Do zoo-housed primates retreat from crowds? A simple study of five primate species.

An animal's welfare state is directly influenced by the mental state, which is shaped by experiences within the environment throughout the animal's life. For zoo-housed animals, visitors to the zoo are a large part of that environment and a fluctuating influence within it. This study examines the impact of zoo visitors on the space use of five species of zoo-housed primates (Eastern black-and-white colobus monkeys, Colobus guereza, n = 5, Allen's swamp monkeys, Allenopithecus nigroviridis, n = 2, DeBrazza's monkeys, Cercopithecus neglectus, n = 3, Bolivian gray titi monkeys, Callicebus donacophilus, n = 3, and crowned lemurs, Eulemur coronatus, n = 3). Specifically, we considered whether primates' distance from visitor areas changed as crowd sizes increased. Data were collected using the ZooMonitor app. Observers recorded spatial coordinates for each animal over periods ranging from 12 to 32 months. Data were analyzed using two types of regression models (linear and logistic) to examine the influence of visitors on the location of the primates. Both analyses revealed a statistically significant but small decrease in primate distance from visitor viewing glass as the number of visitors increased. Behavioral indicators of welfare were also unaffected by the presence of visitors. These results suggest that, with additional validation, distance from visitors may be one promising, simple way to evaluate the influence of visitors on primate welfare.

Signaling across the senses: a captive case study in pair-bonded red-bellied lemurs (Eulemur rubriventer) at the Duke Lemur Center, NC, USA.

We provide a preliminary case study in red-bellied lemurs (Eulemur rubriventer) to illustrate a multimodal approach to understanding communication strategies within a species with obligate pair-bonds. From June to August 2012, we observed and analyzed signaling behaviors across three established red-bellied lemur pairs at Duke Lemur Center (Durham, NC, USA). Our aim was to assess how individuals combine signal modalities to communicate with pair-mates, and to determine whether these strategies vary by time of day, sex, or pair. We analyzed rates of occurrence of touch (allogrooming, mutual grooming, physical contact, and huddling), scent (scent marking and allomarking), and sound (close-distance contact calls) using Wilcoxon rank sum and exact binomial tests. Time of day impacted rates of occurrence across signal modalities, with higher rates of combined signaling within each modality occurring earlier in the day (p < 0.03). Across time periods, all pairs used auditory signals most frequently, followed by olfactory signals, and finally tactile and tactile-olfactory signals (p < 0.01, all comparisons). In fact, auditory signals frequently overlapped the olfactory signaling modality, and travel rarely occurred without accompanying vocalizations. However, red-bellied lemurs spent the highest percentage of their observed time in tactile signaling bouts (on average, 19.5% of total observed time across pairs). Males and females participated equally in most signaling behaviors (p > 0.1), with the exception of scent marking, which males used more frequently (p < 0.01). The results of this study will aid in developing methods and hypotheses to determine how wild red-bellied lemurs communicate to form, maintain, and advertise their pair-bonds.

Functional analysis of aggression in a black-and-white ruffed lemur (Varecia variegata variegata).

A functional analysis was conducted to assess the antecedent and reinforcing conditions underlying aggressive behavior in a female lemur in captivity. Results showed that her aggression was primarily the result of human attention. A replacement behavior-training program was introduced, and the lemur's aggression was successfully eliminated. These results demonstrate the utility of using functional assessment and analyses in zoos with captive wild nonhuman animals.

Competition for food in a solitarily foraging folivorous primate (Lepilemur leucopus)?

Group-living folivorous primates can experience competition for food, and feeding competition has also been documented for solitarily foraging gummivorous and omnivorous primates. However, little is known about the types and consequences of feeding competition in solitary folivorous foragers. We conducted this study in the spiny forest of Berenty Reserve, southern Madagascar, to characterize the competitive regime of the nocturnal solitarily foraging white-footed sportive lemur (Lepilemur leucopus), a species that lives in dispersed pairs. We analyzed 1,213 hr of behavioral observations recorded simultaneously for the male and female of each of seven social units and recorded seasonal changes in food availability over a complete annual cycle. Lepilemur leucopus exhibited low selectivity in its dietary choice and mainly included the most abundant plant species in its diet. Contrary to our predictions, we did not find evidence for increased rates of contest (i.e., displacement from food trees) or scramble competition (i.e., shared use of food patches) during the lean season, neither within nor between social units. Instead, conflict rates were low throughout the year, and, during these observations, any feeding stress may have been more related to food quality than quantity. The resource defense hypotheses may not explain pair-living in this species as there was no indication that males defend food resources for their female pair-partners. The observed lack of feeding competition may indicate that a cryptic anti-predator strategy is a better predictor of spatial avoidance of pair-partners than conflict over food. While anti-predator benefits of crypsis may explain, at least partly, female-female avoidance, studies on the relationship between territory size/quality and reproductive success are required to understand whether feeding competition reduces the potential for female association in L. leucopus.

Interspecific semantic alarm call recognition in the solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis.

As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This "eavesdropping" was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species' and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect predators early, and that the lemurs' reactions are based on experience and learning.

Brown lemurs (Eulemur fulvus) can master the qualitative version of the reverse-reward contingency.

Behavioral flexibility that requires behavioral inhibition has important fitness consequences. One task commonly used to assess behavioral inhibition is the reverse-reward task in which the subject is rewarded by the non selected items. Lemurs were tested for their ability to solve the qualitative version of the reverse-reward task with the choice between identical quantities of different food items instead of different quantities of the same food. Two of four subjects mastered the task without a correction procedure and were able to generalize the acquired rule to novel combinations of food. One of the two subjects competent on the quality version of the task could transfer this ability to different quantities of the same food. Our results are compared to lemurs' performances when tested under the quantitative version in a previous study and those of capuchin monkeys tested under a similar paradigm. The whole results suggest that the qualitative version of the reverse-reward task may be easier to master than its quantitative counterpart and that lemurs perform better than capuchin monkeys as they were able to later transfer the learning rule to the quantitative version of the task.

Brown (Eulemur fulvus) and ring-tailed lemurs (Lemur catta) use human head orientation as a cue to gaze direction in a food choice task.

Whilst the ability to follow human gaze has been demonstrated in monkeys and apes, there is little evidence that prosimians share this ability. The current study used a food choice paradigm to assess whether captive brown (Eulemur fulvus) and ring-tailed lemurs (Lemur catta) use human gaze direction as a cue when choosing between an attending or non-attending human. Four experiments assessed the use of body, head and eye cues by the lemurs. In experiment 1, the non-attending human stood with her back to a food item; 3 of the 5 lemurs preferentially chose the attending human with an equivalent food item in view. In experiments 2 and 3, which used head angles of 90°, 4 out of 5 lemurs preferentially chose the attending human. In experiment 4, in which the humans differed only by whether their eyes were open or shut, no significant preferences were found. This study provides the first tentative evidence that lemurs are capable of discriminating human gaze direction and can use both body and head direction to do so.

Sex ratio affects sex-specific innovation and learning in captive ruffed lemurs (Varecia variegata and Varecia rubra).

Recent years have witnessed extensive research into problem solving and innovation in primates, yet lemurs have not been subjected to the same level of attention as apes and monkeys, and the social context in which novel behavior appears has rarely been considered. We gave novel foraging puzzlebox devices to seven groups of ruffed lemurs (Varecia variegata and Varecia rubra) to examine the factors affecting rates of innovation and social learning. We found, across a range of group sex ratios, that animals of the less-represented sex were more likely to contact and solve the puzzlebox sooner than those of the more-represented sex. We established that while some individuals were able to solve the puzzleboxes there was no evidence of social learning. Our findings are consistent with previously reported male deference as a sexual strategy, but we conclude that the need for male deference diminishes when, within a group, males are rare.

Can lemurs (Eulemur fulvus and E. macaco) use abstract representations of quantities to master the reverse-reward contingency task?

In previous studies we demonstrated that brown and black lemurs (Eulemur fulvus and E. macaco) showed self-control abilities under a reverse-reward contingency. They were able to significantly select the smaller quantity of food to be rewarded with the larger one and to generalize this ability when presented with two rewards that differed in quality. In the present study, previously trained subjects had to choose between graphic representations of two different quantities of food under the reverse-reward contingency. Three out of four subjects learned to associate a graphic representation of the reward with the corresponding quantity. Only one subject consistently selected the representation of the smaller quantity to be rewarded with the larger quantity of food and therefore showed abstraction as well as relative numerousness skills. Indeed, she was able to discriminate between representations of different quantities and to ordinate them. We discuss how primates mentally represent food quantities and how self-control is involved in foraging strategies.

Sex ratio at birth and age-reversed dominance among female Varecia.

Analysis of 283 offspring born at the Duke University Primate Center show that young female ruffed lemurs, Varecia variegata, produce significantly more daughters, whereas old mothers produce more sons than expected. Data are compared to 3 hypotheses for sex ratio bias: the Trivers-Willard hypothesis which predicts that dominant females produce more males, the local resource competition (LRC) hypothesis which predicts that subordinate females produce more males, and the local resource enhancement (LRE) extension of the LRC hypothesis that females produce the sex that provides later cooperative benefits. In the case of Varecia, this may include alloparenting or cooperative breeding. The results are more consistent with the LRC model. However, observations of 8 mother-daughter relationships show that female dominance rank in free-ranging Varecia groups is age reversed, with daughters aggressively outranking their mothers. Daughters born into the group were not beneficial as future supporters in within-group intermatriline competition as assumed by the LRE model, or as subordinate alloparents, cooperative breeders or aids in territorial defense. Both sex ratio and ranking observations are consistent, however, with the hypothesis that mothers produce daughters when they are young and able to invade elsewhere and sons as they age and are less able to do so. This is supported by a single observation of a mother dispersing which resulted in her daughter inheriting the natal territory. These data are supportive of the LRE model with female alliances and cooperative breeding among dispersed females.

Object permanence in lemurs.

Object permanence, the ability to mentally represent objects that have disappeared from view, should be advantageous to animals in their interaction with the natural world. The objective of this study was to examine whether lemurs possess object permanence. Thirteen adult subjects representing four species of diurnal lemur (Eulemur fulvus rufus, Eulemur mongoz, Lemur catta and Hapalemur griseus) were presented with seven standard Piagetian visible and invisible object displacement tests, plus one single visible test where the subject had to wait predetermined times before allowed to search, and two invisible tests where each hiding place was made visually unique. In all visible tests lemurs were able to find an object that had been in clear view before being hidden. However, when lemurs were not allowed to search for up to 25-s, performance declined with increasing time-delay. Subjects did not outperform chance on any invisible displacements regardless of whether hiding places were visually uniform or unique, therefore the upper limit of object permanence observed was Stage 5b. Lemur species in this study eat stationary foods and are not subject to stalking predators, thus Stage 5 object permanence is probably sufficient to solve most problems encountered in the wild.

Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003.

Eulemur fulvus rufus has been described as having stable multi-male/multi-female groups, a male-biased sex ratio, and female philopatry. However, in a 16-year study of this subspecies we documented a great deal of demographic change as several groups permanently fissioned, some groups disappeared, and new groups formed. We split the dataset into two periods, 1988 to 1993 and 1994 to 2003, which coincided with the first disappearance of a study group (in August 1994) and the first permanent group fission (in December 1994). The average group size decreased by nearly half between the study periods (10.5-5.6), while the frequency of group membership changes increased (2.0-8.3 times/year), and the birth rate decreased (0.56-0.38). Females, as well as males, immigrated into study groups and transferred between groups, something that has been rarely seen in this subspecies. We also found a significant decline in the amount of fruit from the earliest part of the study to the latter part of the study. Study groups did not switch to other types of foods during periods of fruit shortage, but traveled outside of their home range areas more often over the study period. Finally, the density E. f. rufus decreased in the study area while the densities of their main food competitors, Varecia variegata and Eulemur rubriventer, increased. Although few primate populations are numerically stable over time, we suggest that female behavioral responses to decreases in fruit availability may have influenced some of the demographic changes we witnessed in this study.

Habitat use and social structure of a brown lemur hybrid population in the Berenty Reserve, Madagascar.

The population of brown lemurs has rapidly grown since their founders were introduced to the Berenty Reserve. The founders consist of two species (Eulemur fulvus rufus and E. collaris). To characterize the behavior of the population and to examine whether these characteristics affect population growth, I investigated the habitat use and social structure of the population of brown lemurs at Berenty (Berenty Eulemur). Behavior data were collected focusing on horizontal and vertical habitat use, activity rhythms, and intergroup relationships. These data were compared with the data of E. fulvus in other areas, with the previous studies done at Berenty, and with data on Berenty Lemur catta. Berenty Eulemur maintained a home range size comparable to E. f. rufus in the western deciduous dry forest, but was found at a lower level of the forest and had larger overlapping home ranges. Berenty Eulemur use food resources earlier in the morning than L. catta, intergroup conflict was avoided by vocal communication, and Berenty Eulemur made suitable use of their limited habitat. I suggest that a number of behavioral characteristics of Berenty Eulemur may contribute to their population growth.

Diurnal distribution of loud calls in sympatric wild indris (Indri indri) and ruffed lemurs (Varecia variegata): implications for call functions.

We carried out a short study on the diurnal call distribution of two sympatric lemurs in the Réserve Naturelle Intégrale Zahamena (eastern Madagascar). Whereas indris (Indri) song bouts were clearly concentrated in the early morning hours, the roar/shriek choruses of ruffed lemurs (Varecia) exhibited a much more even distribution throughout the day. These differences in distribution pattern support earlier claims that indri song bouts are more likely to serve territorial functions, whereas ruffed lemur loud calls may serve both spacing and/or alarm call functions.

Expectations about numerical events in four lemur species (Eulemur fulvus, Eulemur mongoz, Lemur catta and Varecia rubra).

Although much is known about how some primates--in particular, monkeys and apes--represent and enumerate different numbers of objects, very little is known about the numerical abilities of prosimian primates. Here, we explore how four lemur species (Eulemur fulvus, E. mongoz, Lemur catta, and Varecia rubra) represent small numbers of objects. Specifically, we presented lemurs with three expectancy violation looking time experiments aimed at exploring their expectations about a simple 1+1 addition event. In these experiments, we presented subjects with displays in which two lemons were sequentially added behind an occluder and then measured subjects' duration of looking to expected and unexpected outcomes. In experiment 1, subjects looked reliably longer at an unexpected outcome of only one object than at an expected outcome of two objects. Similarly, subjects in experiment 2 looked reliably longer at an unexpected outcome of three objects than at an expected outcome of two objects. In experiment 3, subjects looked reliably longer at an unexpected outcome of one object twice the size of the original than at an expected outcome of two objects of the original size. These results suggest that some prosimian primates understand the outcome of simple arithmetic operations. These results are discussed in light of similar findings in human infants and other adult primates.

Analog number representations in mongoose lemurs (Eulemur mongoz): evidence from a search task.

A wealth of data demonstrating that monkeys and apes represent number have been interpreted as suggesting that sensitivity to number emerged early in primate evolution, if not before. Here we examine the numerical capacities of the mongoose lemur (Eulemur mongoz), a member of the prosimian suborder of primates that split from the common ancestor of monkeys, apes and humans approximately 47-54 million years ago. Subjects observed as an experimenter sequentially placed grapes into an opaque bucket. On half of the trials the experimenter placed a subset of the grapes into a false bottom such that they were inaccessible to the lemur. The critical question was whether lemurs would spend more time searching the bucket when food should have remained in the bucket, compared to when they had retrieved all of the food. We found that the amount of time lemurs spent searching was indicative of whether grapes should have remained in the bucket, and furthermore that lemur search time reliably differentiated numerosities that differed by a 1:2 ratio, but not those that differed by a 2:3 or 3:4 ratio. Finally, two control conditions determined that lemurs represented the number of food items, and neither the odor of the grapes, nor the amount of grape (e.g., area) in the bucket. These results suggest that mongoose lemurs have numerical representations that are modulated by Weber's Law.

Reciprocal recognition of sifaka ( Propithecus verreauxi verreauxi) and redfronted lemur ( Eulemur fulvus rufus) alarm calls.

Redfronted lemurs ( Eulemur fulvus rufus) and Verreaux's sifakas ( Propithecus verreauxi verreauxi) occur sympatrically in western Madagascar. Both species exhibit a so-called mixed alarm call system with functionally referential alarm calls for raptors and general alarm calls for carnivores and raptors. General alarm calls also occur in other contexts associated with high arousal, such as inter-group encounters. Field playback experiments were conducted to investigate whether interspecific recognition of alarm calls occurs in both species, even though the two species rarely interact. In a crossed design, redfronted lemur and sifaka alarm calls were broadcast to individuals of both species, using the alarm call of chacma baboons ( Papio cynocephalus) as a control. Both species responded with appropriate escape strategies and alarm calls after playbacks of heterospecific aerial alarm calls. Similarly, they reacted appropriately to playbacks of heterospecific general alarm calls. Playbacks of baboon alarm calls elicited no specific responses in either lemur species, indicating that an understanding of interspecific alarm calls caused the responses and not alarm calls in general. Thus, the two lemur species have an understanding of each other's aerial as well as general alarm calls, suggesting that even in species that do not form mutualistic associations and rarely interact, common predator pressure has been sufficient for the development of heterospecific call recognition.

Intersexual dominance, masculinized genitals and prenatal steroids: comparative data from lemurid primates.

Masculinization of female genitalia and female intersexual dominance distinguish spotted hyenas (Crocuta crocuta) and Malagasy primates (Lemuriformes) from most other mammals. An unusual prenatal endocrine environment has been proposed to proximately underlie the development of these traits in hyenas. To examine whether female dominance and genital masculinization are similarly enhanced by the prenatal environment in lemurid primates, we measured androgen and estrogen excretion in pregnant wild redfronted lemurs (Eulemur fulvus rufus). Our results showed that estrogen levels during the second phase of gestation were much higher in females carrying a male fetus than in female-carrying mothers. This may indicate the onset of testicular activity in male fetuses, because androgens of fetal origin are aromatized to maternal estrogens. Levels of androgen excretion were similar in all mothers regardless of the fetus' sex, which may suggest that androgen-independent mechanisms also contribute to female masculinization. The much higher androgen/estrogen ratio in female-carrying mothers indicates that relative, rather than absolute, prenatal steroid concentrations may play a role in female masculinization.

Social system of the Alaotran gentle lemur (Hapalemur griseus alaotrensis): genetic characterization of group composition and mating system.

Group composition and mating system were investigated in wild Alaotran gentle lemurs (Hapalemur griseus alaotrensis) using genetic markers. These small-bodied herbivorous and cathemeral primates are endemic to the reed and papyrus beds around Lac Alaotra in Madagascar. They live in small groups in small, defended territories. Data were collected during the rainy seasons in 1996, 1997, and 1999, and include 99 individuals from 22 neighboring social groups and an additional 30 animals from other areas representing most of the geographic range. Animals were located by researchers canoeing in the marshes bordering the lake. After a group's size was determined by direct observation, all individuals were captured, marked, and released. During handling each individual was weighed and sexed, and hair samples for DNA extraction were collected. A 342 bp mtDNA control region sequence and 10 nuclear microsatellite loci provided multilocus genotypes that were used to assess pedigree relations and population structure. Alaotran gentle lemurs were found in groups of two to nine individuals (mean: 4.3), comprising one or two breeding females, their offspring, and one reproducing male. Solitary individuals of both sexes were encountered rarely. Breeding females were the permanent core of the social groups, whereas intergroup transfer of reproductive males was relatively frequent. Forty percent of all reproducing groups contained two breeding females, which were related to each other as closely as mother-daughter or full sisters. Parentage assessment revealed a variable mating system ranging from serial monogamy to polygyny within social groups. At least 8% of paternities involved extragroup males. Additional data on life history and reproduction are presented, and the social system of the Alaotran gentle lemur is discussed in the light of the new genetic findings.

Special relationships instead of female dominance for redfronted lemurs, Eulemur fulvus rufus.

Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale-multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male-female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male-female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male-female affiliations illuminated developmental and functional aspects of male-female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male-female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male-female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate.