Inferences about the location of food in lemurs (Eulemur macaco and Eulemur fulvus): a comparison with apes and monkeys

The ability of black and brown lemurs (Eulemur macaco and Eulemur fulvus) to make inferences about hidden food was tested using the same paradigm as in Call’s (J Comp Psycol 118:232–241, 2004) cup task experiment. When provided with either visual or auditory information about the content of two boxes (one empty, one baited), lemurs performed better in the auditory condition than in the visual one. When provided with visual or auditory information only about the empty box, one subject out of four was above chance in the auditory condition, implying inferential reasoning. No subject was successful in the visual condition. This study reveals that (1) lemurs are capable of inferential reasoning by exclusion and (2) lemurs make better use of auditory than visual information. The results are compared with the performances recorded in apes and monkeys under the same paradigm.     

THIS ARTICLE HAS BEEN RETRACTED: Enumeration of objects and substances in non‐human primates: experiments with brown lemurs (Eulemur fulvus)

Both human infants and adult non‐human primates share the capacity to track small numbers of objects across time and occlusion. The question now facing developmental and comparative psychologists is whether similar mechanisms give rise to this capacity across the two populations. Here, we explore whether non‐human primates’ object tracking abilities are subject to the same constraints as those of human infants. In particular, we examine whether one primate species, the brown lemur (Eulemur fulvus), also fails to represent and enumerate objects when they behave non‐rigidly or non‐cohesively. We presented lemurs with a series of expectancy violation studies involving simple 1 + 1 addition events in which we varied the entities to be enumerated. Like infants, lemurs successfully enumerated the two objects when those objects were rigid, cohesive individuals, but failed to enumerate similar‐looking non‐rigid piles of sand. In contrast to human infants, however, lemurs successfully enumerated non‐cohesive objects that broke into multiple pieces. These results are discussed in light of recent theories about object processing in human infants and adults.     

Gaze following and gaze priming in lemurs

Although primates have often been found to co-orient visually with other individuals, members of these same species have usually failed to use co-orientation to find hidden food in object-choice experiments. This presents an evolutionary puzzle: what is the function of co-orientation if it is not used for a function as basic as locating resources? Co-orientation responses have not been systematically investigated in object-choice experiments, and requiring co-orientation with humans (as is typical in object-choice tasks) may underestimate other species’ abilities. Using an object-choice task with conspecific models depicted in photographs, we provide experimental evidence that two lemur species (Eulemur fulvus, n = 4, and Eulemur macaco, n = 2) co-orient with conspecifics. Secondly, by analysing together two measures that have traditionally been examined separately, we show that lemurs’ gaze following behaviour and ultimate choice are closely linked. Individuals were more likely to choose correctly after having looked in the same direction as the model, and thus chose objects correctly more often than chance. We propose a candidate system for the evolutionary origins of more complex gaze following: ‘gaze priming.’     

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.This revised version was published online in March 2005 with corrections to Fig. 6.     

Transfer of self-control in black (Eulemur macaco) and brown (Eulemur fulvus) lemurs: choice of a less preferred food item under a reverse-reward contingency

When presented a choice between two food-type arrays of equivalent size under a reverse-reward contingency, black (Eulemur macaco) and brown (Eulemur fulvus) lemurs transposed their self-control abilities, acquired in a previous experiment, to significantly select the less-desired food item in order to gain access to the more desired one. However, when presented with the choice between two different food-type arrays in which the amount of the less desired food array was larger than the more desired one, large individual differences were revealed: Some subjects established a consistent rule favoring quality or quantity, whereas others exhibited various point of trade-off. These results show that lemurs seem to manage the task considering not only food quantity but also food quality.     

Reciprocal recognition of sifaka (<Emphasis Type="Italic">Propithecus verreauxi verreauxi</Emphasis>) and redfronted lemur (<Emphasis Type="Italic">Eulemur fulvus rufus</Emphasis>) 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.     

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 Webers Law.     

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.     

Agonistic behavior and growth in newly emerged brown trout (Salmo trutta L) of sea‐ranched and wild origin

Selection experiments and game theory models have revealed that the changes in agonistic behavior following selection for rapid growth rate of fish depend on the access of food. If food is spatially restricted and in excess of demand, the intensity of agonistic behaviors will decrease. This prediction was tested in an experiment on wild and sea‐ranched brown trout (Salmo trutta L.) fry originating from a common stock. Agonistic behavior, activity, and specific growth rate were studied in tanks (56 × 56 cm) at high (159.4 fry/m²) and low (9.6 fry/m²) stocking densities given either a large or small food ration (3.0% and 1.5%, respectively, food per total body weight and day). Observations were done during 4 days in each trial. Generally, fry of sea‐ranched origin had a higher growth rate. No differences in activity were found. Intensity of agonistic behavior was higher among wild groups. There was a tendency for interaction between density and strain, e.g., wild fish were relatively more aggressive at higher densities. Food ration had no effect on level of agonistic behavior. These results indicate that the selection for rapid growth in hatcheries may indirectly select for reduced aggressiveness. Genetic integrity and diversity of wild populations may be threatened when interbreeding occurs between wild and hatchery fish. Aggr. Behav. 28:145–153, 2002. © 2002 Wiley‐Liss, Inc.     

Agonistic and sociable behaviors in the mound‐building mice,Mus spicilegus: A comparative study with Mus musculus domesticus

Present social organization and mating systems result from selective pressures and ecological conditions but also from proximate interactions between individuals. Many studies report on a polygynous mating system with a social group territoriality in commensal populations of Mus musculus domesticus. However, little is known about the social organization of other Mus species living in outdoor conditions, such as the mound‐building mouse Mus spicilegus. Comparative studies between M. m. domesticus and M. spicilegus have already shown behavioral differences in female sexual preferences and paternal care. To study agonistic and sociable interactions and gain insight into the social organization and the mating system of M. spicilegus, the present study compared intraspecific dyadic encounters between unfamiliar adults in these two species. Results demonstrated less tolerance between females and between the sexes in M. spicilegus than in M. m. domesticus unfamiliar mice. The consequences of those differences between M. spicilegus and M. m. domesticus on social organization and mating system are discussed. Aggr. Behav. 28:75–84, 2002. © 2002 Wiley‐Liss, Inc.     

Lemurs and macaques show similar numerical sensitivity

We investigated the precision of the approximate number system (ANS) in three lemur species (Lemur catta, Eulemur mongoz, and Eulemur macaco flavifrons), one Old World monkey species (Macaca mulatta) and humans (Homo sapiens). In Experiment 1, four individuals of each nonhuman primate species were trained to select the numerically larger of two visual arrays on a touchscreen. We estimated numerical acuity by modeling Weber fractions (w) and found quantitatively equivalent performance among all four nonhuman primate species. In Experiment 2, we tested adult humans in a similar procedure, and they outperformed the four nonhuman species but showed qualitatively similar performance. These results indicate that the ANS is conserved over the primate order.     

The ecology of spatial memory in four lemur species

Evolutionary theories suggest that ecology is a major factor shaping cognition in primates. However, there have been few systematic tests of spatial memory abilities involving multiple primate species. Here, we examine spatial memory skills in four strepsirrhine primates that vary in level of frugivory: ruffed lemurs (Varecia sp.), ring-tailed lemurs (Lemur catta), mongoose lemurs (Eulemur mongoz), and Coquerel’s sifakas (Propithecus coquereli). We compare these species across three studies targeting different aspects of spatial memory: recall after a long-delay, learning mechanisms supporting memory and recall of multiple locations in a complex environment. We find that ruffed lemurs, the most frugivorous species, consistently showed more robust spatial memory than the other species across tasks—especially in comparison with sifakas, the most folivorous species. We discuss these results in terms of the importance of considering both ecological and social factors as complementary explanations for the evolution of primate cognitive skills.     

Social aggression and power relations among preschool children

Social agonism and dominance relations were assessed in two preschool groups. An average of 30 hours of observational data was obtained for each group during free-play over a six-week period. A Social Agonism Inventory describing specific initiation and response behaviors during episodes of social conflict was used to code agonistic activity. Dyadic interactions were examined to determine whether the resolution of agonistic interactions conformed to a linear model of social dominance. Although there were group differences in the relative frequency of different forms of conflict, systematic comparison of agonistic wins and losses re vealed similarly rigid and linear dominance structures at both preschools. The relation of aggression and dominance was empirically examined by comparing the initiation and receipt of agonism by high vs low dominance status children. Higher dominance status children engaged in more agonistic interactions, but a majority of these interactions were directed toward other high-ranking group members.     

How prosimian primates represent tools: experiments with two lemur species (Eulemur fulvus and Lemur catta)

The authors examined how 2 lemur species (Eulemur fulvus and Lemur catta) reason about tools. Experiment 1 allowed subjects to use 1 of 2 canes to retrieve an inaccessible food reward. Lemurs learned to solve this problem as quickly as other primates. Experiment 2 then presented subjects with novel tools differing from the originals along one featural dimension. Subjects attended more to tools' sizes than to their colors and made no distinction between tools' shapes and textures. Experiments 3 and 4 presented problems in which some of the tools' orientations had to be modified relative to the food. Subjects performed well on these problems, sometimes modifying the position of the tool. These results are discussed in light of the performance of other primates on this task.     

Development of the Social Behavior of Two Mice Species With Contrasting Social Systems

The house mouse (Mus musculus) and the mound‐building mouse (M. spicilegus) differ in their mating and social systems. The M. musculus is polygynous and females tend to breed cooperatively while M. spicilegus is known to be monogamous and famous for its unique cooperative behavior; the communal overwintering. Mus spicilegus is considered as a highly aggressive species in the genus Mus. In the present study, we attempted to analyze the development of aggressive and sociable behavior in these species and to discover how familiarity with the target moderates the development of sociable and aggressive behaviors and moderates the differences between the species. Dyadic social interaction tests in neutral cages were performed on 21‐, 60‐, and 120‐day‐old mice of both genders and both species. Each individual was tested against a sibling and an unfamiliar individual at all three ages. Our results showed that the development of aggressive and sociable behavior with age differed between the species and sexes; however, familiarity with the other mouse moderated the effect of species on aggression. At 21 days, both genders of M. spicilegus were more aggressive against strangers than siblings. This became true of both species at 60 days. When facing a stranger, both sexes of M. spicilegus were more aggressive than M. musculus at 120 days. However, when facing a sibling, neither gender of M. spicilegus was more agonistic than M. musculus, indicating that either kinship or early social experiences elicit tolerance. Aggr. Behav. 38:288‐297, 2012. © 2012 Wiley Periodicals, Inc.     

Parental play styles and sibling interaction during a problem‐solving task

Associations between parental play styles and sibling interaction were investigated in 30 same‐sex preschool‐ and school‐aged sibling dyads (first‐borns were 4–9 years, M=6.6 years; second‐borns were 2–7 years, M=4.2 years), divided into older and younger sibling groups. Participants completed puzzles under three conditions: (a) siblings alone, (b) together with mother, and (c) together with father. Prosocial and agonistic sibling‐directed behaviors and positive and negative parent–child behaviors were coded. Siblings engaged in both more prosocial and agonistic interactions when alone than with either parent; there were no differences in sibling interactions in the mother versus father episodes. Paternal negative behavior was associated with sibling agonistic behavior when the children were alone, indicating second‐order effects, however, mother–child and sibling interactions were not significantly associated. Nevertheless, reciprocity in positive and negative behaviors directed by children to parents and vice versa was evident, demonstrating synchrony in patterns of exchanges. The findings underscore the necessity of studying both parents in order to understand more fully the dynamics involved in family relationships. Copyright © 1999 John Wiley & Sons, Ltd.     

Social dominance and priority of access to drinking in Lemur macaco

Social dominance was analyzed in a group of Lemur macaco over a one-year period. A gonistic dominance was assessed by computing a dominance index for each individual in baseline conditions and in a competitive drinking situation, where success was measured as the amount of time in possession of the resource (a hottle of fruit juice). Dominance indexes during drinking competition were significantly correlated with baseline dominance indexes but were not correlated with individual drinking success. Adult females were agonistically do, omsmy over all other individuals, but were frequently challenged by juveniles of both sexes for access to the drinking bottle. In males, there was a significant negative correlation between age and dominance indexes during competition tests, and between age and drinking success. Results are analysed in the ligh of recent theories concerning the emergence of female social dominance. © 1993 Wiley-Liss, Inc.     

Aggression and commensalism in house mouse: a comparative study across Europe and the near east

Species specific differences of house mouse social behavior compared to its closest relatives (aboriginal species Mus macedonicus, Mus spicilegus, and Mus spretus) have recently been suggested. However, substantial variation of behavioral traits between mouse populations has been also evidenced. Agonistic behavior of laboratory‐born house mice from five commensal populations (Mus musculus musculus: central Czech Republic, Mus musculus domesticus: Bulgaria, Greece, Turkey, and natural Mus m. musculus/domesticus hybrids from the Czech part of the hybrid zone) and five non‐commensal populations of M. m. domesticus (C. Syria, E. Syria, Jordan, Iran, Libya) was studied. Dyadic interactions in a neutral cage were performed and the effects of sex and population on time spent by agonistic behavior evaluated. In all studied populations, the male‐male interactions were more agonistic than the female‐female ones. Male‐male behavior gradually increased from the least agonistic population of M. m. musculus from Central Europe to the Near East populations of M. m. domesticus exhibiting the highest scores of agonistic behavior. Between‐population differences were even stronger when female‐female encounters were considered. While females of commensal populations belonging to both M. m. musculus and M. m. domesticus were tolerant of each other, those coming from non‐commensal populations of M. m. domesticus were highly agonistic, reaching even the level of aggression between the females of some aboriginal mouse species. This phenomenon may be attributed to increased competition for food in non‐commensal populations when compared to commensal ones supplied by superabundant resources. Social behavior of house mice, therefore, appears to be pliable rather than rigid and species specific. It can be changed rapidly according to ecological needs and such adaptability allows house mice to colonize various habitats. Aggr. Behav. 31:283–293, 2005. © 2005 Wiley‐Liss, Inc.     

Aggressive interactions and consistency of dominance hierarchies of the native and nonnative cichlid fishes of the Balsas basin

Dominance hierarchies are generally established based on the levels of aggressiveness that animals present. Frequently, animals fight to establish a dominance hierarchy and obtain a disputed resource. The Mexican mojarra Cichlasoma istlanum is a native species of the Balsas river basin and coexists there with four nonnative cichlids: tilapia Oreochromis sp., convict cichlid Amatitlania nigrofasciata, spotcheek cichlid Thorichthys maculipinnis, and green terror Andinoacara rivulatus. These five cichlid species compete for spaces for reproduction, feeding, and shelter and frequently engage in aggressive interactions to obtain these resources. We quantified dominance indices to evaluate the hierarchical structure of dominance among these five cichlids and the duration of aggressive behaviors of the Mexican mojarra during experimental contests between the native species and each of the four nonnative species. The Mexican mojarra was consistently dominant over the other four cichlid species, performing a larger number of aggressive behaviors and investing more time in attacking than the nonnative cichlids, which resulted in a higher hierarchical position. Our results show that the native fish, Mexican mojarra, established dominance over all four nonnative cichlid fish of the Balsas basin. Thus, the establishment of nonnative cichlid species in the Balsas basin is likely associated with factors other than behavioral dominance.     

Spatial memory in the grey mouse lemur (Microcebus murinus)

Wild animals face the challenge of locating feeding sites distributed across broad spatial and temporal scales. Spatial memory allows animals to find a goal, such as a productive feeding patch, even when there are no goal-specific sensory cues available. Because there is little experimental information on learning and memory capabilities in free-ranging primates, the aim of this study was to test whether grey mouse lemurs (Microcebus murinus), as short-term dietary specialists, rely on spatial memory in relocating productive feeding sites. In addition, we asked what kind of spatial representation might underlie their orientation in their natural environment. Using an experimental approach, we set eight radio-collared grey mouse lemurs a memory task by confronting them with two different spatial patterns of baited and non-baited artificial feeding stations under exclusion of sensory cues. Positional data were recorded by focal animal observations within a grid system of small foot trails. A change in the baiting pattern revealed that grey mouse lemurs primarily used spatial cues to relocate baited feeding stations and that they were able to rapidly learn a new spatial arrangement. Spatially concentrated, non-random movements revealed preliminary evidence for a route-based restriction in mouse lemur space; during a subsequent release experiment, however, we found high travel efficiency in directed movements. We therefore propose that mouse lemur spatial memory is based on some kind of mental representation that is more detailed than a route-based network map. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.