Wild birds inspect food objects asymmetrically and this helps them to feed efficiently

Wild pigeons show visual lateralization in feeding and its direction depends on the type of food objects. Moreover, one-eye preferences impact pigeons’ feeding success. This is an illustrative example of brain lateralization being a plastic adaptation to ecological demands.
Published in Ecology & Evolution
Wild birds inspect food objects asymmetrically and this helps them to feed efficiently

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Many of us have watched birds eating berries or fruits one by one. This simple behaviour (perhaps like any other) is much more interesting than it might look. Our new study revealed that wild fruit-eating pigeons prefer different (left/right) eyes to inspect the fruits and flowers for edibility which seems to be an adaptation for feeding on different types of food objects.

Asymmetrical functioning of the nervous system and associated al lateralizations (one-sided biases in behavioural responses) is intriguingly widespread across animals. Current theories agree that the emergence of asymmetry of brain and behaviour is underpinned by fitness benefits, and the growing amount of empirical evidence suggests that it is indeed. The prevalence of lateralization in the animal kingdom implies that individuals with lateralized cognitive functions and lateralized reactions get selective advantages over non-lateralized individuals. To date, however, we have a very limited understanding of why a particular side is preferred in a particular process and what benefits does this preference confer. The knowledge we do have is based predominantly on the results obtained under controlled conditions of laboratory experiments. Acknowledging the importance of these findings, we emphasize the need to intensify investigations in natural habitats of species to examine the relevance of brain lateralization under ecological pressures.

The visual system of birds is a well-established research model to investigate the function of brain lateralization. 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. In many bird species, the eyes are positioned laterally on the sides of their head and the visual fields of the two eyes are largely independent with only a small binocular overlap. As a result, the viewed stimuli cannot be seen binocularly for much of the time and birds adopt independent scanning movements to inspect the environments, for example, during foraging. The preferred side, on which the bird is turning its head to use the monocular visual field, can serve as a marker to measure visual lateralization.

In our study, preferences for the left or right eye use in feeding were examined unobtrusively in wild yellow-footed green pigeons, Treron phoenicoptera. The aim of the study was to investigate lateralized behaviour of birds in feeding situations resembling those in the previous laboratory experiments but occurring naturally in the wild. We observed pigeons feeding on two types of food differing in visual characteristics and spatial distribution. One type of food was flowers of Mahua tree, Madhuca longifolia, larger and more discrete, uniformly coloured objects which can be present or absent in the patch viewed by a pigeon. The focus on the food detection resembled the requirements of the experimental task with scattered grains used to test the lateralization of visuospatial attention in birds. Another type of food, sacred fig, Ficus religiosa, was a smaller and more abundant food object with colour cues signalling its ripeness. In this case, the need to distinguish ripe fruits from those not ready to consume resembled the conditions of the pebble-grain test used to study the lateralization of birds’ discrimination abilities.

Figure 1 Monocular inspection prior to feeding on two types of food objects by a yellow-footed green pigeon

We observed pigeons during their feeding visits to trees in the rural areas bordering the national parks in Madhya Pradesh, India.  The time for fieldwork was chosen to take full advantage of drought providing good visibility due to almost absent foliage. For each individual pigeon, we recorded every peck during the feeding visit. When looking for food, pigeons followed the pattern of visual search typical for birds with primarily monocular. After approaching the branch tip where most flowers/fruits were clustered, the birds examined the patch monocularly. Based on the head position, we recorded the eye (left/right) used for monocular inspection of the patch prior to peck. Whether or not the peck was successful was assessed based on the presence of swallowing head movement after the peck.

The pattern of lateralization we showed in wild birds appeared to correspond to the specific properties of the left and right brain hemispheres known from the lab studies, bridging the knowledge obtained using the experimental and observational approaches. In experimental settings, birds demonstrate left eye–right hemisphere preference in the tasks requiring attention to the spatial location of potential food objects. In line with this, green pigeons preferentially inspected the patch of mahua flowers just before pecking with their left eye, implicating the right hemisphere advantage. When feeding on mahua flowers, pigeons are looking for the presence of edible flowers with thick fleshy corollas among immature or decayed flowers that requires systematic searching with the attention to spatial relations between objects.  As these are known properties of the right hemisphere, the left-eye preference found in pigeons feeding on flowers corresponds to the general pattern of hemispheric functions.

In contrast, when feeding on sacred fig fruits, pigeons demonstrated a general preference for the right eye. Smaller food objects, sacred figs, are more numerous and scattered within a single patch and have colour cues signalling its ripeness, with ripe fruits preferred by birds. Choosing a ripe fig to consume, a pigeon faces many alternative targets placed close together and belonging to different categories of ripeness. Previously, the right eye (left hemisphere) advantage for discrimination of food and non-food objects has been found in several bird species in the experimental tasks. In addition, the left brain hemisphere plays the dominant role in colour discrimination in pigeons, implying that discrimination of ripe figs by colour may trigger left-hemispheric processing and preferential right-eye use.

Figure 2 Visual lateralization in the green pigeon: when feeding on mahua flowers (left), the significant majority of lateralized individuals showed the preference to view the patch with the left eye (LE) prior to pecking. In contrast, when feeding on sacred fig fruits (right), the majority of lateralized pigeons preferred to use the right eye (RE). *p < 0.05

While both left- and right eye preferences have been previously found in separate studies on birds, our results indicate that birds can adopt distinct lateralized viewing strategies depending on the cognitive demands of the particular feeding situation in the wild. Specific characteristics of the food objects may trigger different hemispheric dominance, and green pigeons rely on the hemisphere providing more advantages for the consumption of the particular type of food. Our study, corroborating previous research, do not indicate any specialization of one hemisphere on the control of feeding but demonstrate the flexibility of hemispheric dominance as a plastic adaptation to ecological demands. The flexibility in adopting hemispheric-specific processing strategies depending on the feeding context may be crucial for understanding fitness advantages associated with lateralization.

We further explored the link between visual lateralization and individual success in foraging. First, we compared the number of pecking errors (pecks not resulted in food consumption) when feeding on mahua flowers in lateralized and non-lateralized pigeons. Lateralized pigeons (with significant visual preferences) were more successful in pecking food items suitable for consumption, demonstrating the impact of lateralization on food discrimination accuracy. Second, we found that feeding accuracy was higher when the individuals with the right-eye preference used their right eye and the individuals with the left-eye preference used their left eye to examine the patch prior to pecking. That is, regardless of the direction of preference, the use of the preferred eye provided better discrimination of food items.

Another analysis we used to test the link between lateralization and feeding success was based on the comparison of feeding efficiency reflected in ingestion rate (food items consumed per minute) between lateralized and non- lateralized pigeons. Faster consumption can be especially advantageous in the case of foraging on a fruiting (flowering) tree when the food is available only for a limited time, and there are numerous hetero- and conspecific competitors around. Our results showed that the lateralized individuals outperformed their non-lateralized counterparts in feeding efficiency. Besides faster consumption, lateralized pigeons started to feed sooner after landing on a tree than their non- lateralized counterparts. This suggests a higher speed of decision making in lateralized pigeons and highlights general differences in the al patterns of individuals with different levels of lateralization. To conclude, our study illustrates the fitness consequences of lateralization for animals in their natural environments. The results support the growing amount of evidence for a positive association between the strength of lateralization and cognitive performance.

 Link to paper: https://doi.org/10.1002/ece3.8598

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Life Sciences > Biological Sciences > Ecology