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. 2012 Feb 22;279(1729):663-8.
doi: 10.1098/rspb.2011.1127. Epub 2011 Jul 27.

Electroreception in the Guiana dolphin (Sotalia guianensis)

Affiliations

Electroreception in the Guiana dolphin (Sotalia guianensis)

Nicole U Czech-Damal et al. Proc Biol Sci. .

Abstract

Passive electroreception is a widespread sense in fishes and amphibians, but in mammals this sensory ability has previously only been shown in monotremes. While the electroreceptors in fish and amphibians evolved from mechanosensory lateral line organs, those of monotremes are based on cutaneous glands innervated by trigeminal nerves. Electroreceptors evolved from other structures or in other taxa were unknown to date. Here we show that the hairless vibrissal crypts on the rostrum of the Guiana dolphin (Sotalia guianensis), structures originally associated with the mammalian whiskers, serve as electroreceptors. Histological investigations revealed that the vibrissal crypts possess a well-innervated ampullary structure reminiscent of ampullary electroreceptors in other species. Psychophysical experiments with a male Guiana dolphin determined a sensory detection threshold for weak electric fields of 4.6 µV cm(-1), which is comparable to the sensitivity of electroreceptors in platypuses. Our results show that electroreceptors can evolve from a mechanosensory organ that nearly all mammals possess and suggest the discovery of this kind of electroreception in more species, especially those with an aquatic or semi-aquatic lifestyle.

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Figures

Figure 1.
Figure 1.
Vibrissal crypts of the Guiana dolphin. (a) Location on the rostrum. (b) Close-up view. Arrows indicate a single vibrissal crypt.
Figure 2.
Figure 2.
Experimental setup for the psychophysical experiments on the electrosensitivity in the Guiana dolphin. The dolphin was trained to position itself in a hoop and rest its rostrum on a jaw station. This way, the position of the rostrum was reproducible from trial to trial. Electrical signals were delivered by two electrodes at a distance of 10 cm from the rostrum in half of the trials. The dolphin received a food reward for leaving the station when a signal was present and for remaining in station when no signal was present.
Figure 3.
Figure 3.
Histology of the vibrissal crypts in the Guiana dolphin. (a) Longitudinal section through a representative vibrissal crypt stained with Masson–Goldner trichrome. (b) Schematic drawing. The vibrissal crypt consists of an ampulla-shaped invagination of the epidermal integument lacking most characteristic morphological features of mammalian follicle-sinus complexes (F-SCs). (c) Vibrissal crypt innervation with lanceolate endings. (d) Intraepithelial nerve fibre reaches close to the lumen. Ep, epidermis; Lu, Lumen; K, meshwork of corneocytes and keratinous fibres; Afc, agglomeration of fat cells (probably the former hair papilla); Ar, artery; Nb, nerve bundles of the deep vibrissal nerve; Le, lanceolate endings; Inf, intraepithelial nerve fibre.
Figure 4.
Figure 4.
Experimental results from the psychophysical study on the electrosensitivity in the Guiana dolphin. Abscissa: the electric field strength at the location of the nearest vibrissal crypt, calculated from the current through the stimulus electrodes. Ordinate: percentage of correct choice during stimulus-present trials (hit rate) or, respectively, percentage of go responses during stimulus-absent trials (false alarm rate). Black circles: hit rate (i.e. the animal left the station correctly in response to an electric stimulus). White circles: false alarms (i.e. the animal left the station erroneously when no signal was present). At 50 per cent hit rate, the dolphin's absolute detection threshold for the electrical signals is defined (4.6 µV cm−1).

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