How harbour seals (Phoca vitulina) encode goals relative to landmarks.

Visual landmarks are defined as objects with prominent shape or size that distinguish themselves from the background. With the help of landmarks, animals can orient themselves in their natural environment. Yet, the way in which landmarks are perceived and encoded has previously only been described in insects, fish, birds, reptiles and terrestrial mammals. The present study aimed to provide insight into how a marine mammal, the harbour seal, encodes goals relative to landmarks. In our expansion test, three harbour seals were trained to find a goal inside an array of landmarks. After diagonal, horizontal or vertical expansion of the landmark array, the search behaviour displayed by the animals was documented and analyzed regarding the underlying encoding strategy. The harbour seals mainly encoded directional vector information from landmarks and did neither search arbitrarily around a landmark nor used a rule-based approach. Depending on the number of landmarks available within the array, the search behaviour of some harbor seals changed, indicating flexibility in landmark-based search. Our results present the first insight into how a semi-aquatic predator could encode landmark information when swimming along the coastline in search of a goal location.

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.

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.

"Cognition in marine mammals: the strength of flexibility in adapting to marine life".

In this theme issue, our multidisciplinary contributors highlight the cognitive adaptations of marine mammals. The cognitive processes of this group are highly informative regarding how animals cope with specifics of and changes in the environment, because, not only did modern marine mammals evolve from numerous, non-related terrestrial animals to adapt to an aquatic lifestyle, but some of these species regularly move between two worlds, land and sea. Here, we bring together scientists from different fields and take the reader on a journey that begins with the ways in which modern marine mammals (whales, dolphins, seals, sea lions and manatees) utilize their perceptual systems, next moves into studies of the constraints and power of individuals' cognitive flexibility, and finally showcases how those systems are deployed in social and communicative contexts. Considering the cognitive processes of the different marine mammals in one issue from varying perspectives will help us understand the strength of cognitive flexibility in changing environments-in marine mammals and beyond.

Single target acuity in the common sunfish (Lepomis gibbosus).

Vision contributes to foraging, territorial and reproductive behavior in sunfish. In these contexts, sunfish need to perceive single targets, such as prey items or body markings from either conspecifics or individuals of other sunfish species, from some distance. We determined the single target acuity of six common sunfish in a behavioral experiment to assess whether the visual abilities of sunfish correspond with behavioral observations or reactive distance measures, and thus assessed the limits of vision for the mentioned behaviors. Single target acuity for full-contrast single targets amounted to 0.17 deg (0.13-0.32 deg). When contrast was reduced to Weber contrasts of 0.67 and 0.41, single target acuity dropped to 0.34 deg (0.31-0.37 deg), and finally to 0.42 deg (0.34-0.54 deg). Single target acuity would thus allow common sunfish to perceive biologically relevant stimuli at reasonable distances even when contrast is reduced.

Visual timing abilities of a harbour seal (Phoca vitulina) and a South African fur seal (Arctocephalus pusillus pusillus) for sub- and supra-second time intervals.

Timing is an essential parameter influencing many behaviours. A previous study demonstrated a high sensitivity of a phocid, the harbour seal (Phoca vitulina), in discriminating time intervals. In the present study, we compared the harbour seal's timing abilities with the timing abilities of an otariid, the South African fur seal (Arctocephalus pusillus pusillus). This comparison seemed essential as phocids and otariids differ in many respects and might, thus, also differ regarding their timing abilities. We determined time difference thresholds for sub- and suprasecond time intervals marked by a white circle on a black background displayed for a specific time interval on a monitor using a staircase method. Contrary to our expectation, the timing abilities of the fur seal and the harbour seal were comparable. Over a broad range of time intervals, 0.8-7 s in the fur seal and 0.8-30 s in the harbour seal, the difference thresholds followed Weber's law. In this range, both animals could discriminate time intervals differing only by 12 % and 14 % on average. Timing might, thus be a fundamental cue for pinnipeds in general to be used in various contexts, thereby complementing information provided by classical sensory systems. Future studies will help to clarify if timing is indeed involved in foraging decisions or the estimation of travel speed or distance.

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.

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.

Understanding fiber mixture by simulation in 3D Polarized Light Imaging.

3D Polarized Light Imaging (3D-PLI) is a neuroimaging technique that has opened up new avenues to study the complex architecture of nerve fibers in postmortem brains. The spatial orientations of the fibers are derived from birefringence measurements of unstained histological brain sections that are interpreted by a voxel-based analysis. This, however, implies that a single fiber orientation vector is obtained for each voxel and reflects the net effect of all comprised fibers. The mixture of various fiber orientations within an individual voxel is a priori not accessible by a standard 3D-PLI measurement. In order to better understand the effects of fiber mixture on the measured 3D-PLI signal and to improve the interpretation of real data, we have developed a simulation method referred to as SimPLI. By means of SimPLI, it is possible to reproduce the entire 3D-PLI analysis starting from synthetic fiber models in user-defined arrangements and ending with measurement-like tissue images. For the simulation, each synthetic fiber is considered as an optical retarder, i.e., multiple fibers within one voxel are described by multiple retarder elements. The investigation of different synthetic crossing fiber arrangements generated with SimPLI demonstrated that the derived fiber orientations are strongly influenced by the relative mixture of crossing fibers. In case of perpendicularly crossing fibers, for example, the derived fiber direction corresponds to the predominant fiber direction. The derived fiber inclination turned out to be not only influenced by myelin density but also systematically overestimated due to signal attenuation. Similar observations were made for synthetic models of optic chiasms of a human and a hooded seal which were opposed to experimental 3D-PLI data sets obtained from the chiasms of both species. Our study showed that SimPLI is a powerful method able to test hypotheses on the underlying fiber structure of brain tissue and, therefore, to improve the reliability of the extraction of nerve fiber orientations with 3D-PLI.

Aerial single target acuity of harbor seals (Phoca vitulina) for stationary and moving targets of varying contrast.

Harbor seals (Phoca vitulina) need to detect single objects for example when orienting to landmarks or hunting prey. The detection of single objects, described by the single target acuity (STA), cannot be deduced from formerly determined grating acuity (GA) as different mechanisms underlie STA and GA. Thus, we assessed STA for stationary and moving single targets with varying contrast in two harbor seals in a first approach in air. In a two-alternative-forced-choice discrimination task, the seals had to indicate whether the single target was presented in a left or right stimulus field on a monitor. The STA for full-contrast stationary targets was determined as 0.27 deg of visual angle for both experimental animals. Contrary to our expectations, neither adding motion nor reducing contrast had a strong impact on STA. Additionally, we also determined GA in the two harbor seals (1.2 and 1.1 cycles/deg or 0.42 and 0.45 deg for a single stripe of the grating at threshold) to be slightly inferior to STA. Our results are in good correspondence with contrast sensitivity and allow calculating viewing distances in the context of for example visual orientation.

Single target acuity for moving targets in the common sunfish (Lepomis gibbosus).

The common sunfish (Lepomis gibbosus) likely relies on vision for many vital behaviors that require the perception of small objects such as detection of prey items or body marks of conspecifics. A previous study documented the single target acuity (STA) for stationary targets. Under many, if not most, circumstances, however, objects of interest are moving, which is why the current study tested the effect of the ecologically relevant parameter motion on sunfish STA. The STA was determined in two sunfish for targets moving randomly at a velocity of 3.4 deg/s. The STA for moving targets (0.144±0.002 deg) was equal to the STA for stationary targets obtained from the same fish individuals under the experimental conditions of this/the previous study. Our results contribute to a comprehensive understanding of fish vision, extending the large data set available on grating acuity.

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.

Open questions in marine mammal sensory research.

Although much research has focused on marine mammal sensory systems over the last several decades, we still lack basic knowledge for many of the species within this diverse group of animals. Our conference workshop allowed all participants to present recent developments in the field and culminated in discussions on current knowledge gaps. This report summarizes open questions regarding marine mammal sensory ecology and will hopefully serve as a platform for future research.

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.

Beyond the classic sensory systems: Characteristics of the sense of time of harbor seals (Phoca vitulina) assessed in a visual temporal discrimination and a bisection task.

Beyond the classic sensory systems, the sense of time is most likely involved from foraging to navigation. As a prerequisite for assessing the role time is playing in different behavioral contexts, we further characterized the sense of time of a harbor seal in this study. Supra-second time intervals were presented to the seal in a temporal discrimination and a temporal bisection task. During temporal discrimination, the seal needed to discriminate between a standard time interval (STI) and a longer comparison interval. In the bisection task, the seal learnt to discriminate two STIs. Subsequently, it indicated its subjective perception of test time intervals as resembling either the short or long STI more. The seal, although unexperienced regarding timing experiments, learnt both tasks fast. Depending on task, time interval or duration ratio, it achieved a high temporal sensitivity with Weber fractions ranging from 0.11 to 0.26. In the bisection task, the prerequisites for the Scalar Expectancy Theory including a constant Weber fraction, the bisection point lying close to the geometric mean of the STIs, and no significant influence of the STI pair condition on the probability of a long response were met for STIs with a ratio of 1:2, but not with a ratio of 1:4. In conclusion, the harbor seal's sense of time allows precise and complex judgments of time intervals. Cross-species comparisons suggest that principles commonly found to govern timing performance can also be discerned in harbor seals.

Marine mammal sensory systems: Special issue overview.

Marine mammals are a unique group of organisms that are secondarily adapted to the aquatic environment. Their specific lifestyle requires numerous adaptations of anatomy and physiology in general, and sensory physiology in particular. During the course of evolution, marine mammal senses changed to fit with the specific requirements of underwater sensing, while at the same time retaining aerial sensing to various degrees. In this special issue, state of the art science in the field of marine mammal sensory research is reported for representatives of all marine mammal groups, unfortunately with the exclusion of the polar bear. The articles focus on somatosensation of the glabrous skin of cetaceans and mechanoreception, including haptics, hydrodynamics, and acoustics, to chemoreception. Articles even deal with electroreception, highlighting that the bottlenose dolphin can perceive weak electric stimuli, and vision, indicating that harbor seals are able to derive temporal information from an optical stimulus. Altogether this special issue illustrates the diversity of research in the field regarding sensory systems, species, or experimental approaches. The strength of this special issue lies in the combination of carefully conducted anatomical studies paired with observations and behavioral studies attempting to relate "form" and "function" as well as in the many impulses and future avenues mentioned by numerous contributions.

Specializations of somatosensory innervation in the skin of humpback whales (Megaptera novaeangliae).

Cetacean behavior and life history imply a role for somatosensory detection of critical signals unique to their marine environment. As the sensory anatomy of cetacean glabrous skin has not been fully explored, skin biopsy samples of the flank skin of humpback whales were prepared for general histological and immunohistochemical (IHC) analyses of innervation in this study. Histology revealed an exceptionally thick epidermis interdigitated by numerous, closely spaced long, thin diameter penicillate dermal papillae (PDP). The dermis had a stratified organization including a deep neural plexus (DNP) stratum intermingled with small arteries that was the source of intermingled nerves and arterioles forming a more superficial subepidermal neural plexus (SNP) stratum. The patterns of nerves branching through the DNP and SNP that distribute extensive innervation to arteries and arterioles and to the upper dermis and PDP provide a dense innervation associated through the whole epidermis. Some NF-H+ fibers terminated at the base of the epidermis and as encapsulated endings in dermal papillae similar to Merkel innervation and encapsulated endings seen in terrestrial mammals. However, unlike in all mammalian species assessed to date, an unusual acellular gap was present between the perineural sheaths and the central core of axons in all the cutaneous nerves perhaps as mechanism to prevent high hydrostatic pressure from compressing and interfering with axonal conductance. Altogether the whale skin has an exceptionally dense low-threshold mechanosensory system innervation most likely adapted for sensing hydrodynamic stimuli, as well as nerves that can likely withstand high pressure experienced during deep dives.

Contrast sensitivity in a harbor seal (Phoca vitulina).

In this study, the contrast sensitivity function (CSF) of one harbor seal was determined behaviorally in a go-/no-go-experiment at an ambient light of 0.9 lx in air. Contrast sensitivity was assessed as the reciprocal value of the threshold contrast for spatial frequencies varying between 0.03 and 1.5 cycles/deg, which were displayed with contrast ranging from 0.02 to 1 on a TFT monitor with a mean luminance of 3.8 cd/m². The CSF of the harbor seal shows the general characteristics described for other species with a peak at an intermediate frequency, a low frequency roll-off and a high frequency cut-off towards the harbor seal's resolution limit determined in a previous study. The position of the CSF's peak lies at approximately 0.5 cycles/deg and adopts an absolute height of 40. These results compare well with the cat's CSF assessed at a comparable adaptation light which might reflect similarities in lifestyle and optics.