Abstract Background Apart from findings on both functional and motor asymmetries in captive aquatic mammals, only few studies have focused on lateralized behaviour of these species in the wild. Methodology/Principal Findings In this study we focused on lateralized visual behaviour by presenting wild striped dolphins with objects of different degrees of familiarity (fish, ball, toy). Surveys were conducted in the Gulf of Taranto, the northern Ionian Sea portion delimited by the Italian regions of Calabria, Basilicata and Apulia. After sighting striped dolphins from a research vessel, different stimuli were presented in a random order by a telescopic bar connected to the prow of the boat. The preferential use of the right/left monocular viewing during inspection of the stimuli was analysed. Conclusion Results clearly showed a monocular viewing preference with respect to the type of the stimulus employed. Due to the complete decussation of the optical nerves in dolphin brain our results reflected a different specialization of brain hemispheres for visual scanning processes confirming that in this species different stimuli evoked different patterns of eye use. A preferential use of the right eye (left hemisphere) during visual inspection of unfamiliar targets was observed supporting the hypothesis that, in dolphins, the organization of the functional neural structures which reflected cerebral asymmetries for visual object recognition could have been subjected to a deviation from the evolutionary line of most terrestrial vertebrates.

Citation: Siniscalchi M, Dimatteo S, Pepe AM, Sasso R, Quaranta A (2012) Visual Lateralization in Wild Striped Dolphins (Stenella coeruleoalba) in Response to Stimuli with Different Degrees of Familiarity. PLoS ONE 7(1): e30001. https://doi.org/10.1371/journal.pone.0030001 Editor: Verner Peter Bingman, Bowling Green State Universtiy, United States of America Received: October 28, 2011; Accepted: December 8, 2011; Published: January 13, 2012 Copyright: © 2012 Siniscalchi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research is part of the following projects: “Jonian Cetacean Project” supported by the University of Bari, Italy, through a financial grantship to AQ, and “Cetacea” supported by Fondazione Cassa di Risparmio di Puglia, Bari, Italy, through a financial grantship to AQ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction Brain lateralization i.e. the different specialization of the left and right hemisphere is a phenomenon widespread among different animals [1]. Although several studies have reported the presence of both motor and sensory lateralization in aquatic mammals, at present very little information concerning cetecean functional asymmetries in the wild is available [2], [3]. Laterality in visual sensory domain has been reported in many species (fish: [1]–[7] chick: [8]–[11] dog: [12]) and, overall, results supported the general hypothesis that asymmetries in visual perception reflect the different specialization of the right (analysis of novelty/higher emotional valence stimuli) and the left (analysis of familiar stimuli) brain hemispheres. Visual analyses in bottlenose dolphins showed a general superiority of the right visual field (left hemisphere) for visual stimuli discrimination and for visual spatial tasks [13]–[16]. In accordance with these findings, Killian [17] reported a right-visual field advantage for discriminating relational dimensions between stimuli differing in numerosity in a two-choice discrimination paradigm. More recently, the influence of familiarity on the preferential use of one eye to look at human visual stimuli were tested in five captive dolphins and results showed that, at group level, dolphins preferentially use their left eye to look at both familiar and unfamiliar humans [18]. Regarding studies on behavioural laterality in the wild, several studies reported a right-side-down bias during feeding behaviour in gray whales [19] hump-back whales (bottom feeding) [20] and coastal bottlenose dolphins [21]–[23] which could be directly caused by laterality of eye use (right eye→left hemisphere→control of feeding behaviour). Moreover, two studies focused on the visual laterality of social interactions in wild cetacean. The first reported a population-level left-eye use in wild Indo-Pacific bottlenose dolphin (Tursiops aduncus) during flipper-to-body rubbing, in which one dolphin (“rubber”) rubs the body of another (“rubbe”) with its flipper [3]; the second report showed a similar left-eye preference during calf-mother interactions in wild belugas whales (Delphinapterus leucas), indicating that analysis of socially significant visual information occurs in both dolphins and whales in the right brain hemisphere [2]. Overall, these data demonstrate that asymmetries of eye-use in response to a visual stimulus could be influenced by stimulus characteristics (familiarity, novelty, complexity) [12], [4], [8] as well as subjects' characteristics (age, social environment) [18]. The novel aspect of this study was to investigate visual lateralization in striped dolphins (Stenella coeruleoalba) in response to objects of different degrees of familiarity “in the wild”.

Discussion Our results suggest that different stimuli evoked different patterns of eye use in wild striped dolphins: the fish target tended to be viewed with the left eye whereas both the toy and the ball targets were viewed with the right. Due to the complete crossover of the optic chiasm in dolphins, a right eye bias during visual inspection of “toy” and “ball” targets reflects an overall left hemisphere dominance for visual object processes confirming what has been reported previously in the bottlenose dolphin (Tursiops truncatus) and other cetaceans [26]–[30]. In particular, a clear right eye/left hemisphere advantage in a pattern discrimination and acquisition task was reported in adult bottlenose dolphins tested under monocular condition (the animal had to discriminate between simultaneously presented pairs of different patterns with a rubber eyecup fixed onto one of the subjects eyes) [14], [15]. In addition, several studies on dolphins housed in circular tanks reported a strong counterclockwise swimming direction bias: using this particular route, dolphins placed their right eye towards the enclosure wall and thus towards any events outside the pool which could be of importance for the dolphins favouring the activation of the left hemisphere when approaching or scrutinising objects [13]. More recently, Delfour and Marten [16] reported an advantage of the dolphins right visual field when processing different visual stimuli displayed on an underwater touch-screen (two-dimensional figures, three-dimensional figures and dolphin/human video sequences) supporting a left hemispheric dominance in visual information analysis. In contrast, a right eye/left hemisphere bias occurred during visual inspection of “fish” shaped target. This result is quite interesting since “fish” model represented the target with the highest degree of familiarity for dolphins. In a similar way, Sovrano [4] reported that, when accustomed to the presence of artificial stimuli, fish (Xenopoecilus sarasinorum) showed a left bias only when presented with a familiar version of these stimuli, but not when presented with an unfamiliar version. Overall our findings supported the hypothesis that, in dolphins, asymmetries in eye use during analysis of visual objects reflected a different specialization of brain hemispheres for visual scanning processes which is directly related to the amount of familiarity of the target: the initial learning process of a specific visual pattern (e.g. object's parts and their spatial relationships) have to be encoded separately before creating a stored structural description. This process that is mainly under the control of the left hemisphere (local details of stimuli) seems to occur in our experiment during right eye use in response to toy and ball targets (unfamiliar objects). On the other hand, when object's form has become familiar, its global shape can be directly matched to information stored in memory by configurational analyses (right hemisphere→global stimulus analysis) and this could explain the use of the left eye/right hemisphere in response to the fish target (familiar stimulus) [31]–[33]. Intriguingly, a different complementary specialization of the two hemispheres has been observed repeatedly in the vertebrate brain, in a variety of species (e.g., fish: [4], birds: [8]), with the right hemisphere taking charge of novel information followed by the left hemisphere taking charge of behaviour during visual analysis of familiar stimuli (see for reviews of evidence: [1], [8], [34], [35]). Thus, our data in line with the work of Killian et al [13] supported the hypothesis that, in dolphins, the organization of the functional neural structures which reflected cerebral asymmetries for visual object recognition could have been subjected to a deviation from the evolutionary line of most terrestrial vertebrates.

Acknowledgments We are grateful to Alessandro Quarta for his photographic technical assistance.

Author Contributions Conceived and designed the experiments: MS AQ. Performed the experiments: MS SD AMP RS AQ. Analyzed the data: MS SD AMP RS AQ. Contributed reagents/materials/analysis tools: MS AQ. Wrote the paper: MS AQ.