Multisensory Contributions to the Shelter-Seeking Behavior of a Mormyrid Fish, Gnathonemus petersii Günther (Mormyridae, Teleostei): The Role of Vision, and the Passive and Active Electrosenses

This study examined how weakly electric fish, Gnathonemus petersii, integrate multiple sensory modalities (passive and active electrosenses, and vision) to maintain proximity to tubular structures, serving as the fish’s hiding place or shelter during the daytime. By moving the shelter along a linear 2-meter path, causing a mechanical disturbance, we challenged the fish’s shelter-seeking behavior and used the length of travel that shelter proximity was maintained (contact distance) as an indicator of how well the animal maintained its shelter. In order to determine the contribution of vision and electrosense to this behavior, four groups of fish were tested in which: (1) all three modalities were intact; (2) vision alone was eliminated by optic nerve transection; (3) the active electrosense was silenced by spinal cord transection rendering the electric organ inoperative; and (4) both vision and active electrosense were deactivated. Further elimination or minimization of various sensory cues was achieved by testing the fish with optically transparent, acrylic shelters (Plexiglas) that stimulate active, but not passive, electrosense, and aluminum shelters that theoretically stimulate all three modalities. As expected, performance was optimal when all three modalities were operating, but better than expected from quantitative models based on additive processes alone. Although the absence of one sense (vision or active electrosense) caused initial deficits, these were fully compensated for over repeated daily exposure to the task, suggesting that learning might generate sensory substitution and/or the formation of sensory expectation. Finally, environmental conditions, such as shelter opacity, also affected shelter-seeking performance, sometimes in a negative direction. These results demonstrate that: (1) the integration of multiple sensory inputs in G. petersii can be synergistic, additive, redundant, or even inhibitory, and (2) multisensory processes also take into account the respective sensory cues; i.e. (a) the prevailing ambient light intensity and optical qualities of the object; (b) the geometry and strength of the DC potential emanating from the object (‘battery effect’); and (c) the complex perceived impedance differential with the surrounding medium.