Electroreception in mammals – the Guiana dolphin

By Karan Patel (Pitzer College) [Edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only.]

The wide variety of aquatic habitats in the world feature diverse sensory environments. Depending on the amount of sunlight and water quality, the use of visual systems by organisms occupying the habitat may become limited. Under such conditions, organisms may depend on special abilities such as echolocation, active touch or the perception of electrical signals. Electroreception, the capacity of an organism to perceive the presence of an electric field, functions solely within an aquatic habitat, as it depends on movements within the water itself. It is known to be of two types:1) active electroreception, in which the organism generates its own electric field and gauges disturbances produced by objects in the vicinity, and 2) passive electroreception, in which case the organism senses weak electric fields generated by other organisms.

Passive electroreception is a predominant sense in most fishes and many amphibians, but in the case of mammals this sensory capability has been observed only in the echidna and the platypus (monotremes) (Scheich et al. 1986, Gregory et al. 1989, Proske et al. 1998), and even for these two taxa the evidence is interpreted controversially by some. The electroreceptive organs in amphibians and “fish” evolved on the basis of a mechanosensory lateral line organ system, whereas in case of the echidna and the platypus the electroreceptors are based on jelly filled cutaneous glands. In a fairly recent study by Nicole Czech-Damal on the Guiana dolphin, Sotalia guianensis, it was discovered that hairless vibrissal crypts on the rostrum function as passive electroreceptors (Czech-Damal et al. 2012). A closer examination of the crypts showed that the structure was similar to well innervated ampullary electroreceptors and was associated with whiskers. Psychophysical experiments with the Guiana dolphin were able to establish a detection threshold for weak electric fields; approximately 4.6 µV, which is comparable to electric sensitivity in platypuses (Gregory et al. 1987). This discovery has a lot of significance because most marine mammals, including whales, resort to the use of echolocation and vision while foraging for food. The Guiana dolphin, with its electroreceptive capabilities, seems to be different in that respect.

In the case of mammals, vibrissae (or whiskers) are placed in structures that are surrounded by abundant blood sinus complexes and dense tissue capsules. The Guiana dolphin, however, loses its vibrissae postnatally and only empty crypts (called vibrissal crypts) without hair follicles are present on the rostrum (Figure 1). For many years, these structures were speculated to be vestigial in function due to the loss of the vibrissae (Czech-Damal et al. 2012). However, the study conducted by Czech refutes this claim and proves that these crypts are responsible for the passive perception of electric stimuli within the water. Thus, the study also corroborates previous findings that some mammalian species possess the ability of passive electroreception.

Figure 1. Vibrissal crypts of the Guiana dolphin, (a) Location on the rostrum. (b) Close-up view. Arrows indicate a single vibrissal crypt. [Figure taken from Czech-Damal et al. 2011]

Figure 1. Vibrissal crypts of the Guiana dolphin, (a) Location on the rostrum. (b) Close-up view. Arrows indicate a single vibrissal crypt. [Figure taken from Czech-Damal et al. 2012]

Anatomical cross-sections of the vibrissal crypts (Figure 2) show that they possess close to 300 axons per crypt. A large abundance of intraepithelial nerve fibers was observed traversing the crypts. This makes the vibrissal crypts extremely sensitive to even the slightest of stimulation, giving the dolphin a great advantage in analyzing its environment. Such features have not been observed in any other mammalian species, making it an important new discovery.

Figure 2. Cross section of the vibrissal crypts, (a)shows the stained section. (b) shows the nerve bundle containing the axons. [Figure taken from Czech-Damal et al. 2011]

Figure 2. Cross section of the vibrissal crypts, (a)shows the stained section. (b) shows the nerve bundle containing the axons. [Figure taken from Czech-Damal et al. 2012]

A special set up was created to test the effect of an electric stimulus on the behavior of the Guiana dolphin (Figure 3). The dolphin was trained to place its rostrum on a specially designed jaw station, while it was held in place with a hoop. Battery operated copper electrodes were positioned 10 cm above the rostrum. The dolphin was rewarded with food (probably deliciously fresh fish) if it left the station on the application of an electric signal (positive response) or if it decided to stay in place when no signal was applied (negative response).

Figure 3. Experimental setup to test the hypothesis. [Figure taken from Czech-Damal et al. 2011]

Figure 3. Experimental setup to test the hypothesis. [Figure taken from Czech-Damal et al. 2012]

The Guiana dolphin only reacted to electrical stimuli below 8 µV in a total of 5 sets with 31 randomized trials (trials with or without stimulus) in each set. The threshold was determined close to 4.6 µV by extrapolating the percentage of positive and negative responses above and below the threshold value. As a control measure the vibrissal crypts of the dolphin were covered with a plastic cap and the trials were conducted again in a randomized order. It was observed that the dolphin did not perceive any electrical stimuli when the vibrissal crypts were capped, as no sea water was able to come in contact with the opening of the crypts. We can clearly see that the vibrissal crypts on the rostrum of the Guiana dolphin are not vestigial structures but instead are a form of modified electroreceptors. This discovery is of great importance, because it takes us one step closer to having some good evidence that some mammals indeed possess the ability to passively detect an electric field.

Furthermore, the Guiana dolphin’s feeding behavior also demonstrates the importance of vibrissal crypts. The Guiana dolphin is a benthic feeder. Similar to bottlenose dolphins it may adopt a peculiar method to catch its prey, mainly small and medium sized fish, by partially burying itself in the sand and grasp hiding fish. This method is known as ‘crater feeding’ and requires the dolphin to rely solely on its vibrissal crypts to detect the electric signals of moving prey in the vicinity. The vibrissal crypts of the dolphin can be said to have a lot of evolutionary significance in regards to other mammals and “fish”. The crypts resemble the electroreceptors found in most fish species and the mucous/cutaneous gland electroreceptors found in the echidna and the platypus (monotremes). Given their distant phylogenetic placement the evolution of passive electroreception likely has occurred independently, many times (Alves-Gomes, 2001).

The dolphins also use their ability of echolocation to forage for prey, but it is not clear whether echolocation or electroreception is the method of choice. They may work as supplemental abilities to achieve the same result. One could conduct experiments to test whether the dolphin relies on one sense more than the other, and which one is more effective. Another interesting experiment that we can conduct would be to place the dolphin in conditions with varying light intensity and turbidity, to test at what point the dolphin will utilize electroreception/echolocation instead of vision.

References:

Alves-Gomes J. A. 2001 The evolution of electroreception and bioelectrogenesis in teleost fish: a phylogenetic perspective. J Fish Biol 58,1489–1511. (DOI:10.1006/jfbi.2001.1625)

Czech-Damal, Liebschner A., Miersch L., Klauer G., Hanke F., Marshall C., Dehnhardt G. and Hanke W. 2011 Proc R Soc B 2012, 279. (DOI: 10.1098/rspb.2011.1127279)

Gregory J. E., Iggo A., McIntyre A. K., Proske U. 1987 Electroreceptors in the platypus. Nature 326, 386–387. (DOI:10.1038/326386a0)

Gregory J. E., Iggo A., McIntyre A. K., Proske U. 1989 Responses of electroreceptors in the snout of the echidna. J. Physiol. Lond. 414, 521–538. (DOI:10.1038/326386a0)

Proske U., Gregory J. E., Iggo A. 1998 Sensory receptors in monotremes. Phil Trans R Soc Lond B 353, 1187–1198. (DOI:10.1098/rstb.1998.0275)

Scheich H., Langner G., Tidemann C., Coles R. B., Guppy A. 1986 Electroreception and electrolocation in platypus. Nature 319,401–402. (DOI:10.1038/319401a)

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