Lateralized tool use in wild New Caledonian crows

Many vertebrate species exhibit sensory and motor asymmetries. Laterality studies of tool use have focused on primates, where hemispheric asymmetries, manifested behaviourally in hand preferences, are thought to be associated with complex motor tasks. Here we report strong individual lateralization for tool use in birds. New Caledonian crows, Corvus moneduloides, hold stick tools with their bills while foraging, often with the nonworking end laterally positioned on one side of the head and the working end possibly positioned in the binocular field. We observed four wild crows to determine whether tools were consistently held on one side. All crows showed a significant preference (two right, two left). This preference was independent of any asymmetry in tool manufacture and held for artificial holes similarly accessible for tools held on either side. This is the first demonstration of lateralized tool use in a nonprimate. In addition, all 173 tools used unilaterally were held only on a crow's preferred side. Such pronounced individual laterality for tool use in natural conditions has previously been reported only in humans and chimpanzees.     

Behavioural Lateralization in Budgerigars Varies with the Task and the Individual

Handedness/footedness and side biases are a well-known phenomenon in many animals, including humans. However, these so-called biases have mostly been studied at the population level - individual biases have received less attention, especially with regard to consistency over different tasks. Here we investigate behavioral lateralization in 12 male Budgerigars, Melopsittacus undulatus, a social parrot inhabiting the Australian bushlands. We performed 5 types of experiments to investigate lateralization, in tasks that involved climbing onto a perch, or landing on perches arranged in various configurations. The birds displayed highly significant, individually varying biases. The bias displayed by any particular individual varied with the task, in strength as well as polarity. Analysis of the data revealed that the preferred foot used for climbing did not coincide with the foot that was used while landing. Thus, landing choices are probably not determined by foot bias. Furthermore, these individual preferences were overridden completely when a bird had to perform a task simultaneously with another bird.     

Optic flow cues guide flight in birds

Although considerable effort has been devoted to investigating how birds migrate over large distances, surprisingly little is known about how they tackle so successfully the moment-to-moment challenges of rapid flight through cluttered environments [1]. It has been suggested that birds detect and avoid obstacles [2] and control landing maneuvers [3-5] by using cues derived from the image motion that is generated in the eyes during flight. Here we investigate the ability of budgerigars to fly through narrow passages in a collision-free manner, by filming their trajectories during flight in a corridor where the walls are decorated with various visual patterns. The results demonstrate, unequivocally and for the first time, that birds negotiate narrow gaps safely by balancing the speeds of image motion that are experienced by the two eyes and that the speed of flight is regulated by monitoring the speed of image motion that is experienced by the two eyes. These findings have close parallels with those previously reported for flying insects [6-13], suggesting that some principles of visual guidance may be shared by all diurnal, flying animals.     

Sexual differences in certain forms of motor asymmetry in rats

Using three tests, studies have been made on locomotor lateralization in Wistar rats. It was shown that rat prefer the left paw for obtaining food from a tube, this preference being more pronounced in females. Females are more asymmetric also in preference of a side turn in a labyrinth: they choose the right side. In males, the preference of the right and left turns, as well as the absence of locomotor asymmetry were almost equal. These data are rather similar to those obtained for human subjects. Studies on the direction of rotation of rats after apomorphine injections did not reveal any sex differences or populational preferences.     

Eye-specific learning of routes and “signposts” by walking honeybees

This study investigates the honeybee's ability to learn routes based on visual stimuli presented to a single eye, and to then navigate these routes using the other (naive) eye. Bees were trained to walk through a narrow tunnel carrying visual stimuli on the two walls. At the end of the tunnel the bees had to choose between two arms, one of which led to a feeder. In a first experiment, bees had to learn to choose the left arm to get a reward when the right wall carried a yellow grating, but the right arm when the left wall carried a blue grating. The bees learned this task well, indicating that stimuli encountered by different eyes could be associated with different routes. In a second experiment, bees had to turn left when the right eye saw a blue grating, but to the right when the same eye saw a yellow grating. They also learned this task well. In subsequent tests, they chose the correct arm even when these gratings were presented to the untrained eye. These results suggest that there is interocular transfer of route-specific learning with respect to visual stimuli that function as navigational “signposts”. Accepted: 18 December 1997     

Lateralization of lateral displays in convict cichlids

We examine lateralization of lateral displays in convict cichlids, Amatitlania nigrofasciata, and show a population level preference for showing the right side. This enables contesting pairs of fish to align in a head-to-tail posture, facilitating other activities. We found individuals spent a shorter mean time in each left compared with each right lateral display. This lateralization could lead to contesting pairs using a convention to align in a predictable head-to-tail arrangement to facilitate the assessment of fighting ability. It has major implications for the common use of mirror images to study fish aggression, because the 'opponent' would never cooperate and would consistently show the incorrect side when the real fish shows the correct side. With the mirror, the 'normal' head-to-tail orientation cannot be achieved.     

RAPTOR MIGRATION ACROSS THE STRAITS OF GIBRALTAR

The visible migration of birds of prey at Gibraltar is analysed from records kept throughout the spring passages of 1967–70 and the autumn passages of 1967–69. In early spring most visible passage is noted in the afternoons, whereas radar observations by Houghton (1970) indicate passage in the mornings. Later in the year an additional burst of visible passage sometimes occurs in the early morning, but it is concluded that most morning movements take place above visible range. Visible migration is recorded on most days of westerly wind during the migration seasons at Gibraltar. Passage is rarely seen when the winds are easterly. It is argued that under the latter conditions a strong upcurrent of air (standing wave) is formed over Gibraltar, and that this carries nearly all migrants above visible range.
Observations of visible passage elsewhere in the Straits suggest that, in spring, raptors of all species cross on a broad front from Tangier to Ceuta, except Honey Buzzards, which probably cross chiefly near Ceuta. In autumn, all species from northern Europe cross chiefly between Tarifa and to the east of Gibraltar, while birds from western Iberia probably cross mainly near Tarifa.
The periods of passage of the common migrant species are summarised.
On the basis of visual observations and published radar results, it is argued that raptors can compensate for lateral drift by the wind and so fly on chosen courses; but that in very strong cross-winds, e.g. the easterly Levanters, they may have to let themselves be drifted off-course.     

Human adipose-derived mesenchymal stem cells: serial passaging, doubling time and cell senescence

Adult adipose-derived mesenchymal stem cells (AD-MSC) are very interesting to our research group because they are easy to harvest, they are abundant in humans, and they have potential clinical applications in autologous cell therapy for disc degeneration. We examined these cells through sequential serial passages to assess osteogenic and chondrogenic capabilities, mean doubling time and cell senescence. Osteogenic and chondrogenic potencies were maintained through 13 passages. Mean passage doubling time increased significantly with increasing passage number. When donor age was evaluated, passages 1-4 from older donors had significantly longer doubling times compared to cells from younger donors. Passages 5-11 showed similar findings when analyzed by donor age. The mean percent senescence increased significantly with cell passaging, rising from 0% at passage 1 to 3.4% at passage 13. These novel data suggest that caution should be exercised when using AD-MSC with long passage times.     

Human adipose-derived mesenchymal stem cells: serial passaging,doubling time and cell senescence

Adult adipose-derived mesenchymal stem cells (AD-MSC) are very interesting to our research group because they are easy to harvest, they are abundant in humans, and they have potential clinical applications in autologous cell therapy for disc degeneration. We examined these cells through sequential serial passages to assess osteogenic and chondrogenic capabilities, mean doubling time and cell senescence. Osteogenic and chondrogenic potencies were maintained through 13 passages. Mean passage doubling time increased significantly with increasing passage number. When donor age was evaluated, passages 1-4 from older donors had significantly longer doubling times compared to cells from younger donors. Passages 5-11 showed similar findings when analyzed by donor age. The mean percent senescence increased significantly with cell passaging, rising from 0% at passage 1 to 3.4% at passage 13. These novel data suggest that caution should be exercised when using AD-MSC with long passage times.     

Lateralization in the predatory behaviour of the common wall lizard (Podarcis muralis)

Ectotherms have been shown being lateralized as well as mammals and birds. This is particularly evident in visual lateralization, i.e. the different use of the eyes, leading to use a specific eye to observe specific kind of stimuli and to process them with the correspondent contralateral hemisphere. Several lower vertebrates are facilitated in this from the lateral position of the eyes, enabling them to carry out more tasks simultaneously, controlled by different eyes and relative hemispheres. Predatory responses seem usually mediated by the right eye/left hemisphere in fishes, amphibians and some sauropsids, but there are no strong evidences of this in lizards. Eighteen wild males of the Common wall lizard Podarcis muralis were tested individually in captivity to ascertain whether they are lateralized to look at prey with a specific eye. The lizards were gently induced entering a 30-cm long central arm of a T-maze which led to a 44.5-cm long arm cross-arm at whose extremities there were two identical prey, Tenebrio molitor larvae, familiar to the lizards. We recorded what direction the lizards chose to reach the prey and the frequency and duration of head turning, indicative of looking either prey with the left or the right eye. We found that individuals show being lateralized at individual level. The preferred direction taken to reach the prey is the right for the majority of those (4 of 5) showing an evident preference, indicating also a possible form of laterality at population level. In addition, lizards maintained the same head side of the direction taken turned for more time towards the prey than the opposite head side, revealing an eye preference for observing this kind of cue. Our study demonstrates how males of Podarcis muralis have a visual lateralization to capture prey. Furthermore, it is another support to the hypothesis of vertebrate lateralization derivation from a common ancestor.     

Lateralization When Monitoring Predators in the Wild: A Left Eye Control in the Common Wall Lizard (Podarcis muralis)

Lateralization is the function specialization between left and right brain hemispheres. It is now ascertained in ectotherms too, where bias in eye use for different tasks, i.e., visual lateralization, is widespread. The lateral eye position on the head of ectotherm animals, in fact, allows them to observe left/right stimuli independently and allows lateralized individuals to carry out left and right perceived tasks at the same time. A recent study conducted on common wall lizards, Podarcis muralis, showed that lizards predominantly monitor a predator with the left eye while escaping. However, this work was conducted in a controlled laboratory setting owing to the difficulty of carrying out lateralization experiments under natural conditions. Nevertheless, field studies could provide important information to support what was previously found in the laboratory and demonstrate that these traits occur in nature. In this study, we conducted a field study on the antipredatory behavior of P. muralis lizards. We simulated predatory attacks on lizards in their natural environment. We found no lateralization in the measure of eye used by the lizard to monitor the predator before escaping from it, but the eye used was probably determined by the relative position of the lizard and the predator just before the attack. This first eye used did not affect escape decisions; lizards chose to escape toward the nearest refuge irrespective of whether it was located to the lizard’s left or right side. However, once they had escaped to a refuge, lizards had a left eye–mediated bias to monitor the predator when first emerging from the refuge, and this bias was likely independent of other environmental variables. Hence, these field findings support a left eye–mediated observation of the predator in P. muralis lizards, which confirms previous findings in this and other species.     

Lateralization in response to social stimuli in a cooperatively breeding cichlid fish

Cerebral lateralization, an evolutionarily ancient and widespread phenomenon among vertebrates, is thought to bestow cognitive advantages. The advantages of lateralization at the individual-level do not necessarily require that the entire population share the same pattern of lateralization. In fact, directional bias in lateralization may lead to behavioural predictability and enhanced predator success or prey evasion. Recent theory has suggested that population-level lateralization may be favored if individuals are better able to perform coordinated behaviours, providing a distinct advantage in cooperative contexts. Here we test whether the highly social, cooperatively breeding cichlid fish Neolamprologus pulcher shows lateralized responses to a social stimulus. We found population-level biases in males; on average male N. pulcher use their right eye/left hemisphere to view their mirror image. Individual females had a preferred hemisphere, but these preferences appeared not to be directionally aligned among females. We discuss these results in the context of coordinated social behaviour and suggest future research directions.     

Hand preferences for a haptic searching task by tufted capuchins (Cebus apella)

We tested the effects of a haptic search task on hand preferences in capuchins(Cebus apella) and compare this situation to a visual by guided reaching task. In the haptic task, 21 monkeys searched for sunflower seeds on the top or side surfaces of 12 objects. A left-hand preference emerged at the group level, suggesting a greater involvement of the right hemisphere. The percentage of preferred hand usage and the direction of the preference were influenced by both sex and age of the subjects: adult males tended to be less lateralized than the other groups of subjects were. Shape had an insignificant effect on the direction of hand preferences or on the percentage of preferred hand use. No lateral bias emerge in the visually guided reaching task, and the percentage of left-hand usage fell significantly across tasks, demonstrating that the haptic demands of the task enhance the use of the left hand at the group level. We discuss these results with regard to current theories on manual lateralization in nonhuman primates.     

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

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

Preference for consonant music over dissonant music by an infant chimpanzee

It has been shown that humans prefer consonant sounds from the early stages of development. From a comparative psychological perspective, although previous studies have shown that birds and monkeys can discriminate between consonant and dissonant sounds, it remains unclear whether nonhumans have a spontaneous preference for consonant music over dissonant music as humans do. We report here that a five-month-old human-raised chimpanzee (Pan troglodytes) preferred consonant music. The infant chimpanzee consistently preferred to produce, with the aid of our computerized setup, consonant versions of music for a longer duration than dissonant versions. This result suggests that the preference for consonance is not unique to humans. Further, it supports the hypothesis that one major basis of musical appreciation has some evolutionary origins.     

Common principle of guidance by echolocation and vision

1. Using echolocation, bats move as gracefully as birds through the cluttered environment, suggesting common principles of optic and acoustic guidance. We tested the idea by analysing braking control of bats (Macroderma gigas) flying through a narrow aperture with eyes covered and uncovered. 2. Though braking control would seem to require rapid detection of distance and velocity and computation of deceleration, simpler control is possible using the tau function of any sensory variable S that is a power function of distance to aperture. Tau function of S is tau (S) = S/S (the dot means time derivative). Controlled braking is achievable by keeping tau (S) constant. 3. Previous experiments indicated the tau (S) constant procedure is followed by humans and birds in visually controlling braking. Analysis of the bats' flight trajectories indicated they too followed the braking procedure using echolocation. 4. The tau function of echo-delay or of echo-intensity or of angle subtended by directions of echoes from two points on the approach surface could be used to control braking. Aperture size was modulated during flight on some trials in an attempt to test between these possibilities, but the results were inconclusive.     

Left hemispheric advantage for numerical abilities in the bottlenose dolphin

In a two-choice discrimination paradigm, a bottlenose dolphin discriminated relational dimensions between visual numerosity stimuli under monocular viewing conditions. After prior binocular acquisition of the task, two monocular test series with different number stimuli were conducted. In accordance with recent studies on visual lateralization in the bottlenose dolphin, our results revealed an overall advantage of the right visual field. Due to the complete decussation of the optic nerve fibers, this suggests a specialization of the left hemisphere for analysing relational features between stimuli as required in tests for numerical abilities. These processes are typically right hemisphere-based in other mammals (including humans) and birds. The present data provide further evidence for a general right visual field advantage in bottlenose dolphins for visual information processing. It is thus assumed that dolphins possess a unique functional architecture of their cerebral asymmetries.     

Bilateral song production in domestic canaries

We studied the mechanism of song production in the outbred common or domestic canary (Serinus canaria). The contribution that each side of the syrinx makes to song was investigated by observing the effect of unilaterally occluding the left or right primary bronchus, followed by section of the ipsilateral branch of the tracheosyringeal nerve. In other birds with a bilaterally intact vocal system we monitored airflow through each side of the syrinx, together with subsyringeal pressure, during spontaneous song. Song production by domestic canaries is not strongly lateralized as it is in the conspecific song-bred waterslager strain. Some syllables are produced entirely on the left or right side of the syrinx, whereas others contain sequential contributions from each side. Low fundamental frequencies are produced with the left syrinx and high frequencies by the right syrinx, increasing the frequency range of domestic canary song compared to that of the waterslager strain. Midrange frequencies can be generated by either side. Syllables at repetition rates below about 25 s(-1) were accompanied by minibreaths, which were usually bilateral. Unilateral minibreaths were typically on the left side. At higher syllable repetition rates, minibreaths were replaced by a respiratory pattern of pulsatile expiration. Our data show that strong unilateral dominance in song production, present in the waterslager strain, is not a trait of the species as a whole and that the pattern of song lateralization can be altered by selective breeding for particular song characteristics.     

Visually guided avoidance in the chameleon (Chamaeleo chameleon): response patterns and lateralization

The common chameleon, Chamaeleo chameleon, is an arboreal lizard with highly independent, large-amplitude eye movements. In response to a moving threat, a chameleon on a perch responds with distinct avoidance movements that are expressed in its continuous positioning on the side of the perch distal to the threat. We analyzed body-exposure patterns during threat avoidance for evidence of lateralization, that is, asymmetry at the functional/behavioral levels. Chameleons were exposed to a threat approaching horizontally from the left or right, as they held onto a vertical pole that was either wider or narrower than the width of their head, providing, respectively, monocular or binocular viewing of the threat. We found two equal-sized sub-groups, each displaying lateralization of motor responses to a given direction of stimulus approach. Such an anti-symmetrical distribution of lateralization in a population may be indicative of situations in which organisms are regularly exposed to crucial stimuli from all spatial directions. This is because a bimodal distribution of responses to threat in a natural population will reduce the spatial advantage of predators.     

Response of carnivores to existing highway culverts and underpasses: implications for road planning and mitigation

Roads with high traffic volumes are a source of animal mortality, can disrupt normal animal movements and dispersal, and may represent a potentially serious threat to wildlife population stability and viability. Retrofitting existing structures built for other purposes (e.g., drainage culverts or small below-grade access roads) to facilitate wildlife crossing by animals and to reduce mortality may be expensive if modifications to the existing structures themselves were involved. However, the environmental context surrounding these structures may influence the willingness of animals to cross, and management of some of these attributes may enhance the attractiveness of these structures. Culverts and underpasses are two common structures along roads in Portugal. We quantified the response of small and medium-sized carnivores to the presence of both types of existing passages by determining: (1) frequency of use; (2) whether use differed by type of passage, and if so; (3) by examining if associated environmental attributes might explain the differences observed. We surveyed 57 different passages along 252 km of highway with a total sampling effort of 2,330 passage trap-days. The mean passage rate for carnivores combined was 0.7 complete passages per crossing structure per day. Crossings by weasel, polecat, otter, and wildcat were infrequent or absent. Red fox, badger, genet and Egyptian mongoose used the crossing structures regularly and without obvious preference; stone marten preferred underpasses. Regression analyses showed the frequency of use by carnivores varied with structural, landscape, road-related features, and human disturbance with 17 of 26 (65%) attributes being significant. Larger passages with vegetation close to the passage entrances, favorable habitat in the surrounding area, and low disturbance by humans were important key features to regular use by the guild of species studied. Mitigation planning in areas with ecological significance for carnivores will be beneficial. Structural attributes and human disturbances are more difficult or expensive to change, even though related significantly to crossing use. Management of vegetation at passage entrances and restricting human use near passages in carnivore suitable areas may substantially improve crossing attractiveness for the guild of carnivore species.