Ad. J. Kalmijn

Hydrodynamic and Acoustic Field Detection

Fishes have an impressive complement of hydrodynamic and acoustic sensors, commonly referred to as the lateral-line and inner-ear sense organs. The basic receptor elements are the hair cells, which detect the minute displacements imparted to their apical ciliary bundles (Fig. 4.1a). The directional sensitivity of the individual receptor cells is indicated by the asymmetric position of the single kinocilium relative to the several rows of stereocilia. Morphologically, the hair cells of the various sensory clusters are strikingly uniform. Their diversity in function is determined mainly by the peripheral structures coupling the ciliary bundles to the physical world that the animals inhabit.

Electro-perception in Sharks and Rays

SHARKS and rays are extremely sensitive to alternating electric fields. A potential gradient of only 0.1 µV/cm is sufficient to evoke in Scyliorhinus canicula a reflex contraction of the eyelids (“winking of the eyes”), and to affect the respiratory rhythm of Raia clavata (“spiraculum reflex”)1,2. Such a weak electric field is perceived with the ampullae of Lorenzini. The ampullae are not only very sensitive to thermal and mechanical influences as found electrophysiologically3–5, but also respond to electrical stimuli6–8. Partial denervation of the ampullary system makes the head of Scyliorhinus canicula insensitive to weak electrical stimuli in the area where the eliminated ampullae open9. In the past few years, our investigations have been focused on the biological significance of the electro-perception in sharks and rays.

Detection of Weak Electric Fields

Electric fields in natural waters present a wealth of sensory information. Bioelectric fields direct electrosensitive fishes to their prey, environmental fields provide important orientational cues, and the fields induced by the animals’ motion through the earth’s magnetic field offer oceanic species complete compass data. Particularly sensitive to electric fields are the marine sharks, skates, and rays, but the weakly electric fishes, the common catfishes, and several of the more primitive fishes are also known for their keen electric sense.

Experimental Evidence of Geomagnetic Orientation in Elasmobranch Fishes

Marine sharks, skates, and rays are endowed with an electric sense that enables them to detect voltage gradients as low as 0.01 μV/cm within the frequency range of direct current (DC) up to about 8 Hz. Their electroreceptor system comprises the ampullae of Lorenzini, which are delicate sensory structures in the snouts of these elasmobranch fishes. Sharks, skates, and rays use their electric sense in predation, sharply cueing in on the DC and low-frequency bioelectric fields of their prey. Swimming through the earth’s magnetic field, they also induce electric fields that may provide them with the physical basis of an electromagnetic compass sense. Their ability to orient magnetically has in fact been demonstrated in recent training experiments.

The Magnetic Behavior of Mud Bacteria

When separated from the substrate, Blakemore’s mud bacteria swim back to the bottom of the sea following the earth’s magnetic field lines. Their magnetotactic response appears to be due to the presence of internal ferromagnetic dipole moments of single-domain properties.

Physical Principles of Electric, Magnetic, and Near-Field Acoustic Orientation

To elucidate the weakly electric and earth’s magnetic sensory capabilities of sharks and rays and to introduce the concept of inertial hearing in the acoustic near field, this chapter discusses the physical features of the underwater world, the particular receptivities of the sense organs, and the spatial information the animals seek to orient at sea and to arrive at their prey. The objective is to establish the logical connections between the directional cues in the natural environment and the orientational responses they elicit from the animals. The features of the underwater world are presented in their most simple form, just as they are detected, processed, and perceived by the animals. In this chapter, we observe early fishes proficiently practice the laws of physics, purely from eons of experience. The remarkable similarity in the electric and lowfrequency acoustic fields of underwater objects is emphasized to reveal the close relationship between the two sensory modalities.

Magnetic Effects on Lower Organisms

Bacteria that orient and swim in a preferred direction in magnetic fields have been observed in diverse aquatic environments.1 These magnetotactic bacteria include a variety of morphologically distinct forms. Kalmijn and Blakemore2 found that these bacteria orient in uniform magnetic fields of about 0.5 G. Reversal of the geomagnetic field with Helmholtz coils caused the swimming bacteria to turn around in large U-turns and swim in the opposite direction. Killed bacteria also orient to align with imposed magnetic fields. Richard Blakemore