Gymnotiform fish: truly “shocking” creatures

by Rahul Nalamasu, Pitzer 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].

In the vast expanse of the aquatic realms, certain fish have evolved a truly “shocking” sensory system. For a second, imagine that you are walking down the street. Then, out of nowhere, you feel someone running up behind you. But, you can’t hear, see, or smell them. Instead, you sense them based on the disturbance of an electric field around you. If you were an electroreceptive fish, interactions like this would occur on a daily basis.

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Figure 1: South American knife fish (Gymnotus ssp.) are a lineage of weakly electric fish [by Clinton & Charles Robertson – Flickr: Gymnotidae Gymnotus sp, CC BY 2.0]

Gymnotiformes (South American knife fish, Figure 1), represent one of the present day groups of weakly electric fish. For many years, knife fish have been a subject of study due to their unique electroreceptive ability. Gymnotiform fish have the ability to emit an electrical field using a specialized electrical organ (EO) consisting of modified muscle cells, located on their underside (Pedraja et al. 2016). This organ emits wave-like discharges, referred to as Electrical Organ Discharges, or EODs. These EODs are controlled by a section of the gymnotiform brain called the pacemaker nucleus (Salazar et al., 2013). As the name suggests, this set of specialized neurons acts as a control mechanism for the pace of release of EODs, which are then interpreted by channel-like structures on the skin (Figure 2; Salazar et al., 2013). As electrical impulses travel through the channels on the highly conductive skin, they are interpreted by the pacemaker nucleus and its supporting cast, the sublemniscal and central posterior pacemaker nuclei (SPPN and CP respectively), which relay information to different areas of the body surface through which electrical output is delivered (Salazar et al., 2013). These structures dictate the speed and intensity of the EOD, helping knife fish respond to changes in their surroundings quickly and efficiently.

While these weakly electric fish swim, they constantly put out EODs at different rates, and can interpret changes in their own EOD’s to inform themselves about their surroundings. Gymnotiforms come in contact with many different types of organisms and obstacles and are essentially in constant motion. To have a functioning electroreceptive sensory system, they need to constantly adjust their sensory neurons to interpret different stimuli for their electroreception to be effective (Marquez et al., 2013).

In their lab in Uruguay, Pedraja et al. studied the implications of EOD sensing in antagonistic interactions of knife fish. They focused on the role of EODs in aggressive or competitive behavior, as they were curious as to how size difference plays a role in the aggressive behaviors of gymnotiform fish. Much like our own fight or flight syndrome, when gymnotiform fish encounter competitive scenarios, they assess whether or not to act in an aggressive manner to secure territory or resources.

To evaluate how interpretation of size plays a role in these decisions, Pedraja et al. placed two knife fish of different sizes in the same tank, separated by a partition for 2 hours (Figure 2, Panel A; Pedraja et al., 2016). This partition prevented fish from communicating with their contender via electrical signals. Next, the researchers turned off the lights and allowed the fish to acclimate for 10 minutes. Afterwards, the researchers removed the partition and observed the behaviors of the two fish, which couldn’t use any visual signals to evaluate their opponent because of complete darkness. Sizing up their contender had to be done with their electroreception (or possibly with their lateral lines).

To record the unfolding scene, the researchers fitted the electrically isolated enclosure with 2 sets of electrodes on opposite sets of walls. The water was kept at roughly 20 degrees Celsius, which has been found in many other experiments to be ideal for gymnotiform EOD, and the subjects were filmed at 30 FPS from below, with the tank illuminated by infrared light (Pedraja et al., 2016).

The larger fish emerged as the winner in most rounds, showing its dominance by driving away its smaller contender on three consecutive attacks without eliciting a counter strike (Pedraja et al. 2016). If knife fish were capable of assessing the size of their opponent by using their electric sense one might think smaller knife fish wouldn’t pick a fight with a larger contender, but that was not the case. It is of course possible that the very much constrained arena didn’t leave them much of a choice, and behavior in natural habitats may well be different. However, through observations of behavior during interactions and modeling of electric fields Pedraja et al. provide evidence to support that the detection and interpretation of electric fields in antagonistic behaviors plays an important role.

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Figure 2: Stills and schematics of the experimental procedure used by Pedraja et al. (2016).

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Figure 3: Size effect on dominance in the gymnotiform pairs. Data show that larger gymnotiforms are statistically significantly more dominant than smaller fish (Pedraja et al., 2016).

Now, all of this is interesting as it illustrates how electric fields can be used by fish to monitor their surroundings, but you’re probably sitting there reading this, thinking “why does all of this matter to me? I’m not a fish.” Well, the basic principles behind gymnotiform electrolocation have much potential to revolutionize the operation of robotic technology in deep-sea exploration. It is a well-known fact that our exploration of the vast ocean has been all but comprehensive. As of now, our exploration of the vast depths of the oceans is quite limited by the availability of light in deep sea conditions. However, the principles behind gymnotiform electroloction may prove to be useful in expanding our horizons, so to speak. If we could use the same bio-electroreceptive principles utilized by gymnotiforms, it would be possible to have unmanned submarines accurately and thoroughly depict deep-ocean life and the unseen wonders it has to offer (MacIver et al., 2001, 2004).

References

MacIver, M.A. and M.E. Nelson 2001 Toward a biorobotic electrosensory system. Autonomous Robots 11(3), 263–266.

MacIver, M.A., Fontaine, E., and J.W. Burdick 2004 Designing future underwater vehicles: principles and mechanisms of the weakly electric fish. IEEE Journal of Oceanic Engineering 29(3), 651-659.

Márquez, B.T., Krahe, R., and Chacron, M.J. 2013 Neuromodulation of early electrosensory processing in gymnotiform weakly electric fish. Journal of Experimental Biology 216, 2442–2450.  DOI 10.1242/jeb.082370

Pedraja, F., Perrone, R., Silva, A., and R. Budelli 2016 Passive and active electroreception during agonistic encounters in the weakly electric fish Gymnotus omarorum. Bioinspiration and Biomimetics 11(6).

Salazar, V. L., Krahe, R., and J.E. Lewis 2013 The energetics of electric organ discharge generation in gymnotiform weakly electric fish. Journal of Experimental Biology 216, 2459–2568. http://doi.org/10.1242/jeb.082735

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