RESUMEN
Deforestation and habitat fragmentation is the primary threat to primate populations. The primates that live within degraded and anthropogenically disturbed habitats typical of fragmented landscapes have to cope with lower availability of resources in comparison to primates in continuous, undisturbed forests. While some species are sensitive to forest fragmentation, some evidence exists to suggest that primates can alter their behavior and adapt to such changes, which enables their survival in suboptimal habitat. In this study, we assessed how forest fragmentation and its associated edge-effects impact the feeding ecology and activity levels of a nocturnal primate community in the Sahamalaza-Iles Radama National Park, North West Madagascar. From March 06, 2019 to May 17, 2022, we collected data on tree and invertebrate phenology at our study site, and feeding ecology and activity for 159 lemur individuals from four species. Fruit and flower availability varied significantly between continuous and fragmented forest, and between forest core and edge areas, with continuous forest exhibiting higher continuous fruit and flower availability. Lemur feeding ecology varied significantly too, as the feeding niches of all four species were significantly different between continuous and fragmented forest and between core and edge areas. However, lemur activity levels were mostly consistent among all forest areas. The results of this study suggest that nocturnal lemurs are able to adapt their dietary ecology in response to the available food sources within their habitat. Due to this flexible ecology and dietary plasticity, the lemurs do not need to significantly alter their behavior in different environments to fulfill their dietary needs. While nocturnal lemurs demonstrate adaptability and flexibility to degraded habitat, it is unclear how far this plasticity will stretch considering that Madagascar's forests are still being cleared at an alarming rate. Urgent conservation action is therefore needed to ensure the future of lemur habitat.
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Lemur , Lemuridae , Strepsirhini , Animales , Lemur/fisiología , Madagascar , Ecología , Lemuridae/fisiología , Ecosistema , BosquesRESUMEN
The degree of dietary flexibility in primates is species specific; some incorporate a wider array of resources than others. Extreme interannual weather variability in Madagascar results in seasonal resource scarcity which has been linked to specialized behaviors in lemurs. Prolemur simus, for example, has been considered an obligate specialist on large culm bamboo with >60% of its diet composed of woody bamboos requiring morphological and physiological adaptations to process. Recent studies reported an ever-expanding list of dietary items, suggesting that this species may not be an obligate specialist. However, long-term quantitative feeding data are unavailable across this species' range. To explore the dietary flexibility of P. simus, we collected data at two northern sites, Ambalafary and Sahavola, and one southern site, Vatovavy, from September 2010 to January 2016 and May 2017 to September 2018, respectively. In total, we recorded 4022 h of behavioral data using instantaneous sampling of adult males and females from one group in Ambalafary, and two groups each in Sahavola and Vatovavy. We recorded 45 plant species eaten by P. simus over 7 years. We also observed significant differences in seasonal dietary composition between study sites. In Ambalafary, bamboo was the most frequently observed resource consumed (92.2%); however, non-bamboo resources comprised nearly one-third of the diet of P. simus in Sahavola and over 60% in Vatovavy. Consumption of all bamboo resources increased during the dry season at Ambalafary and during the wet season at Vatovavy, but never exceeded non-bamboo feeding at the latter. Culm pith feeding was only observed at Ambalafary, where it was more common during the dry season. We identify P. simus as a bamboo facultative specialist capable of adjusting its feeding behavior to its environment, indicating greater dietary flexibility than previously documented, which may enable the species to survive in increasingly degraded habitats.
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Lemur , Lemuridae , Femenino , Masculino , Animales , Madagascar , Lemuridae/fisiología , Lemur/fisiología , Conducta Alimentaria/fisiología , Dieta/veterinariaRESUMEN
Due to their potential impact on population growth, many studies have investigated factors affecting infant survival in mammal populations under human care. Here we used more than 30 years of Association of Zoos and Aquariums (AZA) studbook data and contraception data from the AZA Reproductive Management Center, along with logistic regression models, to investigate which factors affect infant survival in four Eulemur species managed as Species Survival Plans® in AZA. Across species, infant survival to 1 month ranged from 65% to 78%. Previous experience producing surviving offspring was positively correlated to infant survival in collared (Eulemur collaris), crowned (Eulemur coronatus), and mongoose (Eulemur mongoz) lemurs. Both dam age and previous use of contraception were negatively correlated to infant survival for collared lemurs, though our results suggest the latter may be confounded with other factors. Blue-eyed black lemurs (Eulemur flavifrons) were affected by birth location, suggesting differences in husbandry that may affect infant survival. These results can be used to assist in reproductive planning or to anticipate the likelihood of breeding success. Population managers may also be able to focus their reproductive planning on younger dams or those with previous experience to predict successful births. Future studies should seek to determine what aspects of previous dam success are most important to infant survival, investigate sire-related factors, and examine factors related to cause of death in infants that may lead to differential survival. Our hope is to present a framework that may be useful for investigating infant survival in other mammal species' breeding programs.
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Crianza de Animales Domésticos , Animales de Zoológico , Animales , Femenino , Crianza de Animales Domésticos/métodos , Lemuridae/fisiología , Masculino , Animales Recién Nacidos , Reproducción/fisiología , Lemur/fisiologíaRESUMEN
Measuring glucocorticoids is one of the most reliable and widely used techniques to monitor stress responses, however invasive techniques to collect plasma samples may not be applicable for wild populations. Monitoring excreted glucocorticoids is an effective noninvasive technique that researchers have used increasingly over the past two decades, and it has allowed the investigation of glucocorticoids in a variety of species with a range of activity patterns. Many species exhibit predictable circadian patterns of glucocorticoid secretion in accordance with their daily activity pattern. There remains a gap in our understanding of how excreted glucocorticoid metabolites vary throughout the day and across species, despite the utility of this information when developing sampling protocols and analyzing data. We investigated circadian patterns of glucocorticoid excretion in a cathemeral primate species, Eulemur rubriventer (red-bellied lemur), in Ranomafana National Park, Madagascar. We collected fecal samples from 10 individuals throughout the day and analyzed fecal glucocorticoid levels across three time points (Early, Midday, and Late), and again across two time points (Morning and Afternoon). We also investigated whether activity pattern, sex (as a control variable), and other traits associated with gut passage rate (diet, body mass) could help predict the presence and timing of circadian patterns of fecal glucocorticoid metabolites across mammal species. We found that fecal glucocorticoid metabolite levels in E. rubriventer fluctuate throughout the day, with lowest levels in the morning and peak levels in the afternoon. None of the variables that we tested predicted whether daily fecal glucocorticoid metabolites changed significantly throughout the day, nor when levels were likely to peak, across species. We stress the importance of controlling for sampling time and reporting these results as standard practice in studies of fecal glucocorticoid metabolites.
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Lemur , Lemuridae , Animales , Glucocorticoides , Lemur/fisiología , Primates , Madagascar , Heces , MamíferosRESUMEN
Measuring energy balance and energy metabolism can provide crucial information for understanding the ecological and behavioral drivers of an animal's energetic and physiological condition. Both urinary C-peptide (uCP) of insulin and urinary total triiodothyronine (uTT3) have been validated as noninvasive biomarkers of energy balance and metabolic activity in haplorrhine primates. This study attempts to validate uCP and uTT3 measures in strepsirrhines, a phylogenetically distinct primate clade, using the ruffed lemur (genus Varecia) as a model. We experimentally manipulated the diet of captive black-and-white (Varecia variegata) and red (Varecia rubra) ruffed lemurs at Duke Lemur Center across a 4-week period. We collected urine samples from subjects (n = 5) each day during 1 week of control diet, 2 weeks of calorie-restricted diet and 1 week of refeeding, designed to temporarily reduce energy balance and metabolism. We also tested the outcome of filter paper as a storage method by comparing to controls (frozen at -20°C) to assess its suitability for studies of wild populations. We successfully measured uCP and uTT3 levels in frozen urine samples using commercial enzyme immunoassay kits and found that both biomarkers were excreted at lower concentrations (C-peptide: 1.35 ng/mL, 54% reduction; TT3: 1.5 ng/mL, 37.5% reduction) during calorie-restricted periods compared to normal diet periods. Filter paper recovery for uCP was 19%, though values were significantly positively correlated with frozen control samples. uTT3 could not be recovered at measurable concentrations using filter paper. These methods enable noninvasive measurement of energetic conditions in wild strepsirrhines and subsequent assessment of relationships between energy balance and numerous socioecological drivers in primate populations.
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Lemur , Lemuridae , Strepsirhini , Animales , Lemur/fisiología , Péptido C , TriyodotironinaRESUMEN
Animals' foraging behavior and dietary choices are, in part, driven by their ultimate function: to meet nutritional demands. However, depending on their degree of dietary specialization and the availability and distribution of food resources in their environment, species may utilize different nutritional strategies. With shifting plant phenology, increasing unpredictability of fruiting, and declining food quality in response to anthropogenic climate change, existing nutritional constraints may become exacerbated. Such changes are especially concerning for Madagascar's endemic fruit specialists given the nutrient-limitation of the island's landscapes. In this study, we examined the nutritional strategy of one such fruit-specialist primate, the black-and-white ruffed lemur (Varecia variegata), over a 12-month period (January to December 2018) in Ranomafana National Park, Madagascar. We hypothesized that Varecia would balance nonprotein energy (NPE) to protein (AP) at a high ratio similar to other frugivorous primates, and that they would prioritize protein intake given their high degree of frugivory. We found that Varecia balance NPE:AP at a ratio of 11:1, higher than in any other primate studied to date; however, diets shifted such that nutrient balancing varied seasonally (12.6:1 abundant-9.6:1 lean). Varecia meet NRC suggested recommendations of 5-8% of calories from protein, despite having a diet mostly comprising fruits. However, seasonal shifts in NPE intakes result in significant energy shortfalls during fruit-lean seasons. Flowers provide an important source of NPE during these periods, with flower consumption best predicting lipid intake, suggesting this species' ability to shift resource use. Nevertheless, achieving adequate and balanced nutrient intakes may become precarious in the face of increasing unpredictability in plant phenology and other environmental stochasticities resulting from climate change.
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Lemur , Lemuridae , Animales , Frutas , Lemuridae/fisiología , Primates , Plantas , Nutrientes , Lemur/fisiologíaRESUMEN
One of the most fundamental aspects of a species' behavioral strategy is its activity budget; for primates this generally involves the allocation of available time among resting, feeding, traveling, and social behavior. Comparisons between species, populations, or individuals can reveal divergences in adaptive strategies and current stressors, and reflect responses to such diverse pressures as predation, thermoregulation, nutrition, and social needs. Further, variation across seasons is an important part of behavioral strategies to survive food scarcity; this can involve increasing or decreasing effort. We documented activity over the 24-h cycle for the cathemeral, frugivorous Eulemur fulvus and the diurnal, folivorous Propithecus diadema across 13-18 months at Tsinjoarivo, Madagascar. Their activity budgets were dominated by resting (E. fulvus: 74.1%; P. diadema: 85.2%), followed by feeding (15.8%, 12.4%), traveling (9.31%, 1.74%) and social activities (0.76%, 0.70%), respectively. The lower feeding and higher resting in P. diadema likely reflect slower gastrointestinal transit and higher reliance on microbial fermentation to extract energy from fibrous food. The two species showed opposite lean season strategies. E. fulvus increased activity, with more feeding but less travel time, consistent with a shift to less-profitable fruits, and some leaves and flowers, while increasing feeding effort to compensate ("energy maximizing"). P. diadema showed less variation across months, but the lean season still evoked reduced effort across the board (feeding, travel, and social behavior), consistent with a "time minimizing" strategy prioritizing energy conservation and microbe-assisted digestion. Understanding these divergent shifts is key to understanding natural behavior and the extent of behavioral flexibility under stressful conditions. Finally, the complex patterns of fruit availability (intra- and interannually) and the species' behavioral responses across months underscore the need to move beyond simplistic "lean/abundant season" and "fruit/leaf" dichotomies in understanding underlying energetic strategies, and species' vulnerability to habitat change.
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Lemur , Strepsirhini , Animales , Lemur/fisiología , Estaciones del Año , Ecosistema , Frutas , Madagascar , Conducta Alimentaria/fisiologíaRESUMEN
In the decades since female social dominance was first described in strepsirrhine primates, researchers have sought to uncover the proximate and ultimate explanations for its development. In the females of various female-dominant species, androgens have been implicated as regulators of behavior and/or predictors of seasonal fluctuations in aggression (the 'Female Masculinization Hypothesis'). Males, more generally, respond to changing social demands via seasonal fluctuations in androgen-mediated behavior (the 'Challenge Hypothesis'), that may also entail changes in activation of the hypothalamic-pituitary-adrenal axis. Here, we explore if androgens, glucocorticoids, and intersexual behavior fluctuate seasonally in the female-dominant, blue-eyed black lemur (Eulemur flavifrons), with potential consequences for understanding female aggression and male deference. Across two studies conducted during the breeding and nonbreeding seasons, we assessed rates of mixed-sex, dyadic social behavior (aggression and affiliation) and concentrations of fecal glucocorticoid metabolites (Study 1) and serum sex hormones (androstenedione, testosterone, and estradiol; Study 2). Our results align with several predictions inspired by the Female Masculinization and Challenge Hypotheses for intersexual relations: During the breeding season, specifically, both aggression and androstenedione peaked in females, while female-initiated affiliation decreased, potentially to facilitate female resource access and reproductive control. By comparison, all target hormones (androgens, estrogen, and glucocorticoids) peaked in males, with glucocorticoid concentrations potentially increasing in response to the surge in female aggression, and unusually high estrogen concentrations year-round potentially facilitating male deference via male-initiated affiliation. These results suggest complex, seasonally and hormonally mediated behavior in Eulemur flavifrons.
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Androstenodiona , Lemur , Agresión/fisiología , Andrógenos/metabolismo , Androstenodiona/metabolismo , Animales , Estrógenos/metabolismo , Femenino , Glucocorticoides/metabolismo , Sistema Hipotálamo-Hipofisario/metabolismo , Lemur/fisiología , Masculino , Sistema Hipófiso-Suprarrenal/metabolismo , Estaciones del AñoRESUMEN
Female dominance, a trait common to some Malagasy lemurs, has been viewed as an adaptation that decreases intersexual feeding competition. A hypothesized relationship exists between male "deference" (male submission in the absence of female aggression) and food availability. Sauther (1993) suggested that male ring-tailed lemurs at the Duke Lemur Center (Pereira et al., 1990) show more deference to females than do males in the wild owing to food abundance in captivity. To reexamine the link between food availability and male deference, we studied agonism and foraging in two nonwild ring-tailed lemur (Lemur catta) populations: the Los Angeles Zoo and St. Catherines Island (SCI). On SCI, we collected data under two feeding conditions: Low Provisions (low food availability) and High Provisions (high food availability). As expected, male deference measures at our study sites were more similar to measures of deference from other studies of L. catta in captivity than in the wild. Additionally, the change at SCI from low to high food availability was associated with increased male deference to females. Interestingly, male proximity to females during foraging at this location did not notably change between the low to high food availability conditions, suggesting that males were food competitors of females just as often under both feeding conditions. The increase in male deference under conditions of high food availability on SCI was due to males withdrawing more rapidly from female approaches during agonistic interactions. Hence, where food is more abundant, male L. catta are more likely to show submission to females, which appears to be a self-serving means of avoiding female aggression. Lemur males who are well-fed appear less apt to risk female aggression to obtain resources than more nutritionally stressed males. Our results support the view of female dominance in lemurs as an adaptive evolutionary response to conditions of resource limitation.
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Lemur , Agresión , Animales , Femenino , Alimentos , Lemur/fisiología , Madagascar , MasculinoRESUMEN
OBJECTIVES: As many primates live in forests where visibility is limited, the ability to detect the aroma of distant fruit and navigate odor plumes would be highly adaptive. Our study is the first to investigate this ability with strepsirrhine primates. MATERIALS AND METHODS: We tested the ability of a group of ring-tailed lemurs to detect hidden fruit from afar using scent alone. We hid containers in the underbrush of a semi-natural forest, some baited with real cantaloupe and some with sham cantaloupe, 4-17 m from a path routinely used by the lemurs. Crucially, the containers were not visible from the path. Therefore, the lemurs had to use olfactory cues, but did not have to prioritize them to locate the bait. RESULTS: The lemurs found the real cantaloupe on days that the wind blew the scent of the fruit toward the trail. They did not find the sham cantaloupe. Upon detecting the odor of the bait, the lemurs sniffed the air at one or more locations as they moved toward the bait, a process of navigation known as klinotaxis. DISCUSSION: The traditional belief is that primates are unable to track odor plumes. The untrained lemurs in this study were able to detect the odor of the cantaloupe among the complex odors of the forest and navigate the odor plume to the fruit. The results indicate that olfaction may be used to respond to cues from distant sources. The ability to track odor plumes may be a critical foraging skill for strepsirrhines.
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Conducta Apetitiva/fisiología , Frutas , Lemur/fisiología , Olfato/fisiología , Animales , Antropología Física , Evolución Biológica , Femenino , MasculinoRESUMEN
OBJECTIVES: Asymmetrical behavior patterns are observed in many animal species, but the potential adaptive significance of lateralization and the evolutionary forces driving it remain unclear. Most laterality studies have focused on a single species, which makes interspecies comparisons difficult. The aim of this study was to examine differences in the strength and direction of lateralization in multiple lemur species when engaged in a standardized, novel cognitive task. MATERIALS AND METHODS: We assessed laterality in seven lemur species at the Duke Lemur Center when using a novel puzzle-box. We recorded which hand opened the apparatus door and which hand picked up the food reward. We also recorded whether the mouth was used for either action instead of the hands. We then calculated handedness indices (HI), z-scores, and mouth-use rates. RESULTS: Overall, 62% of individuals were more lateralized than chance. However, within-genera, there were relatively equal numbers of individuals with a left- or right-hand bias, which resulted in ambipreference at the genus level. The hand a lemur used on its first success in the task predicted its overall HI value, and the strength of lateralization increased as the number of successes increased. Varecia had significantly higher mouth-use rates than all other genera. DISCUSSION: We found evidence of an individual learning trajectory in which the hand used on a lemur's first success was canalized as the preferred (and lateralized) hand, in support of the "cognitive simplicity" hypothesis. Individual variability in hand preference was high, which is consistent with previous research. Between-genera differences in mouth use appear to reflect species-specific feeding postures and differences in manual dexterity.
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Conducta Animal/fisiología , Lateralidad Funcional/fisiología , Lemur/fisiología , Animales , Antropología Física , Conducta Alimentaria/fisiología , FemeninoRESUMEN
Habitat fragmentation is an increasingly serious issue affecting primates in most regions where they are found today. Populations of Lemur catta (ring-tailed lemur) in Madagascar's south-central region are increasingly restricted to small, isolated forest fragments, surrounded by grasslands or small-scale agriculture. Our aim was to evaluate the potential for population viability of L. catta in nine forest fragments of varying sizes (2-46 ha, population range: 6-210 animals) in south-central Madagascar, using a set of comparative, quantitative ecological measures. We used Poisson regression models with a log link function to examine the effects of fragment size, within-fragment food availability, and abundance of matrix resources (food and water sources) on L. catta population sizes and juvenile recruitment. We found a strong association between overall population size and (a) fragment size and (b) abundance of key food resources Melia azedarach and Ficus spp. (per 100 m along transect lines). Juvenile recruitment was also associated with fragment size and abundance of the two above-mentioned food resources. When the largest population, an outlier, was removed from the analysis, again, the model containing fragment size and abundance of M. azedarach and Ficus spp. was the best fitting, but the model that best predicted juvenile recruitment contained only fragment size. While our results are useful for predicting population presence and possible persistence in these fragments, both the potential for male dispersal and the extent of human disturbance within most fragments play crucial roles regarding the likelihood of long-term L. catta survival. While seven of the nine fragments were reasonably protected from human disturbance, only three offered the strong potential for male dispersal, thus the long-term viability of many of these populations is highly uncertain.
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Ecosistema , Bosques , Lemur/fisiología , Animales , Conservación de los Recursos Naturales , Dieta , Femenino , Ficus , Frutas , Actividades Humanas , Madagascar , Masculino , Melia azedarach , Densidad de PoblaciónRESUMEN
Affiliative vocalizations occur across primate taxa and may be used to maintain spatial cohesion and/or to regulate social interactions in group-living species. For gregarious strepsirhines like the ring-tailed lemur (Lemur catta), with large vocal repertoires and several distinct affiliative vocalizations including the chirp and wail, it is important to understand behavioural usage of these vocalizations to gain insight into their social interactions. To determine whether chirp and wail vocalizations facilitate group cohesion, regulate interactions to achieve socially positive outcomes, and are correlated with differences in individual characteristics such as dominance rank and age, I collected 565 h of focal data on 31 males aged ≥1 year at Beza Mahafaly Special Reserve, Madagascar, from March to July 2010. I found that chirp and wail vocalizations occurred at the highest rates during group-wide travel compared to other behaviours. Although nearest neighbour distance did not influence calling rate, focal animals maintained the same distance or were located closer to nearest neighbours after calling. Both chirp and wail calls were heard in behavioural contexts without agonism rather than agonistic contexts. No relationship was found between male calling rate and dominance rank or age, although the chirp showed a non-significant tendency to be produced at higher rates by younger males. Overall, my results indicated that ring-tailed lemur males of all ages and dominance ranks used both chirp and wail vocalizations as contact calls during group-wide travel events, helping individuals maintain proximity to other group members during movement. Chirp and wail vocalizations may additionally help regulate the caller's social interactions and promote increased tolerance from conspecifics. These findings add to our understanding of the breadth of communication behaviour in wild lemurs, thus furthering our knowledge of the social lives and cognitive abilities of strepsirhines. Through examining the complexity of vocalization use by a living lemur species with a communication system much like early social primates, we gain broad insight into the evolution of primate sociality.
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Comunicación Animal , Lemur/fisiología , Conducta Social , Factores de Edad , Animales , Locomoción , Madagascar , Masculino , Predominio SocialRESUMEN
Previous primate research has demonstrated social learning related to accepting novel foods, but little evidence suggests social learning of food avoidance. Ring-tailed lemurs (Lemur catta)have been observed to shake their heads rapidly in response to sour and bitter stimuli. This study investigated whether this head-shaking behavior may have a social function. The experiment presented a performing lemur with two items of the same type of fruit, one of which had been manipulated to take on a sour flavor, and the other which was not manipulated and served as a control. The performer could taste each of the stimuli while an observing lemur had the opportunity to watch the performer's behavior from an adjacent enclosure. The observer was then presented with two stimuli with the same qualities. This study evaluated whether a preceding head-shaking reaction by the performer improved the success rate of the observer avoiding bitter stimuli to greater than chance. Our results reveal that following a head shake by the performer in response to the sour stimuli, observer avoidance of sour stimuli was statistically greater than chance, indicating that there may be social influences on food avoidance in this species. Further research should focus on confirming this effect and characterizing the full set of socially influential food reaction behaviors.
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Conducta de Elección , Lemur/fisiología , Conducta Social , Animales , Ácido Cítrico , Citrullus , Frutas , Aprendizaje , GustoRESUMEN
Bitter taste enables the detection of potentially harmful substances and is mediated by bitter taste receptors, TAS2Rs, in vertebrates. Few antagonists and inverse agonists of TAS2Rs have been identified, especially natural compounds. TAS2R16s in humans, apes and Old World monkeys (Catarrhini, Anthropoidea) recognize ß-glucoside analogues as specific agonists. Here, we investigated responses of TAS2R16 to ß-glucosides in non-anthropoid primates, namely lemurs (Lemuriformes, Strepsirrhini). Salicin acted as an agonist on lemur TAS2R16. Arbutin acted as an agonist in the ring-tailed lemur ( Lemur catta) but as an inverse agonist in black lemur ( Eulemur macaco) and black-and-white ruffed lemur ( Varecia variegata). We identified a strepsirrhine-specific amino acid substitution responsible for the inverse agonism of arbutin. In a food preference test, salicin bitterness was inhibited by arbutin in the black lemur. Structural modelling revealed this locus was important for a rearrangement of the intracellular end of transmembrane helix 7 (TM7). Accordingly, arbutin is the first known natural inverse agonist of TAS2Rs, contributing to our understanding of receptor-ligand interactions and the molecular basis of the unique feeding habit diversification in lemurs. Furthermore, the identification of a causal point mutation suggests that TAS2R can acquire functional changes according to feeding habits and environmental conditions.
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Arbutina/química , Lemur/genética , Mutación Puntual , Receptores Acoplados a Proteínas G/genética , Gusto/genética , Sustitución de Aminoácidos , Animales , Conducta Alimentaria , Preferencias Alimentarias , Lemur/fisiología , Receptores Acoplados a Proteínas G/agonistasRESUMEN
The role of androgens in shaping "masculine" traits in males is a core focus in behavioral endocrinology, but relatively little is known about an androgenic role in female aggression and social dominance. In mammalian models of female dominance, including the ring-tailed lemur (Lemur catta), links to androgens in adulthood are variable. We studied the development of ring-tailed lemurs to address the behavioral basis and ontogenetic mechanisms of female dominance. We measured behavior and serum androgen concentrations in 24 lemurs (8 males, 16 females) from infancy to early adulthood, and assessed their 'prenatal' androgen milieu using serum samples obtained from their mothers during gestation. Because logistical constraints limited the frequency of infant blood sampling, we accounted for asynchrony between behavioral and postnatal hormone measurements via imputation procedures. Imputation was unnecessary for prenatal hormone measurements. The typical sex difference in androgen concentrations in young lemurs was consistent with adult conspecifics and most other mammals; however, we found no significant sex differences in rough-and-tumble play. Female (but not male) aggression increased beginning at approximately 15â¯months, coincident with female puberty. In our analyses relating sexually differentiated behavior to androgens, we found no relationship with activational hormones, but several significant relationships with organizational hormones. Notably, associations of prenatal androstenedione and testosterone with behavior were differentiated, both by offspring sex and by type of behavior within offspring sexes. We discuss the importance of considering (1) missing data in behavioral endocrinology research, and (2) organizational androgens other than testosterone in studies of female dominance.
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Agresión/fisiología , Androstenodiona/sangre , Conducta Animal/fisiología , Lemur/fisiología , Madres , Caracteres Sexuales , Maduración Sexual/fisiología , Predominio Social , Testosterona/sangre , Factores de Edad , Animales , Femenino , Lemur/sangre , MasculinoRESUMEN
The ring-tailed lemur (Lemur catta), one of the most iconic and widely recognized primates in the world, is threatened in its native range and classified as endangered by the International Union for Conservation of Nature. The global conservation strategy for the species includes ex situ conservation efforts led by zoological institutions in the framework of regional captive breeding programs. To maximize the conservation of genetic diversity and optimize breeding programs, an accurate pedigree must be established in captive populations. Our study documents the formation and subsequent monitoring of a large ring-tailed lemur group in a French zoological institution. Based on staff's behavioral observations and DNA analyses using 11 microsatellite markers, we were able to document the survival and reproduction rates of the lemurs in this situation and reconstruct the pedigree of infants born in the institution. In total, 22 of the 28 imported animals as well as 4 locally born individuals gave birth to 58 infants of which 28 survived. The consistent genotypes obtained from the 53 sampled animals allowed us to identify 25 of the sires and 27 of the dams for the 28 surviving infants. A total of 12 different females and 14 different males produced the 28 surviving infants, suggesting that no individual dominates reproduction. This pioneering study has practical applications for the captive management of the species, which can be raised to the individual level instead of the group level.
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Cruzamiento , Lemur/genética , Lemur/fisiología , Animales , Animales de Zoológico/genética , Conservación de los Recursos Naturales , Femenino , Francia , Masculino , Repeticiones de Microsatélite , LinajeRESUMEN
BACKGROUND: Species recognition, i.e., the ability to distinguish conspecifics from heterospecifics, plays an essential role in reproduction. The role of facial cues for species recognition has been investigated in several non-human primate species except for lemurs. We therefore investigated the role of facial cues for species recognition in wild red-fronted lemurs (Eulemur rufifrons) at Kirindy Forest. We presented adult red-fronted lemurs pictures of male faces from five species including red-fronted lemurs, three closely related species, white-fronted lemurs (E. albifrons), brown lemurs (E. fulvus), rufous brown lemurs (E. rufus), and genetically more distant red-bellied lemurs (E. rubriventer), occurring in allopatry with the study population. We predicted that red-fronted lemurs respond stronger to conspecific than to heterospecific pictures and that females show stronger responses than males. In addition, if genetic drift has played a role in the evolution of facial color patterns in the members of this genus, we predicted that responses of red-fronted lemurs correlate negatively with the genetic distance to the different species stimuli. RESULTS: Red-fronted lemurs looked significantly longer at pictures of their own species than at those of heterospecifics. Females spent less time looking at pictures of white-fronted, brown and red-bellied lemurs than males did, but not to pictures of red-bellied lemurs and a control stimulus. Individuals also exhibited sniffing behavior while looking at visual stimuli, and the time spent sniffing was significantly longer for pictures of conspecifics compared to those of heterospecifics. Moreover, the time spent looking and sniffing towards the pictures correlated negatively with the genetic distance between their own species and the species presented as stimulus. CONCLUSIONS: We conclude that red-fronted lemurs have the ability for species recognition using visual facial cues, which may allow them to avoid costly interbreeding. If so, sexual selection might have influenced the evolution of facial patterns in eulemurs. Since responses also correlated with genetic distance, our findings suggest a potential role of genetic drift as well as sexual selection in influencing the evolution of facial variation in eulemurs. Because study subjects looked and sniffed towards the presented pictures, red-fronted lemurs might have the ability for multi-modal species recognition.
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Reconocimiento Facial/fisiología , Lemur/fisiología , Animales , Conducta Animal , Cara , Femenino , Geografía , Modelos Lineales , Madagascar , Masculino , Reproducción , Especificidad de la Especie , Factores de TiempoRESUMEN
The ecological function of fruit colour has been the focus of many studies. The most commonly tested hypothesis is that fruit colour has evolved to facilitate detection by seed-dispersing animals. We tested whether distributions of fruit colours are consistent with the hypothesis that colour is an evolved signal to seed dispersers using a comparative community approach. We compared the contrast between ripe fruits and leaf backgrounds at two sites, one in Madagascar where seed dispersers are primarily night-active, red-green colour-blind lemurs, and the other in Uganda, where most vertebrate seed dispersers are day-active primates and birds with greater capacity for colour vision. We show that fruits in Uganda have higher contrast against leaf background in the red-green and luminance channels whereas fruits in Madagascar contrast more in the yellow-blue channel. These results indicate that fruit colour has evolved to contrast against background leaves in response to the visual capabilities of local seed disperser communities.
Asunto(s)
Visión de Colores , Color , Frutas , Adaptación Biológica , Animales , Evolución Biológica , Aves/fisiología , Lemur/fisiología , Madagascar , Hojas de la Planta , Primates/fisiología , Dispersión de Semillas , UgandaRESUMEN
Living nonhuman primates generally inhabit tropical forests, and torpor is regarded as a strategy employed by cold-adapted organisms. Yet, some primates employ daily torpor or hibernation (heterothermy) under obligatory, temporary, or emergency circumstances. Though heterothermy is present in most mammalian lineages, there are only three extant heterothermic primate lineages: bushbabies from Africa, lorises from Asia, and dwarf and mouse lemurs from Madagascar. Here, we analyze their phenotypes in the general context of tropical mammalian heterothermy. We focus on Malagasy lemurs as they have been the most intensively studied and also show an unmatched range of flexibility in their heterothermic responses. We discuss the evidence for whether heterothermy should be considered an ancestral or derived condition in primates. This consideration is particularly intriguing given that an understanding of the underlying mechanisms for hibernation in lemurs opens the possibility for insight into genotype-phenotype interactions, including those with biomedical relevance for humans.