Testing brown lemurs (Eulemur fulvus) on the reverse-reward contingency task without a modified procedure

A common paradigm used to study inhibitory control is the reverse-reward contingency task in which the subject is presented with a choice between two different quantities of food and is rewarded with the non-chosen item. Most animals have problems inhibiting their impulsive choice towards the larger quantity, and need correction procedures to master the reverse-reward task. Recent studies have nonetheless shown that rhesus macaques and white crowned mangabeys were able to master the task without correction procedures after a large number of trials were applied.We previously demonstrated that, similar to other primates tested under the reverse-reward contingency task, lemurs initially showed an impulsive bias towards the larger quantity of food. But following introduction of a large-or-none contingency, all the subjects learned to reliably select the smaller quantity in order to gain access to the larger one. Here, we assessed the possibility that, similar to rhesus macaques and mangabeys, lemurs could master the reverse-reward task, without a modified procedure, by presenting a large number of trials. One of 5 subjects was able to master the task and then generalize performance to novel food arrays.     

Can lemurs (<Emphasis Type="Italic">Eulemur fulvus</Emphasis> and <Emphasis Type="Italic">E. macaco</Emphasis>) 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.     

Lateral bias to the leading limb in an olfactory social signal by male ring-tailed lemurs

Because ring-tailed lemurs (Lemur catta) show handedness during feeding, I investigated whether they also show lateral preference in the limbs used by males during scent marking. During a bout of marking, a male alternates a variable number of shoulder rubs and arm marks. It is a complex social signal that has both olfactory and visual components and is frequently part of intrasexual agonistic interactions. I used all-occurrences behavior sampling, manually recorded all totally visible bouts, and required a minimum of 50 bouts per animal. The subjects included six wild and four group-living captive male lemurs. I considered limb usage to be lateralized for each individual lemur if the frequency of use of one side was significantly above chance as determined by binomial z-scores at P<.05. I measured consistency of lateral preference by calculating handedness index (HI) scores for each individual. Overall, I recorded 1,583 bouts of scent marking, and 66% of the bouts began with shoulder rubbing. Eight of the 10 males showed a significant, moderately strong lateral preference for the lead limb in the first shoulder rub performed in a bout, and for six of these eight the preferred lead limb for shoulder rubbing was the left one. Six of the 10 males showed a significant but weak lateral preference in the first arm mark, and five of these preferred the opposite limb to that used for the first shoulder rub. Although the preferences were not at the population level, eight of the 10 lemurs showed a lateral bias in the lead limb used for a component of this complex social signal.     

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.     

Intertemporal choice in lemurs

Different species vary in their ability to wait for delayed rewards in intertemporal choice tasks. Models of rate maximization account for part of this variation, but other factors such as social structure and feeding ecology seem to underly some species differences. Though studies have evaluated intertemporal choice in several primate species, including Old World monkeys, New World monkeys, and apes, prosimians have not been tested. This study investigated intertemporal choices in three species of lemur (black-and-white ruffed lemurs, Varecia variegata, red ruffed lemurs, Varecia rubra, and black lemurs, Eulemur macaco) to assess how they compare to other primate species and whether their choices are consistent with rate maximization. We offered lemurs a choice between two food items available immediately and six food items available after a delay. We found that by adjusting the delay to the larger reward, the lemurs were indifferent between the two options at a mean delay of 17 s, ranging from 9 to 25 s. These data are comparable to data collected from common marmosets (Callithrix jacchus). The lemur data were not consistent with models of rate maximization. The addition of lemurs to the list of species tested in these tasks will help uncover the role of life history and socio-ecological factors influencing intertemporal choices.     

Tokens improve capuchin performance in the reverse–reward contingency task

In humans and apes, one of the most adaptive functions of symbols is to inhibit strong behavioural predispositions. However, to our knowledge, no study has yet investigated whether using symbols provides some advantage to non-ape primates. We aimed to trace the evolutionary roots of symbolic competence by examining whether tokens improve performance in the reverse–reward contingency task in capuchin monkeys, which diverged from the human lineage approximately 35 Ma. Eight capuchins chose between: (i) two food quantities, (ii) two quantities of ‘low-symbolic distance tokens’ (each corresponding to one unit of food), and (iii) two ‘high-symbolic distance tokens’ (each corresponding to a different amount of food). In all conditions, subjects had to select the smaller quantity to obtain the larger reward. No procedural modifications were employed. Tokens did improve performance: five subjects succeeded with high-symbolic distance tokens, though only one succeeded with food, and none succeeded with low-symbolic distance tokens. Moreover, two of the five subjects transferred the rule to novel token combinations. Learning effects or preference reversals could not account for the successful performance with high-symbolic distance tokens. This is, to our knowledge, the first demonstration that tokens do allow monkeys to inhibit strong behavioural predispositions, as occurs in chimpanzees and children.     

Laterality in semi‐free‐ranging black and white ruffed lemurs (Varecia variegata variegata): head‐tilt correlates with hand use during feeding

Previous studies in human and chimpanzee infants have identified a predictive relationship between early rightward head orientation and later right hand use. Data from lemurs suggest a leftward bias in hand preference, but there are no data on head positioning. The purpose of this study was to examine the relationship between head and hand preferences in the black and white ruffed lemur (Varecia variegata variegata). Ruffed lemurs rotate the head vertically during chewing in a behavior called head‐tilting. Frequency of head‐tilting and bouts of unimanual hand use were measured during normal feeding in a semi‐free‐ranging population of lemurs. Subjects were provisioned at feeding platforms twice daily with fresh fruits, vegetables, and other food items. Sampling was spontaneous and all observations were videotaped. No group‐level bias was found for head‐tilting, but a left hand bias emerged for hand use. A positive relationship was found between direction of head‐tilting preference and direction of hand use preference such that left head‐tilts increased as left hand use increased. Furthermore, left head‐tilts increased as the degree of hand preference lateralization increased. When the hand used to bring food to the mouth just before head‐tilting was examined, there was a strong bias for the left hand to precede left head‐tilts. For right head‐tilts, however, lemurs were equally likely to use either hand before head‐tilting. Overall a strong relationship was found between the left hand and left head‐tilting in black and white ruffed lemurs, suggesting a common link between these behaviors. However, the direction of bias was different from that seen in human and chimpanzee studies. Additional studies on patterns of laterality would be informative for understanding how laterality has changed across the primate order and the adaptive significance of laterality in primates. Am. J. Primatol. 71:1032–1040, 2009. © 2009 Wiley‐Liss, Inc.     

Motivational state and reward content determine choice behavior under risk in mice

Risk is a ubiquitous feature of the environment for most organisms, who must often choose between a small and certain reward and a larger but less certain reward. To study choice behavior under risk in a genetically well characterized species, we trained mice (C57BL/6) on a discrete trial, concurrent-choice task in which they must choose between two levers. Pressing one lever (safe choice) is always followed by a small reward. Pressing the other lever (risky choice) is followed by a larger reward, but only on some of the trials. The overall payoff is the same on both levers. When mice were not food deprived, they were indifferent to risk, choosing both levers with equal probability regardless of the level of risk. In contrast, following food or water deprivation, mice earning 10% sucrose solution were risk-averse, though the addition of alcohol to the sucrose solution dose-dependently reduced risk aversion, even before the mice became intoxicated. Our results falsify the budget rule in optimal foraging theory often used to explain behavior under risk. Instead, they suggest that the overall demand or desired amount for a particular reward determines risk preference. Changes in motivational state or reward identity affect risk preference by changing demand. Any manipulation that increases the demand for a reward also increases risk aversion, by selectively increasing the frequency of safe choices without affecting frequency of risky choices.     

Ecological correlates to social structure in two lemur species in Madagascar

In this study, I tested two hypotheses regarding the relationship of ecological variables (size, density, and distribution of patches) and infant developmental patterns to lemur social structure using two prosimian primates in Ranomafana, Madagascar: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). Three predictions regarding the general effects of patch size and subgroup size on lemur feeding rates were supported: (1) Rufous lemurs used large patches; red-bellied lemurs used smaller patches; (2) larger subgroups of rufous lemurs used larger patches; and (3) rufous lemur feeding rates decreased significantly with increases in subgroup size and patch size, whereas size and patch size had no significant effect on red-bellied lemur feeding rates. However, food item size (fruit) had a more significant effect on rufous and red-bellied lemur feeding rates than either patch size or subgroup size. When similar-sized fruits were compared, rufous lemur feeding rates on small fruit were most affected by patch size, yet feeding rates on medium-sized fruit were most affected by subgroup size. Neither lemur species used patches in consistent ways seasonally. During periods of food abundance, rufous lemurs used many small, common, and clumped patches. In food scarcity periods, they used fewer, larger, rarer, and less clumped patches; groups migrated when food became most scarce. Red-bellied lemurs also used patches in variable ways, but these patterns were not linked with food availability. Finally, infant development patterns differed between lemur species; red-bellied lemur males cared for offspring and infants reached developmental landmarks faster than rufous lemur infants. Therefore, red-bellied lemur group size may be constrained by the need for additional infant care by other group members. In contrast, rufous lemur group size may be constrained by patch availability during the most critical period of food scarcity. © 1996 Wiley-Liss, Inc.     

Repeatability of Male Mate Choice in the Mosquitofish, Gambusia holbrooki

Male mate choice has evolved in many species in which female fecundity increases with body size. In these species, males are thought to have been selected to favour mating with large females over smaller ones, thereby potentially increasing their reproductive success. While male mate choice is known to occur, it is less well studied than female mate choice and little is known about variation in mating preference among individual males. Here, we presented individual male eastern mosquitofish ( Gambusia holbrooki ) with paired females that differed in body size, and we quantified their mate preference on two consecutive days, allowing us to assess repeatability of preferences expressed. When males were allowed to view paired stimulus females, but not to acquire chemical or tactile cues from them, they exhibited a strong preference for large females over smaller ones. However, individual males were not consistent in the strength of their preference and repeatability was not significant. When individual males were allowed to fully interact with pairs of females, the males again exhibited a preference for large females over smaller ones, as revealed by a greater number of attempted copulations with large females than with smaller ones. In the latter social context, individual male preference was significantly repeatable. These results indicate that male eastern mosquitofish from our Florida study population possess, on average, a mating preference for larger females and that this preference is repeatable when males socially interact freely with females. The significant repeatability for mating preference, based on female body size, obtained for male mosquitofish in the current study is consistent with the presence of additive genetic variation for such preferences in our study population and thus with the opportunity for the further evolution of large body size in female mosquitofish through male mate choice.     

Mate preference in female electric fish, Brachyhypopomus pinnicaudatus

Weakly electric fish communicate with brief electrostatic field pulses called electric organ discharges (EODs). EOD waveforms are sexually dimorphic in most genera, a condition thought to result from mate choice acting to shape the electric signal's constituent action potentials. We have no direct behavioural evidence that sexual selection by either mate choice or intrasexual competition is responsible for sex differences in the EOD waveforms of electric fish. We explored sexual selection in electric fish by conducting two-choice unforced preference tests with live, unaltered gymnotiform electric fish,Brachyhypopomus pinnicaudatus , which are sexually dimorphic. In the initial test, gravid females selected males over females only when the males were larger than average. Gravid females in later tests preferred larger males to smaller males in a significant majority of those trials in which they showed a preference. In about one-third of those trials, females spawned with their preferred male, confirming their preference. We concluded that passage through the choice apparatus was related to mate choice. The signals of chosen males had larger EOD amplitudes and longer EOD durations. These findings show that femaleB. pinnicaudatus do have a preference for a certain male phenotype. The system requires additional study to dissociate correlated male phenotypic characters to identify which male traits the female prefers. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Patterns of hand and mouth lateral biases in bamboo leaf shoot feeding and simple food reaching in the gentle lemur (Hapalemur griseus)

Lateralized feeding behaviors of 7 wild-born and 6 captive-born Hapalemur griseus sp. were evaluated in two conditions, simple food reaching and species-typical bamboo foraging. Gentle lemurs were found to have the strongest lateral hand preference in simple food reaching of any prosimian species yet studied. However in this small sample, population-level lateralization was not found: 5 preferred the right hand and 8 the left. The movement pattern used by hapalemurs when feeding on bamboo leaf shoots was categorized into four components: PULL IN, COUNTERFORCE, TURN, and FEED IN. Lateral hand bias was scored for all four components and lateral mouth preference was scored for the two components that involved the mouth (COUNTERFORCE and FEED IN). Strong positive correlations were found between hand preference in the most lateralized components of shoot eating (TURN and FEED IN) and simple food reaching. This suggests that the gentle lemurs' species-typical bamboo feeding behavior may contribute to the exceptionally strong hand preference for simple food reaching seen in this species. There were negative correlations between the component measure of shoot feeding that required strength (COUNTERFORCE) and the components that required manipulation (TURN and FEED IN). Within the COUNTERFORCE and FEED IN components, mouth preference and hand preference were positively associated in a manner that suggested one side of the mouth was preferred for removing the shoot and the other side for mastication. Asymmetrical dental wear may provide a means of dating behavioral lateralization in ancestral species. © 1993 Wiley-Liss, Inc.     

Effects of number of alternatives on choice in humans

The present study examined human choice between a task including a single alternative (i.e. a single-alternative task), and a task including multiple alternatives (i.e. a multi-alternative task). The subjects were divided into three groups and were exposed to three conditions. The multi-alternative task included two alternatives in two groups and included three alternatives in one group. An alternative in the single-alternative task was identical to one in the multi-alternative task. Amount of reinforcement for alternatives specific to the multi-alternative tasks was manipulated under three conditions in each group. When the amount of reinforcement was equal to or larger than that in the alternative common to both tasks, the subjects preferred the multi-alternative task over the single-alternative task. When amount of reinforcement was smaller, there was no difference in preference between the multi-alternative and the single-alternative tasks. In addition, the degree of preference for the multi-alternative task depended on the number of alternatives that produced larger reinforcers.     

Preference for structured environment in zebrafish (Danio rerio) and checker barbs (Puntius oligolepis)

Information about the welfare and husbandry of pet and laboratory fish is scarce although millions of fish are sold in pet shops and used in laboratory research every year. Inadequate housing conditions can cause behavioural problems also in fish since they are complex animals with sophisticated behaviour. In this study, we investigated the influence of environmental complexity on compartment preference and behaviour in zebrafish (Danio rerio) and checker barbs (Puntius oligolepis). For the preference test, large aquaria were divided by two semi-transparent walls of Plexiglas into an empty compartment, a structured compartment enriched with plants and clay pots, and a smaller compartment in-between, where food was provided. For observation, the empty and structured compartments were divided into six zones of similar size by defining three vertical layers and two horizontal areas (back vs. front area). Seven groups of six to nine zebrafish and seven groups of seven or eight checker barbs were observed on four days each (within a time period of ten days) to assess compartment use and activity, and to assess behavioural diversity and use of zones within compartments. Both zebrafish and checker barbs showed a significant preference for the structured compartment. Nevertheless, in neither species did behavioural diversity differ between the empty and structured compartment. Zebrafish used all zones in both compartments to the same extent. Checker barbs, however, used the structured compartment more evenly than the empty compartment, where they mainly used the lower and middle zones. These results suggest that zebrafish and checker barbs have a preference for complex environments. Furthermore, they indicate that the behavioural and ecological needs of fish may vary depending on species, and recommendations for husbandry should be specified at species level.     

Honeybee navigation: linear perception of short distances travelled

Recent evidence indicates that honeybees measure distance flown to a food source by integrating, over time, the apparent visual motion of the environment that they experience en route to the goal. Is the bee's perception of distance travelled a linear function of distance, or is it some other function? This question was investigated by training bees to fly into a tunnel and receive a food reward. The walls and floor of the tunnel were lined with a random texture, and the reward was placed at one of two fixed distances, “near” or “far”, from the tunnel entrance. The feeder containing the reward was placed in a box which could be accessed through one of two openings, one on the left side of the box, and the other on the right. When the box was at the “near” position, the reward could only be accessed through the left-hand opening; when the box was at the “far” position, the reward could only be accessed through the right-hand opening. When the trained bees were tested individually in an identical, fresh tunnel with the reward removed from the box, they showed a strong preference for the left-hand opening when tested at the “near” distance, and for the right-hand opening when tested at the “far” distance. At intermediate positions, the bees' preference for the two openings varies linearly with distance. These findings suggest that the honeybee's perception of distance travelled is linear, at least over the distances and range of image motions experienced in our experiments. The implications for navigation and for the encoding of distance information in the dance are discussed.     

The effect of claw size and wave rate on female choice in a fiddler crab

How do females select a mate when they have mating preferences for multiple male traits? In experimental studies, female fiddler crabs (Uca mjoebergi) show a strong preference for males with larger claws and higher wave rates. In the field, there is no correlation between male claw size and observed wave rate. Here we document natural mating behaviour and show that females approach males who wave at a higher rate than nearby competitors. On average, an approached male had a significantly larger claw than his two nearest neighbours but did not differ in size from his two closest waving competitors. In general, smaller males were less likely to wave at approaching females. Females therefore approached mates based directly on wave rate but, because smaller males were less likely to wave, this indirectly resulted in female choice for larger than average males. Our study raises two issues. First, how do we relate the field results to previous experimental studies showing a female preference for larger claws? Second, in U. mjoebergi, males defend smaller neighbours against intruders. Our study suggests that one benefit of such defence coalitions is to decrease the number of immediate competitors present during female mate choice by retaining smaller neighbours.     

Manual lateralization in early primates: a comparison of two mouse lemur species

In humans, 90% of the population is right handed. Although population hand preference has been found in some primate species, the evolution of manual lateralization in primates is not yet clear. To gain insight into manual lateralization of ancestral primates, we studied hand usage in unspecialized quadrupedal, nocturnal lemurs, using a large sample size. We compared two closely related mouse lemur species to explore the variation of hand preference within the same genus. We tested 44 gray mouse lemurs and 19 Goodman's mouse lemurs in a forced food grasping task. The tests were videotaped. Measures of hand preference (i.e. the hand that is spontaneously chosen for a specific task) and successful hand usage (i.e. the hand that is successful in completing a specific task) were taken to explore manual lateralization. Both species showed manual lateralization at an individual, but not at a population level. Goodman's mouse lemurs showed stronger individual hand preferences than gray mouse lemurs. This suggests that strength in hand preference is variable within the same genus. No sex and age effects were found. The hand preference of offspring was negatively correlated to that of their mothers, but not correlated to that of their fathers. Thus, no clear genetic effect can be derived from these results. In the Goodman's mouse lemurs, hand preference increased with increasing task experience. However, successful hand usage was not affected by task experience, suggesting that successful hand usage is a more stable measurement for manual lateralization than hand preference.     

Patterns of female choice in mottled sculpins (Cottidae,teleostei)

large male sculpins (Cottus bairdi) breed earlier in the spawning season and mate with more females than do smaller males. These patterns are attributable to female preference for large mates, and reflect the fact that larger males make better egg guardians. Results of a computer simulation of female choice in which females mated with a male who was larger than or equal to the last male encountered are consistent with many of the observed patterns of male courtship success.     

The effect of sex and shoal size on shoaling behaviour in Danio rerio

Male and female zebra fish Danio rerio were given choices of shoals that differed in sex and size. Male zebra fish preferred to associate with female shoals over male shoals, but had no preference when given a choice between a mixed‐sex shoal and either a male or female shoal. Female zebra fish showed no significant preference when given a choice between male and females shoals, nor between mixed‐sex shoals and either male or female shoals. When given choices between shoals of differing size, females preferred to associate with the larger shoal, whether or not they were composed of males or females. Males, however, had no preference for larger shoals over smaller shoals, whether or not they were composed of males or females. These results showed that male zebra fish were capable of distinguishing between males and females solely on the basis of visual cues. Furthermore, these results demonstrated a significant difference between the shoaling choices of male and female zebra fish, which may indicate a difference in the function of shoaling for the two sexes.     

Parameters of rewards on choice behavior in Siamese fighting fish (Betta splendens)

Five experiments were conducted with Siamese fighting fish (Betta splendens) to investigate how choices in a T-maze were affected by parameters of a social reward (aggression display to another male): presence or absence, amount, delay and distance traveled. Bettas showed a preference for the side associated with the presence of another male rather than the side associated with nothing (Exp 1), a greater length of time of the reward (Exp 2) and shorter delay (Exp 3). The animals were indifferent when one side offered a longer delay to a longer reward time compared with a shorter delay to a shorter reward time (Exp 4). What was most surprising, however, was that fish preferred to choose the side that was associated with swimming a greater distance to reach an opponent male (Exp 5). These experiments demonstrate that, while some parameters of a visual reward affect behavior in predicable ways (greater amount, shorter delay), the complex motivations underlying inter-male aggression can produce what appear to be paradoxical results.