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.

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.

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.

Reversal of a Spatial Discrimination Task in the Common Octopus (Octopus vulgaris).

Reversal learning requires an animal to learn to discriminate between two stimuli but reverse its responses to these stimuli every time it has reached a learning criterion. Thus, different from pure discrimination experiments, reversal learning experiments require the animal to respond to stimuli flexibly, and the reversal learning performance can be taken as an illustration of the animal's cognitive abilities. We herein describe a reversal learning experiment involving a simple spatial discrimination task, choosing the right or left side, with octopus. When trained with positive reinforcement alone, most octopuses did not even learn the original task. The learning behavior changed drastically when incorrect choices were indicated by a visual signal: the octopuses learned the task within a few sessions and completed several reversals thereby decreasing the number of errors needed to complete a reversal successively. A group of octopus trained with the incorrect-choice signal directly acquired the task quickly and reduced their performances over reversals. Our results indicate that octopuses are able to perform successfully in a reversal experiment based on a spatial discrimination showing progressive improvement, however, without reaching the ultimate performance. Thus, depending on the experimental context, octopus can show behavioral flexibility in a reversal learning task, which goes beyond mere discrimination learning.

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.

Reconsideration of Serial Visual Reversal Learning in Octopus (Octopus vulgaris) from a Methodological Perspective.

Octopuses (Octopus vulgaris) are generally considered to possess extraordinary cognitive abilities including the ability to successfully perform in a serial reversal learning task. During reversal learning, an animal is presented with a discrimination problem and after reaching a learning criterion, the signs of the stimuli are reversed: the former positive becomes the negative stimulus and vice versa. If an animal improves its performance over reversals, it is ascribed advanced cognitive abilities. Reversal learning has been tested in octopus in a number of studies. However, the experimental procedures adopted in these studies involved pre-training on the new positive stimulus after a reversal, strong negative reinforcement or might have enabled secondary cueing by the experimenter. These procedures could have all affected the outcome of reversal learning. Thus, in this study, serial visual reversal learning was revisited in octopus. We trained four common octopuses (O. vulgaris) to discriminate between 2-dimensional stimuli presented on a monitor in a simultaneous visual discrimination task and reversed the signs of the stimuli each time the animals reached the learning criterion of ≥80% in two consecutive sessions. The animals were trained using operant conditioning techniques including a secondary reinforcer, a rod that was pushed up and down the feeding tube, which signaled the correctness of a response and preceded the subsequent primary reinforcement of food. The experimental protocol did not involve negative reinforcement. One animal completed four reversals and showed progressive improvement, i.e., it decreased its errors to criterion the more reversals it experienced. This animal developed a generalized response strategy. In contrast, another animal completed only one reversal, whereas two animals did not learn to reverse during the first reversal. In conclusion, some octopus individuals can learn to reverse in a visual task demonstrating behavioral flexibility even with a refined methodology.

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.

Comparative analysis of the fecal bacterial community of five harbor seals (Phoca vitulina).

The gut microbiota has many beneficial effects on host metabolism and health, and its composition is determined by numerous factors. It is also assumed that there was a co-evolution of mammals and the bacteria inhabiting their gut. Current knowledge of the mammalian gut microbiota mainly derives from studies on humans and terrestrial animals, whereas those on marine mammals are sparse. However, they could provide additional information on influencing factors, such as the role of diet and co-evolution with the host. In this study, we investigated and compared the bacterial diversity in the feces of five male harbor seals (Phoca vitulina). Because this small population included two half-brother pairs, each sharing a common father, it allowed an evaluation of the impact of host relatedness or genetic similarity on the gut microbial community. Fresh feces obtained from the seals by an enema were analyzed by fluorescence in situ hybridization and amplicon sequencing of 16S rRNA genes. The results showed that the bacterial communities in the seals' feces mainly consisted of the phyla Firmicutes (19-43%), Bacteroidetes (22-36%), Fusobacteria (18-32%), and Proteobacteria (5-17%) . Twenty-one bacterial members present in the fecal samples of the five seals contributed an average relative abundance of 93.7 + 8.7% of the total fecal microbial community. Contrary to all expectations based on previous studies a comparison of the fecal community between individual seals showed a higher similarity between unrelated than related individuals.

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.

Saccadic Movement Strategy in Common Cuttlefish (Sepia officinalis).

Most moving animals segregate their locomotion trajectories in short burst like rotations and prolonged translations, to enhance distance information from optic flow, as only translational, but not rotational optic flow holds distance information. Underwater, optic flow is a valuable source of information as it is in the terrestrial habitat, however, so far, it has gained only little attention. To extend the knowledge on underwater optic flow perception and use, we filmed the movement pattern of six common cuttlefish (Sepia officinalis) with a high speed camera in this study. In the subsequent analysis, the center of mass of the cuttlefish body was manually traced to gain thrust, slip, and yaw of the cuttlefish movements over time. Cuttlefish indeed performed short rotations, saccades, with rotational velocities up to 343°/s. They clearly separated rotations from translations in line with the saccadic movement strategy documented for animals inhabiting the terrestrial habitat as well as for the semiaquatic harbor seals before. However, this separation only occurred during fin motion. In contrast, during jet propelled swimming, the separation between rotational and translational movements and thus probably distance estimation on the basis of the optic flow field is abolished in favor of high movement velocities. In conclusion, this study provides first evidence that an aquatic invertebrate, the cuttlefish, adopts a saccadic movement strategy depending on the behavioral context that could enhance the information gained from optic flow.

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.

Unique fur and skin structure in harbour seals (Phoca vitulina)--thermal insulation, drag reduction, or both?

Vertebrate surface structures, including mammalian skin and hair structures, have undergone various modifications during evolution in accordance with functional specializations. Harbour seals rely on their vibrissal system for orientation and foraging. To maintain tactile sensitivity even at low temperatures, the vibrissal follicles are heated up intensely, which could cause severe heat loss to the environment. We analysed skin samples of different body parts of harbour seals, and expected to see higher hair densities at the vibrissal pads as a way to reduce heat loss. In addition to significantly higher hair densities around the vibrissae than on the rest of the body, we show a unique fur structure of hair bundles consisting of broad guard hairs along with hairs of a new type, smaller than guard hairs but broader than underhairs, which we defined as 'intermediate hairs'. This fur composition has not been reported for any mammal so far and may serve for thermal insulation as well as drag reduction. Furthermore, we describe a scale-like skin structure that also presumably plays a role in drag reduction.

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.

Sensitivity of a harbor seal (Phoca vitulina) to coherent visual motion in random dot displays.

Motion vision is one of the fundamental properties of the visual system and is involved in numerous tasks. Previous work has shown that harbor seals are able to perceive visual motion. Tying in with this experimental finding, we assessed the sensitivity of harbor seals to visual motion using random dot displays. In these random dot displays, either all or a percentage of the dots plotted in the display area move into one direction which is referred to as percent coherence. Using random dot displays allows determining motion sensitivity free from form or position cues. Moreover, when reducing the lifetime of the dots, the experimental subjects need to rely on the global motion over the display area instead of on local motion events, such as the streaks of single dots. For marine mammals, the interpretation of global motion stimuli seems important in the context of locomotion, orientation and foraging. The first experiment required the seal to detect coherent motion directed upwards in one out of two stimulus displays and psychophysical motion coherence detection thresholds were obtained ranging from 5% to 35% coherence. At the beginning of the second experiment, which was conducted to reduce the differential flickering of the motion stimulus as secondary cue, the seal was directly able to transfer from coherent motion detection to a discrimination of coherent motion direction, leftward versus rightward. The seal performed well even when the duration of the local motion event was extremely short in the last experiment, in which noise was programmed as random position noise. Its coherence threshold was determined at 23% coherence in this experiment. This motion sensitivity compares well to the performance of most species tested so far excluding monkeys, humans and cats. To conclude, harbor seals possess an effective global motion processing system. For seals, the interpretation of global and coherent motion might e. g. play a role in the interpretation of optic flow information or when breaking the camouflage of cryptic prey items.