Abstract
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.
Similar content being viewed by others
References
Ahl AS (1986) The role of vibrissae in behavior—a status review. Vet Res Commun 10:245–268
Blake RW (1983) Functional design and burst-and-coast swimming in fishes. Can J Zool 61:2491–2494
Bleckmann H (1993) Role of the lateral line in fish behaviour. In: Pitcher TJ (ed) Behaviour of teleost fishes. Chapman and Hall, London, pp 202–245
Bleckmann H (1994) Reception of hydrodynamic stimuli in aquatic and semiaquatic animals. Gustav Fischer, Stuttgart
Bleckmann H (2004) 3-D orientation with the octavolateralis system. J Physiol Paris 98:53–63
Bleckmann H (2008) Peripheral and central processing of lateral line information. J Comp Physiol A 194:145–158
Bleckmann H, Münz H (1990) Physiology of lateral-line mechanoreceptors in a teleost with highly branched, multiple lateral lines. Brain Behav Evol 35:240–250
Bleckmann H, Zelick R (2009) Lateral line system of fish. Integr Zool 4:13–25
Bleckmann H, Waldner I, Schwartz E (1981) Frequency discrimination of the surface feeding fish Aplocheilus lineatus—a prerequisite for prey localization? J Comp Physiol 143:485–490
Bleckmann H, Weiss O, Bullock TH (1989) Physiology of the lateral line mechanoreceptive regions in the elasmobranch brain. J Comp Physiol A 164:459–474
Bleckmann H, Breithaupt T, Blickhan R, Tautz J (1991a) The time course and frequency content of hydrodynamic events caused by moving fish, frogs, and crustaceans. J Comp Physiol A 168:749–757
Bleckmann H, Budelmann BU, Bullock TH (1991b) Peripheral and central nervous responses evoked by small water movements in a cephalopod. J Comp Physiol 168:247–257
Bleckmann H, Borchardt M, Horn P, Görner P (1994) Stimulus discrimination and wave source localization in fishing spiders (Dolomedes triton and D. okefinokensis). J Comp Physiol 174:305–316
Bleckmann H, Mogdans J, Engelmann J, Kröther S, Hanke W (2004) Das Seitenliniensystem: Wie Fische das Wasser fühlen. Biol Unserer Zeit 34:2–9
Bowen WD, Tully D, Boness DJ, Bulheier BM, Marshall GJ (2002) Prey-dependent foraging tactics and prey profitability in a marine mammal. Mar Ecol Prog Ser 244:235–245
Braun CB, Coombs S (2010) Vibratory sources as compound stimuli for the octavolateralis systems: dissection of specific stimulation channels using multiple behavioral approaches. J Exp Psychol 36:243–257
Breithaupt T, Schmitz B, Tautz J (1995) Hydrodynamic orientation of crayfish (Procambarus clarkii) to swimming fish prey. J Comp Physiol 177:481–491
Budelmann BU, Bleckmann H (1988) A lateral line analogue in cephalopods: water waves generate microphonic potentials in the epidermal head lines of Sepia and Lolliguncula. J Comp Physiol 164:1–5
Burgess PR, Perl ER (1973) Cutaneous mechanoreceptors and nociceptors. In: Iggo A (ed) Handbook of sensory physiology 2: somatosensory systems. Springer, Berlin, pp 29–78
Casaux R, Baroni A, Ramon A, Carlini A, Bertolin M, DiPrinzio CY (2009) Diet of the leopard seal Hydrurga leptonyx at the Danco Coast, Antarctic Peninsula. Polar Biol 32:307–310
Conley RA, Coombs S (1998) Dipole source localization by mottled sculpin. III. Orientation after site-specific, unilateral denervation of the lateral line system. J Comp Physiol 183:335–344
Coombs S, Janssen J (1990) Behavioral and neurophysiological assessment of lateral line sensitivity in the mottled sculpin, Cottus bairdi. J Comp Physiol 167:557–567
Coombs S, Patton P (2009) Lateral line stimulation patterns and prey orienting behavior in the Lake Michigan mottled sculpin (Cottus bairdi). J Comp Physiol A 195:279–297
Coombs S, Janssen J, Webb JF (1988) Diversity of lateral line systems: evolutionary and functional considerations. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 553–593
Coombs S, Görner P, Münz H (1989) The mechanosensory lateral line. Neurobiology and evolution. Springer, New York
Coombs S, Braun CB, Donovan B (2001) The orienting response of Lake Michigan mottled sculpin is mediated by canal neuromasts. J Exp Biol 204:337–348
Crespo JG (2011) A review of chemosensation and related behavior in aquatic insects. J Insect Sci 11:11–39
Dailey DD, Braun CB (2009) The detection of pressure fluctuations, sonic audition, is the dominant mode of dipole-source detection in goldfish (Carassius auratus). J Exp Psychol 35:212–223
Dailey DD, Braun CB (2011) Perception of frequency, amplitude, and azimuth of a vibratory dipole source by the octavolateralis system of goldfish (Carassius auratus). J Comp Psychol 125:286–295
Dehn L-A, Sheffield GG, Follmann EH, Duffy LK, Thomas DL, O’Hara TM (2007) Feeding ecology of phocid seals and some walrus in the Alaskan and Canadian Arctic as determined by stomach contents and stable isotope analysis. Polar Biol 30:167–181
Dehnhardt G (2002) Sensory systems. In: Hoelzel AR (ed) Marine mammal biology. Blackwell, Oxford, pp 116–141
Dehnhardt G, Kaminski A (1995) Sensitivity of the mystacial vibrissae of harbour seals (Phoca vitulina) for size differences of actively touched objects. J Exp Biol 198:2317–2323
Dehnhardt G, Mauck B (2008) Mechanoreception in secondarily aquatic vertebrates. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkely, pp 295–314
Dehnhardt G, Mauck B, Bleckmann H (1998a) Seal whiskers detect water movements. Nature 394:235–236
Dehnhardt G, Mauck B, Hyvärinen H (1998b) Ambient temperature does not affect the tactile sensitivity of mystacial vibrissae of harbour seals. J Exp Biol 201:3023–3029
Dehnhardt G, Mauck B, Hanke W, Bleckmann H (2001) Hydrodynamic trail following in harbor seals (Phoca vitulina). Science 293:102–104
Dehnhardt G, Mauck B, Hanke W (2004) Hydrodynamic perception in seals. In: Ilg U, Bülthoff HH, Mallot A (eds) Dynamic perception. Akademische Verlagsgesellschaft Aka GmbH, Berlin
Denton EJ, Gray J (1985) Lateral-line-like antennae of certain of the Penaeidea (Crustacea, Decapoda, Natantia). Proc R Soc B 226:249
Denton EJ, Gray JAB (1988) Mechanical factors in the excitation of the lateral line of fishes. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 595–617
Drucker EG, Lauder GV (2002) Experimental hydrodynamics of fish locomotion: functional insights from wake visualization. Integr Comp Biol 42:243–257
Dykes RW (1975) Afferent fibers from mystacial vibrissae of cats and seals. J Neurophysiol 38:650–662
Ebara S, Kumamoto K, Matsuura T, Mazurkiewicz JE, Rice FL (2002) Similarities and differences in the innervation of mystacial vibrissal follicle–sinus complexes in the rat and cat: a confocal microscopic study. J Comp Neurol 449:103–119
Engelmann J, Hanke W, Bleckmann H (2002) Lateral line reception in still- and running water. J Comp Physiol 188:513–526
Fay FH (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens Illiger. N Am Fauna 74:1–279
Fields DM, Shaeffer DS, Weissburg MJ (2002) Mechanical and neural responses from the mechanosensory hairs on the antennule of Gaussia princeps. Mar Ecol Prog Ser 227:173–186
Gellermann LW (1933) Chance orders of alternating stimuli in visual discrimination experiments. J Genet Psychol 42:206–208
Gentry RL (2009) Eared seals. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, Amsterdam, pp 339–342
Ginter CC, Fish FE, Marshall CD (2010) Morphological analysis of the bumpy profile of phocid vibrissae. Mar Mamm Sci 26:733–743
Ginter CC, DeWitt TJ, Fish FE, Marshall CD (2012) Fused traditional and geometric morphometrics demonstrate pinniped whisker diversity. PLoS ONE 7:1–10
Gläser N, Wieskotten S, Otter C, Dehnhardt G, Hanke W (2011) Hydrodynamic trail following in a California sea lion (Zalophus californianus). J Comp Physiol A 197:141–151
Goodman-Lowe GD (1998) Diet of the Hawaiian monk seal (Monachus schauinslandi) from the Northwestern Hawaiian islands during 1991 to 1994. Mar Biol 132:535–546
Görner P (1973) The importance of the lateral line system for the perception of surface waves in the clawed toad, Xenopus laevis. Experientia 9:295–296
Gottschaldt KM, Iggo A, Young DW (1973) Functional characteristics of mechanoreceptors in sinus hair follicles of cat. J Physiol Lond 235:287–315
Green K, Williams R (1986) Observations on food remains in feces of elephant, leopard and crab-eater seals. Polar Biol 6:43–45
Halata Z (1975) The mechanoreceptors of the mammalian skin ultrastructure and morphological classification. Adv Anat Embryol Cell Biol 50:3–77
Halata Z, Munger BL (1980) Sensory nerve-endings in rhesus-monkey sinus hairs. J Comp Neurol 192:645–663
Hall-Aspland S, Rogers T (2007) Identification of hairs found in leopard seal (Hydrurga leptonyx) scats. Polar Biol 30:581–585
Hammond PS, Hall AJ, Prime JH (1994a) The diet of gray seals around Orkney and other islands and mainland sites in north-eastern Scotland. J Appl Ecol 31:340–350
Hammond PS, Hall AJ, Prime JH (1994b) The diet of grey seals in the inner and Outer Hebrides. J Appl Ecol 31:737–746
Hanke W, Bleckmann H (2004) The hydrodynamic trails of Lepomis gibbosus (Centrarchidae), Colomesus psittacus (Tetraodontidae) and Thysochromis ansorgii (Cichlidae) measured with scanning particle image velocimetry. J Exp Biol 207:1585–1596
Hanke W, Brücker C, Bleckmann H (2000) The ageing of the low-frequency water disturbances caused by swimming goldfish and its possible relevance to prey detection. J Exp Biol 203:1193–1200
Hanke FD, Dehnhardt G, Schaeffel F, Hanke W (2006a) Corneal topography, refractive state, and accommodation in harbor seals (Phoca vitulina). Vis Res 46:837–847
Hanke W, Römer R, Dehnhardt G (2006b) Visual fields and eye movements in a harbor seal (Phoca vitulina). Vis Res 46:2804–2814
Hanke FD, Hanke W, Scholtyssek C, Dehnhardt G (2009) Basic mechanisms in pinniped vision. Exp Brain Res 199:299–311
Hanke W, Witte M, Miersch L, Brede M, Oeffner J, Michael M, Hanke F, Leder A, Dehnhardt G (2010) Harbor seal vibrissa morphology suppresses vortex-induced vibrations. J Exp Biol 213:2665–2672
Hanke FD, Scholtyssek C, Hanke W, Dehnhardt G (2011) Contrast sensitivity in a harbor seal (Phoca vitulina). J Comp Physiol 197:203–210
Hanke W, Wieskotten S, Niesterok B, Miersch L, Witte M, Brede M, Leder A, Dehnhardt G (2012) Hydrodynamic perception in pinnipeds. In: Tropea C, Bleckmann H (eds) Nature-inspired fluid mechanics. Springer, Berlin, pp 225–240
Harris GG, van Bergeijk W (1962) Evidence that the lateral-line organ responds to near-field displacements of sound sources in water. J Acoust Soc Am 34:1831–1841
Hartmann MJ, Johnson NJ, Towal RB, Assad C (2003) Mechanical characteristics of rat vibrissae: resonant frequencies and damping in isolated whiskers and in the awake behaving animal. J Neurosci 23:6510–6519
Heath CB, Perrin WF (2009) California, Galapagos, and Japanese sea lions (Zalophus californianus, Zalophus wollebaeki, and Zalophus japonicus). In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, Amsterdam, pp 170–176
Heinisch P, Wiese K (1987) Sensitivity to movement and vibration of water in the north-sea shrimp Crangon crangon. J Crustac Biol 7:401–413
Hjelset AM, Andersen M, Gjertz I, Lydersen C, Gulliksen B (1999) Feeding habits of bearded seals (Erignathus barbatus) from the Svalbard area, Norway. Polar Biol 21:186–193
Hückstädt LA, Burns JM, Koch PL, McDonald BI, Crocker DE, Costa DP (2012) Diet of a specialist in a changing environment: the crabeater seal along the western Antarctic Peninsula. Mar Ecol Prog Ser 455:287–301
Humphrey JAC, Barth FG (2008) Medium-flow sensing hairs: biomechanics and models. In: Casas J, Simpson SJ (eds) Advances in insect physiology: insect mechanics and control, vol 34. Academic Press, London, pp 1–80
Hyvärinen H, Palviainen A, Strandberg U, Holopainen IJ (2009) Aquatic environment and differentiation of vibrissae: comparison of sinus hair systems of ringed seal, otter and pole cat. Brain Behav Evol 74:268–279
Kastelein RA, Muller M, Terlouw A (1994) Oral suction of the Pacific walrus (Odobenus rosmarus divergens) in air and under water. Z Säugetierk Intern J Mamm Biol 59:105–115
Killian KA, Page CH (1992) Mechanosensory afferents innervating the swimmerets of the lobster. 2. Afferents activated by hair deflection. J Comp Physiol A 170:501–508
King JE (1983) Seals of the world. Cornell University Press, Ithaca
Ladygina TF, Popov VV, Supin AY (1985) Topical organization of somatic projections in the fur seal cerebral cortex. Neurophysiology 17:246–252
Ling JK (1977) Vibrissae of marine mammals. In: Harrison RJ (ed) Functional anatomy of marine mammals. Academic Press, London, pp 387–415
Marshall CD, Amin H, Kovacs KM, Lydersen C (2006) Microstructure and innervation of the mystacial vibrissal follicle–sinus complex in bearded seals, Erignathus barbatus (Pinnipedia : Phocidae). Anat Rec A 288:13–25
Marshall CD, Kovacs KM, Lydersen C (2008) Feeding kinematics, suction and hydraulic jetting capabilities in bearded seals (Erignathus barbatus). J Exp Biol 211:699–708
McConnell BJ, Fedak MA, Lovell P, Hammond PS (1999) Movements and foraging areas of grey seals in the North Sea. J Appl Ecol 36:573–590
McKenzie J, Wynne KM (2008) Spatial and temporal variation in the diet of Steller sea lions in the Kodiak Archipelago, 1999 to 2005. Mar Ecol Prog Ser 360:265–283
Mecenero S, Kirkman SP, Roux JP (2005) Seabirds in the diet of Cape fur seals Arctocephalus pusillus pusillus at three mainland breeding colonies in Namibia. Afr J Mar Sci 27:509–512
Mecenero S, Roux JP, Underhill LG, Bester MN (2006) Diet of Cape fur seals Arctocephalus pusillus pusillus at three mainland breeding colonies in Namibia. 1. Spatial variation. Afr J Mar Sci 28:57–71
Meyer G, Klein A, Mogdans J, Bleckmann H (2012) Toral lateral line units of goldfish, Carassius auratus, are sensitive to the position and vibration direction of a vibrating sphere. J Comp Physiol A 198:639–653
Miersch L (2002) Konstruktion eines Messaufbaus zur Untersuchung strömungsinduzierter Schwingungen an natürlichen Haarsensoren (Vibrissen). Fachbereich Physik, Freie Universität Berlin, Berlin
Miersch L, Hanke W, Wieskotten S, Hanke FD, Oeffner J, Leder A, Brede M, Witte M, Dehnhardt G (2011) Flow sensing by pinniped whiskers. Phil Trans R Soc B 366:3077–3084
Milne-Thompson LM (1968) Theoretical hydrodynamics. Macmillan, London
Mitchinson B, Gurney KN, Redgrave P, Melhuish C, Pipe AG, Pearson M, Gilhespy I, Prescott TJ (2004) Empirically inspired simulated electro-mechanical model of the rat mystacial follicle–sinus complex. Proc R Soc B 271:2509–2516
Mogdans J, Nauroth IE (2011) The oscar, Astronotus ocellatus, detects and discriminates dipole stimuli with the lateral line system. J Comp Physiol A 197:959–968
Münz H (1985) Single unit activity in the peripheral lateral line system of the cichlid fish Sarotherodon niloticus L. J Comp Physiol A 157:555–568
Nauen JC, Lauder GV (2002) Hydrodynamics of caudal fin locomotion by chub mackerel, Scomber japonicus (Scombridae). J Exp Biol 205:1709–1724
Nauroth IE, Mogdans J (2009) Goldfish and oscars have comparable responsiveness to dipole stimuli. Naturwissenschaften 96:1401–1409
Neimark MA, Andermann ML, Hopfield JJ, Moore CI (2003) Vibrissa resonance as a transduction mechanism for tactile encoding. J Neurosci 23:6499–6509
Niesterok B, Hanke W (2012) Hydrodynamic patterns from fast-starts in teleost fish and their possible relevance to predator–prey interactions. J Comp Physiol A. doi:10.1007/s00359-012-0775-5
Rice FL, Mance A, Munger BL (1986) A comparative light microscopical analysis of the sensory innervation of the mysticial pad. 1. Innervation of vibrissal follicle–sinus complexes. J Comp Neurol 252:154–174
Rice FL, Kinnman E, Aldskogius H, Johansson O, Arvidsson J (1993) The innervation of the mystacial pad of the rat as revealed by PGP 9.5 immunofluorescence. J Comp Neurol 337:366–385
Rice FL, Fundin BT, Arvidsson J, Aldskogius H, Johansson O (1997) Comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat. J Comp Neurol 385:149–184
Schulte-Pelkum N, Wieskotten S, Hanke W, Dehnhardt G, Mauck B (2007) Tracking of biogenic hydrodynamic trails in a harbor seal (Phoca vitulina). J Exp Biol 210:781–787
Schwalbe MAB, Bassett DK, Webb JF (2012) Feeding in the dark: lateral-line-mediated prey detection in the peacock cichlid Aulonocara stuartgranti. J Exp Biol 215:2060–2071
Shariff K, Leonard A (1992) Vortex rings. Annu Rev Fluid Mech 24:235–279
Sharples RJ, Arrizabalaga B, Hammond PS (2009) Seals, sandeels and salmon: diet of harbour seals in St. Andrews Bay and the Tay Estuary, southeast Scotland. Mar Ecol Prog Ser 390:265–276
Simpkins MA, Kelly BP, Wartzok D (2001a) Three-dimensional analysis of search behaviour by ringed seals. Anim Behav 62:67–72
Simpkins MA, Kelly BP, Wartzok D (2001b) Three-dimensional diving behaviors of ringed seals (Phoca hispida). Mar Mamm Sci 17:909–925
Simpkins MA, Kelly BP, Wartzok D (2001c) Three-dimensional movements within individual dives by ringed seals (Phoca hispida). Can J Zool 79:1455–1464
Siniff DB, Stirling I, Bengston JL, Reichle RA (1979) Social and reproductive behavior of crabeater seals (Lobodon carcinophagus) during the Australian spring. Can J Zool 57:2243–2255
Suuronen P, Lehtonen E (2012) The role of salmonids in the diet of grey and ringed seals in the Bothnian Bay, northern Baltic Sea. Fish Res 125:283–288
Tautz J, Masters MW, Aicher B, Markl H (1981) A new type of water vibration receptor on the crayfish antenna. J Comp Physiol 144:533–541
Watkins WA, Wartzok D (1985) Sensory biophysics of marine mammals. Mar Mamm Sci 1:219–260
Weiffen M, Möller B, Mauck B, Dehnhardt G (2006) Effect of water turbidity on the visual acuity of harbor seals (Phoca vitulina). Vis Res 46:1777–1783
Welch HE, Bergmann MA, Siferd TD, Martin KA, Curtis MF, Crawford RE, Conover RJ, Hop H (1992) Energy-flow through the marine ecosystem of the Lancaster sound region, Arctic Canada. Arctic 45:343–357
Westerweel J (1997) Fundamentals of digital particle image velocimetry. Meas Sci Technol 8:1379–1392
Wiese K (1974) Mechanoreceptive system of prey localization in Notonecta. 2. Principle of prey localization. J Comp Physiol 92:317–325
Wiese K (1976) Mechanoreceptors for near-field water displacements in crayfish. J Neurophysiol 39:816–833
Wieskotten S, Dehnhardt G, Mauck B, Miersch L, Hanke W (2010a) Hydrodynamic determination of the moving direction of an artificial fin by a harbour seal (Phoca vitulina). J Exp Biol 213:2665–2675
Wieskotten S, Dehnhardt G, Mauck B, Miersch L, Hanke W (2010b) The impact of glide phases on the trackability of hydrodynamic trails in harbour seals (Phoca vitulina). J Exp Biol 213:3734–3740
Wieskotten S, Mauck B, Miersch L, Dehnhardt G, Hanke W (2011) Hydrodynamic discrimination of wakes caused by objects of different size or shape in a harbour seal (Phoca vitulina). J Exp Biol 214:1922–1930
Witte M, Hanke W, Wieskotten S, Miersch L, Brede M, Dehnhardt G, Leder A (2012) On the wake flow dynamics behind harbor seal vibrissae—a fluid mechanical explanation for an extraordinary capability. In: Tropea C, Bleckmann H (eds) Nature-inspired flow mechanics. Springer, Berlin, pp 241–260
Yen J, Lenz PH, Gassie DV, Hartline DK (1992) Mechanoreception in marine copepods—ecophysiological studies on the 1st antennae. J Plankton Res 14:495–512
Acknowledgments
The authors’ original work was funded by grants of the German Research Foundation (DFG) to W.H. and G.D., and the Volkswagenstiftung to G.D. We thank the DFG and the Office of Naval Research Global for supporting a conference on Sensory Biology of Aquatic Mammals in October 2012 at the Marine Science Center Rostock, accompanying this special issue of the Journal of Comparative Physiology A.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hanke, W., Wieskotten, S., Marshall, C. et al. Hydrodynamic perception in true seals (Phocidae) and eared seals (Otariidae). J Comp Physiol A 199, 421–440 (2013). https://doi.org/10.1007/s00359-012-0778-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-012-0778-2