The Neuroecology of the Elasmobranch Electrosensory World: Why Peripheral Morphology Shapes Behavior

Abstract

The adaptations of elasmobranch sensory systems can be studied by linking the morphological structure with the natural behavior and ecology of the organism. This paper presents the first step in a ‘neuroecological’ approach to interpret the spatial arrangement of the electrosensory ampullary organs in elasmobranch fishes. A brief review of the structure and function of the ampullae of Lorenzini is provided for interpretation of the organ system morphology in relation to the detection of dipole and uniform electric fields. The spatial projections of canals from discrete ampullary clusters were determined for the barndoor skate, Raja laevis, based upon a published figure in Raschi (1986), and measured directly from the head of the white shark, Carcharodon carcharias. The dorsoventrally flattened body of the skate restricts the projections of long canals to the horizontal plane. There is a distinct difference between dorsal and ventral projection patterns in all groups. Notable within-cluster features include a relatively long canal subgroup in the dorsal superficial ophthalmic (SOd) and dorsal hyoid (HYOd) clusters that are oriented parallel (bidirectionally) to the longitudinal axis of the body. It is postulated that this subgroup of canals may be important for detection and orientation to weak uniform fields. Ventral canal projections in the skate are primarily lateral, with the exception of the hyoid (HYOv) that also projects medially. This wide dispersion may function for the detection of prey located below the body and pectoral fins of the skate, and may also be used for orientation behavior. The mandibular canals located near the margin of the lower jaw (of both study species) are ideally positioned for use during prey manipulation or capture, and possibly for interspecific courtship or biting. The head of the white shark, which lacks the hyoid clusters, is ovoid in cross section and thus ampullary canals can project into three-dimensional space. The SOd and superficial ophthalmic ventral (SOv) clusters show strong rostral, dorsal and lateral projection components, whereas the SOv also detects rostral fields under the snout. In the sagittal plane, the SOv and SOd have robust dorsal projections as well as ventral in the SOv. Most notable are canal projections in the white shark buccal (BUC) ampullary cluster, which has a radial turnstile configuration on the ventrolateral side of the snout. The turnstile design and tilt between orthogonal planes indicates the white shark BUC may function in detection of uniform fields, including magnetically induced electric fields that may be used in orientation behaviors. These data can be used in future neuroecology behavioral performance experiments to (1) test for possible specializations of cluster groups to different natural electric stimuli, (2) the possibility of specialized canal subgroups within a cluster, and (3) test several models of navigation that argue for the use of geomagnetically induced electric cues.