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.

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.

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.

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.

"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.

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.

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.

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.

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.

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.

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.

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.

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.

The Pupillary Response of the Common Octopus (Octopus vulgaris).

Cephalopods have very conspicuous eyes that are often compared to fish eyes. However, in contrast to many fish, the eyes of cephalopods possess mobile pupils. To increase the knowledge of pupillary and thus visual function in cephalopods, the dynamics of the pupil of one of the model species among cephalopods, the common octopus (Octopus vulgaris), was determined in this study. We measured pupillary area as a function of ambient luminance to document the light and dark reaction of the octopus eye. The results show that weak light (<1 cd/m2) is enough to cause a pupil constriction in octopus, and that the pupil reacts fast to changing light conditions. The t50-value defined as the time required for achieving half-maximum constriction ranged from 0.45 to 1.29 s and maximal constriction from 10 to 20% of the fully dilated pupil area, depending on the experimental condition. Axial light had a stronger influence on pupil shape than light from above, which hints at a shadow effect of the horizontal slit pupil. We observed substantial variation of the pupil area under all light conditions indicating that light-independent factors such as arousal or the need to camouflage the eye affect pupil dilation/constriction. In conclusion, the documentation of pupil dynamics provides evidence that the pupil of octopus is adapted to low ambient light levels. Nevertheless it can quickly adapt to and thus function under brighter illumination and in a very inhomogeneous light environment, an ability mediated by the dynamic pupil in combination with previously described additional processes of light/dark adaptation in octopus.

E Pluribus Octo - Building Consensus on Standards of Care and Experimentation in Cephalopod Research; a Historical Outlook.

The Directive 2010/63/EU "on the protection of animals used for scientific purposes" originally induced some concern among cephalopod researchers, because of the inclusion of cephalopod mollusks as the only invertebrates among the protected species. Here we reflect on the challenges and issues raised by the Directive on cephalopod science, and discuss some of the arguments that elicited discussion within the scientific community, to facilitate the implementation of the Directive 2010/63/EU in the scientific research context. A short overview of the aims of the COST Action FA1301 "CephsInAction," serves as a paradigmatic instance of a pragmatic and progressive approach adopted to respond to novel legislative concerns through community-building and expansion of the historical horizon. Between 2013 and 2017, the COST Action FA1301 has functioned as a hub for consolidation of the cephalopod research community, including about 200 representatives from 21 countries (19 European). Among its aims, CephsInAction promoted the collection, rationalization, and diffusion of knowledge relevant to cephalopods. In the Supplementary Material to this work, we present the translation of the first-published systematic set of guidelines on the care, management and maintenance of cephalopods in captivity (Grimpe, 1928), as an example of the potential advantages deriving from the confluence of pressing scientific concerns and historical interests.

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.

The Eye of the Common Octopus (Octopus vulgaris).

Octopus vulgaris, well-known from temperate waters of the Mediterranean Sea and a well-cited model species among the cephalopods, has large eyes with which it scans its environment actively and which allow the organism to discriminate objects easily. On cursory examination, the single-chambered eyes of octopus with their spherical lenses resemble vertebrate eyes. However there are also apparent differences. For example, the retina of the octopus is everted instead of inverted, and it is equipped with primary rhabdomeric photoreceptors rather than secondary ciliary variety found in the retina of the vertebrate eye. The eyes of octopus are well adapted to the habitat and lifestyle of the species; the pupil closes quickly as a response to sudden light stimuli mimicking a situation in which the octopus leaves its den in shallow water during daytime. Although the many general anatomical and physiological features of octopus vision have been described elsewhere, our review reveals that a lot of information is still missing. Investigations that remain to be undertaken include a detailed examination of the dioptric apparatus or the visual functions such as brightness discrimination as well as a conclusive test for a faculty analogous to, or in lieu of, color vision. For a better understanding of the octopus eye and the functions mediated by it, we suggest that future studies focus on knowledge gaps that we outline in the present review.

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.