Passive electroreception in bottlenose dolphins (Tursiops truncatus): implication for micro- and large-scale orientation.

For the two dolphin species Sotalia guianensis (Guiana dolphin) and Tursiops truncatus (bottlenose dolphin), previous research has shown that the vibrissal crypts located on the rostrum represent highly innervated, ampullary electroreceptors and that both species are correspondingly sensitive to weak electric fields. In the present study, for a comparative assessment of the sensitivity of the bottlenose dolphin's electroreceptive system, we determined detection thresholds for DC and AC electric fields with two bottlenose dolphins. In a psychophysical experiment, the animals were trained to respond to electric field stimuli using the go/no-go paradigm. We show that the two bottlenose dolphins are able to detect DC electric fields as low as 2.4 and 5.5 µV cm-1, respectively, a detection threshold in the same order of magnitude as those in the platypus and the Guiana dolphin. Detection thresholds for AC fields (1, 5 and 25 Hz) were generally higher than those for DC fields, and the sensitivity for AC fields decreased with increasing frequency. Although the electroreceptive sensitivity of dolphins is lower than that of elasmobranchs, it is suggested that it allows for both micro- and macro-scale orientation. In dolphins pursuing benthic foraging strategies, electroreception may facilitate short-range prey detection and target-oriented snapping of their prey. Furthermore, the ability to detect weak electric fields may enable dolphins to perceive the Earth's magnetic field through induction-based magnetoreception, thus allowing large-scale orientation.

A harbour seal (Phoca vitulina) can learn geometrical relationships between landmarks.

Marine mammals travel the world's oceans. Some species regularly return to specific places to breathe, haul-out or breed. However, the mechanisms they use to return are unknown. Theoretically, landmarks could mediate the localisation of these places. Occasionally, it might be beneficial or even required to localise places using geometrical information provided by landmarks such as to apply a 'middle rule'. Here, we trained a harbour seal to find its goal in the middle of numerous vertically and horizontally orientated two-landmark arrays. During testing, the seal was confronted with unfamiliar two-landmark arrays. After having successfully learnt to respond to the midpoint of multiple two-landmark arrays, the seal directly and consistently followed a 'middle rule' during testing. It chose the midpoint of the two-landmark arrays with high precision. Harbour seals with the ability to localise goals based on geometrical information would be able to home in on places even from unknown positions relative to goal-defining features. Altogether, the results obtained with our harbour seal individual in the present and a previous study, examining the basis of landmark orientation, provide evidence that this seal can use landmark information very flexibly. Depending on context, this flexibility is adaptive to an environment in which the information content can vary over time.

Behavioral and anatomical evidence for electroreception in the bottlenose dolphin (Tursiops truncatus).

In the order of cetacean, the ability to detect bioelectric fields has, up to now, only been demonstrated in the Guiana dolphin (Sotalia guianensis) and is suggested to facilitate benthic feeding. As this foraging strategy has also been reported for bottlenose dolphins (Tursiops truncatus), we studied electroreception in this species by combining an anatomical analysis of "vibrissal crypts" as potential electroreceptors from neonate and adult animals with a behavioral experiment. In the latter, four bottlenose dolphins were trained on a go/no-go paradigm with acoustic stimuli and afterward tested for stimulus generalization within and across modalities using acoustic, optical, mechanical, and electric stimuli. While neonates still possess almost complete vibrissal follicles including a hair shaft, hair papilla, and cavernous sinus, adult bottlenose dolphins lack these features. Thus, their "vibrissal crypts" show a similar postnatal morphological transformation from a mechanoreceptor to an electroreceptor as in Sotalia. However, innervation density was high and almost equal in both, neonate as well as adult animals. In the stimulus generalization tests the dolphins transferred the go/no-go response within and across modalities. Although all dolphins responded spontaneously to the first presentation of a weak electric field, only three of them showed perfect transfer in this modality by responding continuously to electric field amplitudes of 1.5 mV cm-1 , successively reduced to 0.5 mV cm-1 . Electroreception can explain short-range prey detection in crater-feeding bottlenose dolphins. The fact that this is the second odontocete species with experimental evidence for electroreception suggests that it might be widespread in this marine mammal group.

Underwater sound localization abilities of harbor seals (Phoca vitulina) for high-frequency noise band stimuli in the median plane.

Pinnipeds use a variety of acoustic information underwater for social interactions, hunting, and predator avoidance. Thus, the ability to accurately localize a sound source in the environment can have a clear survival value. Nonetheless, the sound localization mechanisms for seals underwater still have to be clarified, especially for sounds received in the median plane. In this study, the sound localization abilities of five harbor seals for high-frequency noise band stimuli were measured underwater in the median plane. The seals' minimum audible angles (MAAs) were determined for two different high-frequency noise band stimuli using a two-alternative forced-choice procedure. Noise 1 had a frequency range between 8 and 16 kHz. Noise 2 contained frequencies between 14 and 16 kHz. Psychoacoustic results for the tested harbor seals show that the seals were able to localize these stimuli in the median plane underwater with MAAs between 5.1° and 17.5°. The results suggest that spectral cues improve the seals' ability to localize high-frequency sound signals in the median plane.

Detection and direction discrimination of single vortex rings by harbour seals (Phoca vitulina).

Harbour seals possess highly sensitive vibrissae that enable them to track hydrodynamic trails left behind by a swimming fish. Most of these trails contain vortex rings as a main hydrodynamic component. They may reveal information about their generator as the trails differ depending on the fish species, the fish's body shape, size and swimming style. In addition, fish generate single vortex rings in diverse natural situations. In this study, the ability of blindfolded stationary harbour seals to detect and analyse single vortex rings regarding directional information has been investigated. In three different behavioural experiments, the animals were trained to respond to single artificially generated vortex rings. The results show that harbour seals are able to respond to a variety of different vortex rings upon vibrissal stimulation. The investigation of the minimum hydrodynamically perceivable angle revealed that it is at least as small as 5.7 deg, which was the smallest adjustable angle. Moreover, harbour seals are capable of analysing the travel direction of a vortex ring perceived by the mystacial vibrissae irrespective of whether the vibrissae were stimulated ipsilaterally or contralaterally. In situations in which no complex hydrodynamic trail is available, it is advantageous for a hunting seal to be able to extract information from a single vortex ring.

Underwater sound localization of pure tones in the median plane by harbor seals (Phoca vitulina).

In an underwater environment the physical characteristics of sound propagation differ considerably from those in air. For this reason, sound localization underwater is associated with difficulties, especially in the median plane. It was the approach of the present study to investigate whether harbor seals (Phoca vitulina) are able to determine the direction of a tonal signal form above or below in the underwater environment. Minimum audible angles (MAAs) or the angular range in which the animals could localize a pure tone stimulus in the vertical plane were obtained for frequencies from 0.35 up to 16 kHz. Testing was conducted with four male harbor seals in a semi-circle area of 6 m in diameter in about 2.5 m depth, by using a two alternative forced choice method. The results show that harbor seals are able to localize a pure tone in the median plane under water with a high performance for low frequency stimuli between 350 Hz and 2 kHz with MAAs ranging from below 2.5° up to about 25°. For higher frequencies the animals show strong individual differences.

Are harbour seals (Phoca vitulina) able to perceive and use polarised light?

Harbour seals are active at night and during the day and see well in both air and water. Polarised light, which is a well-known visual cue for orientation, navigation and foraging, is richly available in harbour seal habitats, both above and below the water surface. We hypothesised that an ability to detect and use polarised light could be valuable for seals, and thus tested if they are able to see this property of light. We performed two behavioural experiments, one involving object discrimination and the other involving object detection. These objects were presented to the seals as two-dimensional stimuli on a specially modified liquid crystal display that generated objects whose contrast was purely defined in terms of polarisation (i.e. objects lacked luminance contrast). In both experiments, the seals' performance did not deviate significantly from chance. In contrast, the seals showed a high baseline performance when presented with objects on a non-modified display (whose contrast was purely defined in terms of luminance). We conclude that harbour seals are unable to use polarised light in our experimental context. It remains for future work to elucidate if they are polarisation insensitive per se.

Electroreception in the Guiana dolphin (Sotalia guianensis).

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.

Hydrodynamic discrimination of wakes caused by objects of different size or shape in a harbour seal (Phoca vitulina).

Harbour seals can use their mystacial vibrissae to detect and track hydrodynamic wakes. We investigated the ability of a harbour seal to discriminate objects of different size or shape by their hydrodynamic signature and used particle image velocimetry to identify the hydrodynamic parameters that a seal may be using to do so. Hydrodynamic trails were generated by different sized or shaped paddles that were moved in the calm water of an experimental box to produce a characteristic signal. In a two-alternative forced-choice procedure the blindfolded subject was able to discriminate size differences of down to 3.6 cm (Weber fraction 0.6) when paddles were moved at the same speed. Furthermore the subject distinguished hydrodynamic signals generated by flat, cylindrical, triangular or undulated paddles of the same width. Particle image velocimetry measurements demonstrated that the seal could have used the highest velocities and the steepness of the gradients within the wake to discriminate object size, beside the size of counter-rotating vortices and the spatial extension of a wake. For shape discrimination the subject could have used the spatial extension of the whole wake, in addition to the arrangement of the vortices. We tested whether the seal used highest velocities, the steepness of the gradients and the spatial extension of the wake in a second set of experiments by varying moving speed and paddle size, respectively. The subject was still able to discriminate between the respective object sizes, but the minimum detectable size difference increased to 4.4 cm (Weber fraction 3.6). For the shape discrimination task, the seal was only able to distinguish flat from triangular paddles. Our results indicate that the seal's discrimination abilities depend on more than one hydrodynamic parameter.

Harbor seal vibrissa morphology suppresses vortex-induced vibrations.

Harbor seals (Phoca vitulina) often live in dark and turbid waters, where their mystacial vibrissae, or whiskers, play an important role in orientation. Besides detecting and discriminating objects by direct touch, harbor seals use their whiskers to analyze water movements, for example those generated by prey fish or by conspecifics. Even the weak water movements left behind by objects that have passed by earlier can be sensed and followed accurately (hydrodynamic trail following). While scanning the water for these hydrodynamic signals at a swimming speed in the order of meters per second, the seal keeps its long and flexible whiskers in an abducted position, largely perpendicular to the swimming direction. Remarkably, the whiskers of harbor seals possess a specialized undulated surface structure, the function of which was, up to now, unknown. Here, we show that this structure effectively changes the vortex street behind the whiskers and reduces the vibrations that would otherwise be induced by the shedding of vortices from the whiskers (vortex-induced vibrations). Using force measurements, flow measurements and numerical simulations, we find that the dynamic forces on harbor seal whiskers are, by at least an order of magnitude, lower than those on sea lion (Zalophus californianus) whiskers, which do not share the undulated structure. The results are discussed in the light of pinniped sensory biology and potential biomimetic applications.

Underwater localization of pure tones by harbor seals (Phoca vitulina).

The underwater sound localization acuity of harbor seals (Phoca vitulina) was measured in the horizontal plane. Minimum audible angles (MAAs) of pure tones were determined as a function of frequency from 0.2 to 16 kHz for two seals. Testing was conducted in a 10-m-diam underwater half circle using a right/left psychophysical procedure. The results indicate that for both harbor seals, MAAs were large at high frequencies (13.5 degrees and 17.4 degrees at 16 kHz), transitional at intermediate frequencies (9.6 degrees and 10.1 degrees at 4 kHz), and particularly small at low frequencies (3.2 degrees and 3.1 degrees at 0.2 kHz). Harbor seals seem to be able to utilize both binaural cues, interaural time differences (ITDs) and interaural intensity differences (IIDs), but a significant decrease in the sound localization acuity with increasing frequency suggests that IID cues may not be as robust as ITD cues under water. These results suggest that the harbor seal can be regarded as a low-frequency specialist. Additionally, to obtain a MAA more representative of the species, the horizontal underwater MAA of six adult harbor seals was measured at 2 kHz under identical conditions. The MAAs of the six animals ranged from 8.8 degrees to 11.7 degrees , resulting in a mean MAA of 10.3 degrees .

Underwater auditory localization by a swimming harbor seal (Phoca vitulina).

The underwater sound localization acuity of a swimming harbor seal (Phoca vitulina) was measured in the horizontal plane at 13 different positions. The stimulus was either a double sound (two 6-kHz pure tones lasting 0.5 s separated by an interval of 0.2 s) or a single continuous sound of 1.2 s. Testing was conducted in a 10-m-diam underwater half circle arena with hidden loudspeakers installed at the exterior perimeter. The animal was trained to swim along the diameter of the half circle and to change its course towards the sound source as soon as the signal was given. The seal indicated the sound source by touching its assumed position at the board of the half circle. The deviation of the seals choice from the actual sound source was measured by means of video analysis. In trials with the double sound the seal localized the sound sources with a mean deviation of 2.8 degrees and in trials with the single sound with a mean deviation of 4.5 degrees. In a second experiment minimum audible angles of the stationary animal were found to be 9.8 degrees in front and 9.7 degrees in the back of the seal's head.

Sensitivity of a tucuxi (Sotalia fluviatilis guianensis) to airborne sound.

Auditory systems of cetaceans are considered highly specialized for underwater sound processing, whereas the extent of their hearing capacity in air is still a point of issue. In this study, the sensitivity to airborne sound in a male tucuxi (Sotalia fluviatilis guianensis) was tested by means of a go/no go response paradigm. Auditory thresholds were obtained from 2 to 31.5 kHz. Compared to the hearing thresholds of other dolphins as well as of amphibian mammals, the sensitivity to airborne sound of the test subject is low from 2 to 8 kHz, with the highest threshold at 4 kHz. Thresholds at 16 and 31.5 kHz reveal a sharp increase in hearing sensitivity. Thus, although not obtained in this study, the upper aerial hearing limit is in the ultrasonic range. A comparison of the present data with the underwater audiogram of the same test subject referred to sound intensity indicates that the sensitivity of Sotalia to underwater sound is generally better than to airborne sound.