural behaviors and defenses in captive‐born animals.     

Black lemur (Lemur macaco) hand preference in food reaching

The present study assessed the hand preferences exhibited by 33 black lemurs during routine feeding. Individual animals displayed hand preferences that were consistent across observations separated by as much as seven months. Within this population, 20 were left hand preferent, 12 right preferent, and 1 was ambidextrous. Correlational analysis of age and percentage left hand use indicated an inverse relationship in which younger animals tended towards the preferential use of the left hand and older animals the preferential use of the right hand. Similar analysis found no relationship between either sex and hand preference or familial relationship and hand preference. The skewed distribution of age in this sample renders tentative conclusions regarding age-related variations in hand preference. It is suggested that if the hand preferences of the black lemur are not age-related, then this species may be characterized as having a bias towards the preferential use of the left hand for food reaching.     

Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus)

Physiologically related features of muscle morphology are considered with regard to functional adaptation for locomotor and postural behavior in the brown lemur (Lemur fulvus). Reduced physiological cross-sectional area, estimated maximum excursion of the tendon of insertion, length of tendon per muscle fasciculus, and areal fiber type composition were examined in the quadriceps femoris in order to assess the extent of a "division of labor" among four apparent synergists. Each of these four muscles in this prosimian primate displays a distinguishing constellation of morphological features that implies functional specialization during posture and normal locomotion (walk/run, galloping, leaping). Vastus medialis is best suited for rapid whole muscle recruitment and may be reserved for relatively vigorous activities such as galloping and leaping (e.g., small cross-sectional area per mass, long excursion, predominance of fast-low oxidative fibers, relatively little tendon per fasciculus). In theory, rectus femoris could be employed isometrically in order to store elastic strain energy during all phasic activities (e.g., large cross-sectional area per mass, short excursion, predominance of fast-high oxidative fibers, large amount of tendon per fasciculus). Vastus intermedius exhibits an overall morphology indicative of a typical postural muscle (e.g., substantial cross-sectional area, short excursion, predominance of slow-high oxidative fibers, large amount of tendon per fasciculus). The construction of vastus lateralis reflects an adaptation for high force, relatively high velocity, and resistance to fatigue (e.g., large cross-sectional area, long excursion, most heterogeneous distribution of fiber types, large amount of tendon per fasciculus); this muscle is probably the primary contributor to a wide range of locomotor behaviors in lemurs. Marked dramatic architectural disparity among the four bellies, coupled with relative overall fiber type heterogeneity, suggests the potential for exceptional flexibility in muscle recruitment within this mass. One interpretation of this relatively complex neuromuscular organization in the brown lemur is that it represents an adaptation for the exploitation of a three-dimensional arboreal environment by rapid quadrupedalism and leaping among irregular and spatially disordered substrates.     

Survey and comparison of major intestinal flora in captive and wild ring-tailed lemur (Lemur catta) populations

A survey to identify the major intestinal species of aerobic bacteria, protozoa and helminths was conducted on captive and wild populations of ring-tailed lemurs (Lemur catta). Samples were collected from 50 captive lemurs at 11 zoological institutions in the United States. In Madagascar, 98 aerobic bacteria samples and 99 parasite samples were collected from eight sites chosen to cover a variety of populations across the species range. Identical collection, preservation and lab techniques were used for captive and wild populations. The predominant types of aerobic bacteria flora were identified via five separate tests. The tests for parasites conducted included flotation, sedimentation and FA/GC. Twenty-seven bacteria unique to either the captive or wild populations were cultured with eight of these being statistically significantly different. Fourteen bacteria common to both populations were cultured, of which six differed significantly. Entamoeba coli was the only parasite common to both the captive and wild populations. Giardia spp., Isospora spp., strongyles-type ova, Entamoeba spp. and Entamoeba polecki were found only in captive samples. Cryptosporidium, Balantidium coli, pinworm-type ova, and two fluke-like ova were seen only in wild samples. In addition, samples were compared for both bacteria and parasites from three unique field sites in Madagascar. In this three-site comparison, six types of bacteria were statistically significantly different. No significant differences regarding parasites were seen. Significant differences were found between the captive and wild populations, whereas fewer differences were found between sites within Madagascar. Although we isolated Campylobacter and Giardia, all animals appeared clinically healthy.     

Avian nest predation by a semi-captive collared lemur (Lemur fulvus collaris)

A lemur (Lemur fulvus collaris) in a semi-captive group of six animals at the Duke University Primate Center (DUPC) was observed eating an egg from the nest of a mourning dove (Zenaida macroura). The manner in which the animal had been foraging prior to this incident, and the fact that wild birds at the DUPC frequently direct antipredator behaviors, such as mobbing toward thisL. f. collaris group, suggest that nest predation is part of normal foraging behavior in these animals.     

Agonistic and grooming behavior of captive crowned lemurs (Lemur coronatus) during the breeding season

Captive breeding of rare and endangered prosimians may be enhanced by an increased understanding of all aspects of their seasonal mating behavior. In this study, the agonistic and grooming behaior of captiveL. coronatus were studied during their annual breeding season. Between October and March, selected aspects of agonistic and grooming behavior of four male-female groups were recorded. Males initiated significantly more allogrooming than females. The frequency of this behavior pattern increased significantly in the weeks of estrus. Females performed significantly more agonistic behavior patterns than males. The mean frequency of agonistic interactions decreased significantly during the breeding season. In successfully reproducing groups males showed much less agonism towards females, than they did in unsuccessful groups. Inter-specific comparisons demonstrated that the patterns of agonistic interactions during the breeding season are very different among closely related species of lemurids. The conclusions drawn from this study are that captive breeding of crowned lemurs may be enhanced by keeping permanent multi-male, multi-female groups.     

Reproduction in Coquerel's dwarf lemur (Mirza coquereli)

Most nocturnal Malagasy primates, as well as many diurnal species, are highly endangered in their natural habitat. Captive breeding programs have been established for many species, but detailed information on reproduction is only available for three nocturnal taxa: the mouse lemur (Microcebus murinus), the dwarf lemur (Cheirogaleus medius), and the greater dwarf lemur (Cheirogaleus major). In this study, we present data for another nocturnal Malagasy primate, Coquerel's dwarf lemur (Mirza coquereli), which has been propagated since 1982 at the Duke University Primate Center. Unlike all other Malagasy primates bred in captivity, M. coquereli cycles throughout the year, and is clearly less seasonal in its birth distribution than is C. medius or M. murinus. Estrous intervals ranged between 19 and 30.5 days. Estrus lasted no longer than 1 day. After an average gestation length of 89.2 days, litters of one or two were born. Females cycled for the first time between 8 and 15 months of age, and gave birth for the first time between 12.8 and 33.5 months of age. The earliest mating of a male leading to conception was observed at the age of 17 months. For males and females, an increase in daylength appears to trigger pubertal development. Males had seasonal changes in testicular volume which were not explained by covariation with body weight. Maximum testis size occurred in spring, when breeding activity was highest. The occurrence of year-round reproduction in M. coquereli, and the absence of seasonal fattening and/or hibernation, along with their specialized winter diet, may be correlated. © 1995 Wiley-Liss, Inc.     

Behavior of the mayotte lemur,Lemur fulvus mayottensis,in captivity

A group of one male and two female Mayotte lemurs was observed at Chester Zoo, and their behaviors compared with published observations of wild populations of this and related forms of the brown lemur. It was found that the captive animals were active by both day and night, but that the pattern of activity was different from wild lemurs. The captive lemurs were less active than their wild counterparts and showed different timing of activity because of the feeding regimen at the zoo. The animals did not ignore the public at the zoo, but, on the contrary, directed some behaviors at the zoo visitors, particularly if the zoo visitors attempted to interact with the lemurs; under these conditions there was also an increase in the movements of the lemurs in the cage. Levels of aggression in the zoo lemurs were higher than those reported for wild populations, and aggression appeared to occur predominantly in the birth season. Levels of affiliative behaviors, particularly allogrooming, were comparable with those in the wild. Olfactory behaviors such as scent marking and anogenital sniffing also showed seasonal peaks and again appeared to occur at higher rates than in the wild.     

Reproduction of Asian chipmunks (Tamias sibiricus) in captivity

Factors affecting reproduction in captive Asian chipmunks, Tamias sibiricus, were examined by means of a survey of chipmunk breeders in Great Britain. Sixteen breeders were asked about the conditions under which their chipmunks were kept and their success in breeding them. Results covered 205 female-years of pairing. Breeding was promoted by large cage size and early weaning of young, and inhibited by the presence of other rodent species nearby and by extended photoperiod. A diet of seeds and nuts, with some fresh fruits and vegetables, appeared to be adequate for breeding. Breeding occurred in 80–91& of female-years when neither extra lighting nor other rodents were present, irrespective of cage size. Weaning age affected the occurrence of second litters in a year. Second litters were born less often (0–13&) of breeding (female-years) if young of the first litter remained with the mother 8 weeks or longer. Second litters were more frequent (14–45& of breeding female-years) if first litters were removed by 6.5 weeks of age, and this frequency increased with cage size. Litter size also increased with cage size (means ranged from 3 to 7). Overall breeding success increased with cage size and decreased with the presence of other rodents. In most colonies without other rodents near, mean success rate ranged from 3.1 to 8.5 young/female-year. In colonies with other rodents present mean success rate varied from 0 to 3.3 young/female-year. It is suggested that the mechanisms that control population size in the wild also act to inhibit or promote breeding in captivity.     

Observations on reproduction,hormones, copulatory behavior,and neonatal mortality in captive Lemur mongoz (Mongoose lemur)

This study examines correlates of reproduction in Lemur mongoz, an endangered prosimian primate with a history of poor captive reproduction. Male testicular growth and regression were quantified via testicular indices (TI). Although TIs could be used to predict male breeding condition, they were not indicators of ability to sire offspring. Serum estradiol (E₂) and progesterone (P) concentrations, along with vaginal cytology, were used to monitor female reproductive cyclicity. E₂ and P profiles showed no abnormalities. An elevation of E₂ with low P, approximately one estrous cycle length (31.4 days) prior to the onset of fertile cycles, was consistent with the phenomenon of ‘pseudoestrus’ observed in other lemur species. The copulatory pattern, consisting of thrusting, multiple intromissions, single or multiple ejaculations, and no copulatory lock, was more complex than expected for an animal with a supposedly monogamous mating system. The preference for natural arboreal substrata during copulation suggests that enclosure furnishings may influence copulatory behavior. A 30% neonatal mortality rate tempered recent success in breeding L. mongoz at the Duke University Primate Center (DUPC). Although infant sex and parity of the mother were not predictive of neonatal mortality, mother's natal status was, with captive-born females having a 67% infant mortality rate, compared with 15% in wild-caught females. Based on these observations, a number of factors, including housing, behavior, and photoperiod, may be relevant to successful captive propagation of L. mongoz. © 1992 Wiley-Liss, Inc.     

Contact calling behaviour in the male ring‐tailed lemur (Lemur catta)

The ring‐tailed lemur (Lemur catta) is a group‐living strepsirhine primate endemic to Madagascar that has a complex vocal repertoire including affiliative moan and hmm calls. Past research has suggested that both vocalisations may be contact calls, and we assessed their usage in addition to examining the effect of individual differences and social factors on male calling behaviour. We tested three hypotheses: the group cohesion, preferred companion and individual differences hypotheses. From March to July 2010, 565 h of focal animal data were collected on 31 males aged ≥1 year at the Beza Mahafaly Special Reserve, Madagascar. Focal males were observed for 30 min, with vocalisations, allogrooming and agonistic interactions noted using one‐zero sampling, and general behaviour, nearest neighbour identity and distance noted using instantaneous point sampling, all at 2.5 min intervals. We found support for the group cohesion hypothesis for both vocalisations, and support for the preferred companion and individual differences hypotheses for the hmm but not the moan vocalisation. Moan and hmm calls maintained the distance between a male and his nearest neighbour, and were made at higher rates during behaviours which may lead to separation from conspecifics, such as travel and vigilance. Males made hmm calls at higher rates when they were low‐ranking, and/or when the nearest neighbour of a male or a preferred companion of either sex. Low‐ranking males may hmm call to maintain proximity to specific individuals within social groups who will show them increased tolerance, with the hmm signalling peaceful intent. Ring‐tailed lemurs are one of the best living models of gregarious primate ancestors, and gaining a better knowledge of the function and range of usage of their contact calls informs our understanding of the evolution of primate cognition.     

Animal behavior and the captive management of wild mammals: A personal view

Behaviorists can undertake noninvasive studies of zoo animals using only the simplest of research tools, unlike those biologists who are concerned with functions below the level of the whole, living organism. With careful interpretation, the results of behavioral studies can be applied to improve the management, husbandry, and exhibition of wild mammals in captivity. This often involves comparisons with research results obtained from studies of animals in the wild, since the behavior of captive specimens may in some measure be altered. Examples are given involving the breeding biology or social organization of three species: (1) barasingha or swamp deer (Cervus duvauceli), (2) mongoose lemur (Lemur mongoz), and (3) drill (Papio leucophaeus). Suggestions are made to improve the allocation of time and resources for research by zoo personnel, including a greater reliance on cooperative efforts to solve problems of common interest.     

Selected aspects of Lemur variegatus reproductive biology

Results from data collected during the 1978–1979 breeding season on the reproduction of Lemur variegatus at the San Diego Zoo provide information which generally supports previously published reports on this species. Comparison of selected results from these data to a larger data base of which they are a part makes it possible to resolve some of the discrepancies between reports. Certain aspects of the reproductive biology of this species may then be generally characterized with confidence: The onset of seasonal breeding as evidenced by estrous behavior begins as early as mid-December in the northern hemisphere and may continue through March; genital changes associated with estrus in females last 9.85 ± 1.67 days (± SD); female receptivity occurs 7.0 ± 1.53 days after the onset of these genital changes and lasts 12-24 hours, during which breeding occurs; gestation averages 99.47 ± 4.19 days; the peak birth season is April–May; litters normally contain two to three offspring, with full-term neonates weighing an average of 104.63 ± 19.10 grams. In addition, L variegatus appears to be highly resistant to the impact of captivity on both its reproductive physiology and behavior, as indicated by the 100% breeding success of the diversely reared and managed groups of study animals.