Abstract
Manatees live in shallow, frequently turbid waters. The sensory means by which they navigate in these conditions are unknown. Poor visual acuity, lack of echolocation, and modest chemosensation suggest that other modalities play an important role. Rich innervation of sensory hairs that cover the entire body and enlarged somatosensory areas of the brain suggest that tactile senses are good candidates. Previous tests of detection of underwater vibratory stimuli indicated that they use passive movement of the hairs to detect particle displacements in the vicinity of a micron or less for frequencies from 10 to 150 Hz. In the current study, hydrodynamic stimuli were created by a sinusoidally oscillating sphere that generated a dipole field at frequencies from 5 to 150 Hz. Go/no-go tests of manatee postcranial mechanoreception of hydrodynamic stimuli indicated excellent sensitivity but about an order of magnitude less than the facial region. When the vibrissae were trimmed, detection thresholds were elevated, suggesting that the vibrissae were an important means by which detection occurred. Manatees were also highly accurate in two-choice directional discrimination: greater than 90% correct at all frequencies tested. We hypothesize that manatees utilize vibrissae as a three-dimensional array to detect and localize low-frequency hydrodynamic stimuli.
Similar content being viewed by others
Abbreviations
- FSC:
-
Follicle-sinus complex
- F:
-
Frequency (Hz)
References
Bachteler D, Dehnhardt G (1999) Active touch performance in the Antillean manatee: evidence for a functional differentiation of facial tactile hairs. Zool 102:61–69
Barth FG (2014) The slightest whiff of air: airflow sensing in arthropods. In: Bleckmann H, Mogdans J, Coombs SL (eds) Flow sensing in air and water. Springer, Heidelberg, pp 169–196
Bauer GB, Gaspard JC III, Colbert DE, Leach JB, Stamper SA, Mann DA, Reep RL (2012) Tactile discrimination of textures by Florida manatees (Trichechus manatus latirostris). Mar Mammal Sci 28:E456–471
Bauer GB, Colbert DE, Gaspard JC, Littlefield B, Fellner W (2003) Underwater visual acuity of Florida manatees (Trichechus manatus latirostris). Int J Comp Psych 16:130–142
Bell CC (1982) Properties of a modifiable efference copy in an electric fish. J Neurophysiol 47:1043–1056
Bleckmann H (1994) Reception of hydrodynamic stimuli in aquatic and semiaquatic animals. Prog Zool 41:1–115
Bleckmann H, Mogdans J, Dehnhardt G (2001) Lateral line research: the importance of using natural stimuli in studies of sensory systems. In: Barth FG, Schmid A (eds) Ecology of sensing. Springer, Berlin, pp 149–167
Bryden MM, Marsh H, MacDonald BW (1978) The skin and hair of the dugong, Dugong dugon. J Anat 126:637–638
Budelmann BU (1989) Hydrodynamic receptor systems in invertebrates. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line, neurobiology and evolution. Springer, New York, pp 607–632
Campenhausen CV, Riess I, Weissert R (1981) Detection of stationary objects in the blind cave fish Anoptichthys jordani (Characidae). J Comp Physiol A 143:369–374
Colbert D, Fellner W, Bauer GB, Manire CA, Rhinehart HL (2001) Husbandry and research training of two Florida manatees (Trichechus manatus latirostris). Aquat Mamm 27:16–23
Colbert DE, Gaspard JC, Reep R, Mann DA, Bauer GB (2009) Four–choice sound localization abilities of two Florida manatees, Trichechus manatus latirostris. J Exp Biol 12:2105–2122
Coombs S (1994) Nearfield detection of dipole sources by the goldfish (Carassius auratus) and the mottled sculpin (Cottus bairdi). J Exp Biol 190:109–129
Coombs S, Montgomery JC (1999) The enigmatic lateral line system. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 319–362
Coombs S, New JG, Nelson M (2002) Information–processing demands in electrosensory and mechanosensory lateral line systems. J Physiol Paris 96:341–354
Cornsweet TN (1962) The staircase method in psychophysics. Am J Psychol 75:485–491
Czech-Damal NU, Liebschner A, Miersch L, Klauer G, Hanke FD, Marshall C, Dehnhardt G, Hanke W (2012) Electroreception in the Guiana dolphin (Sotalia guianensis). Proc R Soc B 279:663–668
Dehnhardt G (1994) Tactile size discrimination by a California sea lion (Zalophus californianus) using its mystacial vibrissae. J Comp Physiol A 175:791–800
Dehnhardt G, Dücker G (1996) Tactile discrimination of size and shape by a California sea lion (Zalophus californianus). Ani Learn Beh 24:366–374
Dehnhardt G, Kaminski A (1995) Sensitivity of the mystacial vibrissae of harbor seals (Phoca vitulina) for size differences of actively touched objects. J Exp Biol 198:2317–2323
Dehnhardt G, Mauck B, Bleckmann H (1998) Seal whiskers detect water movements. Nature 394:235–236
Dehnhardt G, Hyvarinen H, Palviainen A, Klauer G (1999) Structure and innervation of the vibrissal follicle–sinus complex in the Australian water rat, Hydromys chrysogaster. J Comp Neurol 411:550–562
Dehnhardt G, Mauck B, Hanke W, Bleckmann H (2001) Hydrodynamic trail–following in harbor seals (Phoca vitulina). Science 293:102–104
Dosch F (1915) (translated by Sinclair DA) Structure and development of the integument of Sirenia. Tech Trans No 1626. National Research Council of Canada, Ottawa, 1973. (Bau und entwicklung des integuments der Sirenen. Jenaische Zeitschrift 53:805–854, 1914–1915)
Fay FH (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens. USFWS, North American Fauna 74, Washington, DC
Fay RR (1984) The goldfish ear codes the axis of acoustic particle motion in three dimensions. Science 225:951–954
Fay RR, Olsho LW (1979) Discharge patterns of lagenar and saccular neurons of the goldfish eighth nerve: displacement sensitivity and directional characteristics. Comp Biochem Physiol 62:377–386
Fay RR, Edds–Walton PL, Highstein SM (1994) Directional sensitivity of saccular afferents of the toadfish to linear acceleration at audio frequencies. Biol Bull 187:258–259
Gaspard JC III, Bauer GB, Reep RL, Dziuk K, Read L, Mann DA (2013) Detection of hydrodynamic stimuli by the Florida manatee (Trichechus manatus latirostris). J Comp Physiol A 199:441–450
Gaspard JC, Bauer GB, Reep RL, Dziuk K, Cardwell A, Read L, Mann DA (2012) Audiogram and auditory critical ratios of two Florida manatees (Trichechus manatus latirostris). J Exp Biol 215:1442–1447
Gerstein ER, Gerstein L, Forsythe S, Blue J (1999) Underwater audiogram of a West Indian manatee (Trichechus manatus). J Acoust Soc Amer 105:3575–3583
Ginter C, Fish F, Marshall CD (2010) Morphological analysis of the bumpy profile of phocid vibrissae. Mar Mammal Sci 26:733–743
Glaser 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
Hanke W, Wieskotten S, Kruger Y, Glaser N, Marshall CD, Dehnhardt G (2013) Hydrodynamic perception in true seals (Phocidae) and eared seals (Otariidae). J Comp Physiol A 199:421–440
Hartman DS (1979) Ecology and behavior of the manatee (Trichechus manatus). Am Soc Mam Spec Pub 5:1–153
Hassan ES (1986) On the discrimination of spatial intervals by the blind cave fish (Anoptichthys jordani). J Comp Physiol A 159:701–710
Hassan ES (1989) Hydrodynamic imaging of the surroundings by the lateral line of the blind cave fish Anoptichthys jordani. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line, neurobiology and evolution. Springer, New York, pp 217–227
Kalmijn AJ (1988) Hydrodynamics and acoustic field detection. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 83–130
Kamiya T, Yamasaki F (1981) A morphological note on the sinus hair of the dugong. In: Marsh H (ed) The dugong. Dept. of Zoology. James Cook University of North Queensland, Australia, pp 111–113
Kastelein RA, Van Gaalen MA (1988) The tactile sensitivity of the mystacial vibrissae of a Pacific walrus (Odobenus rosmarus divergens). Part 1. Aquat Mamm 14:123–133
Layne JN, Caldwell DK (1964) Behavior of the Amazon dolphin, Inia geoffrensis (Blainville), in captivity. Zool 49:81–108
Leitch DB, Catania KC (2012) Structure, innervation and response properties of integumentary sensory organs in crocodilians. J Exp Biol 214:4217–4230
Levin MJ, Pfieffer CJ (2002) Gross and microscopic observations on the lingual structure of the Florida manatee Trichechus manatus latirostris. Anat Histol Embryol 31:278–285
Ling JK (1977) Vibrissae of marine mammals. In: Harrison JB (ed) Functional anatomy of marine mammals, vol 3. Academic Press, London, pp 387–415
Mackay–Sim A, Duvall D, Graves BM (1985) The West Indian manatee, Trichechus manatus, lacks a vomeronasal organ. Brain Behav Evol 27:186–194
Mann D, Colbert DE, Gaspard JC, Casper B, Cook MLH, Reep RL, Bauer GB (2005) Temporal resolution of the Florida manatee (Trichechus manatus latirostris) auditory system. J Comp Physiol 191:903–908
Marshall CD, Reep RL (1995) Manatee cerebral cortex: cytoarchitecture of the caudal region in Trichechus manatus latirostris. Brain Behav Evol 45:1–18
Marshall CD, Huth GD, Edmonds VM, Halin DL, Reep RL (1998) Prehensile use of perioral bristles during feeding and associated behaviors of the Florida manatee (Trichechus manatus latirostris). Mar Mammal Sci 14:274–289
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 288A:13–25
Mass AM, Ketten DR, Odell DK, Supin AY (2012) Ganglion cell distribution and retinal resolution in the Florida manatee, Trichechus manatus latirostris. Anat Rec 295:177–186
Mercado E III (2014) Tubercles: what sense is there? Aquat Mamm 40:95–103
Northcutt RG (1989) The phylogenetic distribution and innervation of craniate mechanoreceptive lateral lines. In: Coombs S, Görner P, Mü nz H (eds) The mechanosensory lateral line, neurobiology and evolution. Springer, New York, pp 17–78
Pruszynski JA, Johansson RS (2014) Edge–orientation processing in first–order tactile neurons. Nature Neurosci 17:1404–1409
Reep RL, Johnson JI, Switzer RC, Welker WI (1989) Manatee cerebral cortex: cytoarchitecture of the frontal region in Trichechus manatus latirostris. Brain Behav Evol 34:365–386
Reep RL, Marshall CD, Stoll ML, Whitaker DM (1998) Distribution and innervation of facial bristles and hairs in the Florida manatee (Trichechus manatus latirostris). Marine Mammal Sci 14:257–273
Reep RL, Marshall CD, Stoll ML, Homer BL, Samuelson DA (2001) Microanatomy of perioral bristles in the Florida manatee, Trichechus manatus latirostris. Brain Behav Evol 58:1–14
Reep RL, Marshall CD, Stoll ML (2002) Tactile hairs on the postcranial body in Florida manatees: a mammalian lateral line? Brain Behav Evol 59:141–154
Reynolds JE III (1979) The semisocial manatee. Nat Hist 88:44–53
Rice FL, Mance A, Munger BL (1986) A comparative light microscopic analysis of the innervation of the mystacial pad. I. Vibrissal follicles. J Comp Neurol 252:154–174
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
Sarko DK, Reep RL (2007) Somatosensory areas of manatee cerebral cortex: histochemical characterization and functional implications. Brain Behav Evol 69:20–36
Sarko DK, Johnson JI, Switzer RC, Welker WI, Reep RL (2007a) Somatosensory nuclei of the brainstem and thalamus in Florida manatees. Anat Rec 290:1138–1165
Sarko DK, Rice FL, Reep RL, Mazurkiewicz JE (2007b) Adaptations in the structure and innervation of follicle–sinus complexes to an aquatic environment as seen in the Florida manatee (Trichechus manatus latirostris). J Comp Neurol 504:217–237
Schulte–Pelkum N, Wieskotten S, Hanke W, Dehnhardt G, Mauck B (2007) Tracking of biogenic hydrodynamic trails in harbour seals (Phoca vitulina). J Exp Biol 210:781–787
Slone DH, Reid JP, Kenworthy WJ, diCarlo G, Butler SM (2012) Manatees mapping seagrass. Seagrass Watch 46:8–11
Sokolov VE (1986) Manatee—morphological description. Nauka Press, Moscow (Russian)
Sterbing–D’Angelo SJ, Moss CF (2014) Air flow sensing in bats. In: Bleckmann H, Mogdans J, Coombs SL (eds) Flow sensing in air and water. Springer, Heidelberg, pp 197–213
Teyke T (1989) Learning and remembering the environment in the blind cave fish Anoptichthys jordani. J Comp Physiol A 164:655–662
Weissert R, von Campenhausen C (1981) Discrimination between stationary objects by the blind cave fish Anoptichthys jordani. J Comp Physiol A 143:375–382
Windsor SP (2014) Hydrodynamic imaging by blind Mexican cavefish. In: Bleckmann H, Mogdans J, Coombs SL (eds) Flow sensing in air and water. Springer, Heidelberg, pp 103–125
Woollard P, Vestjens WJM, MacLean L (1978) Ecology of eastern water rat Hydromys chrysogaster at Griffith, NSW food and feeding habits. Austr Wild Res 5:59–73
Acknowledgements
We appreciate the support of Mote Marine Laboratory in providing the animals and facilities for this project. Thanks to the many volunteers from Mote Marine Laboratory and students from New College of Florida that assisted on this project. We gratefully acknowledge Guido Dehnhardt and Wolf Hanke for their expertise and equipment loan during training, as well as Ronnie and John Enander, the Thurell family, and New College Foundation. Yareli Alvarez and Madi Huffstickler provided assistance in the preparation of the manuscript. This work was conducted under US Fish and Wildlife Service Permit MA837923. It was supported by the National Science Foundation (IOS-0920022/0919975/0920117). All experimental procedures were approved by the Mote Marine Laboratory IACUC prior to implementation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gaspard, J.C., Bauer, G.B., Mann, D.A. et al. Detection of hydrodynamic stimuli by the postcranial body of Florida manatees (Trichechus manatus latirostris). J Comp Physiol A 203, 111–120 (2017). https://doi.org/10.1007/s00359-016-1142-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-016-1142-8