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.

Serial visual reversal learning in harbor seals (Phoca vitulina).

Progressively improving performance in a serial reversal learning (SRL) test has been associated with higher cognitive abilities and has served as a measure for cognitive/behavioral flexibility. Although the cognitive and sensory abilities of marine mammals have been subject of extensive investigation, and numerous vertebrate and invertebrate species were tested, SRL studies in aquatic mammals are sparse. Particularly in pinnipeds, a high degree of behavioral flexibility seems probable as they face a highly variable environment in air and underwater. Thus, we tested four harbor seals in a visual two-alternative forced-choice discrimination task and its subsequent reversals. We found significant individual differences in performance. One individual was able to solve 37 reversals showing progressive improvement of performance with a minimum of 6 errors in reversal 33. Two seals mastered two reversals, while one animal had difficulties in learning the discrimination task and failed to complete a single reversal. In conclusion, harbor seals can master an SRL experiment; however, the performance is inferior to results obtained in other vertebrates in comparable tasks. Future experiments will need to assess whether factors such as the modality addressed in the experiment have an influence on reversal learning performance or whether indeed, during evolution, behavioral flexibility has not specifically been favored in harbor seals.

Well-developed spatial reversal learning abilities in harbor seals (Phoca vitulina).

In this study, behavioral plasticity in harbor seals was investigated in spatial reversal learning tasks of varying complexities. We started with a classic spatial reversal learning experiment with no more than one reversal per day. The seals quickly learned the task and showed progressive improvement over reversals, one seal even reaching one-trial performance. In a second approach, one seal could complete multiple reversals occurring within a session. Again, a number of reversals were finished with only one error occurring at the beginning of a session as in experiment 1 which provides evidence that the seal adopted a strategy. In a final approach, reversals within a session were marked by an external cue. This way, an errorless performance of the experimental animal was achieved in up to three consecutive reversals. In conclusion, harbor seals master spatial, in contrast to visual, reversal learning experiments with ease. The underlying behavioral flexibility can help to optimize behaviors in fluctuating or changing environments.

Hydrodynamic reception in the Australian water rat, Hydromys chrysogaster.

The Australian water rat, Hydromys chrysogaster, preys on a wide variety of aquatic and semiaquatic arthropods and vertebrates, including fish. A frequently observed predatory strategy of Hydromys is sitting in wait at the water's edge with parts of its vibrissae submersed. Here we show that Hydromys can detect water motions with its whiskers. Behavioural thresholds range from 1.0 to 9.4 mm s-1 water velocity, based on maximal horizontal water velocity in the area covered by the whiskers. This high sensitivity to water motions would enable Hydromys to detect fishes passing by. No responses to surface waves generated by a vibrating rod and resembling the surface waves caused by struggling insects were found.

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.

Hydrodynamic sensory threshold in harbour seals (Phoca vitulina) for artificial flatfish breathing currents.

Harbour seals have the ability to detect benthic fish such as flatfish using the water currents these fish emit through their gills (breathing currents). We investigated the sensory threshold in harbour seals for this specific hydrodynamic stimulus under conditions which are realistic for seals hunting in the wild. We used an experimental platform where an artificial breathing current was emitted through one of eight different nozzles. Two seals were trained to search for the active nozzle. Each experimental session consisted of eight test trials of a particular stimulus intensity and 16 supra-threshold trials of high stimulus intensity. Test trials were conducted with the animals blindfolded. To determine the threshold, a series of breathing currents differing in intensity was used. For each intensity, three sessions were run. The threshold in terms of maximum water velocity within the breathing current was 4.2 cm s-1 for one seal and 3.7 cm s-1 for the other. We measured background flow velocities from 1.8 to 3.4 cm s-1 Typical swimming speeds for both animals were around 0.5 m s-1 Swimming speed differed between successful and unsuccessful trials. It appears that swimming speed is restricted for the successful detection of a breathing current close to the threshold. Our study is the first to assess a sensory threshold of the vibrissal system for a moving harbour seal under near-natural conditions. Furthermore, this threshold was defined for a natural type of stimulus differing from classical dipole stimuli which have been widely used in threshold determination so far.

Saccadic movement strategy in a semiaquatic species - the harbour seal (Phoca vitulina).

Moving animals can estimate the distance of visual objects from image shift on their retina (optic flow) created during translational, but not rotational movements. To facilitate this distance estimation, many terrestrial and flying animals perform saccadic movements, thereby temporally separating translational and rotational movements, keeping rotation times short. In this study, we analysed whether a semiaquatic mammal, the harbour seal, also adopts a saccadic movement strategy. We recorded the seals' normal swimming pattern with video cameras and analysed head and body movements. The swimming seals indeed minimized rotation times by saccadic head and body turns, with top rotation speeds exceeding 350 deg s-1 which leads to an increase of translational movements. Saccades occurred during both types of locomotion of the seals' intermittent swimming mode: active propulsion and gliding. In conclusion, harbour seals share the saccadic movement strategy of terrestrial animals. Whether this movement strategy is adopted to facilitate distance estimation from optic flow or serves a different function will be a topic of future research.

Hydrodynamic detection and localization of artificial flatfish breathing currents by harbour seals (Phoca vitulina).

Harbour seals are known to be opportunistic feeders, whose diet consists mainly of pelagic and benthic fish, such as flatfish. As flatfish are often cryptic and do not produce noise, we hypothesized that harbour seals are able to detect and localize flatfish using their hydrodynamic sensory system (vibrissae), as fish emit water currents through their gill openings (breathing currents). To test this hypothesis, we created an experimental platform where an artificial breathing current was emitted through one of eight different openings. Three seals were trained to search for the active opening and station there for 5 s. Half of the trials were conducted with the seal blindfolded with an eye mask. In blindfolded and non-blindfolded trials, all seals performed significantly better than chance. The seals crossed the artificial breathing current (being emitted into the water column at an angle of 45 deg to the ground) from different directions. There was no difference in performance when the seals approached from in front, from behind or from the side. All seals responded to the artificial breathing currents by directly moving their snout towards the opening from which the hydrodynamic stimulus was emitted. Thus, they were also able to extract directional information from the hydrodynamic stimulus. Hydrodynamic background noise and the swimming speed of the seals were also considered in this study as these are aggravating factors that seals in the wild have to face during foraging. By creating near-natural conditions, we show that harbour seals have the ability to detect a so-far overlooked type of stimulus.

Harbour seals (Phoca vitulina) are able to time precisely.

Time along with space is one of the two fundamental dimensions of life. Whereas spatial aspects have been considered in experiments with marine mammals, research has so far not focused on timing per se although it is most likely involved in many behaviours such as foraging or navigation. This study investigated whether harbour seals possess a sense of time and how precisely they are able to discriminate time intervals. Experiments took place in a chamber that allowed keeping ambient illumination constant at 40 lx. The animal was presented with a white circle on a black background on a monitor displayed for a preset time interval. In a two-alternative forced-choice experiment, the animal had to indicate the presence of the standard or a longer comparison time interval by moving its head to one out of two response targets. Time difference thresholds were assessed for various standard intervals between 3 to 30 s adopting a staircase procedure. The experimental animal found access to the task easily and discriminated time intervals with difference thresholds partly in the millisecond range. Thus our study revealed a well-developed sense of time in a pinniped species. Time, besides information provided by the classical senses, is thus most likely an important parameter seals can rely on for various tasks including navigation and foraging.

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.

Why do seals have cones? Behavioural evidence for colour-blindness in harbour seals.

All seals and cetaceans have lost at least one of two ancestral cone classes and should therefore be colour-blind. Nevertheless, earlier studies showed that these marine mammals can discriminate colours and a colour vision mechanism has been proposed which contrasts signals from cones and rods. However, these earlier studies underestimated the brightness discrimination abilities of these animals, so that they could have discriminated colours using brightness only. Using a psychophysical discrimination experiment, we showed that a harbour seal can solve a colour discrimination task by means of brightness discrimination alone. Performing a series of experiments in which two harbour seals had to discriminate the brightness of colours, we also found strong evidence for purely scotopic (rod-based) vision at light levels that lead to mesopic (rod-cone-based) vision in other mammals. This finding speaks against rod-cone-based colour vision in harbour seals. To test for colour-blindness, we used a cognitive approach involving a harbour seal trained to use a concept of same and different. We tested this seal with pairs of isoluminant stimuli that were either same or different in colour. If the seal had perceived colour, it would have responded to colour differences between stimuli. However, the seal responded with "same", providing strong evidence for colour-blindness.

Spatial arrangement of the whiskers of harbor seals ( Phoca vitulina ) compared to whisker arrangements of mice ( Mus musculus ) and rats ( Rattus norvegicus ).

Most mammals have specialized facial hairs known as vibrissae (whiskers), sensitive tactile structures that subserve both touch and flow sensing. Different animals have different numbers and geometric arrangements of whiskers, and it seems nearly self-evident that these differences would correlate with functional and behavioral use. To date, however, cross-species comparisons of three-dimensional (3D) whisker array geometry have been limited because standard morphometric techniques cannot be applied. Our laboratory recently developed a novel approach to enable quantitative, cross-species vibrissal array comparisons. Here we quantify the 3D morphology of the vibrissal array of the harbor seal ( Phoca vitulina ), construct a CAD model of the array, and compare array morphologies of harbor seals, mice ( Mus musculus ) and rats ( Rattus norvegicus ). In all three species whisker arclength decreases from caudal to rostral, whisker curvature increases from caudal to rostral, and whiskers emerge from the face in smooth orientation gradients. Two aspects of whisker orientation are strikingly consistent across species: the elevation angle is constant within a row, and the twist of the whisker about its own axis varies smoothly in a diagonal gradient across the array. We suggest that invariant whisker elevation within a row may aid localization behaviors, while variable twist-orientation may help the animal sense stimulus direction. We anticipate this work will serve as a starting point for quantitative comparisons of vibrissal arrays across species, help clarify the mechanical basis by which seal vibrissae enable efficient wake detection and following, and enable the creation of whole-body biomechanical models for neuroscience and robotics.

Hydrodynamic perception in true seals (Phocidae) and eared seals (Otariidae).

Pinnipeds, that is true seals (Phocidae), eared seals (Otariidae), and walruses (Odobenidae), possess highly developed vibrissal systems for mechanoreception. They can use their vibrissae to detect and discriminate objects by direct touch. At least in Phocidae and Otariidae, the vibrissae can also be used to detect and analyse water movements. Here, we review what is known about this ability, known as hydrodynamic perception, in pinnipeds. Hydrodynamic perception in pinnipeds developed convergently to the hydrodynamic perception with the lateral line system in fish and the sensory hairs in crustaceans. So far two species of pinnipeds, the harbour seal (Phoca vitulina) representing the Phocidae and the California sea lion (Zalophus californianus) representing the Otariidae, have been studied for their ability to detect local water movements (dipole stimuli) and to follow hydrodynamic trails, that is the water movements left behind by objects that have passed by at an earlier point in time. Both species are highly sensitive to dipole stimuli and can follow hydrodynamic trails accurately. In the individuals tested, California sea lions were clearly more sensitive to dipole stimuli than harbour seals, and harbour seals showed a superior trail following ability as compared to California sea lions. Harbour seals have also been shown to derive additional information from hydrodynamic trails, such as motion direction, size and shape of the object that caused the trail (California sea lions have not yet been tested). The peculiar undulated shape of the harbour seals' vibrissae appears to play a crucial role in trail following, as it suppresses self-generated noise while the animal is swimming.

Vibrissal touch sensing in the harbor seal (Phoca vitulina): how do seals judge size?

"Whisker specialists" such as rats, shrews, and seals actively employ their whiskers to explore their environments and extract object properties such as size, shape, and texture. It has been suggested that whiskers could be used to discriminate between different sized objects in one of two ways: (i) to use whisker positions, such as angular position, spread or amplitude to approximate size; or (ii) to calculate the number of whiskers that contact an object. This study describes in detail how two adult harbor seals use their whiskers to differentiate between three sizes of disk. The seals judged size very fast, taking <400 ms. In addition, they oriented their smaller, most rostral, ventral whiskers to the disks, so that more whiskers contacted the surface, complying to a maximal contact sensing strategy. Data from this study supports the suggestion that it is the number of whisker contacts that predict disk size, rather than how the whiskers are positioned (angular position), the degree to which they are moved (amplitude) or how spread out they are (angular spread).

Passive electroreception in aquatic mammals.

Passive electroreception is a sensory modality in many aquatic vertebrates, predominantly fishes. Using passive electroreception, the animal can detect and analyze electric fields in its environment. Most electric fields in the environment are of biogenic origin, often produced by prey items. These electric fields can be relatively strong and can be a highly valuable source of information for a predator, as underlined by the fact that electroreception has evolved multiple times independently. The only mammals that possess electroreception are the platypus (Ornithorhynchus anatinus) and the echidnas (Tachyglossidae) from the monotreme order, and, recently discovered, the Guiana dolphin (Sotalia guianensis) from the cetacean order. Here we review the morphology, function and origin of the electroreceptors in the two aquatic species, the platypus and the Guiana dolphin. The morphology shows certain similarities, also similar to ampullary electroreceptors in fishes, that provide cues for the search for electroreceptors in more vertebrate and invertebrate species. The function of these organs appears to be very similar. Both species search for prey animals in low-visibility conditions or while digging in the substrate, and sensory thresholds are within one order of magnitude. The electroreceptors in both species are innervated by the trigeminal nerve. The origin of the accessory structures, however, is completely different; electroreceptors in the platypus have developed from skin glands, in the Guiana dolphin, from the vibrissal system.

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.

A harbor seal can transfer the same/different concept to new stimulus dimensions.

We investigated the formation of an abstract concept of same/different in a harbor seal by means of a two-item same/different task. Stimuli were presented on a TFT monitor. The subject was trained to respond according to whether two horizontally aligned white shapes presented on a black background were the same, or different from each other, by giving a no-go or go response. Training comprised of four stages. First, the same/different task was trained with two shapes forming two same problems (A-A and B-B) and two different problems (A-B and B-A). After the learning criterion was reached, training proceeded with new pairs of shapes. In the second experimental stage, every problem was presented just five times before new problems were introduced. We showed that training to criterion with just two shapes resulted in item-specific learning, whereas reducing the number of presentations to five per problem led to the formation of a same/different learning set as well as some restricted relational learning. Training with trial-unique problems in the third stage of this study resulted in the formation of an abstract concept of same/different which was indicated by a highly significant performance in transfer tests with 120 novel problems. Finally, extra-dimensional transfer of the concept was tested. The harbor seal showed a significantly correct performance on transfer tests with 30 unfamiliar pattern and 60 unfamiliar brightness same/different problems, thus demonstrating that the concept is not restricted to the shape dimension originally learned, but can be generalized across stimulus dimensions.

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.

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.