What Would it Mean if White Sharks, Carcharodon Carcharias, Possessed Disconjugate Optokinetic Stimulation?

The white shark, Carcharodon carcharias, a typical apex predator, relies on a keen sense of vision to hunt down agile prey, in particular pinnipeds such as seals and sea lions [1-3]. It follows that a considerable proportion of the white shark’s brain would be dedicated to processing visual stimuli to enable efficient hunting [4]. As with other shark species, the eyes of white sharks are positioned laterally, meaning that only one eye at a time can observe an object positioned alongside their bodies, and only when the object is between the overlapping fields of vision could both eyes focus on the same object. So, what potential advantages could white sharks acquire if they were able to move both eyes independently, and so observe two objects on both sides of their heads simultaneously?

Disconjugate optokinesis, the ability to move both eyes independently, is a feature that is known to occur in some aquatic animals. While most bony fishes have yoked or conjugate vision [5-7], some species have the ability to move both eyes independently [5,8,9]. Since sharks’ eyes are positioned similarly to those of bony fishes (except for a few species, e.g., the bigeye thresher shark, Alopias superciliosus), it is reasonable to assume that their vision is also characterized by conjugate optokinesis. However, optokinesis has not yet been studied in sharks, so it is not known whether their eyes indeed function in a yoked manner.

The concept that white sharks may utilize a mechanism that could employ more independent eye movements stems from video-evidence. In the video, a white shark seems to use both visual axes to observe objects on opposite sides of its body simultaneously, leading to the possibility of disconjugate optokinesis. This potential ability would confer a considerable advantage when hunting, allowing a shark to scan the areas on both sides while, for instance, closely surveying pinniped haul-outs [10-13]. Disconjugate optokinesis would likewise be useful in efforts to prevent kleptoparasitism; the stealing of already immobilized or killed prey by other white sharks [14]. Such advantages would no doubt largely contribute to the effectiveness of a white shark’s foraging strategy. It is understood that no firm conclusion can be drawn from this single video, but it offers an intriguing perspective into the potential use and selective advantage of disconjugate eye movement among white sharks.

The video was captured on November 21, 2017, off the coast of Guadalupe Island, Mexico. An approximately 4m long male white shark can be seen circling a cage positioned at the surface. Bait was also placed on the surface about 5m distant directly opposite from the videographer in the cage. The video was shot with 1080i and 120fps. Where necessary, sequences were analyzed frame-by-frame, using Final Cut Pro X (version 10.4.8) by Apple® and sequential pictures examined at intervals of 1/60 second. The shark’s left eye motions were interpreted primarily based on changes in the positions of its lens relative to the outer rim of its eye socket.

Chronology of the encounter

The shark made several passes by the side of the cage facing the videographer, during which it maintained an average relative speed of approximately 0.3 tailbeats/second. During one of these passes that started in a slight ascent, the shark approached, based on its longitudinal axis, in the general direction of the videographer and so seemed to look directly at him. As the shark drew closer, its eye contact with the videographer became confined to the shark’s left visual field. Once the shark was closest to the videographer, its left eye was slightly above the videographer’s head but stayed fixed on him. As the shark’s head started to turn away from the videographer, the left eye, which could not see the surface-positioned bait on the other side of the head, kept focusing on the videographer. The left eye stayed in this fixed position until the field of vision of the left eye could also catch sight of the bait; at that point, that eye moved in a slightly temporo-nasal direction to enable a stereoscopic view of the bait. Since the turn of the head was swift, with only 0.70 seconds elapsing until the shark aligned the entire frontal portion of its body with the bait, the left eye remained on the diver no longer than 0.40 seconds after it began to turn its head. The presented observation can be gathered from the supplementary video.

The main driver of an animal’s visual system seems to be its foraging ecology [15]. Given the high speed and agility of the animals on which white sharks feed, in particular, pinnipeds [14,16,17], their visual system needs to be highly evolved. Among the strategies that white sharks have developed for attacking such swift prey [14,17,18], their primary preference seems to be to ambush from behind and below [12,16-18]. When a shark is approaching a loose group of pinnipeds, various potential targets may present themselves at the same time on either side of the shark. Thus, in such situations, the shark must decide which member of the group to attack. It could be invaluable to the shark to have the ability to observe potential targets with each eye working independently at the same time, essentially doubling the area that it can survey. First, we discuss the very moment of the video that offers potential evidence that could indeed indicate some form of independent eye movement and debate this possibility from different perspectives. We then look at this potential ability from the viewpoint of how it could enhance a white shark’s hunting behavior.

Disconjugate eye movements

The precise moment on the video that indicates the potential existence of independent eye movements is when the shark’s head turned away from the diver before the left eye-which was still fixed on the videographer- and was able to see the bait. This very moment indicates that the shark must have been aware of the exact position of the bait, while still looking at the diver with its left eye. The ability to compare two objects in opposite fields of view has been demonstrated in such teleosts as sandlances, Limnichthyes fasciatus, and pipefish, Corythoichthyes intestinalis [5,6,9]. These species can perform the operation described above, fixing one eye on a stationary object. In contrast, the opposite eye proceeds to follow another stimulus or, in the case of such species as pipefish and goldfish, Carassius auratus, moving their eyes independently when surveying their surroundings but in a coordinated fashion when tracking a target [6,19]. Butterflyfishes, Chaetodon rainfordi, and red-eared sliders, Pseudemys scripta, on the other hand, display a more yoked form of optokinesis but can operate their eyes independently during specific responses [6,20].

The observation of a white shark, as seen in the video footage, could be similar to any of the above visual configurations. Another possibility could be that the shark could have shifted its focus alternately between its two eyes. Kirmse [21] suggests during such a shift that the visual input from the less attended eye would gather continuous information until a more conspicuous target within the entire visual field is selected, at which point the animal would adopt binocular vision. However, it is unlikely that visual information from the less attended eye remains unprocessed owing to the blocking or suppression of the fovea, the minute depression in the retina where vision is most acute, as has been observed in other animals, including some bird species [22-24].

Additionally, there is the possibility of cognitive mapping [25-27]. Could the white shark have memorized the exact position of the bait relative to the cage from a distance where both objects were still in its binocular vision, during its first few passes, and then just acted on it? The cognitive mapping may indeed play a role in the chronology of this event, but it would not indicate what the right eye was doing during the encounter with the videographer. At this point, the possibility cannot be excluded that at least some degree of independence between the two shark’s eyes could exist, allowing the ability to keep track of two visual targets, one within each of its visual fields simultaneously. The fact that the white shark changed its head direction before the bait entered its left field of vision suggests that its right eye had indeed kept the bait in view, at least peripherally within its functional or retinal visual field [28,29], but possibly on a lower level of processing, until the shark’s primary focus shifted [30].

If white sharks did possess disconjugate eyesight, then each eye would also focus independently of the other. This capacity would be especially crucial for tracking objects that are at unequal distances from the two eyes. Focusing on multiple objects in this way would likely be challenging, with the oscillating head movements of the white shark while swimming necessitating gaze stabilization and fixation [31]. However, such a mechanism has already been documented in tadpoles, which compensate for the retinal shifting caused by their form of locomotion through compensatory movements of the eyes and head [32]. Since previous research suggests that sharks prefer to keep their eyes as stable as possible to limit optic flow [7,33], they would thereby obtain the highest resolution possible with the least amount of blur.

Could light intensity also play a factor?

In some regions, white sharks prefer to attack pinnipeds in low light conditions [14,34,35], and several studies have shown that sharks maintain a delicate balance between detectability and visibility when chasing their prey [11,16,36]. Thus, the fovea, where visual acuity is highest, of white sharks consists primarily of the rod photoreceptors that are used in low-light situations [37], likely as a result of this species’ adaptation to hunting in such conditions [10,14,35]. Although the reaction time of rods is slower than that of cone photoreceptors, which are used for color vision [38-40], the latter is likely unimportant for this species owing to this hunting preference of dark-colored pinnipeds. Through the use of eyes, and thus fovea, with independent movement, a shark could determine which prey to follow based on improved contrast.

Disconjugate eye movement and white sharks

The success rate of a white shark when attacking fast-swimming prey such as seals is close to 60% during its preferred low-light conditions [35]. This is quite astonishing, considering the agility of pinnipeds. Therefore, it cannot be rejected that this high success rate could be due to the ability to observe more than one potential target and to scan the entire visual field with two eyes functioning independently. In light of the potential existence of disconjugate eye movement in sharks, research should investigate the fitness benefits of this conceivable characteristic, for example, by performing a choice experiment in which two food sources of different caloric values are offered simultaneously to an approaching shark.

Fitness benefits are a constant mechanism in the evolution of animals, so if this phenotype exists, it also must have been a force throughout the evolution of Carcharodon. The first species of this lineage likely appeared in the Thanetian period approximately 55 million years ago [41]. Although there is not much known regarding how these early sharks hunted, they already possessed serrated, sawblade teeth, enabling them to feed on early marine mammals, and then seals in the present evolutionary period [42-44]. Considering that the agility of pinnipeds likely improved over time, optimizing eye use in Carcharodon to the extent discussed here, could have helped to turn white sharks into the most overpowering super predators among today’s shark species.

We thank “Pro Win Pro Nature” for financially supporting this project.

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