By Kimberly Coombs (Claremont McKenna College) [Edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only].
Sharks are most commonly known as visual predators; however, this does not tell the whole story of why sharks are such successful predators. It is true that sharks have highly developed vision. Yet, sharks actually rely upon a variety of different senses that have allowed them to evolve as apex predators of the oceans. For example, sharks rely upon hearing, their lateral line, electroreception, and chemoreception (Hart & Collin, 2015). All of these senses are important for sharks to be effective hunters and maintain their position at the top of the food chain. What happens if a shark loses one of its senses (i.e., that particular sense is no longer functional)? This is exactly what O’Connell and his fellow colleagues decided to study.
O’Connell et al.were specifically interested in lemon sharks’ detection of magnetic fields when visually deprived, such as when they are in turbid waters (poor visibility waters). Sharks’ ability to sense magnetic and electrical fields was first discovered in 1935, when blindfolded small spotted catsharks, Scyliorhinus canicula, demonstrated escape responses when a steel wire was brought near their heads (Hart & Collin, 2015).
In order to test shark magnetic field detection, the authors gathered 24 juvenile lemon sharks (14 male, 10 female) of roughly the same size and placed them in a holding pen. They set up an experimental pen that contained three compartments (experimental arena, recovery and acclimation pen, and a corridor). The experimental arena was further split into four zones: magnet zone, control zone, separation, and observation. The control and magnet zones were identical in that they both had three 1.75m tall polyvinyl chloride (PVC) columns facing perpendicular to the ground. However, the control zone had sham magnets or clay bricks placed in the PVC, while the magnet zone had grade C8 barium ferrite magnets placed in the PVC (Figure 2).
They denoted four different types of treatments for the sharks and had six sharks per treatment. The treatments consisted of a control (no manipulation to the sharks vision), procedural control ‘eyebrow’ (sharks had one suture above each eye), procedural control ‘one eye’ (sharks had either the left or the right nictitating membrane closed), and ‘visually deprived’ (sharks had both nictitating membranes closed). Hold up, what is a nictitating membrane you ask? Well, the nictitating membrane acts as an opaque third eyelid in several species, such as sharks. The upper and lower eyelids of sharks are mostly immobile; therefore, the nictitating membrane may be drawn over the eye (essentially, the nictitating membrane acts as our eyelids do when we blink) (Gruber & Schneiderman, 1975; Figure 3).
After surgery was complete, experimental testing began. O’Connell et al. had one shark enter the experimental arena at a time and three different behaviors were recorded for a 30min testing period: entrances (shark went to observation zone and swam through the PVC), visits (shark swam in one of the observation zones), and avoidances (shark changed direction suddenly and/or accelerated away after visiting one of the observation zones).
O’Connell et. al. found that juvenile lemon sharks do rely heavily on their electrosensory system to forage and navigate through turbid waters. They discovered that the magnets acted as a repellent for the sharks, causing the sharks to change their swimming behavior abruptly in order to avoid the magnets. This is consistent with other studies that found that white sharks also avoid magnets placed in the water (O’Connell et al., 2014). The authors further found that the visually deprived sharks got the closest to the magnets before exhibiting an avoidance behavior than the other experimental shark groups (Figure 4).
They believe this could be due to the electrosensory system of the sharks operating on a shorter range than vision. The control and the one eye sharks were farthest away from the magnets when they exhibited an avoidance behavior, which O’Connell et al.believe is due to both their visual and electrosensory systems being stimulated. The visually deprived sharks visited the magnet zone more frequently than the other shark types, yet they entered through the PVC much less than the other sharks (Figure 5, 6).
This result suggests that when lemon sharks are more visually deprived, they rely more heavily on electroreception. This is congruent with other studies that have shown a reliance on short-range senses, such as electroreception and mechanoreception, when environmental parameters restrict vision (Hutchinson et al., 2012, O’Connell et al., 2014). Though the authors’ method of simulating turbidity may have been invasive and not exactly representative of what it would be like in the natural environment, this is the first study to show evidence of context-dependent switching (the ability to change behavior in response to the current biological and ecological state) in shark electroreception.
So what? Why should you care? Well, this is very important from an evolutionary standpoint. Since context-dependent switching has been found in sharks, it is highly possible that this ability may also be found in other elasmobranchs. In fact, context-dependent switching has been documented in other organisms, such as teleosts, mammals, and amphibians (O’Connell et al., 2014)-. This indicates that context-dependent switching probably evolved with a common ancestor of elasmobranchs, teleosts, mammals, and amphibians. Studies should be looking into whether other elasmobranchs have this capability as well as where in the tree of life did species start to demonstrate context-dependent switching.
Furthermore, it is not presently known if suturing closed the nictitating membrane of sharks represents how these sharks would respond in natural turbid waters. If it is accurate, the authors suggest that using magnet repellents in the field would be successful at manipulating shark behavior in turbid water environments. Meaning that if accidental shark attacks and shark bycatches wanted to be avoided, magnets should be placed in the water as sharks will avoid these areas. Future studies should be focused on examination of turbid water conditions, as this factor might be the quintessential factor for determining the most successful repellents to use in turbid waters. Also, studying turbid water conditions will aid in the understanding of how and why sharks’ change the senses they rely upon in these conditions. Researchers should look at the effectiveness of magnetic repellents in areas that are well known as being turbid, such as inshore areas influenced by eutrophication, runoff, and riverine input. Such studies should further look at the impact magnetic repellents have on other species besides sharks, as these repellents may have a negative impact on other species and could cause a change in the ecology of the area the repellents are emplaced.
Gruber, S.H., Schneiderman, N. 1975. Classical conditioning of the nictitating membrane response of the lemon shark (Negaprion brevirostris). Behavior Research Methods and Instrumentation 7(5), 430-434.
Hart, N.S., Colling, S.P. 2015. Sharks senses and shark repellents. Integrative Zoology 10, 38-64. (DOI: 10.1111/1749-4877.12095).
Hutchinson, M., Wang, J.H., Swimmer, Y., Holland, K., Kohin, S., Dewar, H., Wraith, J. Vetter, R., Heberer, C., Martinez, J. 2012. The effects of a lanthanide metal alloy on shark catch rates. Fisheries Research 131-133, 45-51. (DOI: 10.1016/j.fishres.2012.07.006).
O’Connell, C.P., Andreotti, S., Rutzen, M., Meÿer, M., Matthee, C.A., He, P. 2014. Effects of Sharksafe barrier on white shark (Carcharodon carcharias) behavior and its implications for future conservation technologies. Journal of Experimental Marine Biology and Ecology 460, 37-46. (DOI:10.1016/j.jembe.2014.06.004).
O’Connell, C.P., Guttridge, T.L., Gruber, S.H., Brooks, J., Finger, J.S., He, P. 2014. Behavioral modification of visually deprived lemon sharks (Negaprion brevirostris) towards magnetic fields. Journal of Experimental Marine Biology and Ecology 453, 131-137. (DOI: 10.1016/j.jembe.2014.01.009).