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.

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.

Flow generation by the corona ciliata in Chaetognatha - quantification and implications for current functional hypotheses.

The corona ciliata of Chaetognatha (arrow worms) is a circular or elliptical groove lined by a rim from which multiple lines of cilia emanate, located dorsally on the head and/or trunk. Mechanoreception, chemosensation, excretion, respiration, and support of reproduction have been suggested to be its main functions. Here we provide the first experimental evidence that the cilia produce significant water flow, and the first visualisation and quantification of this flow. In Spadella cephaloptera, water is accelerated toward the corona ciliata from dorsal and anterior of the body in a funnel-shaped pattern, and expelled laterally and caudally from the corona, with part of the water being recirculated. Maximal flow speeds were approximately 140µms-1 in adult specimens. Volumetric flow rate was Q=0.0026µls-1. The funnel-shaped directional flow can possibly enable directional chemosensation. The flow measurements demonstrate that the corona ciliata is well suited as a multifunctional organ.

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.

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.

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.

Feeding kinematics, suction, and hydraulic jetting performance of harbor seals (Phoca vitulina).

The feeding kinematics, suction and hydraulic jetting capabilities of captive harbor seals (Phoca vitulina) were characterized during controlled feeding trials. Feeding trials were conducted using a feeding apparatus that allowed a choice between biting and suction, but also presented food that could be ingested only by suction. Subambient pressure exerted during suction feeding behaviors was directly measured using pressure transducers. The mean feeding cycle duration for suction-feeding events was significantly shorter (0.15±0.09 s; P<0.01) than biting feeding events (0.18±0.08 s). Subjects feeding in-water used both a suction and a biting feeding mode. Suction was the favored feeding mode (84% of all feeding events) compared to biting, but biting comprised 16% of feeding events. In addition, seals occasionally alternated suction with hydraulic jetting, or used hydraulic jetting independently, to remove fish from the apparatus. Suction and biting feeding modes were kinematically distinct regardless of feeding location (in-water vs. on-land). Suction was characterized by a significantly smaller gape (1.3±0.23 cm; P<0.001) and gape angle (12.9±2.02°), pursing of the rostral lips to form a circular aperture, and pursing of the lateral lips to occlude lateral gape. Biting was characterized by a large gape (3.63±0.21 cm) and gape angle (28.8±1.80°; P<0.001) and lip curling to expose teeth. The maximum subambient pressure recorded was 48.8 kPa. In addition, harbor seals were able to jet water at food items using suprambient pressure, also known as hydraulic jetting. The maximum hydraulic jetting force recorded was 53.9 kPa. Suction and hydraulic jetting where employed 90.5% and 9.5%, respectively, during underwater feeding events. Harbor seals displayed a wide repertoire of behaviorally flexible feeding strategies to ingest fish from the feeding apparatus. Such flexibility of feeding strategies and biomechanics likely forms the basis of their opportunistic, generalized feeding ecology and concomitant breadth of diet.

Coping with heat: function of the natal coat of cape fur seal (Arctocephalus Pusillus Pusillus) pups in maintaining core body temperature.

Cape fur seal (Arctocephalus pusillus) pups spend the first weeks of life exclusively or mainly ashore. They are exposed to intense solar radiation and high temperatures for long time periods, which results in temperatures up to at least 80°C on their black natal coat. To test the hypothesis that the natal coat has a crucial function in coping with these extreme conditions, we investigated the insulating properties of the natal coat in six captive newborn Cape fur seals during the first 50 days after birth. The natal fur differs from the adult fur not only in colour, but also in density, structure, and water repellence. We measured temperature on the fur surface and within the fur, as well as skin and rectal temperature under varying environmental conditions, comparable to the species' habitat. Experiments were designed to not influence the spontaneous behaviour of the pups. Rectal temperature was constant as long as the pups stayed dry, even during long-lasting intense solar radiation for up to 3 h. Skin temperature remained close to rectal temperature as long as the fur was dry, while with wet fur, skin temperature was significantly reduced as well. Our results show that the natal coat provides an effective insulation against overheating. The severely reduced insulation of wet natal fur against cold supports the assumption that the natal fur is an adaptation to the pups' terrestrial phase of life.

Hydrodynamic patterns from fast-starts in teleost fish and their possible relevance to predator-prey interactions.

Fast-starts are distributed over a wide phylogenetic range of fish and are used for different purposes such as striking at prey or escaping from predators. Here we investigated 42 fast-starts of rainbow trouts (Oncorhynchus mykiss) elicited by a startle stimulus. We investigated the patterns of water movements left behind by the escaping fish and their possible value as a source of information to piscivorous predators that rely on hydrodynamic sensory systems. Particle image velocimetry (PIV) measurements revealed a temporal extension of up to 25.5 min and a spatial extension of up to 1.53 m (extrapolated) for a certain flow structure called jet 1, that is the flow produced by the tail fin. Duration and spatial extension of jet 2, the flow produced by the body, were on average lower, and both jets differed in size. The fish escaped in a mean direction approximately parallel to jet 1, and antiparallel to jet 2, with a range well above 200°. This study quantified the flow patterns generated by escaping fish and, as piscivorous predators would greatly benefit from being able to analyse these flow patterns, provides cues for the behavioural and physiological investigation of hydrodynamic sensory systems.

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.

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.

Electroreception in the Guiana dolphin (Sotalia guianensis).

Passive electroreception is a widespread sense in fishes and amphibians, but in mammals this sensory ability has previously only been shown in monotremes. While the electroreceptors in fish and amphibians evolved from mechanosensory lateral line organs, those of monotremes are based on cutaneous glands innervated by trigeminal nerves. Electroreceptors evolved from other structures or in other taxa were unknown to date. Here we show that the hairless vibrissal crypts on the rostrum of the Guiana dolphin (Sotalia guianensis), structures originally associated with the mammalian whiskers, serve as electroreceptors. Histological investigations revealed that the vibrissal crypts possess a well-innervated ampullary structure reminiscent of ampullary electroreceptors in other species. Psychophysical experiments with a male Guiana dolphin determined a sensory detection threshold for weak electric fields of 4.6 µV cm(-1), which is comparable to the sensitivity of electroreceptors in platypuses. Our results show that electroreceptors can evolve from a mechanosensory organ that nearly all mammals possess and suggest the discovery of this kind of electroreception in more species, especially those with an aquatic or semi-aquatic lifestyle.

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

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

Hydrodynamic trail following in a California sea lion (Zalophus californianus).

The mystacial vibrissae of pinnipeds constitute a sensory system for active touch and detection of hydrodynamic events. Harbour seals (Phoca vitulina) and California sea lions (Zalophus californianus) can both detect hydrodynamic stimuli caused by a small sphere vibrating in the water (hydrodynamic dipole stimuli). Hydrodynamic trail following has only been shown in harbour seals. Hydrodynamical and biomechanical studies of single vibrissae of the two species showed that the specialized undulated structure of harbour seal vibrissae, as opposed to the smooth structure of sea lion vibrissae, suppresses self-generated noise in the actively moving animal. Here we tested whether also sea lions were able to perform hydrodynamic trail following in spite of their non-specialized hair structure. Hydrodynamic trails were generated by a remote-controlled miniature submarine. Linear trails could be followed with high accuracy, comparable to the performance of harbour seals, but in contrast, increasing delay resulted in a reduced performance as compared to harbour seals. The results of this study are consistent with the hypothesis that structural differences in the vibrissal hair types of otariid compared to phocid pinnipeds lead to different sensitivity of the vibrissae during forward swimming, but still reveal a good performance even in the species with non-specialized hair type.

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.

Harbor seal vibrissa morphology suppresses vortex-induced vibrations.

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

Basic mechanisms in pinniped vision.

Pinnipeds are amphibious mammals. The amphibious lifestyle is challenging for all sensory systems including vision, and specific adaptations of the eyes have evolved in response to the changed requirements concerning vision in two optically very different media, water and air. The present review summarizes the information available on pinniped eyes with an emphasis on harbour seal vision for which most information is available to date. Recent studies in this species have improved the understanding of amphibious vision by reanalysing refraction, by studying corneal topography, and by measuring visual acuity as a function of ambient luminance. The harbour seal eye can be characterized as an eye that balances high resolution, supported by data on ganglion cell density and topography, and sensitivity. Furthermore, it was shown that seals have multifocal lenses, broad visual Welds, and distinct eye movement abilities. The mechanisms described here form the basis for future research on visually guided behaviour.

Optokinetic nystagmus in harbor seals (Phoca vitulina).

Harbor seals experience motion due to self-motion and to movement in the external world. However, motion vision has not been studied yet in marine mammals moving in the underwater world. To open up this research, optokinetic nystagmus (OKN) as a basic motion sensing and retinal image stabilizing reflex was studied in four harbor seals during stimulation with moving black-and-white stripe patterns. All seals responded with optokinetic eye movements. Detailed measurements obtained with one animal revealed a moderate gain for horizontal binocular OKN. Monocularly stimulated, the seal displayed a symmetrical OKN with slightly stronger responses to leftward moving stimuli, and, surprisingly, a symmetrical OKN was found in the vertical domain.

Visual fields and eye movements in a harbor seal (Phoca vitulina).

The boundaries of the visual fields of a harbor seal were measured using static perimetry. In the seal lying on a plane surface (fixation point "0 degrees" straight ahead at eye-level), the visual field with fixed eyes extended over 208 degrees horizontally and reached from -12 degrees to +69 degrees vertically. The binocular visual field amounted to 67 degrees. Eye movements of 12 degrees (+/-2) degrees to both sides and 64 degrees upwards could be induced. In the seal performing eye movements, a visual field of 210 degrees in the horizontal plane and 121 degrees to the dorsal side was determined. From the measured eye movements, a visual field of 232 degrees in the horizontal plane appears possible.