Limited spread of innovation in a wild parrot, the kea (Nestor notabilis)

In the local population of kea in Mount Cook Village, New Zealand, some keas open the lids of rubbish bins with their bill to obtain food scraps within. We investigated the extent to which this innovation has spread in the local population, and what factors limit the acquisition of bin opening. Only five males of 36 individually recognised birds were observed to have performed successful bin opening. With one exception there were always other keas present, watching successful bin opening. Seventeen additional individuals were seen to have benefitted from lid opening. Their foraging success was less than that of the bin openers. Social status of bin openers did not differ from scrounging males. Among the individuals that were regularly seen at the site of the bins but were not successful in bin opening, social status and the ratio of feeding directly from open bins correlated with the amount of opening attempts. We conclude that scrounging facilitated certain behavioural aspects of bin opening rather than inhibiting them. The fact that only 9% of opening attempts were successful, and the long period of time required to increase efficiency in lid opening shows that mainly individual experience, and to a lesser extent insight and social learning, play key roles in acquisition of the opening technique. The results indicate that the spread of innovative solutions of challenging mechanical problems in animals may be restricted to only a few individuals.     

The effect of social learning on avoidance of aposematic prey in juvenile great tits (<Emphasis Type="Italic">Parus major</Emphasis>)

Social learning plays an important role in acquiring new foraging skills and food preferences in many bird species but its potential role in learning to avoid aposematic prey has never been studied. We tested the effect of social learning on the acquisition of avoidance of aposematic insect prey (firebug Pyrrhocoris apterus; Heteroptera) in juvenile, hand-reared great tits (Parus major). Behaviour towards aposematic prey was compared between two groups of birds: (1) the observers that were, prior to encounter with firebugs, allowed to watch the experienced conspecific demonstrator repeatedly refuse to attack the prey, and (2) the control birds that lacked this opportunity. Observing an experienced demonstrator was not sufficient for learning complete avoidance, because birds from both groups attacked at least the first firebug they had encountered in avoidance training. However, the opportunity to observe the avoidance behaviour of another bird significantly increased the rate of subsequent individual learning of observers in comparison with control birds. Social learning also decreased mortality of firebugs killed by the birds during the avoidance learning. Socially enhanced learning to avoid aposematic prey might be a mechanism important especially for naive juvenile birds learning from their parents, but it could also enhance learning in adults from their more experienced flock mates. Because social learning of avoidance may also lead to decreased mortality of aposematic prey, its effect should be taken into account in scenarios considering evolution and maintenance of prey warning signals.     

Big brains are not enough: performance of three parrot species in the trap-tube paradigm

The trap-tube task has become a benchmark test for investigating physical causality in vertebrates. In this task, subjects have to retrieve food out of a horizontal tube using a tool and avoiding a trap hole in the tube. Great apes and corvids succeeded in this task. Parrots with relative brain volumes comparable to those of corvids and primates also demonstrate high cognitive abilities. We therefore tested macaws, a cockatoo, and keas on the trap-tube paradigm. All nine parrots failed to solve the task. In a simplified task, trap tubes with a slot inserted along the top were offered. The slot allowed the birds to move the reward directly with their bills. All but one individual solved this task by lifting the food over the trap. However, the parrots failed again when they were prevented from lifting the reward, although they anticipated that food will be lost when moved into the trap. We do not think that the demanding use of an external object is the main reason for the parrots’ failure. Moreover, we suppose these parrots fail to consider the trap’s position in the beginning of a trial and were not able to stop their behaviour and move the reward in the trap’s opposite direction.     

Performance on the Hamilton search task,and the influence of lateralization,in captive orange-winged Amazon parrots (Amazona amazonica)

Psittacines are generally considered to possess cognitive abilities comparable to those of primates. Most psittacine research has evaluated performance on standardized complex cognition tasks, but studies of basic cognitive processes are limited. We tested orange-winged Amazon parrots (Amazona amazonica) on a spatial foraging assessment, the Hamilton search task. This task is a standardized test used in human and non-human primate studies. It has multiple phases, which require trial and error learning, learning set breaking, and spatial memory. We investigated search strategies used to complete the task, cognitive flexibility, and long-term memory for the task. We also assessed the effects of individual strength of motor lateralization (foot preference) and sex on task performance. Almost all (92 %) of the parrots acquired the task. All had significant foot preferences, with 69 % preferring their left foot, and showed side preferences contralateral to their preferred limb during location selection. The parrots were able to alter their search strategies when reward contingencies changed, demonstrating cognitive flexibility. They were also able to remember the task over a 6-month period. Lateralization had a significant influence on learning set acquisition but no effect on cognitive flexibility. There were no sex differences. To our knowledge, this is the first cognitive study using this particular species and one of the few studies of cognitive abilities in any Neotropical parrot species.     

Transfer of physical understanding in a non-tool-using parrot

Physical cognition has generally been assessed in tool-using species that possess a relatively large brain size, such as corvids and apes. Parrots, like corvids and apes, also have large relative brain sizes, yet although parrots rarely use tools in the wild, growing evidence suggests comparable performances on physical cognition tasks. It is, however, unclear whether success on such tasks is facilitated by previous experience and training procedures. We therefore investigated physical comprehension of object relationships in two non-tool-using species of captive neotropical parrots on a new means-end paradigm, the Trap-Gaps task, using unfamiliar materials and modified training procedures that precluded procedural cues. Red-shouldered macaws (Diopsittaca nobilis) and black-headed caiques (Pionites melanocephala) were presented with an initial task that required them to discriminate between pulling food trays through gaps while attending to the respective width of the gaps and size of the trays. Subjects were then presented with a novel, but functionally equivalent, transfer task. Six of eight birds solved the initial task through trial-and-error learning. Four of these six birds solved the transfer task, with one caique demonstrating spontaneous comprehension. These findings suggest that non-tool-using parrots may possess capacities for sophisticated physical cognition by generalising previously learned rules across novel problems.     

Short-term observational spatial memory in Jackdaws (<Emphasis Type="Italic">Corvus monedula</Emphasis>) and Ravens (<Emphasis Type="Italic">Corvus corax</Emphasis>)

Observational spatial memory (OSM) refers to the ability of remembering food caches made by other individuals, enabling observers to find and pilfer the others' caches. Within birds, OSM has only been demonstrated in corvids, with more social species such as Mexican jays (Aphelocoma ultramarine) showing a higher accuracy of finding conspecific' caches than less social species such as Clark's nutcrackers (Nucifraga columbiana). However, socially dynamic corvids such as ravens (Corvus corax) are capable of sophisticated pilfering manoeuvres based on OSM. We here compared the performance of ravens and jackdaws (Corvus monedula) in a short-term OSM task. In contrast to ravens, jackdaws are socially cohesive but hardly cache and compete over food caches. Birds had to recover food pieces after watching a human experimenter hiding them in 2, 4 or 6 out of 10 possible locations. Results showed that for tests with two, four and six caches, ravens performed more accurately than expected by chance whereas jackdaws did not. Moreover, ravens made fewer re-visits to already inspected cache sites than jackdaws. These findings suggest that the development of observational spatial memory skills is linked with the species' reliance on food caches rather than with a social life style per se.     

Chimpanzees (Pan troglodytes) and the question of cumulative culture: an experimental approach

There is increasing evidence for cultural variations in behaviour among non-human species, but human societies additionally display elaborate cumulative cultural evolution, with successive generations building on earlier achievements. Evidence for cumulative culture in non-human species remains minimal and controversial. Relevant experiments are also lacking. Here we present a first experiment designed to examine chimpanzees' capacity for cumulative social learning. Eleven young chimpanzees were presented with a foraging device, which afforded both a relatively simple and a more complex tool-use technique for extracting honey. The more complex 'probing' technique incorporated the core actions of the simpler 'dipping' one and was also much more productive. In a baseline, exploration condition only two subjects discovered the dipping technique and a solitary instance of probing occurred. Demonstrations of dipping by a familiar human were followed by acquisition of this technique by the five subjects aged three years or above, whilst younger subjects showed a significant increase only in the elements of the dipping technique. By contrast, subsequent demonstrations of the probing task were not followed by acquisition of this more productive technique. Subjects stuck to their habitual dipping method despite an escalating series of demonstrations eventually exceeding 200. Supplementary tests showed this technique is within the capability of chimpanzees of this age. We therefore tentatively conclude that young chimpanzees exhibit a tendency to become 'stuck' on a technique they initially learn, inhibiting cumulative social learning and possibly constraining the species' capacity for cumulative cultural evolution.     

The Effect of Stress on Spontaneous Nest Leaving Behavior in the Mouse: An Improved Model of Stress-Induced Behavioral Pathology

The present experiments were conducted to develop a more sensitive and reliable model of stress-induced behavioral pathology in the mouse. Male mice were housed singly in nest cages connected to either a circular tunnel, a recreational cage or a large box with food foraging apparatus. Spontaneous nocturnal out of nest activity or food foraging behavior in these environments was continuously monitored for a two week period during which time the effects of stress were examined. It was found that both repeated restraint and aggression stress markedly and persistently reduced out of nest nocturnal activity or food foraging behavior in all 3 environments but did not alter activity in a novel open field or plus maze or food or saccharin intake in the nest cage. In a preliminary experiment the reduction in out of nest activity by stress was attenuated by prior chronic treatment with the antidepressant, desmethylimipramine. Plasma corticosterone was elevated immediately after aggression stress but reduced 5 hr after chronic aggression stress. The reduction in activity did not appear the result of increased anxiety as measured by spontaneous risk assessment behavior in the nest. It is concluded that the decrease in out of nest activity after stress in the present studies models a withdrawn behavioral state and may be due to either or both a decrease in appetitive motivation to leave the nest or an increased aversion to the external environment which does not apparently involve anxiety.     

Pilfering ravens, Corvus corax, adjust their behaviour to social context and identity of competitors

Like other corvids, food-storing ravens protect their caches from being pilfered by conspecifics by means of aggression and by re-caching. In the wild and in captivity, potential pilferers rarely approach caches until the storers have left the cache vicinity. When storers are experimentally prevented from leaving, pilferers first search at places other than the cache sites. These behaviours raise the possibility that ravens are capable of withholding intentions and providing false information to avoid provoking the storers' aggression for cache protection. Alternatively, birds may refrain from pilfering to avoid conflicts with dominants. Here we examined whether ravens adjust their pilfer tactics according to social context and type of competitors. We allowed birds that had witnessed a conspecific making caches to pilfer those caches either in private, together with the storer, or together with a conspecific bystander that had not created the caches (non-storer) but had seen them being made. Compared to in-private trials, ravens delayed approaching the caches only in the presence of storers. Furthermore, they quickly engaged in searching away from the caches when together with dominant storers but directly approached the caches when together with dominant non-storers. These findings demonstrate that ravens selectively alter their pilfer behaviour with those individuals that are likely to defend the caches (storers) and support the interpretation that they are deceptively manipulating the others' behaviour.This contribution is part of the special issue “Animal Logics” (Watanabe and Huber 2006).     

The chimpanzee mind: in search of the evolutionary roots of the human mind

One advantage of living in a social group is the opportunity to use information provided by other individuals. Social information can be based on cues provided by a conspecific or even by a heterospecific individual (e.g., gaze direction, vocalizations, pointing gestures). Although the use of human gaze and gestures has been extensively studied in primates, and is increasingly studied in other mammals, there is no documentation of birds using these cues in a cooperative context. In this study, we tested the ability of three African gray parrots to use different human cues (pointing and/or gazing) in an object-choice task. We found that one subject spontaneously used the most salient pointing gesture (looking and steady pointing with hand at about 20 cm from the baited box). The two others were also able to use this cue after 15 trials. None of the parrots spontaneously used the steady gaze cues (combined head and eye orientation), but one learned to do so effectively after only 15 trials when the distance between the head and the baited box was about 1 m. However, none of the parrots were able to use the momentary pointing nor the distal pointing and gazing cues. These results are discussed in terms of sensitivity to joint attention as a prerequisite to understand pointing gestures as it is to the referential use of labels.     

Testing for social learning and imitation in common marmosets, <Emphasis Type="Italic">Callithrix jacchus</Emphasis>, using an artificial fruit

We tested for social learning and imitation in common marmosets using an artificial foraging task and trained conspecific demonstrators. We trained a demonstrator marmoset to open an artificial fruit, providing a full demonstration of the task to be learned. Another marmoset provided a partial demonstration, controlling for stimulus enhancement effects, by eating food from the outside of the apparatus. We thus compared three observer groups, each consisting of four animals: those that received the full demonstration, those that received the partial demonstration, and a control group that saw no demonstration prior to testing. Although none of the observer marmosets succeeded in opening the artificial fruit during the test periods, there were clear effects of demonstration type. Those that saw the full demonstration manipulated the apparatus more overall, whereas those from the control group manipulated it the least of the three groups. Those from the full-demonstration group also contacted the particular parts of the artificial fruit that they had seen touched (localised stimulus enhancement) to a greater extent than the other two groups. There was also an interaction between the number of hand and mouth touches made to the artificial fruit for the full- and partial-demonstration groups. Whether or not these data represent evidence for imitation is discussed. We also propose that the clear differences between the groups suggest that social learning mechanisms provide real benefits to these animals in terms of developing novel food-processing skills analogous to the one presented here.     

Human-directed behaviour in goats is not affected by short-term positive handling

In addition to domestication, interactions with humans or task-specific training during ontogeny have been proposed to play a key role in explaining differences in human–animal communication across species. In livestock, even short-term positive interactions with caretakers or other reference persons can influence human–animal interaction at different levels and over different periods of time. In this study, we investigated human-directed behaviour in the ‘unsolvable task’ paradigm in two groups of domestic goats (Capra aegagrus hircus). One group was positively handled and habituated to a plastic box by the experimenter to retrieve a food reward, while the other group only received standard husbandry care and was habituated to the box without human assistance. In the unsolvable task, the lid was fixed to the box, with the reward inaccessible to the subjects. The goats were confronted with the unsolvable task three times. We observed no difference between the two groups regarding gaze and contact alternations with the experimenter when confronted with the task they cannot solve by themselves. The goats did not differ in their expression rates of both gaze and contact alternations over three repetitions of the unsolvable task; however, they showed earlier gaze and contact alternations in later trials. The results do not support the hypothesis that short-term positive handling or task-specific training by humans facilitates human-directed behaviour in goats. In contrast, standard husbandry care might be sufficient to establish humans as reference persons for farm animals in challenging situations.     

Motivation and memory in zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>) foraging behavior

Remembering combinations of information such as what resources have been seen in which locations could play an important role in enhancing individual survival through increased foraging success. To date, there have been relatively few investigations of avian memory involving more than one category of information. This study explored zebra finches’ (Taeniopygia guttata) capacity to recall two categories in combination, namely food-type and spatial location. Birds were trained to remove variously weighted flaps to find two types of food hidden beneath. Memory for food-types and locations was assessed by pre-feeding the birds to satiety on and devaluing one food-type, and then testing the birds’ efficiency at finding the non-devalued food. When allowed one trial to learn locations of two food rewards that were hidden beneath lightly weighted flaps, birds performed better than chance at locating a food reward. However, they did not preferentially search for the non pre-fed food, suggesting that they were unable to recall both food type and location in combination. Zebra finches made fewer errors when tested on the one-trial task using more heavily weighted flaps than with lightly weighted flaps; there was equivocal evidence that they remembered which food type was hidden where on this task. When given repeated exposures to the locations of the two food rewards, finches located a food reward more accurately than on the one-trial tasks, and were also more likely to recall the locations of the different food types. In this foraging paradigm, experience and motivation may have influenced the birds’ performance.     

Cooperative problem solving in African grey parrots (<Emphasis Type="Italic">Psittacus erithacus</Emphasis>)

One of the main characteristics of human societies is the extensive degree of cooperation among individuals. Cooperation is an elaborate phenomenon, also found in non-human primates during laboratory studies and field observations of animal hunting behaviour, among other things. Some authors suggest that the pressures assumed to have favoured the emergence of social intelligence in primates are similar to those that may have permitted the emergence of complex cognitive abilities in some bird species such as corvids and psittacids. In the wild, parrots show cooperative behaviours such as bi-parental care and mobbing. In this study, we tested cooperative problem solving in African grey parrots (Psittacus erithacus). Our birds were tested using several experimental setups to explore the different levels of behavioural organisation between participants, differing in temporal and spatial complexity. In our experiments, African grey parrots were able to act simultaneously but mostly failed during the delay task, maybe because of a lack of inhibitory motor response. Confronted with the possibility to adapt their behaviour to the presence or absence of a partner, they showed that they were able to coordinate their actions. They also collaborated, acting complementarily in order to solve tasks, but they were not able to place themselves in the partner’s role.     

Testing problem-solving capacities: differences between individual testing and social group setting

Testing animals individually in problem-solving tasks limits distractions of the subjects during the test, so that they can fully concentrate on the problem. However, such individual performance may not indicate the problem-solving capacity that is commonly employed in the wild when individuals are faced with a novel problem in their social groups, where the presence of a conspecific influences an individual’s behaviour. To assess the validity of data gathered from parrots when tested individually, we compared the performance on patterned-string tasks among parrots tested singly and parrots tested in social context. We tested two captive groups of orange-winged amazons (Amazona amazonica) with several patterned-string tasks. Despite the differences in the testing environment (singly vs. social context), parrots from both groups performed similarly. However, we found that the willingness to participate in the tasks was significantly higher for the individuals tested in social context. The study provides further evidence for the crucial influence of social context on individual’s response to a challenging situation such as a problem-solving test.     

Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark

Top predators inhabiting a dynamic environment, such as coastal waters, should theoretically possess sufficient cognitive ability to allow successful foraging despite unpredictable sensory stimuli. The cognition-related hunting abilities of marine mammals have been widely demonstrated. Having been historically underestimated, teleost cognitive abilities have also now been significantly demonstrated. Conversely, the abilities of elasmobranchs have received little attention, despite many species possessing relatively large brains comparable to some mammals. The need to determine what, if any, cognitive ability these globally distributed, apex predators are endowed with has been highlighted recently by questions arising from environmental assessments, specifically whether they are able to learn to distinguish between anthropogenic electric fields and prey bioelectric fields. We therefore used electroreceptive foraging behaviour in a model species, Scyliorhinus canicula (small-spotted catshark), to determine cognitive ability by analysing whether elasmobranchs are able to learn to improve foraging efficiency and remember learned behavioural adaptations. Positive reinforcement, operant conditioning was used to study catshark foraging behaviour towards artificial, prey-type electric fields (Efields). Catsharks rewarded with food for responding to Efields throughout experimental weeks were compared with catsharks that were not rewarded for responding in order to assess behavioural adaptation via learning ability. Experiments were repeated after a 3-week interval with previously rewarded catsharks this time receiving no reward and vice versa to assess memory ability. Positive reinforcement markedly and rapidly altered catshark foraging behaviour. Rewarded catsharks exhibited significantly more interest in the electrical stimulus than unrewarded catsharks. Furthermore, they improved their foraging efficiency over time by learning to locate and bite the electrodes to gain food more quickly. In contrast, unrewarded catsharks showed some habituation, whereby their responses to the electrodes abated and eventually entirely ceased, though they generally showed no changes in most foraging parameters. Behavioural adaptations were not retained after the interval suggesting learned behaviour was not memorised beyond the interval. Sequences of individual catshark search paths clearly illustrated learning and habituation behavioural adaptation. This study demonstrated learning and habituation occurring after few foraging events and a memory window of between 12 h and 3 weeks. These cognitive abilities are discussed in relation to diet, habitat, ecology and anthropogenic Efield sources.     

Social learning of optimal responding and producer-scrounger strategies in flocks of pigeons

Social learning of optimal responding and producer-scrounger strategies in flocks of pigeons. This experiment evaluated the effect of varying the effort required in order to access food upon the acquisition of a novel response, and upon utilizing producer-scrounger strategies, in flocks of pigeons exposed to an expert conspecific. Flocks of na?ve observers were exposed to a pigeon trained to open the seals on food deposits. The colors of the seals were correlated with differing required efforts. Later, the trained pigeon was removed while the color-effort correlation was maintained. The results showed that the observers acquired the response of opening the seals and that they executed it discriminatingly, responding in a greater proportion to the color that signaled the least required effort. They also assumed the roles of both producers and scroungers, which varied as a function of the composition of the group. The data obtained are congruent with prior findings regarding social learning, and also with the concepts proposed by the optimal foraging theory.     

Social learning in captive African elephants (Loxodonta africana africana)

Social learning is a more efficient method of information acquisition and application than trial and error learning and is prevalent across a variety of animal taxa. Social learning is assumed to be important for elephants, but evidence in support of that claim is mostly anecdotal. Using a herd of six adult female African bush elephants (Loxodonta africana africana) at the San Diego Zoo’s Safari Park, we evaluated whether viewing a conspecific’s interactions facilitated learning of a novel task. The tasks used feeding apparatus that could be solved in one of two distinct ways. Contrary to our hypothesis, the method the demonstrating animal used did not predict the method used by the observer. However, we did find evidence of social learning: After watching the model, subjects spent a greater percentage of their time interacting with the apparatus than they did in unmodeled trials. These results suggest that the demonstrations of a model may increase the motivation of elephants to explore novel foraging tasks.     

Does social environment influence learning ability in a family-living lizard?

Early developmental environment can have profound effects on individual physiology, behaviour, and learning. In birds and mammals, social isolation during development is known to negatively affect learning ability; yet in other taxa, like reptiles, the effect of social isolation during development on learning ability is unknown. We investigated how social environment affects learning ability in the family-living tree skink (Egernia striolata). We hypothesized that early social environment shapes cognitive development in skinks and predicted that skinks raised in social isolation would have reduced learning ability compared to skinks raised socially. Offspring were separated at birth into two rearing treatments: (1) raised alone or (2) in a pair. After 1 year, we quantified spatial learning ability of skinks in these rearing treatments (N = 14 solitary, 14 social). We found no effect of rearing treatment on learning ability. The number of skinks to successfully learn the task, the number of trials taken to learn the task, the latency to perform the task, and the number of errors in each trial did not differ between isolated and socially reared skinks. Our results were unexpected, yet the facultative nature of this species’ social system may result in a reduced effect of social isolation on behaviour when compared to species with obligate sociality. Overall, our findings do not provide evidence that social environment affects development of spatial learning ability in this family-living lizard.     

How do African grey parrots (Psittacus erithacus) perform on a delay of gratification task?

Humans and other animals often find it difficult to choose a delayed reward over an immediate one, even when the delay leads to increased pay-offs. Using a visible incremental reward procedure, we tested the ability of three grey parrots to maintain delay of gratification for an increasingly valuable food pay-off. Up to five sunflower seeds were placed within the parrot’s reach, one at a time, at a rate of one seed per second. When the parrot took a seed the trial was ended and the birds consumed the accumulated seeds. Parrots were first tested in daily sessions of ten trials and then with single daily trials. For multiple trial sessions, all three parrots showed some limited improvement across 30 sessions. For single trial sessions, only one parrot showed any increase in seed acquisition across trials. This parrot was also able to consistently obtain two or more seeds per trial (across both multiple and single trial conditions) but was unable to able to wait 5 s to obtain the maximum number of seeds. This parrot was also tested on a slower rate of seed presentation, and this significantly reduced her mean seed acquisition in both multiple and single trial conditions, suggesting that both value of reward available and delay duration impact upon self-control. Further manipulation of both the visibility and proximity of seeds during delay maintenance had little impact upon tolerance of delays for both parrots tested in this condition. This task demanded not just a choice of delayed reward but the maintenance of delayed gratification and was clearly difficult for the parrots to learn; additional training or alternative paradigms are required to better understand the capacity for self-control in this and other species.