Abstract
The electrosense of sharks and rays is used to detect weak dipole-like bioelectric fields of prey, mates and predators, and several models propose a use for the detection of streaming ocean currents and swimming-induced fields for geomagnetic orientation. We assessed pore distributions, canal vectors, complementarity and possible evolutionary divergent functions for ampullary clusters in two sharks, the scalloped hammerhead (Sphyrna lewini) and the sandbar shark (Carcharhinus plumbeus), and the brown stingray (Dasyatis lata). Canal projections were determined from measured coordinates of each electrosensory pore and corresponding ampulla relative to the body axis. These species share three ampullary groups: the buccal (BUC), mandibular (MAN) and superficial ophthalmic (SO), which is subdivided into anterior (SOa) and posterior (SOp) in sharks. The stingray also has a hyoid (HYO) cluster. The SOp in both sharks contains the longest (most sensitive) canals with main projections in the posterior-lateral quadrants of the horizontal plane. In contrast, stingray SO canals are few and short with the posterior-lateral projections subsumed by the HYO. There was strong projection coincidence by BUC and SOp canals in the posterior lateral quadrant of the hammerhead shark, and laterally among the stingray BUC and HYO. The shark SOa and stingray SO and BUC contain short canals located anterior to the mouth for detection of prey at close distance. The MAN canals of all species project in anterior or posterior directions behind the mouth and likely coordinate prey capture. Vertical elevation was greatest in the BUC of the sandbar shark, restricted by the hammerhead cephalofoil and extremely limited in the dorsoventrally flattened stingray. These results are consistent with the functional subunit hypothesis that predicts specialized ampullary functions for processing of weak dipole and geomagnetic induced fields, and provides an anatomical basis for future experiments on central processing of different forms of relevant electric stimuli.
Highlights
The transduction and encoding of directional information from an external stimulus is critical for localization of other organisms and environmental cues
Both the ampullary chamber and canal are filled with a continuous ion-rich hydrogel that has similar dc conductivity but different electrical admittance properties than seawater that contribute to frequency response properties [11,12,13]
Array morphology The adult hammerhead shark had a total of 1362 ampullae on the left side of the head and the greatest number for any of our study species, with 45% of pores on the dorsal surface of the head and 55% of pores on the ventral surface (Table 1)
Summary
The transduction and encoding of directional information from an external stimulus is critical for localization of other organisms and environmental cues. The identification and location of a target can involve different processing of stimuli that originate from a visual [1], chemical [2,3] or acoustic [4,5,6] target Some organisms such as bats actively query the environment with self-generated acoustic pulses [7,8] or electric stimuli as in some teleost fish [9,10]. The receptor cells function as voltage detectors in the lumen and encode the potential difference between the apical membrane in the lumen and the basal membrane in the surrounding extra-ampullary tissues [14] These stimuli control release of neurotransmitter that modulates the discharge rates of primary afferent neurons that convey neural codes to the brain. Behavioral experiments demonstrate lower orientation thresholds of 2 gV/cm [19]
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