Defining Natural Categories in Acoustic Signals: Comparison of Three Methods Applied to ‘Chick-a-dee’ Call Notes

Chicks were trained to discriminate between two identical boxes on the basis of their position. Subsequently, the colour of parts of the positive (reinforced) box was changed and chicks were retrained. Results showed that chicks were more or less impaired during retraining depending on the spatial distribution of the changed stimuli. Chicks behaved as if a figure (a disc or a spot of dots) painted on a box was irrelevant to them, whereas they did respond to changes in the colour of a uniformly coloured box or of scattered dots painted on a box. Similar results were obtained in simultaneous discrimination learning tasks involving addition of cues (e.g. colour plus position). Addition of cues facilitated learning using boxes the same colour all over or with painted scattered dots, but not using boxes with a disc or a spot of dots. Furthermore, addition of shape and position information had different outcomes depending on the use of three-dimensional objects or of painted figures: learning facilitation occurred only using three-dimensional objects. Results are interpreted in terms of an “object hypothesis”, and the validity and usefulness of traditional terms such as cues is questioned.     

Learning of colour and position cues in domestic chicks: Males are better at position,females at colour

Male and female chicks were trained to discriminate between two boxes for food reinforcement. The correct box was indicated by a colour cue (red or brown) and a position cue (right or left). After learning, the colour and the position cues were dissociated: the right-left location of the two boxes was alternated between trials according to a semi-random sequence.The chicks were thus retrained to discriminate either on the basis of colour (irrespective of position) or on the basis of position (irrespective of colour). There were no sex differences, during training, with both position and colour cues. However, during re-training females performed better on the colour learning task and males performed better on the position learning task.     

Colour categorization by domestic chicks

Spectral stimuli form a physical continuum, which humans divide into discrete non-overlapping regions or categories that are designated by colour names. Little is known about whether non-verbal animals form categories on stimulus continua, but work in psychology and artificial intelligence provides models for stimulus generalization and categorization. We compare predictions of such models to the way poultry chicks (Gallus gallus) generalize to novel stimuli following appetitive training to either one or two colours. If the two training colours are (to human eyes) red and greenish-yellow or green and blue, chicks prefer intermediates, i.e. orange rather than red or yellow and turquoise rather than green or blue. The level of preference for intermediate colours implies that the chicks interpolate between the training stimuli. However, they do not extrapolate beyond the limits set by the training stimuli, at least for red and yellow training colours. Similarly, chicks trained to red and blue generalize to purple, but they do not generalize across grey after training to the complementary colours yellow and blue. These results are consistent with a modified version of a Bayesian model of generalization from multiple examples that was proposed by Shepard and show similarities to human colour categorization.     

Contrast versus colour in aposematic signals

Conspicuousness is an important feature of warning coloration. One hypothesis for its function is that it increases signal efficacy by facilitating avoidance learning. An alternative, based on the handicap hypothesis, suggests that the degree of conspicuousness holds information directly about the quality of the prey, and that predators associate and learn about the conspicuousness of the coloration, and not the actual colour pattern. We studied the relative importance of signal contrast and the colours of signals for predator attention during discrimination. We used young chicks, Gallus gallus domesticus, as predators and small blue or red paper cones on either matching or contrasting paper backgrounds as stimuli associated with palatable or unpalatable chick crumbs. In four treatment groups, birds could use either cone and/or background colour, cone colour only, background colour only or cone-to-background contrast as cues for discrimination. Only birds in the contrast treatment failed to learn their discrimination task. Birds that had a choice between cone and background colour as cues used the cone colour and they learned the task faster than did birds that had to use background colour as a cue. The results suggest that birds primarily attend to the colours of signals and disregard contrast in discrimination tasks; they thus fail to support a handicap function of conspicuous aposematic coloration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Number-Based Visual Generalisation in the Honeybee

Although the numerical abilities of many vertebrate species have been investigated in the scientific literature, there are few convincing accounts of invertebrate numerical competence. Honeybees, Apis mellifera, by virtue of their other impressive cognitive feats, are a prime candidate for investigations of this nature. We therefore used the well-established delayed match-to-sample paradigm, to test the limits of honeybees'' ability to match two visual patterns solely on the basis of the shared number of elements in the two patterns. Using a y-maze, we found that bees can not only differentiate between patterns containing two and three elements, but can also use this prior knowledge to differentiate three from four, without any additional training. However, bees trained on the two versus three task could not distinguish between higher numbers, such as four versus five, four versus six, or five versus six. Control experiments confirmed that the bees were not using cues such as the colour of the exact configuration of the visual elements, the combined area or edge length of the elements, or illusory contours formed by the elements. To our knowledge, this is the first report of number-based visual generalisation by an invertebrate.     

Colour discrimination learning in black-handed tamarin (<Emphasis Type="Italic">Saguinus midas niger</Emphasis>)

Colour is one cue that monkeys use for perceptual segregation of targets and to identify food resources. For fruit-eating primates such as Saguinus, an accurate colour perception would be advantageous to help find ripe fruits at distance. The colour vision abilities of black-handed tamarins (Saguinus midas niger) were assessed through a discrimination learning paradigm using Munsell colour chips as stimuli. Pairs of chips were chosen from an early experiment with protan and deutan humans. The monkeys (three males and one female) were tested with stimuli of the same hue, but different brightness values, in order to make sure that discriminations were based on colour rather than brightness cues. The results showed that the female, but not the males, presented an above-chance performance for stimuli resembling hue conditions under which tamarins forage (oranges vs greens). Colour vision in S. m. niger is discussed according to the advantages and disadvantages of dichromatism in daily search for food as well as to aspects regarding polymorphism in New World monkeys.     

Complex memories in honeybees: can there be more than two?

Foraging honeybees are likely to learn visual and chemical cues associated with many different food sources. Here, we explore how many such sources can be memorized and recalled. Marked bees were trained to visit two (or three) sugar feeders, each placed at a different outdoor location and carrying a different scent. We then tested the ability of the bees to recall these locations and fly to them, when the training scents were blown into the hive, and the scents and food at the feeders were removed. When trained on two feeder locations, each associated with a different scent, the bees could correctly recall the location associated with each scent. However, this ability broke down when the number of scents and feeder locations was increased to three. Performance was partially restored when each of the three training feeders was endowed with an additional cue, namely, a distinct colour. Our results suggest that bees can recall a maximum of two locations when each is associated with a different scent. However, this number can be increased if the scent cues are augmented by visual cues. These findings have implications for the ways in which associations are established and laid down in honeybee memory.     

Spatial reorientation by geometry with freestanding objects and extended surfaces: a unifying view

The macroscopic, three-dimensional surface layout geometry of an enclosure apparently provides a different contribution for spatial reorientation than the geometric cues associated with freestanding objects arranged in arrays with similar geometric shape. Here, we showed that a unitary spatial representation can account for the capability of animals to reorient both by extended surfaces and discrete objects in a small-scale spatial task. We trained domestic chicks to locate a food-reward from an opening on isolated cylinders arranged either in a geometrically uninformative (square-shaped) or informative (rectangular-shaped) arrays. The arrays were located centrally within a rectangular-shaped enclosure. Chicks trained to access the reward from a fixed position of openings proved able to reorient according to the geometric cues specified by the shape of the enclosure in all conditions. Chicks trained in a fixed position of opening with geometric cues provided both by the arena and the array proved able to reorient according to each shape separately. However, chicks trained to access the reward from a variable position of openings failed to reorient. The results suggest that the physical constrains associated with the presence of obstacles in a scene, rather than their apparent visual extension, are crucial for spatial reorientation.     

Activation of cholecystokinin neurons in the dorsal pallium of the telencephalon is indispensable for the acquisition of chick imprinting behavior

Chick imprinting behavior is a good model for the study of learning and memory. Imprinting object is recognized and processed in the visual wulst, and the memory is stored in the intermediate medial mesopallium in the dorsal pallium of the telencephalon. We identified chicken cholecystokinin (CCK)-expressing cells localized in these area. The number of CCK mRNA-positive cells increased in chicks underwent imprinting training, and these cells expressed nuclear Fos immunoreactivity at high frequency in these regions. Most of these CCK-positive cells were glutamatergic and negative for parvalbumin immunoreactivity. Semi-quantitative PCR analysis revealed that the CCK mRNA levels were significantly increased in the trained chicks compared with untrained chicks. In contrast, the increase in CCK- and c-Fos-double-positive cells associated with the training was not observed after closure of the critical period. These results indicate that CCK cells in the dorsal pallium are activated acutely by visual training that can elicit imprinting. In addition, the CCK receptor antagonist significantly suppressed the acquisition of memory. These results suggest that the activation of CCK cells in the visual wulst as well as in the intermediate medial mesopallium by visual stimuli is indispensable for the acquisition of visual imprinting.     

Visual Cues Given by Humans Are Not Sufficient for Asian Elephants (Elephas maximus) to Find Hidden Food

Recent research suggests that domesticated species – due to artificial selection by humans for specific, preferred behavioral traits – are better than wild animals at responding to visual cues given by humans about the location of hidden food. \Although this seems to be supported by studies on a range of domesticated (including dogs, goats and horses) and wild (including wolves and chimpanzees) animals, there is also evidence that exposure to humans positively influences the ability of both wild and domesticated animals to follow these same cues. Here, we test the performance of Asian elephants (Elephas maximus) on an object choice task that provides them with visual-only cues given by humans about the location of hidden food. Captive elephants are interesting candidates for investigating how both domestication and human exposure may impact cue-following as they represent a non-domesticated species with almost constant human interaction. As a group, the elephants (n = 7) in our study were unable to follow pointing, body orientation or a combination of both as honest signals of food location. They were, however, able to follow vocal commands with which they were already familiar in a novel context, suggesting the elephants are able to follow cues if they are sufficiently salient. Although the elephants’ inability to follow the visual cues provides partial support for the domestication hypothesis, an alternative explanation is that elephants may rely more heavily on other sensory modalities, specifically olfaction and audition. Further research will be needed to rule out this alternative explanation.     

Visual memory of shapes in quail chicks: discrimination among 2-dimensional objects

Newly hatched chicks spontaneously peck at conspicuous objects, and soon learn to discriminate between edible food particles and inedible objects. To examine whether this discrimination is based on a chick's ability to memorize objects by shape cues, we analyzed the pecking behavior. One- to 3-day old quail chicks (Coturnix japonica) were presented with dry objects of different shapes (ball, disk, triangle and T-shape) of similar size (4 mm) and color (green). Habituation occurred after repeated presentation of any one of these objects (duration: 30 sec; interval: 4 min). When chicks showed significantly more pecks at a novel object (dishabituation), we assumed that chicks had memorized the habituated shapes and distinguished the novel object. Chicks did not show dishabituation between a ball and a disk. On the other hand, chicks discriminated a triangle or T-shape from the memorized image of disk, but did not memorize either triangle or T-shape by its shape. Similarly, chicks did not memorize the size of disks as a reference for subsequent pecking behavior. Chicks proved to have a limited ability to memorize shape and size cues for selective pecking behavior, in strong contrast to their accurate memorization of colors.     

Recognition of a familiar place by the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Recent work shows that at any one place bees detect a limited variety of simple cues in parallel. At each choice point, they recognize a few cues in the range of positions where the cues occurred during the learning process. There is no need to postulate that they re-assemble the surrounding panorama in memory; only that they retain memories of the coincidences of cues in the expected retinotopic directions. The cues could be stimuli that excite groups of peripheral visual neurons. All the experimentally known cues are described, including modulation of the receptors, the locations of areas of black or colour, the nearness, size, averaged edge orientation, and radial and tangential edges. Cues of each type are separately summed within large fields, the size of which varies with the cue. Local orientation cues from edges at right angles cancel each other within each field, which also suggests that the discrimination of shape and texture is limited. Resolution depends on lateral interactions and the number of ommatidia required for each cue. To identify a new place, a few sparse cues, together with their directions, are learned in orientation flights. When the bee returns, the cues in the panorama are progressively matched as they coincide with the cues in memory. The limited number of cues, though economical for memory, may restrict the foraging behaviour and lead to flower constancy. This kind of a visual system is a candidate model for other animals or machines with economical processing systems.     

Blue colour preference in honeybees distracts visual attention for learning closed shapes

Spatial vision is an important cue for how honeybees (Apis mellifera) find flowers, and previous work has suggested that spatial learning in free-flying bees is exclusively mediated by achromatic input to the green photoreceptor channel. However, some data suggested that bees may be able to use alternative channels for shape processing, and recent work shows conditioning type and training length can significantly influence bee learning and cue use. We thus tested the honeybees’ ability to discriminate between two closed shapes considering either absolute or differential conditioning, and using eight stimuli differing in their spectral characteristics. Consistent with previous work, green contrast enabled reliable shape learning for both types of conditioning, but surprisingly, we found that bees trained with appetitive-aversive differential conditioning could additionally use colour and/or UV contrast to enable shape discrimination. Interestingly, we found that a high blue contrast initially interferes with bee shape learning, probably due to the bees innate preference for blue colours, but with increasing experience bees can learn a variety of spectral and/or colour cues to facilitate spatial learning. Thus, the relationship between bee pollinators and the spatial and spectral cues that they use to find rewarding flowers appears to be a more rich visual environment than previously thought.     

A parametric study of flavoured food avoidance in chicks

It has previously been shown that the ability of the chick toassociate the consumption of novel flavoured substances withsubsequent malaise is specific to the mode of ingestion (Gilletteet al., 1980), i.e., chicks will readily form conditioned aversionsto weakly flavoured solutions but not to relatively stronglyflavoured foods. The present series of four experiments indicatedthat the failure of chicks to develop conditioned aversionsto flavoured food is not due to the parameters of flavour intensity (salience), conditioned stimulus duration, or tastequality. Altering the validity of visual cues did not facilitateflavour avoidance nor did compounding the flavour cue with avisual cue. Although chicks showed increasing neophobia forincreasing concentrations of NaCl flavoured food, they did notlearn to avoid the food relative to controls (Experiment 1).Similarly, varying the amount of time allowed for ingestingthe NaCl flavoured food produced no differences between groups(Experiment 2). Since it was possible that NaCl might produceconsiderable malaise in its own right, the third experimentwas a partial replication of Experiment 2 using sucrose flavouredfood. Again, there was no effect due to conditioned stimulusduration. The final experiment showed, firstly, that the failureto develop flavour aversions cannot be attributed to overshadowingby familiar visual cues and, secondly, that aversions for NaClflavoured food cannot be potentiated by the presence of a noveland highly salient visual cue. These results suggest that previousfailures to demonstrate flavoured food aversions in chicks arenot due to procedural inadequacies but, rather, due to an organismicconstraint. Whether this constraint is associative, physiologicalor attentional remains to be determined. The authors express appreciation to Marion Connors, Paula Halland Graeme Negri for technical assistance.     

Response strategies during acquisition of serial learning in pigeons (Columba livia)

Pigeons were exposed on fixed duration sessions to four chromatic stimuli and trained to perform a 2-item sequence. A detailed analysis of incorrect responses performed on each trial prior to completion of the sequence led to distinguish three learning stages. Already on initial sessions animals responded significantly more frequently to relevant stimuli than to irrelevant ones indicating stimulus control by salience. During an intermediary stage, responding to item 2 increased significantly and animals started an increasing number of trials with item 2, suggesting stimulus control by recency. On the final session the correct sequence outnumbered significantly the reverse sequence, suggesting control by order, while recency and salience effects were present to a lesser extent. Repeated pecks, i.e. consecutive pecks on the same cue, occurred on the four cues on the first session and decreased significantly on the last session for irrelevant colours. In addition, when key pecks were followed by a brief sound signal, repeats on relevant stimuli decreased while efficient colour pecks (i.e. when repeats were ignored) on these stimuli increased. These findings are discussed in the light of those obtained in traditional chaining paradigms.     

Trichromatic colour vision in the hummingbird hawkmoth, Macroglossum stellatarum L.

Hymenopterans have long been shown to choose colours by means of the spectral distribution and independently of the intensity (true colour vision). The same ability has only very recently been proven for two butterfly species. We present evidence for the existence of true colour vision in the European hummingbird hawkmoth, Macroglossum stellatarum. Moths were trained in dual-choice situations to spectral lights of a rewarding and an unrewarding wavelength. After training, unrewarded tests were performed during which the intensities of the lights were changed. The results confirm that the species has three spectral receptor types and uses true colour vision when learning the colour of a food source. If colour vision is not possible since only one receptor type is receiving input from both stimuli, the moths learn to associate some achromatic cue correlated to the receptor quantum catch, with the reward. The moths learn spectral cues rapidly and choose correctly after one to several rewarded visits even when trained to different colours in sequence. Accepted: 24 February 1999     

Comparative effects of form, colour, and pheromone of twospotted spider mite quiescent deutonymphs on male guarding behaviour

Abstract. Effects of form, colour, and pheromone of twospotted spider mite, Tetranychus urticae (Koch), quiescent deutonymphs on adult male guarding behaviour were tested independently and in combination using no-choice and sequential-presentation bioassays. Significantly more males approached yellow stimuli sources than non-yellow sources in all bioassays, suggesting that males orient visually to yellow carotenoid pigments of quiescent deutonymphs. The form and extract (pheromone) of quiescent deutonymphs did not increase male approach frequency. All three cues elicited male arrestment; contrasts of 2 × 3 factorial bioassay data showed that male tactile and/or visual perception of form increased arrestment frequency more than did contact chemoperception of extract, while extract perception caused more arrestments than did visual perception of colour. All three cues prolonged arrestment duration and increased frequency of intermale conflicts near stimuli sources, but form had greater impact than did other cues on the numbers of conflicts observed during coguarding incidents. Significant interactions among stimuli were observed, indicating that presence of multiple stimuli had a synergistic effect on the duration of male response. Males approached and were arrested by all three stimuli combined as often as by quiescent deutonymphs, but arrestments caused by quiescent deutonymphs were longer than those elicited by artificial stimuli. This difference suggests that either additional cues or differences in pheromone release rates are involved in eliciting and prolonging male T. urticae guarding behaviour.     

Fruit or aposematic insect? Context-dependent colour preferences in domestic chicks.

Colours are common stimuli in signalling systems. Requirements to function well as a signal sometimes conflict between different signallers, and the same colour stimulus is used to convey completely different messages to the same receiver. Fruits and aposematic insects both use red coloration as a signal, in the former case to signal profitability and in the latter case as a warning signal. In two experiments, we investigated whether the domestic chick, an omnivorous predator, differed in its unconditioned preference or avoidance of red and green stimuli depending on whether or not the stimulus was an insect. The experiments were designed as preference tests between red and green painted prey. The prey were live insects and artificial fruits (experiment 1), and, to investigate the effect of movement, live and dead insects (experiment 2). The chicks did not show any difference in pecking preference between red and green when fruit-like stimuli were used, but when the prey were insects, green prey were strongly preferred to red prey, and prey movement did not affect this bias. Thus, young chicks may recognize prey as insects and then discriminate between different prey colorations, or one type of food may elicit an unlearned colour preference-avoidance response that is absent with another type of food.     

Darwin's Finch Begging Intensity Does Not Honestly Signal Need in Parasitised Nests

Parental care should be selected to respond to honest cues that increase offspring survival. When offspring are parasitised, the parental food compensation hypothesis predicts that parents can provision extra food to compensate for energy loss due to parasitism. Chick begging behaviour is a possible mechanism to solicit increased feeding from attending parents. We experimentally manipulated parasite intensity from Philornis downsi in nests of Darwin's small ground finch (Geospiza fuliginosa) to test its effects on chick begging intensity and parental food provisioning. We used in‐nest video recordings of individually marked chicks to quantify nocturnal parasite feeding on chicks, subsequent diurnal chick begging intensity and parental feeding care. Our video analysis showed that one chick per brood had the highest parasite intensity during the night (supporting the tasty chick hypothesis) and weakest begging intensity during the day, which correlated with low parental care and rapid death. We observed sequential chick death on different days rather than total brood loss on a given day. Our within‐nest video images showed that (1) high nocturnal larval feeding correlated with low diurnal begging intensity and (2) parent birds ignored weakly begging chicks and provisioned strongly begging chicks. Excluding predation, all parasite‐free chicks survived (100% survival) and all parasitised chicks died in the nest (100% mortality). Weak begging intensity in parasitised chicks, which honestly signalled recent parasite attack, was not used as a cue for parental provisioning. Parents consistently responded to the strongest chick in both parasitised and parasite‐free nests.     

Colour biases in learned foraging preferences in Trinidadian guppies

Learning allows animals to adaptively adjust their behaviour in response to variable but predictable environments. Stable aspects of the environment may result in evolved or developmental biases in the systems impacting learning, allowing for improved learning performance according to local ecological conditions. Guppies (Poecilia reticulata), like many animals, show striking colour preferences in foraging and mating contexts and guppy artificial selection experiments have found that the form and progress of evolved responses to coloured stimuli differ depending on stimulus colour. Blue colouration is thought to typically be a relatively unimportant food cue in guppies. This raises the possibility that learned foraging associations with blue objects are formed less readily than with other colours. Here, guppies were rewarded for foraging at green or blue objects in two experiments. Guppies readily foraged from these objects, but learning performance differed with rewarded object colour. With equal amounts of training, the preference for green objects became stronger than the preference for blue objects. These differences in performance were not attributable to differences in initial preferences or to foraging more on one colour during training. These findings suggest that associative pairings within a single sensory modality that do not have a historic relevancy can be more difficult for animals to learn even when there is no clear initial bias present.