Effects of puzzle feeders on pathological behavior in individually housed rhesus monkeys

Self-injurious behavior (SIB) occurs in about 10% of individually housed monkeys. Monkeys with SIB bite their own bodies frequently, occasionally inflicting wounds as a result. At present, there is no standard treatment for this phenomenon. We examined the effectiveness of puzzle feeders in alleviating SIB in monkeys with a veterinary record of self-inflicted wounding. Two groups of monkeys (SIB and controls) were exposed to puzzle feeders for a 6 week period. Three levels of maze difficulty were examined. All monkeys used the feeders, but manipulation was confined to a brief period immediately after the feeders were loaded each day (1000 h) and was infrequent during the later sampling periods (1100 and 1400 h). The most difficult maze yielded a slight increase in usage at 1100 h. During the puzzle feeder phase, whole body stereotypies, including pacing and rocking, were reduced substantially in all monkeys at 1000 h when feeder manipulation was at its highest. However, self-biting in the SIB group was unchanged. Some monkeys actually bit themselves while manipulating the feeder. Long-term effects on abnormal behavior were assessed by comparing behavior during the feeder phase to baseline periods and to a phase in which the monkeys were provisioned with treats placed directly into their food box. Whole body stereotypies, including pacing, were reduced during both treatment phases; however, the reduction was associated only with the 1000 h observation. Puzzle feeders were more effective than treats alone in alleviating whole body stereotypies. Self-biting was unchanged through all phases. Puzzle feeders are beneficial from the perspective of eliciting manipulation. They also yield transient reductions in whole body stereotypy, an effect that does not extend beyond the direct manipulation of the feeder. Puzzle feeders are ineffective in alleviating self-injurious behavior. Am. J. Primatol. 46:213–227, 1998. © 1998 Wiley-Liss, Inc.     

Can puzzle feeders be used as cognitive screening instruments? Differential performance of young and aged female monkeys on a puzzle feeder task

Conventional cognitive testing of monkeys is time‐consuming and involves single‐caging and food or water deprivation. Here we report a novel test of global cognitive performance that can be completed in a short time period without food/water or social restrictions. Nine mazes of increasing difficulty were developed using a standard puzzle feeder, and the maze‐solving performance of ten young and five aged female cynomolgus monkeys (Macaca fascicularis) was tested. The young monkeys solved maze configurations at higher levels of difficulty and solved the first level of difficulty more quickly than aged monkeys. This task discriminated performance by age in nonhuman primates as do more conventional forms of cognitive testing and indicates that this task may be a quick and easy assessment of global cognitive function. Am. J. Primatol. 49:195–202, 1999. © 1999 Wiley‐Liss, Inc.     

Owl Monkeys (Aotus nigriceps and A. infulatus) Follow Routes Instead of Food-Related Cues during Foraging in Captivity

Foraging at night imposes different challenges from those faced during daylight, including the reliability of sensory cues. Owl monkeys (Aotus spp.) are ideal models among anthropoids to study the information used during foraging at low light levels because they are unique by having a nocturnal lifestyle. Six Aotus nigriceps and four A. infulatus individuals distributed into five enclosures were studied for testing their ability to rely on olfactory, visual, auditory, or spatial and quantitative information for locating food rewards and for evaluating the use of routes to navigate among five visually similar artificial feeding boxes mounted in each enclosure. During most experiments only a single box was baited with a food reward in each session. The baited box changed randomly throughout the experiment. In the spatial and quantitative information experiment there were two baited boxes varying in the amount of food provided. These baited boxes remained the same throughout the experiment. A total of 45 sessions (three sessions per night during 15 consecutive nights) per enclosure was conducted in each experiment. Only one female showed a performance suggestive of learning of the usefulness of sight to locate the food reward in the visual information experiment. Subjects showed a chance performance in the remaining experiments. All owl monkeys showed a preference for one box or a subset of boxes to inspect upon the beginning of each experimental session and consistently followed individual routes among feeding boxes.     

Caged rhesus macaques voluntarily work for ordinary food

Eight single-caged adult rhesus macaques were given the choice of freely collecting their standard food ration, i.e. 33 biscuits, from an ordinary food box or working for its retrieval from a custom-made food puzzle. During a one-hour observation session following the simultaneous distribution of biscuits in both feeders, individuals spent on average a total of 32 sec retrieving 29.0 biscuits from the food box, and 673 sec retrieving 11.3 biscuits from the food puzzle. It was inferred that the animals voluntarily worked for ordinary food, with the expression of foraging activities serving as its own reward.     

Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing Aotus, Callicebus, and Saguinus

Early in their evolution, the ancestors of anthropoid primates radiated from a nocturnal to a diurnal niche. Foraging during the night differs from foraging during the day in terms of the availability of light and color cues, and in the movement of odor molecules through the canopy. In this study, we compared the ability of nocturnal and diurnal New World monkeys to use perceptual cues (i.e., the sight or smell of food) and spatial information (place predictability) in within-patch foraging decisions. An experimental field study was conducted on wild groups of night monkeys (Aotus nigriceps), tamarins (Saguinus imperator imperator and S. fuscicollis weddelli), and titi monkeys (Callicebus cupreus) at the Zoobotanical Park/UFAC, Rio Branco, Brazil. Our research design included the construction of feeding stations located in the home range of the study groups. Each feeding station consisted of eight visually identical feeding platforms located in a circular arrangement. In all test settings, two platforms at each feeding station contained a food reward (banana), and the remaining six platforms contained a sham reward (yellow plastic or inaccessible banana). In the night-monkey experiments, each feeding platform was illuminated by a 40-W red bulb to aid the researcher in observing their behavior. When the location of reward sites was predictable over time, individuals in all four species successfully relocated food rewards based solely on spatial information. Each species was also successful in using visual information to distinguish real from sham food rewards. However, only night monkeys and one group of emperor tamarins used olfactory information alone to locate food rewards. Overall, the species' performances did not clearly differentiate Aotus from diurnal New World primates in these experiments.     

Behavioral Analysis of Social Effects on the Problem-Solving Ability in the House Mouse

The effects of the social context on the problem‐solving ability in the house mouse was evaluated by means of a puzzle box containing food, which could be opened by rotating a revolving door. The aim of the study was to clarify which mechanisms of social learning promote the acquisition of this complex motor skill. Young mice were exposed to the puzzle box in the presence of (i) demonstrators opening of the puzzle box; (ii) adults unable to open the puzzle box; and (iii) adults confined in one part of the cage and not manipulating the puzzle box. Results of the detailed analysis of the sequence of behaviors showed that (i) young mice successful in opening the puzzle box did not copy the sequence of actions performed by demonstrators; and (ii) the presence of adult conspecifics in proximity of the problem apparatus increased the rate of success of young mice. Results suggest that trial‐and‐error learning, social exposure and stimulus enhancement all play a role in the acquisition of the opening ability.     

Capuchin monkeys (Cebus nigritus) use spatial and visual information during within-patch foraging

Foraging in large-scale (navigation between patches), small-scale (choice of within-patch feeding sites), and micro-scale (close inspection of food items) space presents variable cognitive challenges. The reliability and usefulness of spatial memory and perceptual cues during food search in a forest environment vary among these spatial scales. This research applied an experimental field design to test the ability of a free-ranging group composed of eight black-horned capuchin monkeys, Cebus nigritus, inhabiting a forest fragment in Porto Alegre, State of Rio Grande do Sul, Brazil, to use food-associated spatial, visual, olfactory, and quantitative (amount of food) cues during small-scale foraging decisions. The experimental design involved the establishment of a feeding station composed of eight feeding platforms distributed in a circular arrangement. A series of six experiments, each lasting 20 days, was conducted from March to August 2005. Two feeding platforms in each experimental session contained a food reward (real banana), whereas the remaining six platforms contained either a sham banana or an inaccessible real banana. Data on capuchin monkey foraging behavior at the feeding stations were collected by the "all occurrences" sampling method. The performance of the capuchins in the experiments was analyzed based on the first two platforms inspected in each session. The study group inspected feeding platforms in 571 occasions during 113 sessions. Capuchins used visual cues and spatial information (and adopted a win-return strategy) for finding the platforms baited with real bananas and showed weak evidence of the integration of spatial and quantitative cues, but failed to show evidence of using olfactory cues. In addition, individual differences in social rank and foraging behavior affected opportunities for learning and the performance in the cognitive tasks.     

Determinants of problem-solving success inSaimiri andCallicebus

The problem-solving behavior of titis and squirrel monkeys was compared on four tasks. Each task was presented at three levels of complexity, based on the number of responses required to obtain a food reward. At all levels, however, food could be obtained by performing a few relatively simple and generalized responses, such as grasping, lifting, or pulling, that were within the repertoire of each species. The principal measures of problem-solving efficiency were the number of trials on which the reward was obtained, and the time required to achieve it. On both measures squirrel monkeys were superior to titis. These differences were not attributable to appetite for food, availability of the requisite instrumental responses, or cognitive ability. The most important factor contributing to the superior achievement of squirrel monkeys was problem-solving “style,” as reflected in latency to approach the problem, tempo of activity, and vigor and variety of responses emitted. On problems where the relevance of these traits was minimal, the level of successful performance was similar in the two species. The importance of taking style into account in comparative assessments of primate problem-solving ability is emphasized by these results.     

Helping behaviour and regard for others in capuchin monkeys (Cebus apella)

Altruism is an evolutionary puzzle. To date, much debate has focused on whether helping others without regard to oneself is a uniquely human behaviour, with a variety of empirical studies demonstrating a lack of altruistic behaviour in chimpanzees even when the demands of behaving altruistically seem minimal. By contrast, a recent experiment has demonstrated that chimpanzees will help a human experimenter to obtain an out-of-reach object, irrespective of whether or not they are offered a reward for doing so, suggesting that the cognitions underlying altruistic behaviour may be highly sensitive to situational demands. Here, we examine the cognitive demands of other-regarding behaviour by testing the conditions under which primates more distantly related to humans--capuchin monkeys--help an experimenter to obtain an out-of-reach object. Like chimpanzees, capuchin monkeys helped human experimenters even in the absence of a reward, but capuchins systematically failed to take into account the perspective of others when they stood to obtain food for themselves. These results suggest an important role for perspective taking and inhibition in altruistic behaviour and seem to reflect a significant evolutionary development in the roots of altruism, and specifically in other-regarding behaviour, between the divergence of New World monkeys and apes.     

A stingless bee (Melipona seminigra) uses optic flow to estimate flight distances

Foragers of a stingless bee, Melipona seminigra, are able to use the optic flow experienced en route to estimate flight distance. After training the bees to collect food inside a flight tunnel with black-and-white stripes covering the side walls and the floor, their search behavior was observed in tunnels lacking a reward. Like honeybees, the bees accurately estimated the distance to the previously offered food source as seen from the sections of the tunnel where they turned around in search of the food. Changing the visual flow by decreasing the width of the flight tunnel resulted in the underestimation of the distance flown. The removal of image motion cues either in the ventral or lateral field of view reduced the bees' ability to gauge distances. When the feeder inside the tunnel was displaced together with the bees feeding on it while preventing the bee from seeing any image motion during the displacement the bees experienced different distances on their way to the food source and during their return to the nest. In the subsequent test the bees searched for the food predominantly at the distance associated with their return flight.     

Effect of restricted feeding schedule on seasonal shifting of daily demand-feeding pattern and food anticipatory activity in European sea bass (Dicentrarchus labrax L.)

The effect of restricted feeding schedule was investigated on the seasonal shifting of daily demand-feeding pattern and food anticipatory activity in European sea bass (Dicentrarchus labrax) held under natural environmental conditions in an outdoor laboratory. To that end, demand-feeding behavior was continuously monitored for approximately one year in four groups of 15 fish each exposed to natural fluctuations of water temperature (from 13.2 degrees C to 27.4 degrees C) and photophase (from 9.5 h to 14.5 h of light). When the animals were subjected to a time-restricted feeding schedule, the demand-feeding rhythm rapidly synchronized to the three periods of food availability: the first meal (FM) from 08:00 to 09:00 h, the second meal (SM) from 16:00 to 17:00 h, and the third meal (TM) from 00:00 to 01:00 h. The occurrence of demand-feeding activity into the three periods of food availability displayed a double seasonal shift: fish that self-fed mostly during the daytime periods of feeding availability (FM and SM) in summer and autumn changed to nocturnal feeding (TM) from December to April, returning to diurnal preferences in April. Food-demands appeared to be predominantly associated with feed availability, reaching its maximum levels during the hours of reward. In addition, feeding anticipatory activity (FAA) was observed. A relationship was detected between the duration of FAA and feeding-time, with shortest FAA (30-60 min) when mealtime occurred just after sunrise (FM) or sunset (TM). These findings demonstrate the ability of sea bass to self-feed under time-restricted schedules, and show a seasonal-phase inversion in demand-feeding activity in spite of the restrictions in their feeding availability. Sea bass can use external signals as reference to anticipate the time of feed availability. This information may be useful for designing new feeding strategies for European sea bass fish farming.     

Experimental assessment of problem solving by <Emphasis Type="Italic">Milvago chimango </Emphasis>(Aves: Falconiformes)

We report a preliminary assessment of problem solving as an estimate of behavioural innovation and learning ability of a generalist and abundant raptor, Milvago chimango, under controlled conditions in aviaries. Experimental tests consisted in presentation of a Plexiglas box with four lids leading to isolated pieces of meat. We recorded time to first contact with the box and time from this first contact to gaining access to the pieces of meat. We recorded the number of attempts to open the box and reach the first portion of meat, and the total number of lids opened by each individual during five successive daily sessions. We found that individuals of M. chimango quickly approached and made contact with the Plexiglas box, and responded successfully to the novel feeding problem of reaching the food inside. In our study, performance of individuals was enhanced after solution of the novel task for the first time, as indicated by the progressively reduced time taken to access the food. Further, some individuals gained access to an increasing number of sections of the Plexiglas box during subsequent sessions, suggesting significant learning ability. Our results indicated M. chimango has a remarkable ability to obtain food in a novel situation, an observation that agrees with anecdotal reports of opening of receptacles to obtain food in urban environments. The results support the idea of behavioural plasticity in this species.     

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.     

Descriptive study of antennation during trophallactic unloading contacts in honeybees <Emphasis Type="Italic">Apis mellifera carnica</Emphasis>

Summary  Trophallaxis, the mouth-to-mouth transfer of food, is a widespread behavior occurring between individuals of eusocial insect societies. Antennal movements during food transfer are, in honeybees, too rapid to be characterized using standard video recordings. Using a high-speed camera (200 frames/s), we recorded nectar unloading performed by forager honeybees (Apis mellifera carnica Spinola) within the hive once they returned from collecting sugar solution at a feeder that delivered nectar at a variable rate. Frequency patterns attained a mean value of 13 Hz. Antennation intensity showed a tendency to increase with the reward rate recently exploited by the food donor. This raises the question whether or not antennation intensity is a reliable parameter providing modulatory information related to food-source profitability.Received 12 September 2002; revised 21 March 2002; accepted 24 April 2003.     

Assessment of individual differences in the preferred proximity to a human feeder by partitioned raisin test, with two species of macaque monkeys

All animals must acquire food and mates by approaching them despite possibilities of accompanying risks and thus are frequently encountered with approach-avoidance conflicts in daily lives. Behavioral individual differences in such situations may be considered as one of the most biologically fundamental personality trains. “Partitioned raisin test” was devised to assess this trait with macaque monkeys. It involved throwing raisins into groups of monkeys and observing the preferred distance of each from the human feeder, a source of possible harm. The test was administered to 4 groups of Japanese monkeys (30 total) and 3 groups of rhesus monkeys (19 total), all l-yr-old and matched in history. Individual differences in the preferred proximity to the feeder, as expressed by the Proximity Index (PI), were found in both species.PI was not correlated with a measure of dominance over the raisins. Individual differences inPI were also not due to territorial effects unrelated to the location of the feeder.PI was stable in five of the six monkeys re-tested after one year of interval in a newly organized group, where there supposedly had been a change in their social structure. Partitioned raisin test was shown to be capable of depicting individual differences related to differential approach bias in an approach-avoidance conflict situation. Although possible confounding effects by social factors need to be delineated in the following studies, the method may provide a handy and widely applicable way for the assessment of this trait with monkeys.     

Utilization of fruiting trees by monkeys as analyzed from feeding traces under fruiting trees in the tropical rain forest of Cameroon

Individual trees of the food species of monkeys were identified by placing plastic tapes with an identification number on them in the tropical rain forest of Cameroon, West Africa. In order to determine the use of the feeding trees by monkeys, the ground under each of the trees was checked at least once a week to see if there were any fallen fruits or traces of feeding on fruits. Some fruit species were not fed on by either monkeys or large arboreal squirrels. Among the food species common to both the monkeys and large squirrels, a larger proportion in terms of quantity in each species was mainly eaten by the monkeys except in the case of super-abundantly fruit producing species. The monkeys and large arboreal squirrels were well segregated in their diets. Larger proportions (more than 85% for most of the monkeys' major foods) of fruits of larger sizes were made to fall on the ground by the monkeys and squirrels. The monkeys displayed a tendency to visit fruiting trees rather evenly (even rate of visit = even frequency of visit/duration of fruiting) not ignoring any area of the home range, although a small difference in this tendency was observed between the two study periods, one an abundant season and the other a poor fruiting season. On average, one associated polyspecific group of monkeys encountered only 14 fruiting trees per day. On the other hand, fruits were available all around the year, as the fruiting periods of different tree species were widely distributed around the year, or the fruiting periods of some species were very long. Although the monkeys are able to depend heavily on fruits, the quantity of fruits is not so great. The population size of monkeys is well balanced with the available food supply in the tropical rain forest of West Africa.     

Is Working More Costly than Waiting in Monkeys?

We studied how value for instrumental action is discounted by predicted effort and delay. The monkeys were trained to perform instrumental trials that required a bar release when a visual target changed from red-to-green. There were two trial conditions. In delay trials, after the monkeys performed one instrumental trial correctly a reward was delivered 0–7 seconds later. In work trials, the monkeys had to perform 0, 1, or 2 additional instrumental trials to obtain a reward. The lengths of trials in delay matched the time it took to complete work trials. The length of delay or number of trials was indicated by a visual cue presented throughout the trial. Our hypothesis was that the monkeys would all show temporal discounting of reward in the delay trials, and that in the work trials the monkeys’ performance might reflect an additional cost due to working. The error rate increased linearly as remaining cost increased for all 8 monkeys. For 4 monkeys the error rate was significantly larger in work trials than in delay trials (effort sensitive monkeys). For the other 4 monkeys there was no significant difference in error rate (effort insensitive monkeys). Since the error rate has an inverse relation with value for action, these results suggest that value is discounted hyperbolically by effort as well as by delay. Error rates generally increased as the testing sessions progressed and the total reward accumulated (i.e., effect of reward devaluation). The relative impact of delay and effort on error rates was reasonably stable within subjects. Thus, within the monkey population there seems to be a significant dichotomy in the sensitivity governing whether working is more costly than waiting, possibly arising from a constitutional or genetic trait.     

Changes in food source profitability affect Nasonov gland exposure in honeybee foragers Apis mellifera L.

Summary. When arriving at a known artificial food source, foraging honeybees usually perform circular flights around the feeding place prior to landing. During these flights bees expose their Nasonov gland, an exocrine gland located at the base of the 7^th tergum, that releases a complex blend of volatiles. This behavior may continue even after the bee starts food ingestion. The proportion of bees exposing the Nasonov gland and the duration of its exposure before and during feeding for individual bees were quantified. Trained bees collected sugar solution during 12 visits from a feeder located at 160 m from the hive. Five different reward programs were presented: three constant and two variable. The constant programs offered 0.6, 1.2 or 2.4 M sugar for all 12 visits, while the variable programs delivered either 0.6, 1.2, 0.6 M or 0.6, 2.4, 0.6 M, four visits for each molarity. Results showed that sugar concentration changed the thresholds and durations of Nasonov gland exposure. However, this relationship was found only for Nasonov exposure before bees began to feed. During feeding, a protruded Nasonov gland was only observed for bees that had exposed it prior to feeding; suggesting that Nasonov gland exposure before feeding is a releaser of the during-feeding exposure. In variable reward programs, changes in sugar concentration were followed by changes in both thresholds and durations of exposure. However, Nasonov gland exposure during feeding did not appear to decrease based on measurements of the low profitability during the current foraging visit. These results suggest that Nasonov gland exposure is programmed on the basis of reward expectations, with the bees having acquired this information in the previous foraging visits to the food source.     

Foraging,Food Choice,and Food Processing by Sympatric Ripe-Fruit Specialists: <Emphasis Type="Italic">Lagothrix lagotricha poeppigii</Emphasis> and <Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis>

Studies of interspecific competition and niche separation have formed some of the seminal works of ecology. I conducted an 18-mo study comparing the feeding ecologies of 2 sympatric, closely-related ripe-fruit specialists, Humboldt's woolly monkeys (Lagothrix lagotricha poeppigii), and the white-bellied spider monkeys (Ateles belzebuth belzebuth) in Amazonian Ecuador. Woolly monkeys in the terra firme forest live at roughly triple the density of spider monkeys (31 versus 11.5 animals/km²). Woolly monkeys spend 17% of their time foraging, while spider monkeys spend only 1% of their time foraging. Spider monkeys alone fed on soil and termitaria, which are rich in phosphorus. Woolly monkeys are not hard-fruit specialists. Their fruit diet is significantly more diverse than that of spider monkeys. Dietary overlap between the 2 species is high, yet each specializes to some degree on a different set of fruit resources. Woolly monkeys visit more food sources per unit of time, feed lower in the canopy, visit more small food patches, and prey on more seeds. Spider monkeys feed on fewer, richer food sources and are more than twice as likely to return to a particular fruit source than woolly monkeys are. Spider monkeys maximize fruit pulp intake, carrying more intact seeds in their guts, while woolly monkeys minimize seed bulk swallowed through more careful food processing. Surprisingly, several preferred spider monkey foods with high fat content and large seeds are avoided by woolly monkeys. I outline the different ecological dimensions involved in niche separation between the 2 species and discuss the possible impetus for their evolutionary divergence.     

Activity budget and diet of patas monkeys in Kala Maloue National Park,Cameroon: A preliminary report

A preliminary study was carried out on the feeding ecology of patas monkeys in the rainy season in Cameroon. Their daily activity rhythm revealed two active peaks. The proportion of time spent on feeding with respect to waking time was 30%. Patas monkeys largely depended on the flowers and buds of herbaceous plants and the larvae of insects for their diet as they ranged widely. Patas monkeys spent more time in feeding and travelled for a longer distance per day than the sympatric primate species, the tantalus monkey. It is considered that these findings reflected the large amount of food requirement due to the large body size, as well as the low density and high degree of dispersal of their food.