Visual lateralization in the sky: Geese manifest visual lateralization when flying with pair mates.

The brain's sensory lateralization involves the processing of information from the sensory organs primarily in one hemisphere. This can improve brain efficiency by reducing interference and duplication of neural circuits. For species that rely on successful interaction among family partners, such as geese, lateralization can be advantageous. However, at the group level, one-sided biases in sensory lateralization can make individuals predictable to competitors and predators. We investigated lateral preferences in the positioning of pair mates of Greater white-fronted geese Anser albifrons albifrons. Using GPS-GSM trackers, we monitored individual geese in flight throughout the year. Our findings indicate that geese exhibit individual lateral biases when viewing their mate in flight, but the direction of these biases varies among individuals. We suggest that these patterns of visual lateralization could be an adaptive trait for the species with long-term social monogamy, high levels of interspecies communication and competition, and high levels of predator and hunting pressure.

Lateralization in feeding is food type specific and impacts feeding success in wild birds.

Current research suggests that hemispheric lateralization has significant fitness consequences. Foraging, as a basic survival function, is a perfect research model to test the fitness impact of lateralization. However, our understanding of lateralized feeding behavior is based predominantly on laboratory studies, while the evidence from wild animals in natural settings is limited. Here we studied visual lateralization in yellow-footed green pigeons (Treron phoenicoptera) feeding in the wild. We aimed to test whether different types of food objects requiring different searching strategies elicit different eye/hemisphere biases. When feeding on relatively large, uniformly colored food objects (mahua flowers) which can be present or absent in the viewed patch, the majority of pigeons relied mostly on the left eye-right hemisphere. In contrast, when feeding on smaller and more abundant food objects, with color cues signaling its ripeness (sacred figs), right-eye (left-hemisphere) preference prevailed. Our results demonstrate that oppositely directed visual biases previously found in different experimental tasks occur in natural feeding situations in the form of lateralized viewing strategies specific for different types of food. The results suggest that pigeons rely on the hemisphere providing more advantages for the consumption of the particular type of food objects, implying the relevance of brain lateralization as a plastic adaptation to ecological demands. We assessed the success of food discrimination and consumption to examine the link between lateralization and cognitive performance. The use of the preferred eye resulted in better discrimination of food items. Discrimination accuracy and feeding efficiency were significantly higher in lateralized individuals. The results showed that visual lateralization impacted pigeons' feeding success, implicating important fitness benefits associated with lateralization.

Lateralization in monogamous pairs: wild geese prefer to keep their partner in the left hemifield except when disturbed.

Behavioural lateralization, which reflects the functional specializations of the two brain hemispheres, is assumed to play an important role in cooperative intraspecific interactions. However, there are few studies focused on the lateralization in cooperative behaviours of individuals, especially in a natural setting. In the present study, we investigated lateralized spatial interactions between the partners in life-long monogamous pairs. The male-female pairs of two geese species (barnacle, Branta leucopsis, and white-fronted, Anser albifrons geese), were observed during different stages of the annual cycle in a variety of conditions. In geese flocks, we recorded which visual hemifield (left/right) the following partner used to monitor the leading partner relevant to the type of behaviour and the disturbance factors. In a significant majority of pairs, the following bird viewed the leading partner with the left eye during routine behaviours such as resting and feeding in undisturbed conditions. This behavioural lateralization, implicating the right hemisphere processing, was consistent across the different aggregation sites and years of the study. In contrast, no significant bias was found in a variety of geese behaviours associated with enhanced disturbance (when alert on water, flying or fleeing away when disturbed, feeding during the hunting period, in urban area feeding and during moulting). We hypothesize that the increased demands for right hemisphere processing to deal with stressful and emergency situations may interfere with the manifestation of lateralization in social interactions.

Visual lateralization in artiodactyls: A brief summary of research and new evidence on saiga antelope.

The visual system and lifestyle characteristics make the even-toed ungulates an excellent model for the studies of behavioural lateralization. Recent research has focused on these mammals providing evidence of lateralization in a wide range of behaviours. This provides an opportunity for the collation of the current theoretical assumptions and the existing empirical evidence for visual lateralization in artiodactyls. In the present study, we aim first to gain a fuller picture of hemispheric specializations in saiga antelopes by investigating the lateralization of vigilance and novel object inspection in the wild. Second, we summarized the results of the research into visual lateralization in even-toed ungulates and attempted to assess the applicability of two popular hypotheses about the division of hemispheric roles. The results on saigas show a significant preference for head turns to the right visual field during vigilance which was more robust in individuals in larger groups. When an unfamiliar artificial object was placed in their natural setting, saigas preferentially viewed it predominantly with the right eye. These results, together with the cumulative evidence in artiodactyls, do not follow either the approach-withdrawal or positivity-negativity dichotomous patterns widely used to explain the division of functions between the hemispheres.

Differential roles of the right and left brain hemispheres in the social interactions of a free-ranging ungulate.

Despite the abundant empirical evidence on lateralized social behaviours, a clear understanding of the relative roles of two brain hemispheres in social processing is still lacking. This study investigated visual lateralization in social interactions of free-ranging European bison (Bison bonasus). The bison were more likely to display aggressive responses (such as fight and side hit), when they viewed the conspecific with the right visual field, implicating the left brain hemisphere. In contrast, the responses associated with positive social interactions (female-to-calf bonding, calf-to-female approach, suckling) or aggression inhibition (fight termination) occurred more likely when the left visual field was in use, indicating the right hemisphere advantage. The results do not support either assumptions of right-hemisphere dominance for control of various social functions or hypotheses about simple positive (approach) versus negative (withdrawal) distinction between the hemispheric roles. The discrepancy between the studies suggests that in animals, the relative roles of the hemispheres in social processing may be determined by a fine balance of emotions and motivations associated with the particular social reaction difficult to categorize for a human investigator. Our findings highlight the involvement of both brain hemispheres in the control of social behaviour.

What do wild saiga antelopes tell us about the relative roles of the two brain hemispheres in social interactions?

Two brain hemispheres are unequally involved in the processing of social stimuli, as demonstrated in a wide range of vertebrates. A considerable number of studies have shown the right hemisphere advantage for social processing. At the same time, an approach-withdrawal hypothesis, mainly based on experimental evidence, proposes the involvement of both brain hemispheres according to approach and withdrawal motivation. The present study aimed to test the relative roles of the two hemispheres in social responses displayed in a natural context. Visual biases, implicating hemispheric lateralization, were estimated in the social interactions of saiga antelope in the wild. In individually identified males, the left/right visual field use during approach and withdrawal responses was recorded based on the lateral head/body position, relative to the conspecific. Lateralized approach responses were investigated in three types of interactions, with left visual field bias found for chasing a rival, no bias-for attacking a rival, and right visual field bias-for pursuing a female. In two types of withdrawal responses, left visual field bias was found for retreating after fighting, while no bias was evident in fight rejecting. These findings demonstrate that neither the right hemisphere advantage nor the approach-withdrawal distinction can fully explain the patterns of lateralization observed in social behaviour. It is clear that both brain hemispheres play significant roles in social responses, while their relative contribution is likely determined by a complex set of motivational and emotional factors rather than a simple dichotomous distinction such as, for example, approach versus withdrawal motivation.

Mother and offspring lateralized social behavior across mammalian species.

Findings on nonprimate mammals place the issue of mother-infant lateralized relations in a broader context, demonstrating that humans are one of many species showing this feature. The remarkable interspecies consistency in the direction of lateralization points to a continuity between lateralized mother-infant interactions in primates and nonprimate mammals and suggests ancient evolutionary roots of human cradling bias. The results from species which, in contrast to primates, have no direct involvement of forelimbs in mother-infant spatial interactions clearly support the perceptual origin of this type of lateralization. A right hemisphere advantage for social functions relevant to mother-infant interactions is the most probable background for the left-sided biases in the behavior of mothers and infants. Recent findings suggest the contribution of lateralized mother-infant interactions to biological fitness. Mother and infant both can gain advantage from keeping the other on the left side.

Lateralization of mother-infant interactions in wild horses.

The manifestation of behavioural lateralization has been shown to be modified by environmental conditions, life experiences, and selective breeding. This study tests whether the lateralization recently found in feral domestic horse (Equus caballus) is evident in undomesticated horses. Mother-offspring interactions were investigated in Przewalski's horse (E. ferus przewalskii) living in their natural habitat in Mongolia. Lateral position preferences during mare-foal spontaneous reunions were used as a behavioural marker of visual lateralization. Preferences were separately assessed for foals' approaches to their mothers and mares' approaches to their foals. Preference to keep the mother in the visual field of the left eye was found in various types of foals' behaviour. In slow travelling, Przewalski's foals showed stronger preference for the left eye use than feral horse foals. Population-level left-eye bias was also found in mothers approaching their foals. Our results indicate right-hemispheric dominance for control of mother-offspring interactions in Przewalski's horses, similar to what has been reported for other mammals including humans. Benefits conferred by the lateralized social processing of and responding to social stimuli may explain that the left-lateralized social behaviour is a robust trait of equine behaviour, not modified by domestication or specific environmental conditions of the population.

Facing each other: mammal mothers and infants prefer the position favouring right hemisphere processing.

The right hemisphere plays a crucial role in social processing. Human mothers show a robust left cradling/holding bias providing greater right-hemispheric involvement in the exchange of social information between mother and infant. Here, we demonstrate that a similar bias is evident in face-to-face spatial interactions in marine and terrestrial non-primate mammals. Walruses and Indian flying foxes showed a significant population-level preference for the position which facilitates the use of the left visual field in both mother and infant. This behavioural lateralization may have emerged owing to benefits conferred by the enhanced right-hemispheric social processing providing the mother and infant an optimal perception of each other.

Lateralization of mother-infant interactions in a diverse range of mammal species.

Left-cradling bias is a distinctive feature of maternal behaviour in humans and great apes, but its evolutionary origin remains unknown. In 11 species of marine and terrestrial mammal, we demonstrate consistent patterns of lateralization in mother-infant interactions, indicating right hemisphere dominance for social processing. In providing clear evidence that lateralized positioning is beneficial in mother-infant interactions, our results illustrate a significant impact of lateralization on individual fitness.

Early expression of manual lateralization in bipedal marsupials.

Robust lateralization in forelimb use has recently been found in bipedal, but not quadrupedal, marsupial mammals. The link between bipedality and handedness, occurring in both marsupials and primates, remains to be investigated. To shed light on the developmental origins of marsupial manual lateralization, infants of macropod marsupials were examined before and shortly after the acquisition of habitual bipedal posture and locomotion. Forelimb preferences were assessed in natural, not artificially evoked, behaviors of infant red-necked wallaby in the wild and infant eastern gray kangaroo in free-ranging captivity. Pouch young of both species showed population-level left-forelimb preference when manipulating food objects, such as leaves and grass blades. This result provides the first report of lateralization in pouch young marsupials and rare evidence of lateralized manual activity in early mammalian ontogenesis. Young-at-foot juveniles of eastern gray kangaroo preferred to use the left forelimb to manipulate the mother's pouch edge as previously shown for red-necked wallaby. In both species, the direction of biases in manipulative behavior for young-at-foot and pouch young was the same as in adults. Forelimb preferences in offspring were positively correlated with the forelimb preferences of their mothers. Our results strongly suggest that the emergence of individual and population-level forelimb preferences in macropod infants precedes the onset of independent standing and locomotion. In all probability, manual lateralization in bipedal marsupials, such as kangaroos and wallabies, is not determined by the acquisition of habitual bipedality in the course of ontogenesis. (PsycINFO Database Record

Evidence for the perceptual origin of right-sided feeding biases in cetaceans.

Foraging behaviour of many cetacean species features the side biases at the population level. The origin of these behavioural lateralisations remains generally unclear. Here we explored lateralisation in aerial display of resident orcas in different behavioural contexts. Side preferences were analysed in lunging during foraging and breaching. One event of each type of displays per individually identified orca was used for analysis. Orcas showed a population-level preference to lunge on the right side when foraging (75% of lunges). In contrast, no lateralisation was found in breaching (54% of breaches to the right, 45% to the left). The right-sided bias in foraging found in orcas is in line with evidence from other whales, both baleen and toothed, and confirms the uniformity of feeding biases among cetaceans. In contrast to breaching, lunging in orcas was associated with fish pursuit, that is, with focused attention to and sensory perception of prey stimulus. The emergence of lateralisation in lunging and the absence of significant bias in breaching suggest that feeding biases in whales are underpinned by sensory lateralisation, that is, by lateralised hemispheric processing of sensory information about the prey. Evidence from orcas may be extrapolated to other cetaceans since right-sided biases in lunging during foraging is a very widespread phenomenon and likely to have a common origin. Our findings support the hypothesis that right-sided feeding biases are determined by left-hemisphere specialisation.

Parallel Emergence of True Handedness in the Evolution of Marsupials and Placentals.

Recent studies have demonstrated a close resemblance between some handedness patterns in great apes and humans. Despite this, comparative systematic investigations of manual lateralization in non-primate mammals are very limited. Among mammals, robust population-level handedness is still considered to be a distinctive human trait. Nevertheless, the comprehensive understanding of handedness evolution in mammals cannot be achieved without considering the other large mammalian lineage, marsupials. This study was designed to investigate manual lateralization in non-primate mammals using the methodological approach applied in primate studies. Here we show that bipedal macropod marsupials display left-forelimb preference at the population level in a variety of behaviors in the wild. In eastern gray and red kangaroos, we found consistent manual lateralization across multiple behaviors. This result challenges the notion that in mammals the emergence of strong "true" handedness is a unique feature of primate evolution. The robust lateralization in bipedal marsupials stands in contrast to the relatively weak forelimb preferences in marsupial quadrupeds, emphasizing the role of postural characteristics in the evolution of manual lateralization as previously suggested for primates. Comparison of forelimb preferences in seven marsupial species leads to the conclusion that the interspecies differences in manual lateralization cannot be explained by phylogenetic relations, but rather are shaped by ecological adaptations. Species' postural characteristics, especially bipedality, are argued to be instrumental in the origin of handedness in mammals.

Forelimb preferences in quadrupedal marsupials and their implications for laterality evolution in mammals.

BACKGROUND: Acquisition of upright posture in evolution has been argued to facilitate manual laterality in primates. Owing to the high variety of postural habits marsupials can serve as a suitable model to test whether the species-typical body posture shapes forelimb preferences in non-primates or this phenomenon emerged only in the course of primate evolution. In the present study we aimed to explore manual laterality in marsupial quadrupeds and compare them with the results in the previously studied bipedal species. Forelimb preferences were assessed in captive grey short-tailed opossum (Monodelphis domestica) and sugar glider (Petaurus breviceps) in four different types of unimanual behaviour per species, which was not artificially evoked. We examined the possible effects of sex, age and task, because these factors have been reported to affect motor laterality in placental mammals. RESULTS: In both species the direction of forelimb preferences was strongly sex-related. Male grey short-tailed opossums showed right-forelimb preference in most of the observed unimanual behaviours, while male sugar gliders displayed only a slight, not significant rightward tendency. In contrast, females in both species exhibited consistent group-level preference of the left forelimb. We failed to reveal significant differences in manual preferences between tasks of potentially differing complexity: reaching a stable food item and catching live insects, as well as between the body support and food manipulation. No influence of subjects' age on limb preferences was found. CONCLUSIONS: The direction of sex-related differences in the manual preferences found in quadrupedal marsupials seems to be not typical for placental mammals. We suggest that the alternative way of interhemispheric connection in absence of corpus callosum may result in a fundamentally distinct mechanism of sex effect on limb preferences in marsupials compared to placentals. Our data confirm the idea that non-primate mammals differ from primates in sensitivity to task complexity. Comparison of marsupial species studied to date indicate that the vertical body orientation and the bipedalism favor the expression of individual- and population-level forelimb preferences in marsupials much like it does in primates. Our findings give the first evidence for the effect of species-typical posture on the manual laterality in non-primate mammals.

Eye as a key element of conspecific image eliciting lateralized response in fish.

Visual lateralization in different aspects of social behaviour has been found for numerous species of vertebrates ranging from fish to mammals. For inspection of a shoal mate, many fishes show a left eye-right hemisphere preference. Here, we tested the hypothesis that in fish, there is a key cue in the conspecific appearance, which elicits lateralized response to the whole image of the conspecific. In a series of eight experiments, we explored eye preferences in cryptic-coloured Amur sleeper, Perccottus glenii, fry. Fish displayed left-eye preferences at the population level for inspection of a group of conspecifics, their own mirror image, and a motionless flat model of a conspecific. In contrast, no population bias was found for scrutinizing an empty environment or a moving cylinder. When fry were showed a model of a conspecific in a lateral view with the eye displaced from the head to the tail, they again showed a significant preference for left-eye use. On the other hand, 'eyeless' conspecific model elicited no lateralized viewing in fry. Finally, the left-eye preference was revealed for scrutiny of the image of a conspecific eye alone. We argue that in Amur sleeper fry, eye is the element of the conspecific image, which can serve as a 'key' for the initiation of lateralized social response. This key element may serve as a trigger for the rapid recognition of conspecifics in the left eye-right hemisphere system. Possible causes and advantages of lateralized perception of social stimuli and their key elements are discussed in the context of current theories of brain lateralization.

Does bipedality predict the group-level manual laterality in mammals?

BACKGROUND: Factors determining patterns of laterality manifestation in mammals remain unclear. In primates, the upright posture favours the expression of manual laterality across species, but may have little influence within a species. Whether the bipedalism acts the same in non-primate mammals is unknown. Our recent findings in bipedal and quadrupedal marsupials suggested that differences in laterality pattern, as well as emergence of manual specialization in evolution might depend on species-specific body posture. Here, we evaluated the hypothesis that the postural characteristics are the key variable shaping the manual laterality expression across mammalian species. METHODOLOGY/PRINCIPAL FINDINGS: We studied forelimb preferences in a most bipedal marsupial, brush-tailed bettong, Bettongia penicillata in four different types of unimanual behavior. The significant left-forelimb preference at the group level was found in all behaviours studied. In unimanual feeding on non-living food, catching live prey and nest-material collecting, all or most subjects were lateralized, and among lateralized bettongs a significant majority displayed left-forelimb bias. Only in unimanual supporting of the body in the tripedal stance the distribution of lateralized and non-lateralized individuals did not differ from chance. Individual preferences were consistent across all types of behaviour. The direction or the strength of forelimb preferences were not affected by the animals' sex. CONCLUSIONS/SIGNIFICANCE: Our findings support the hypothesis that the expression of manual laterality depends on the species-typical postural habit. The interspecies comparison illustrates that in marsupials the increase of bipedality corresponds with the increase of the degree of group-level forelimb preference in a species. Thus, bipedalism can predict pronounced manual laterality at both intra- and interspecific levels in mammals. We also conclude that quadrupedal position in biped species can slightly hinder the expression of manual laterality, but the evoked biped position in quadrupedal species does not necessarily lead to the enhanced manifestation of manual laterality.

Visual laterality of calf-mother interactions in wild whales.

BACKGROUND: Behavioral laterality is known for a variety of vertebrate and invertebrate animals. Laterality in social interactions has been described for a wide range of species including humans. Although evidence and theoretical predictions indicate that in social species the degree of population level laterality is greater than in solitary ones, the origin of these unilateral biases is not fully understood. It is especially poorly studied in the wild animals. Little is known about the role, which laterality in social interactions plays in natural populations. A number of brain characteristics make cetaceans most suitable for investigation of lateralization in social contacts. METHODOLOGY/PRINCIPAL FINDINGS: Observations were made on wild beluga whales (Delphinapterus leucas) in the greatest breeding aggregation in the White Sea. Here we show that young calves (in 29 individually identified and in over a hundred of individually not recognized mother-calf pairs) swim and rest significantly longer on a mother's right side. Further observations along with the data from other cetaceans indicate that found laterality is a result of the calves' preference to observe their mothers with the left eye, i.e., to analyze the information on a socially significant object in the right brain hemisphere. CONCLUSIONS/SIGNIFICANCE: Data from our and previous work on cetacean laterality suggest that basic brain lateralizations are expressed in the same way in cetaceans and other vertebrates. While the information on social partners and novel objects is analyzed in the right brain hemisphere, the control of feeding behavior is performed by the left brain hemisphere. Continuous unilateral visual contacts of calves to mothers with the left eye may influence social development of the young by activation of the contralateral (right) brain hemisphere, indicating a possible mechanism on how behavioral lateralization may influence species life and welfare. This hypothesis is supported by evidence from other vertebrates.

An eye for a worm: lateralisation of feeding behaviour in aquatic anamniotes.

Some animals, notably birds, preferentially approach and capture food items in their right visual field. However, this lateralised behaviour has not been studied extensively in anamniotes. Here we test eye preference during feeding for a fish, (Perccottus glenii; Teleostei, Perciformes), a newt, (Pleurodeles walti; Amphibia, Caudata), and a frog, (Xenopus laevis; Amphibia, Anura) using a test chamber that assesses reaction to visual stimuli while blocking olfactory and mechanical input. Both the fish and the newt showed right preferences in reactions to food items, but the frog did not. Our data extend our knowledge of the lateralised behaviours of vertebrates and are the first record of lateralised prey capture in a caudate amphibian. This finding dates back the history of the common pattern for visual lateralisation in vertebrates to Devonian, when the fish and quadruped lineages diverged.