Visual lateralisation is manifested in the dominance of one brain hemisphere in the processing of information from one of the eyes. Most studies manifested that the right hemisphere is responsible for the aggression, fear, and detection of predators and other threats, and the left hemisphere is responsible for the positive emotions, food search, and detection of large changes in the environment. Nevertheless, some independent studies manifested the opposite biases in the same behaviour tasks. To evaluate the value of species, behaviour task, locomotion type and breeding status in visual lateralisation biases we studied the behaviour of swimming and flying Whooper swans and Bewick's swans with and without chicks when observing a source of danger and a partner. We found that in the same conditions, the visual lateralisation bias was identical in two species and it differed depending on the type of locomotion in one species. Birds had a significant bias in the observation of the source of disturbance and hadn't in the observation of the leading partner. The presence of chicks strengthened the manifestation of visual lateralisation in the following birds. Therefore, special attention should be paid to details in comparing the results of studies conducted under different circumstances.
Research Article
Visual lateralisation of swans in response to anthropogenic disturbance differs according to observation task, presence of chicks and type of locomotion
https://doi.org/10.21203/rs.3.rs-2751067/v1
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Visual lateralisation
disturbance
anxiety
animal behaviour
anthropogenic factors
swan.
Lateralised processing of sensory information by the nervous system is a property of most bilaterally symmetrical animals (Rogers et al. 2013). The dominance of one brain hemisphere in the implementation of any function can be manifested in animal behaviour in the form of one-sided preferences, for example, the preference to inspect a stimulus with one eye (Rogers et al. 2013). In the avian brain, the optic nerves cross virtually completely, and the input from the left eye is mostly confined to structures of the right hemisphere and vice versa (Rashid and Andrew 1989; Workman and Andrew 1986). The lateralisation bias of the brain avoids conflicts between different behaviours performed simultaneously and increases brain productivity and compactness (Levy 1977; Vallortigara et al. 2011; Vallortigara and Versace, 2017; Vallortigara and Rogers 2020).
The lateralisation bias to the right eye and the left hemisphere appears in the processing of positively connoted emotions (Leliveld et al. 2013), food search, detection of large changes in the environment, and response to them (Vallortigara et al. 1991; Yamazaki et al. 2007). The bias to the left eye is common in the detection of small changes in the environment (Vallortigara et al. 1991; Yamazaki et al. 2007), negative emotions such as aggression (Vallortigara et al. 2001; Rogers et al. 2018; Krakauer et al. 2016) and fear (Dharmaretnam et al. 2005). Furthermore, it is found that the system of the left eye and right hemisphere is responsible for the detection of predators and other threats in many species (Rogers and Kaplan 2005; Martín et al. 2010; Austin and Rogers 2012; Bonati et al. 2013). In contrast, some studies demonstrated the lateralisation bias to the right eye for threat detection in experimental conditions (Dark-eyed junco (Junco hyemalis) (Franklin and Lima, 2001); Swan geese (Anser cygnoides) and Coot (Fulica atra) (Randler, 2005)) and in the wild (Sandpipers (Calidris pusilla) (Beauchamp 2013)). Results on visual lateralisation bias in courtship and copulation attempts are varying too. The lateralisation bias to the left eye was shown in Black-winged stilt (Himantopus himantopus) (Ventolini et al. 2005), Japanese quail (Coturnix japonica) (Gulbetekin et al. 2007), and Domestic chicks (Gallus gallus) (Rogers et al. 1985). On the opposite, the visual lateralisation bias to the right eye was found in Gouldian finch (Chloebia gouldiae) and Zebra finches (Taeniopygia castanotis) (Templeton et al. 2012; Templeton et al.2014).
In addition, for one species and one type of behaviour, bias may differ depending on additional factors. For example, a study of Yellow-footed green pigeons (Treron phoenicoptera) showed that the preference to use one of the eyes depends on the food object types (Karenina and Gilev 2022). Pigeons used the left eye if feeding mahua flowers and the right eye when feeding sacred fig fruits (Karenina and Gilev 2022).
Furthermore, it was found that disturbances could influence the manifestation of the visual lateralisation bias, at least during the interaction between partners in the wild. For example, visual lateralisation was manifested in routine behaviours of Barnacle geese (Branta leucopsis) and Greater white-fronted geese (Anser albifrons), but lateralisation was lacking in disturbing conditions (Zaynagutdinova et al. 2020).
Thus, the manifestation of the visual lateralisation bias could depend on behaviour task, species, and related factors. To compare and evaluate the value of these factors, complex studies should be invented. Consequently, we decided to study the manifestation of the visual lateralisation bias
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in two species – the Whooper swan (Cygnus cygnus) and Bewick’s swan (Cygnus columbianus bewickii),
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in two behaviour tasks – observation of the source of danger and observation of the partner,
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in two locomotion types – swimming and flying,
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in two family conditions – with and without chicks.
Photographic materials were obtained from aerial surveys of swans. The registration of birds from the seaplane was carried out on the Yamal Peninsula and the Gydan Peninsula from 24th June to 3rd October (during brood rearing, moulting, and autumn migration) in 2015–2017 and 2019–2020. The flight altitude was 50–80 m, and the width of the accounting lane was 1600 m (800 m on each side). All the birds encountered were photographed with a Canon Mark IV camera with a 100–400 mm lens. Photographing was carried out from both sides of the aircraft. The coordinates of the aircraft and flight tracks were recorded using a Garmin GPS navigator. The methodology is described in detail in the article by Rosenfeld and co-authors (2017).
We have analyzed 363 photos of pairs of the Bewick’s swan and 129 photos of the Whooper swan. The swans in the photos were swimming and flying. Two swans were recognized as a pair if there were only two of them in the photo and the distance between them was less than 10 meters. Moreover, we considered two swans as a pair if they were in the photo in a flock, but two swans had a distance between each other of up to 3 meters, and other birds were more than 10 meters away from them. We also detected pairs of swans with chicks. The sex of the birds wasn’t identified. We identified the following and a leading individual in a pair. It was determined which eye following and leading swans used to observe the leading bird and the anthropogenic disturbance factor (plane).
For the statistical analysis, only samples of > 50 pairs were used. A binomial z-score was used to analyze the significance of bias to keep the plane or leading partner in the left/right visual field. The chi-squared test was used to find differences in lateralisation bias in Bewick’s swan and Whooper swan, swimming and flying individuals, families with and without chicks, and plane or leading bird observation. The binominal z-scare was calculated using the site http://vassarstats.net/binomialX.html, the chi-squared test was performed using the RStudio (2022.07.1 + 554).
The leading swimming individuals of Bewick’s swan and Whooper swan (Fig. 1a) in pairs without chicks had significant evidence for right-eye preference for observing the source of anthropogenic disturbance (Table 1, Fig. 2). The following birds recorded a similar trend, but it was not significant in Whooper swan and it was significant in Bewick’s swan (Table 1, Fig. 2). No differences between species were found (Chi-square test: χ2 = 0.17, p = 0.68 for leading birds, χ2 = 0.19, p = 0.66 for following birds).
In swimming families of Bewick's swans with (Fig. 1b) and without chicks, both parents (leading and following) had strong evidence of the preference for keeping the plane in the right visual field (Table 1, Fig. 2). No differences between pairs with chicks and without chicks were found for leading birds (Chi-square test: χ2 = 2.53, p = 0.11). A significant difference was found for the following partners with and without chicks (Chi-square test: χ2 = 5.24, p = 0.024). Consequently, the presence of chicks had no significant effect on the behavioural lateralisation bias, but it intensified lateralisation bias for the following partner.
The leading and following flying birds of Bewick's swan (Fig. 1c) in pairs without chicks had a significant bias for left-eye preference to observe the source of anthropogenic disturbance (Table 1, Fig. 2). Thus, swimming individuals preferred to keep the plane in their right visual field, but flying birds more often used the left one. The difference was significant for leading birds (Chi-square test: χ2 = 8.84, p = 0.0034) and for following birds as well (Chi-square test: χ2 = 10.73, p = 0.001).
The presence of visual lateralisation for observing the leading partner in the presence of the factor of anthropogenic disturbance was analyzed in pairs with and without chicks in swimming and flying Bewick’s swans (Table 1, Fig. 2).
No significant visual bias was found for observing the leading partner in swimming pairs of Bewick’s swan with and without chicks while escaping from a plane (Chi-square test: χ2 = 0, p = 1). That is, the presence of chicks did not affect the manifestation of preferences to follow a partner in a stressful situation. So, following birds with and without chicks had no lateralisation bias in observing the leading bird, but had lateralisation bias in observing the plane. The difference between observation task types (observation of the leading bird or plane) was significant for following birds with (Chi-square test: χ2 = 16.3, p < 0.001) and without (Chi-square test: χ2 = 5.28, p = 0.02) chicks.
Following flying birds without chicks had no lateralisation bias in observing the leading bird also (Table 1, Fig. 2). The difference between observation task types (observation of the leading bird or plane) was not significant for flying following birds (Chi-square test: χ2 = 2.82, p = 0.09).
Thus, in Bewick’s swan, in the presence of anthropogenic disturbance, there was no preference to observe the partner with one of the eyes while flying or swimming with or without chicks.
Table 1. The behavioural lateralisation bias toward the source of anthropogenic disturbance and toward to leading partner in swimming and flying pairs of Whooper swan and Bewick’s swan with and without chicks.
No difference between species was found in observing the disturbance source. Despite the fact that for following birds in Whooper swan the visual lateralisation bias was not significant, it had simultaneously tendency as in the following birds in Bewick’s swan. A similar visual lateralisation bias in other species was demonstrated in studies proved in the same conditions. For example, the pebble floor test was conducted in similar experimental conditions in zebra finches (Taeniopygia guttata) (Alonso 1998); domestic chicks (Gallus gallus domesticus) (Mench and Andrew, 1986); homing pigeons (Columba livia domestica) (Güntürkün and Kesch 1987), Australian Magpie (Gymnorhina tibicen) (Rogers and Kaplan 2005) and was shown a preference the right-eye and the left hemisphere for distinguish seeds from pebble. Furthermore, a similar result was found in another class (Common Wall Lizard (Podarcis muralis)) in the test of reaction to a predator (Martín et al. 2010; Bonati et al. 2013). This fact may indicate the specialization of a certain hemisphere for specific tasks.
In our study, birds showed opposite lateralisation biases in observing the disturbance source while swimming and flying. Swimming birds preferred to keep the disturbance source in the visual field of the right eye, while flying birds preferred to keep the disturbance source in the visual field of the left eye. Probably, the swans in flight perceive the presence of a plane as a more threatening situation and experience greater fear than when they are on the water, as a result, the right hemisphere of the brain is more active and the source of disturbance is monitored with the left eye. It was also demonstrated that Australian magpies had the visual lateralisation bias to the left eye when leaving from a predator (Koboroff et al. 2008) or from an approaching person (Hodges et al. 2001), and birds had visual lateralisation bias to the right eye when approaching the monitor lizard to study it during a state of low excitement (Koboroff et al. 2008). In another explanation, the swans in flight need to assess any tiny changes from the potential sources of danger and should immediately react to them. The right hemisphere and left eye are responsible for this task (Rogers 2019; Rogers and Kaplan, 2005). The right hemisphere is also responsible for better orientation in space ((Rogers 2002, 2019), in particular, relative to the plane. In contrast, at the moment when the plane is in the air and the swans are on the water, birds have more time and distance to determine which category the observed object belongs to and whether it will be dangerous. The system of the left hemisphere and the right eye responsible for determining a large difference in an environment (Halpern et al. 2005; Voeckler et al. 2006, Karenina and Gilev 2022) could be used in swimming.
Thus, under experimental conditions, different species can show similar patterns of visual lateralisation. However, in nature, environmental conditions are rich and varied, and some variations could affect the manifestation of the sensory lateralisation in the same type of behaviour.
We found a significant difference between observation task types (observation of the source of disturbance or leading bird). Birds had a significant bias in the observation of the source of disturbance and hadn’t in the observation of the leading partner. This result corresponds to the previous funding for White-fronted geese and Barnacle geese (Zaynagutdinova et al. 2020). In this study, geese had the visual lateralisation bias in following the partner throughout the entire annual cycle, but they hadn't any preferences under the disturbing conditions.
The presence of chicks didn't influence the lateralisation in most cases but strengthened the lateralisation bias for the following partners. This result is difficult to explain because, as far as we know, such work has not been carried out before.
We can conclude that the observation task and the type of locomotion could influence the manifestation of visual lateralisation and presence of chicks could strengthen it in one behaviour type in one species. Therefore, special attention should be paid to details in comparing the results of different studies conducted under different circumstances.
Ethical Approval
No approval of research ethics committees was required to accomplish the goals of this study because this work did not include the conducting experiments with animals. The animals have not been removed from their natural habitat.
Competing interests
The authors declare that there are no competing interests.
Authors' contributions
All authors contributed to the study conception and design. Data collection was performed by Sonia B. Rozenfeld. Material analysis and statistical analysis was performed by Elmira M. Zaynagutdinova and Diana R. Polikarpova. The first draft of the manuscript and figures was performed by Diana R. Polikarpova. The table was performed by Elmira M. Zaynagutdinova. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Funding
This work was supported by the Russian Science Foundation (grant no. 22-24-00346).
Availability of data and materials
Datasets analysed during the current study are available in the figshare repository, https://figshare.com/s/8c717fa43fc41bd6d170.
Acknowledgments: We would like to thank the Russian Goose Specialist Group for their organizational support.
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No competing interests reported.