SUMMARYHarbor 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. Supplementary material available online at
Marine mammals often forage in dark or turbid waters. Whereas dolphins use echolocation under such conditions, pinnipeds apparently lack this sensory ability. For seals hunting in the dark, one source of sensory information may consist of fish-generated water movements, which seals can detect with their highly sensitive whiskers. Water movements in the wake of fishes persist for several minutes. Here we show that blindfolded seals can use their whiskers to detect and accurately follow hydrodynamic trails generated by a miniature submarine. This shows that hydrodynamic information can be used for long-distance prey location.
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 mV cm 21 , 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.
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.
The hydrodynamic trails of fish belonging to the families Centrarchidae, Tetraodontidae and Cichlidae were investigated. Water movements were measured in six horizontal planes, spaced 10-12·mm apart, for up to 5·min after the passage of a fish, using a computer controlled array of modulated laser diodes. We measured continuously and non-continuously swimming fish. Water velocities decayed rapidly in the leading seconds after the passage of a fish, but could still be measured for a period considerably longer than that. In still water (median water velocity <0.5·mm·s -1 ), the hydrodynamic trails of Lepomis gibbosus lasted for more than 5·min. The trails of Colomesus psittacus and Thysochromis ansorgii could be detected for more than 30·s and more than 3·min, respectively. The water disturbance left behind by these fish was sufficient to be sensed by a piscivorous predator at a distance where vision or hearing frequently fail. Acoustic stimuli estimated from a dipole model in a distance that would be covered by the tested fish in 1·min (4-25·m) were 1.5×10 -7 to 3.1×10 -10 ·m·s -2 , while the hearing threshold of a perch is three orders of magnitude above that. By contrast, the fish wakes after 1·min (except for one Colomesus wake) contained water velocities between 0.95 and 2.05·mm·s -1 , which are within the detection range of hydrodynamic sensory systems. The three species differed with respect to water velocities, the spatial extent of the fish-generated water disturbances and the structure of the wake.
Beside their haptic function, vibrissae of harbour seals (Phocidae) and California sea lions (Otariidae) both represent highly sensitive hydrodynamic receptor systems, although their vibrissal hair shafts differ considerably in structure. To quantify the sensory performance of both hair types, isolated single whiskers were used to measure vortex shedding frequencies produced in the wake of a cylinder immersed in a rotational flow tank. These measurements revealed that both whisker types were able to detect the vortex shedding frequency but differed considerably with respect to the signal-to-noise ratio (SNR). While the signal detected by sea lion whiskers was substantially corrupted by noise, harbour seal whiskers showed a higher SNR with largely reduced noise. However, further analysis revealed that in sea lion whiskers, each noise signal contained a dominant frequency suggested to function as a characteristic carrier signal. While in harbour seal whiskers the unique surface structure explains its high sensitivity, this more or less steady fundamental frequency might represent the mechanism underlying hydrodynamic reception in the fast swimming sea lion by being modulated in response to hydrodynamic stimuli impinging on the hair.
The potent and selective Gq protein inhibitor depsipeptide FR900359 (FR), originally discovered as the product of an uncultivable plant endosymbiont, is synthesized by a complex biosynthetic system comprising two nonribosomal peptide synthetase (NRPS) assembly lines. Here we characterize a cultivable bacterial FR producer, enabling detailed investigations into biosynthesis and attachment of the functionally important FR side chain. We reconstitute side chain assembly by the monomodular NRPS FrsA and the non-heme monooxygenase FrsH, and characterize intermolecular side chain transesterification to the final macrocyclic intermediate FR-Core, mediated by the FrsA thioesterase domain. We harness FrsA substrate promiscuity to generate FR analogs with altered side chains and demonstrate indispensability of the FR side chain for efficient Gq inhibition by comparative bioactivity, toxicity and docking studies. Finally, evolution of FR and side chain biosynthesis is discussed based on bioinformatics analyses. Side chain transesterification boosts potency and target affinity of selective Gq inhibitor natural products.
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