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.     

Scent‐Mark Identification and Scent‐Marking Behaviour in African Wild Dogs (Lycaon pictus)

Scent‐marking is common in mammals, but where signals are carried by urine and faeces, distinguishing between scent‐marking and mere elimination is problematic. To do so, we documented behaviours and context variables associated with urination and defecation in free‐ranging endangered African wild dogs (Lycaon pictus) and tested whether these were related to the responses of other dogs to deposits. We found that distinct postures were almost uniquely associated with deposits by dominant wild dogs, were more common during urination than defecation, and increased the likelihood that these deposits would be investigated by other wild dogs. The likelihood of investigation depended on the sex and dominance status of the depositor, the type of deposit and the substrate. Urine from dominant females was more likely to be investigated by other wild dogs than any other deposits, and deposits placed on vegetation were more likely to be investigated than those on bare ground. The likelihood that a deposit would be overmarked was affected by the deposit type and the sex and dominance status of the last depositor. Collectively, these results suggest that dominant wild dog urine is of greatest interest to other dogs. Our results show that some deposits by African wild dogs are not scent‐marks and that detailed observations of behaviours and context variables during elimination events can be used to distinguish deposits that are likely to be of communication value.     

Wet and dry season diets of the Endangered Lemur catta (ring‐tailed lemur) in two mountainous rocky outcrop forest fragments in south‐central Madagascar

Lemur catta's ability to consume a wide variety of plant foods is a key to this species' survival in a time of ecological crisis across its geographic range. We examined seasonal diet variability of L. catta groups inhabiting two rocky outcrop fragments in south‐central Madagascar: Anja Reserve and Tsaranoro Valley forest. Leaves and fruit of Melia azedarach were a keystone resource for Anja lemurs in wet and dry seasons. At Tsaranoro, L. catta relied on M. azedarach and Ficus spp. in dry season, but during the wet season, neither was a dominant food resource. Top food species at both sites differed markedly from those consumed by L. catta in other habitats. At Tsaranoro, a greater proportion of lemurs engaged in feeding during the dry season compared with wet season. We attribute this to resource scarcity during dry season, when greater feeding effort is needed to maintain energy requirements. Because M. azedarach is ubiquitous throughout Anja Reserve, producing fruit and leaves year‐round, Anja lemurs can meet energy requirements with little seasonal adjustment in feeding activity. L. catta's IUCN status has been upgraded to Endangered, thus, greater insight into its diet flexibility and ability to survive on introduced plant species, can inform conservation plans in remaining wild habitats and ex situ programs.     

The ranging behavior of Lemur catta in the region of Cap Sainte‐Marie,Madagascar

Large home ranges and extreme flexibility in ranging behaviors characterize most subarid dwelling haplorhines. However, the most comparable extant strepsirhine, Lemur catta, is characterized as having small home ranges with consistent boundaries. Since ranging studies on this species have been limited to gallery forest habitat, the author's goal is to identify ecological factors that affect range use of L. catta in one of the most resource‐limited environments of its distribution. To conduct this study, ranging and behavioral data were collected on two nonoverlapping groups through all‐day follows in the semidesert scrub environment of Cap Sainte‐Marie (CSM), Madagascar. Data were collected from August 2007 through July 2008. Home range areas and day range lengths were generated using ArcGIS® 9.3. Other variables measured were habitat composition, diet richness, daily activity, and microclimate. Home range areas of CSM L. catta were very large relative to those of gallery forest L. catta, and there was great monthly variation. In contrast, day range lengths at CSM were either smaller than or approximated the size of comparative gallery forest groups. Temperature, sunning, and diet richness were associated with day range length for one but not for both groups and appear to be related to energy management needs. Based on these findings, the author suggests that L. catta is capable of extensive behavioral and ranging flexibility in the extremes of its environment. However, physiological constraints impose limitations that can interfere with its ability to adapt to even seemingly minor variations in microclimate and habitat structure within the same site. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Male life history and intergroup mobility among ringtailed lemurs (Lemur catta)

Lemur catta shares a male-biased dispersal pattern with most primate species and the majority of mammals. Individuals in a free-ranging population of ringtailed lemurs were captured, marked, released, and monitored for a 40-month period. Sixty-four percent of the males (43 of 67) migrated or were missing within this period and all nine censused groups were affected by migration. Males migrate from their natal group and then may migrate again after reaching full adult body weight. Full-sized adult males migrate at a rate of 0.28 per year or once every 3.5 years and may change groups a number of times during their life. Migrations occurred within a 6-month period, ending just after the mating season. However, there is no direct connection between mating success and male migration. Females mate with transferring males, with group males, and with visitors from adjacent groups. The age-related pattern of male migration and the occurrence of extragroup mating inLemur catta is similar to that described for several species of macaques.     

Food Intake and Dietary Overlap in Native Lemur catta and Propithecus verreauxi and Introduced Eulemur fulvus at Berenty,Southern Madagascar

The introduction of Eulemur fulvus in 1975 into the Berenty Reserve and their recent attainment of population densities comparable to those of Lemur catta led us to analyze food partitioning among the 3 large prosimian species in the gallery forest. We assessed the diets of ring-tailed lemurs (Lemur catta), brown lemurs (Eulemur fulvus) and sifakas (Propithecus verreauxi) from food intake measurements during 3 successive short-term studies. All species exhibited marked seasonal changes in their major food categories. Dietary overlap was very high between ring-tailed lemurs and brown lemurs during 2 of 3 seasons, including the middle of the dry season. During the latter period, Eulemur appeared to compensate for a low quality diet by increasing the amount of food eaten. In contrast, Lemur fed on lower amounts of food and seemed more efficient at coping with fibrous plant materials. There is low dietary overlap of Lemur catta and Eulemur fulvus versus Propithecus, which exhibit by far the highest dietary diversity of the 3 species. We discuss sustainable coexistence among them, based on respective dietary adaptations and potential for dietary flexibility.     

Histological examinations of facial glands in <Emphasis Type="Italic">Saccopteryx</Emphasis><Emphasis Type="Italic">bilineata</Emphasis> (Chiroptera,Emballonuridae), and their potential use in territorial marking

Scent marking is widespread among individuals of Mammalia species, especially in resource defence social systems. Apart from urine and faeces that are used for claiming resource ownership, specialised scent glands are the main source of secretions in scent marking individuals. Most previous studies have described secretory epithelia macroscopically, since many glands are conspicuous. But macroscopically inconspicuous scent glands or morphological structures might then be overlooked. In Saccopteryx bilineata (greater sac-winged bat), behavioural observations suggest that both sexes have, apart from the conspicuous gular glands of males, specialised facial glands to display territorial marking. We investigated the facial glands of two males and one female S. bilineata histologically and found, first, that both sexes possess a bilateral symmetrically intermandibular gland, which is composed of a bed of modified apocrine sudoriferous cells. Second, we found lip glands consisting of modified apocrine sudoriferous cell units with pigmented ducts around the upper and the lower lip. Both gland types are probably involved during territorial marking.     

Paternity in wild ring‐tailed lemurs (Lemur catta): Implications for male mating strategies

In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.     

Copulatory Plug Displacement Evidences Sperm Competition in Lemur catta

Male displacement of copulatory (sperm) plugs from female vaginas provides further evidence for sperm competition in ring-tailed lemurs (Lemur catta), a gregarious prosimian species with a multimale, multifemale mating system. During two mating seasons, I studied two groups of free-ranging ring-tailed lemurs on St. Catherines Island, GA, USA. I observed 22 mating pairs in which males achieved penile intromission. Copulatory plug displacement by males occurred in 9 cases. Plugs were displaced during copulation by male penes upon withdrawl following deep vaginal thrusting. In every case of copulatory plug displacement, the male displacing a plug mated to ejaculation with the estrous female. In a mating system in which females typically mate with more than one male during estrous, often in succession, copulatory plug displacement may function to disrupt or preclude other males' successful insemination of estrous females. The effects of sperm plug displacement on paternity in Lemur catta are unknown, as no study had heretofore documented copulatory plug displacement in this species. The first-male mating advantage suggested for Lemur catta should be re-evaluated where mating order is known, and copulatory plug displacement during mating, or lack thereof, is identified. Because there is a tendency for first-mating males to mate-guard for longer periods of time in Lemur catta, the latency period between the first mate's ejaculation and that of subsequent mates may be an important determinant of male fertilization success.     

Seasonal and sex differences in urine marking rates of wild red foxes Vulpes vulpes

Understanding the role of urine marking in the territorial systems of wild mammals can be difficult, especially for nocturnal cryptic species. Even for common species, such as the red fox Vulpes vulpes, a comprehensive analysis of seasonal and sex differences has not been carried out. Using 6 years of infra-red video monitoring, we compared marking rates between months and between sexes. Urine marking was significantly lower during summer (June–August). Males urine marked significantly more frequently than females during late summer and autumn, but not winter. Males marked more frequently than females also during March. There was no increase during the breeding season for either sex. Our results correlate with previous partial data but demonstrate how urine marking rates vary across the year. They also further support the greater role of males in fox territorial maintenance. Urine marking is lowest during summer when territorial intrusions are least, whilst the higher male urine marking rate in March reflects the period when females are denning. Overall, our results provide the first comprehensive analysis of red fox urine marking rates, contributing to a greater understanding of territoriality and olfactory communication.     

Aggressive Signal Design in the Jacky Dragon (Amphibolurus muricatus): Display Duration Affects Efficiency

Design characteristics of signals, such as their duration, may have evolved to maximize signal efficiency. It is commonly assumed that constraints on signal design have usually shaped the most optimal display characteristics to improve signal transmission and information transfer of the signaller, and detection by intended receivers. In this study, we tested whether the characteristics (duration, speed and frequency) of an aggressive display, the push‐up body rock, exhibited by the Jacky dragon (Amphibolurus muricatus) have likely evolved for optimal signal efficiency, as it is able to draw attention to the signaller. We performed two video playback experiments using high‐resolution 3D animations testing the effect of variation in push‐up body rock structure. In experiment 1, we manipulated push‐up body rock display structure. We gradually increased the number of push‐ups exhibited by a digitally animated Jacky dragon increasing the overall display duration. In experiment 2, we developed four stimuli based on population‐typical push‐up body rock display for duration (short and long), and frequency of push‐ups (1 or 5 consecutive push‐ups) by manipulating push‐ups’ speed. In both experiments, we measured the probability of an orienting response and response latency of focal lizards when being exposed to the different stimuli. Our results showed that display duration is critically important for signal efficiency in the aggressive push‐up body rock display. If we are to understand the design characteristics of signals used in animal communication, then it appears important to consider the possible trade‐off between signal efficiency and costs.     

Adult Male Scent-Marking in Lemur catta and Eulemur fulvus rufus

Scent-marking and olfactory communication are used extensively by prosimians and can provide spatial and temporal records of group movement and behavior. We compare rates of male scent-marking in relation to reproductive seasons, male dominance rank, and habitat use in two related prosimians: Lemur catta and Eulemur fulvus rufus. We collected scent-marking data on adult male Lemur catta at Beza-Mahafaly Reserve (dry forest), and on Eulemur fulvus rufus at Ranomafana National Park (rainforest), Madagascar. In Lemur, rates of overall scent-marking differed significantly by reproductive season, with higher rates occurring in mating and lactation/migration periods, whereas in Eulemur, reproductive season did not appear to affect scent-marking rates. Dominance rank of male Lemur catta did not affect rates of scent-marking. Among male Eulemur fulvus, dominance relations were not apparent; however, 2 of the 5 focal males scent-marked somewhat more frequently during the mating season and also experienced greater mating success. In Lemur catta, higher rates of scent-marking in the mating season may relate to indirect reproductive competition during a period of high aggression, while such mating competition was not as marked in Eulemur fulvus. Furthermore, higher rates of marking in resident male Lemur catta during male migration may correlate with vigilance toward immigrating males. Greater overall scent-marking rates in ring-tailed lemurs may relate to extensive intergroup home range overlap and no area of exclusive use, whereas the red-fronted lemur groups tended to forage in areas of their home range where little-to-no intergroup overlap occurred.     

Variation in stimulus,seasonal context,and response to urine marks by captive Iberian wolves (<Emphasis Type="Italic">Canis lupus signatus</Emphasis>)

Urine marking behaviour was observed over 14 months in two captive pairs of Iberian wolves (Canis lupus signatus) by means of behaviour sampling. The study focused on the relative attractiveness of the different stimuli toward which urinations are directed, the seasonal context of urine marking, and the response by mates to sexually dimorphic action patterns. Kinds of marked substrates varied according to the posture used by wolves to urinate [raised-leg urination (RLU), flexed-leg urination (FLU), standing urination (STU), or squat urination (SQU)]. In RLUs and FLUs the wolves mainly used conspicuous substrates, whereas STUs and SQUs were carried out directly onto inconspicuous substrates. Wolves urinated on plants more than on other substrates, mostly selecting trees. A selection of trees according to their trunk diameter was also observed. The posts were chosen or avoided seemingly because of their specific characteristics such as size. In short, wolves marked with urine (RLUs and FLUs) those substrates that secured a greater effectiveness of marking. The mean duration of RLUs was lower than that of FLUs and SQUs. The rate of RLUs in males increased in winter (November–December) and in summer (July–August), while the rate of FLUs and SQUs in females and STUs in males did not increase during these periods. The wolves investigated RLUs more frequently than SQUs. The RLU display appears to be more ancestral than derived, similar in all species of canids and even in the Iberian wolf.     

Scent‐marking behavior by subordinate Eurasian beavers

Chemical communication by scent‐marking is widespread among mammals and can serve different purposes, such as territory demarcation, mate attraction and self‐advertisement. In this study, we examined scent‐marking behavior by subordinate Eurasian beavers (Castor fiber) in a population in southeast Norway. We conducted scent experiments in 18 family groups, simulating a territory intruder using experimental scent mounds (ESM). In total, we recorded 196 territorial reactions (destroying and/or overmarking of scent mounds). Subordinates contributed 14% of all territorial reactions and first overmarked 12% of the ESM, and the number of subordinates in the family group did not increase the total number of territorial reactions. This suggests that the contribution by subordinates plays a minor role in territorial defense. The number of territorial reactions by subordinates was positively related to the age of their parents, suggesting that subordinates might take over territorial duties with increasing parental senescence, likely because they have increased chances of inheriting the territory. Increased experience in territorial activities possibly helps subordinates to successfully gain and defend a territory of their own.     

Individuality in a contact call of the ringtailed lemur (Lemur catta)

A vocalization of the ringtailed lemur (Lemur catta) was examined for individual differences according to several temporal- and frequency-dependent variables. Vocalizations were tape recorded at the Duke University Primate Center (Durham, NC) and spectrographically analyzed. Significant differences were found in pair-wise comparisons of call structure among the study subjects, thus providing the physical basis for individual discrimination. A separate analysis comparing degree of kinship and vocal similarity revealed a positive but nonsignificant correlation between these two variables. This study represents an initial examination of vocal individuality in prosimian primates.     

Assessment of dominance hierarchy through urine scent marking and its chemical constituents in male blackbuck Antelope cervicapra, a critically endangered species

In ungulates the process of chemical communication by urinary scent marking has been directly related to reproductive dominance, territorial defense and proximity to resources. The differences in the frequency of urine marking and chemical composition of urine of males Antelope cervicapra before, during and after the dominance hierarchy period were assessed. The variations in the urine marking and its chemical profiles of dominant males (n = 9), bachelors (n = 5) and sub-adult males (n = 5) were compared to find out how the dominance hierarchy influences the confined blackbuck herd under semi-natural captive conditions. The frequency of urine marking is significantly higher (p < 0.001) in dominant males. Twenty-eight major constituents were identified in the urine of dominant males (before, during and after the dominance hierarchy period), bachelor and sub-adult males. Among these, three specific compounds namely, 3-hexanone (I), 6-methyl-5-hepten-2-one (II) and 4-methyl-3-heptanone (III) were seen only in dominant males urine during the dominance hierarchy period. Based on the behavioural observation and the unique chemical constituents in the urine, it is concluded that the dominant male scent odor suppresses aggression, scent marking, scent production and territorial patrolling activities of subordinate males, through which the dominant male establish their hierarchy and attains success in reproduction.     

An Examination of the Function of Urine Washing in Galago senegalensis

A wild, female Galago senegalensis molohi (lesser bushbaby) was radio collared and followed for 139 h. The occurrence of ‘urine washing’, wetting the hands and feet with urine, was recorded and analysed in terms of when and where it took place and with what other behaviours it was associated. Data from the present study and others indicated that urine washing did not function as an olfactory sign marking territorial boundaries. It was suggested that in this species it facilitated grip.     

Factors Affecting Interspecific Aggression in a Year‐Round Territorial Species,the Jewel Damselfish

Vertebrates live in complex species networks in which interspecific interactions are common. In some contexts, the aggressive behaviours shown in these interspecific interactions are very similar to those shown in intraspecific interactions. It is still an open question whether intra‐ and interspecific aggression share common causality. We studied a year‐round territorial species the jewel damselfish, (Plectroglyphidodon lacrymatus), which cultivate algae they feed on. Territory holders aggressively defend these algae that are an attractive resource for many other species. In this study, we recorded territorial aggression in free‐living individuals and recorded aggressive responses to a standardized territorial intrusion test in captive individuals. Field observations indicated that territorial aggression was selectively targeted towards food competitors. Independent of the size of the species, aggression was more frequent towards common species around their territories. This relationship was confirmed experimentally by confronting the jewel damselfish with novel objects to which the subjects were exposed either frequently or rarely. We suggest that jewel damselfish have to learn which species are competitors and therefore should be chased. In a standardized intrusion test with captive individuals, no significant differences were found in territorial responses towards intra‐ or interspecific intruders. Neither territorial aggression nor the intrusion showed any relationship with plasma androgen levels. Together, these data suggest that experience might be more important in non‐seasonal territorial aggression than circulating hormonal factors.     

Feeding behavior ofLemur catta andLemur fulvus

The feeding behavior of two sympatric species of lemurs, Lemur cattaand Lemur fulvus,was studied in an enclosure simulating a natural habitat at the Duke University Primate Center. L. fulvusspent less time feeding during the day than L. catta.But the former species ate more fruit and had longer feeding bouts on preferred food items than L. catta.They also had a shorter food passage time than L. cattaand their choice of resting places was more influenced by food distribution. Furthermore, the two lemur species ate parts of different plant species and showed different reactions to chemical plant components. According to these results, L. fulvusis a more conservative feeder than L. catta.These interspecific differences in feeding behavior may be one of a number of differences that allow the two species to coexist. In allopatry, however, L. fulvusmay also adopt feeding patterns similar to those of L. catta.But L. cattawas never found to change its feeding strategies in different areas. It may be this option of L. fulvusto adopt different feeding strategies in different situations that allows this species to have the widest range of all Malagasy lemurs. Duke University Primate Center Publication No. 259.     

Nocturnal ranging by a diurnal primate: are ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>) cathemeral?

Cathemerality, an activity pattern comprised of distinct periods of diurnal and nocturnal activity, is a trait found among several of the Malagasy strepsirhines and one species of Aotus. Because occasional anecdotal reports suggest that some diurnal primates can be active at night, I investigated the possibility of nocturnal ranging behavior in the ring-tailed lemur (Lemur catta) by using global positioning system (GPS) collars programmed to collect data across a 24-h period. Five individuals in a provisioned, free-ranging L. catta colony on St. Catherines Island, Georgia, USA, wore GPS collars across 1 week of the mating season. Results revealed that night ranging behavior occurred between the h of 1900 and 0530. An evaluation of the effect of moonlight on nocturnal activity showed that a greater rate of travel occurred during moonlit periods as opposed to periods when the moon had not yet risen. Distance travelled at night decreased across the deployment period, likely because of a decrease in available moonlight over time, as the lemurs were collared during a waning moon. Fewer mating opportunities over time may have also been responsible for the decrease in night ranging, because the number of females in estrus declined across the deployment period. Future research is needed to separate the effects of moonlight and mating activity on night ranging in this species, as well as to evaluate whether L. catta in Madagascar show night ranging similar to L. catta on SCI. These data raise the possibility that L. catta may be cathemeral, with an activity pattern fluctuating between diurnality and cathemerality in accordance with shifts in environmental conditions.