Tradeoffs between bite force and gape in Eulemur and Varecia.

In 1974, Sue Herring described the relationship between two important performance variables in the feeding system, bite force and gape. These variables are inversely related, such that, without specific muscular adaptations, most animals cannot produce high bite forces at large gapes for a given sized muscle. Despite the importance of these variables for feeding biomechanics and functional ecology, the paucity of in vivo bite force data in primates has led to bite forces largely being estimated through ex vivo methods. Here, we quantify and compare in vivo bite forces and gapes with output from simulated musculoskeletal models in two craniofacially distinct strepsirrhines: Eulemur, which has a shorter jaw and slower chewing cycle durations relative to jaw length and body mass compared to Varecia. Bite forces were collected across a range of linear gapes from 16 adult lemurs (suborder Strepsirrhini) at the Duke Lemur Center in Durham, North Carolina representing three species: Eulemur flavifrons (n = 6; 3F, 3M), Varecia variegata (n = 5; 3F, 2M), and Varecia rubra (n = 5; 5F). Maximum linear and angular gapes were significantly higher for Varecia compared to Eulemur (p = .01) but there were no significant differences in recorded maximum in vivo bite forces (p = .88). Simulated muscle models using architectural data for these taxa suggest this approach is an accurate method of estimating bite force-gape tradeoffs in addition to variables such as fiber length, fiber operating range, and gapes associated with maximum force. Our in vivo and modeling data suggest Varecia has reduced bite force capacities in favor of absolutely wider gapes compared to Eulemur in relation to their longer jaws. Importantly, our comparisons validate the simulated muscle approach for estimating bite force as a function of gape in extant and fossil primates.

Benefits but not the dual functions of submissive signals differ between two Malagasy primates.

Many animals use formalized signals to communicate dominance relationships. In some primates, such as macaques, the function of such signals varies with dominance style. Despotic species produce unidirectional submission signals that have a dual function: in conflict contexts, they signal a willingness to withdraw, whereas in peaceful contexts, they indicate the agreement to subordination. More despotic species produce these calls to a lesser extent than less despotic species. Here, we investigated whether the use of unidirectional submission signals is also related to dominance style in two lemur species and whether signalling subordination stabilizes social relationships at the group level. Ring-tailed lemurs (Lemur catta) exhibit a more despotic dominance hierarchy than Verreaux's sifakas (Propithecus verreauxi). We observed social interactions in 75 dyads of Verreaux's sifakas and 118 dyads of ring-tailed lemurs. Both species used unidirectional submissive calls that have a dual function, potentially suggesting convergent evolution of the function of these signals in independent primate lineages. However, signalling subordination did not stabilize social relationships at the group level in both species. Additionally, subordination occurred more frequently in dyads of the more despotic ring-tailed lemurs than in Verreaux's sifakas, indicating opposite patterns to macaques in the coevolution of social traits with dominance style. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Infant survival is significantly impacted by dam- and management-related factors in zoo-managed Eulemur populations.

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.

Dietary flexibility of the greater bamboo lemur (Prolemur simus), a specialized feeder, in eastern Madagascar.

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.

Effects of forest fragmentation on the dietary ecology and activity of a nocturnal lemur community in North West Madagascar.

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.

Activity budget and seasonal activity shifts in sympatric lemurs: Increased lean season effort in a cathemeral frugivore contrasts with energy conservation in a diurnal folivore.

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.

Urinary C-peptide and total triiodothyronine as energetic biomarkers for studies of lemurs.

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.

Diurnal fecal glucocorticoid metabolite rhythms in a cathemeral primate, the red-bellied lemur (Eulemur rubriventer), and across mammalian species.

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.

Nutrient balancing in a fruit-specialist primate, the black-and-white ruffed lemur (Varecia variegata).

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.

The Animal-Visitor Interaction Protocol (AVIP) for the assessment of Lemur catta walk-in enclosure in zoos.

Animal-Visitor Interactions (AVI) are activities offered by zoos and other tourism facilities, in which visitors come into close contact with animals. These activities can promote conservational and educational content, raise conservation mindedness and responsibility for the environment and animal welfare, but if not properly managed can jeopardize visitors' and animals' well-being and conservation efforts. The Animal-Visitor Interaction assessment Protocol (AVIP) has been designed to perform an integrated and multidisciplinary assessment of these activities, encompassing the "One Health, One Welfare" approach. AVIP throughout six different steps allows to assess the effects of AVIs both on animals, visitors, and the staff involved. Results can assist zoos to improve management decisions, ensure a transparent evaluation of their activities and promote conservation education goals. Lemurs walk-in enclosures have become increasingly popular among zoos, nevertheless studies focused on their assessment are still scarce. To validate AVIP to this particular AVI, we applied it to assess a walk-in enclosure hosting five Lemur catta in an Italian zoo. Results of behavioural and physiological analyses suggested no changes in animal welfare level and the Animal Welfare Risk Assessment showed low animal welfare risks. Two Visitor Experience Surveys were used to interview 291 visitors, showing that the assessed AVI could help promote the zoo's conservation objectives and visitor education. Risk Assessment found low and medium risks to the health and safety of visitors. Results were then combined to perform a final ethical assessment. Some potential ethical concerns were detected, but the outcomes indicated that these conflicts were well managed. In the context of recent findings AVIP demonstrated its potential for application also in assessing AVIs involving primates. Our findings confirmed the usefulness of AVIP in assessing and monitoring AVIs, allowing to gain key information in a single process on multiple welfare-related parameters, educational impact, safety of the main stakeholders involved, and ethical concerns.

Food availability and male deference in the female-dominant ring-tailed lemur, Lemur catta.

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.

Integrating the female masculinization and challenge hypotheses: Female dominance, male deference, and seasonal hormone fluctuations in adult blue-eyed black lemurs (Eulemur flavifrons).

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.

The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates.

Life history, brain size and energy expenditure scale with body mass in mammals but there is little conclusive evidence for a correlated evolution between life history and energy expenditure (either basal/resting or daily) independent of body mass. We addressed this question by examining the relationship between primate free-living daily energy expenditure (DEE) measured by doubly labeled water method (n = 18 species), life history variables (maximum lifespan, gestation and lactation duration, interbirth interval, litter mass, age at first reproduction), resting metabolic rate (RMR) and brain size. We also analyzed whether the hypometabolic primates of Madagascar (lemurs) make distinct energy allocation tradeoffs compared to other primates (monkeys and apes) with different life history traits and ecological constraints. None of the life-history traits correlated with DEE after controlling for body mass and phylogeny. In contrast, a regression model showed that DEE increased with increasing RMR and decreasing reproductive output (i.e., litter mass/interbirth interval) independent of body mass. Despite their low RMR and smaller brains, lemurs had an average DEE remarkably similar to that of haplorhines. The data suggest that lemurs have evolved energy strategies that maximize energy investment to survive in the unusually harsh and unpredictable environments of Madagascar at the expense of reproduction.

Ring-tailed lemurs (Lemur catta) use olfaction to locate distant fruit.

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.

Agonistic vocalization behaviour in the male ring-tailed lemur (Lemur catta).

Vocalizations are used by group-living animals as aggressive and submissive signals during agonistic interactions, and are also used to maintain dominance hierarchies in many species. For gregarious strepsirrhines with large vocal repertoires and differentiated dominance ranks like the ring-tailed lemur (Lemur catta), agonistic vocalization use is important to study to better understand their social adaptations.To determine whether ring-tailed lemur vocalizations such as the yip, cackle, twitter, chutter, and plosive bark were used as aggressive or submissive signals during agonism and uttered at different rates by males of differing dominance ranks and ages, 565 h of focal data were collected on 31 individual males aged ≥ 1 year from Beza Mahafaly Special Reserve, Madagascar. Yip, cackle, and twitter vocalizations were consistently used during agonistic submissive interactions with both males and females, chutter vocalizations were used during aggressive agonistic interactions with males and submissive agonistic interactions with males and females, and plosive bark vocalizations were used across behavioural contexts but not particularly during agonism. Males of all ages employed all vocalizations, and while low-ranking males uttered yip calls at higher rates, males of all dominance ranks uttered cackle, twitter, chutter, and plosive bark vocalizations. These results advance our knowledge of how male lemurs utilize agonistic vocalizations to maintain inter-individual relationships with males and females, and improve our overall understanding of the function of different agonistic vocalizations in wild lemurs.

Affiliative Contact Calls during Group Travel: Chirp and Wail Vocalization Use in the Male Ring-Tailed Lemur (Lemur catta).

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.

Social Influences on Food Avoidance in Lemur catta.

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.

Key Male Glandular Odorants Attracting Female Ring-Tailed Lemurs.

Among rodents, information about the external world is mainly acquired via the olfactory system, which is one of five sensory modalities. Several semiochemical signals are used for inter- and intraspecies communication [1]. In contrast, primates are generally regarded as vision-oriented mammals, and have been thought to trade their olfactory sensitivity for good sight. However, strepsirrhines have a well-developed olfactory system [2] and a larger repertoire of functional olfactory and vomeronasal receptor genes than haplorhines [3, 4]. Moreover, strepsirrhines are well known for their use of olfactory communication in social behavior. Ring-tailed lemurs are a species of Malagasy strepsirrhines, and use olfactory cues for conspecific communication. Male lemurs mark their scent by spreading volatiles from the antebrachial gland on their wrists. This study combined ethological and chemical approaches to identify a key odorant(s) in antebrachial secretions involved in the sexual communication of lemurs. The results of a behavioral assay indicated that females sniff the males' antebrachial secretions longer during the breeding season than during the nonbreeding season. By examining seasonal changes in volatiles using gas chromatography-mass spectrometry, we found that the secretion of three C12 and C14 aldehydes with a fruity and floral scent significantly increased during the breeding season in a testosterone-dependent manner. Females sniffed for longer at biologically relevant concentrations of two of the aldehydes (12-methyltridecanal and tetradecanal) and were attracted to a mixture of these plus the third aldehyde, dodecanal. Our results suggest that these aldehydes are putative lemur pheromones involved in the attractiveness of males to females during the breeding season.

Lateralization in seven lemur species when presented with a novel cognitive task.

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.

Do lemurs know when they could be wrong? An investigation of information seeking in three species of lemur (Lemur catta, Eulemur rubriventer, and Varecia variegata).

A total of 16 lemurs, including representatives from three species (Lemur catta, Eulemur rubriventer, and Varecia variegata), were presented with a food-seeking task in which information about the rewards location, in one of two plastic tubes, was either known or not known. We evaluated whether lemurs would first look into the tube before making a choice. This information-seeking task aimed to assess whether subjects would display memory awareness, seeking additional information when they became aware they lacked knowledge of the rewards location. We predicted lemurs would be more likely to look into the tube when they had insufficient knowledge about the rewards position. Lemurs successfully gained the reward on most trials. However, they looked on the majority of trials regardless of whether they had all the necessary information to make a correct choice. The minimal cost to looking may have resulted in checking behavior to both confirm what they already knew and gain knowledge they did not have. When the cost of looking increased (elevating the end of tube, requiring additional energy expenditure to look inside-Experiment 2), lemurs still looked into tubes on both seen and unseen trials; however, the frequency of looking increased when opaque tubes were used (where they could not see the rewards location after baiting). This could suggest they checked more when they were less sure of their knowledge state. (PsycInfo Database Record (c) 2020 APA, all rights reserved).