Advertisement

Reviews in Fish Biology and Fisheries

, Volume 20, Issue 4, pp 571–590 | Cite as

A review of the sensory biology of chimaeroid fishes (Chondrichthyes; Holocephali)

  • Thomas J. Lisney
Article

Abstract

The chimaeroid fishes (Chondrichthyes: Holocephali) are a small, ancient and poorly studied group of cartilaginous fishes that have puzzled and intrigued taxonomists, ichthyologists and evolutionary biologists for over 100 years. Like their close relatives, the elasmobranchs (sharks, skates and rays), chimaeroids possess an extensive battery of sense organs that allow them to detect information about the external environment in order to find mates, locate food and preferred habitats and avoid predators. In recent years the sensory systems of elasmobranchs have received an up-swell of attention from biologists, which has resulted in a greater understanding of the sensory capabilities and behaviour of these fishes. However, very little recent work has been done on the chimaeroids. The aim of this review is to provide a survey of the existing literature on the major senses (vision, smell, taste, mechanoreception, hearing and electroreception) in chimaeroids, in order to stimulate and identify areas for future research. In chimaeroids information on sensory systems is largely restricted to one or two species (with the exception of some aspects of the visual system) and for some sensory systems essentially nothing is known. Most studies are anatomical in nature and so there is a demand for a greater degree of neurophysiological and behavioural assessment of sensory capability in these fishes. The majority of chimaeroids occupy deep-sea habitats and are becoming increasingly threatened by the expansion of deep-sea fisheries, so an understanding of the sensory biology and behaviour of chimaeroids may be important for the protection and management of these fascinating fishes.

Keywords

Brain Callorhinchidae Chimaeridae Electroreception Hearing Mechanoreceptive lateral line Olfaction Rhinochimaeridae Smell Vision 

Notes

Acknowledgments

The author was supported by a post-doctoral stipend from the Carl Tryggers Foundation for Scientific Research while writing this review. The comments from two anonymous reviewers greatly improved the manuscript.

References

  1. Bailey DM, Wagner H-J, Jamieson AJ, Ross MF, Priede IG (2007) A taste of the deep-sea: the roles of gustatory and tactile searching behaviour in the grenadier fish Coryphaenoides armatus. Deep-Sea Res 54(1):99–108CrossRefGoogle Scholar
  2. Banner A (1967) Evidence of sensitivity to acoustic displacements in the lemon shark, Negaprion brevirostris (Poey). In: Cahn P (ed) Lateral line detectors. Indiana University Press, Bloomington, pp 265–273Google Scholar
  3. Barlow HB (1953) Summation and inhibition in the frog’s retina. J Physiol (Lond) 119:69–88Google Scholar
  4. Barnett LAK, Dagit DD, Long DJ, Ebert DA (2006) Hydrolagus mccoskeri sp. nov. a new species of chimaeroid fish from the Galápagos Islands (Holocephali: Chimaeriformes: Chimaeridae). Zootaxa 1328:27–38Google Scholar
  5. Beatty DD (1969) Visual pigments of three species of cartilaginous fishes. Nature 222:285PubMedCrossRefGoogle Scholar
  6. Bell MS (1993) Convergent evolution of nasal structure in sedentary elasmobranchs. Copeia 1993:144–158CrossRefGoogle Scholar
  7. Bigelow HB, Schroder WC (1954) Deep water elasmobranchs and chimaeroids of the Northwestern Atlantic slope. Bull Mus Comp Zool 112:34–87Google Scholar
  8. Bleckmann H, Hofmann MH (1999) Special senses. In: Hamlett WC (ed) Sharks, skates and rays: the biology of elasmobranch fishes. Johns Hopkins University Press, Baltimore, pp 300–328Google Scholar
  9. Bodznick D (1991) Elasmobranch vision: multimodal integration in the brain. J Exp Zool 256(Suppl 5):108–116Google Scholar
  10. Bozzano A (2004) Retinal specialisations in the dogfish Centroscymnus coelolepis from the Mediterranean deep-sea. Sci Mar 68(Suppl 3):185–195Google Scholar
  11. Bozzano A, Collin SP (2000) Retinal ganglion cell topography in elasmobranchs. Brain Behav Evol 55:191–208PubMedCrossRefGoogle Scholar
  12. Bozzano A, Murgia R, Vallerga S, Hirano J, Archer S (2001) The photoreceptor system in the retinae of two dogfishes, Scyliorhinus canicula and Galeus melastomus: possible relationship with depth distribution and predatory lifestyle. J Fish Biol 59:1258–1278CrossRefGoogle Scholar
  13. Breschet G (1838) Recherches anatomiques et physiologiques sur l’organe de l’ouïe des poisons. Extr d Mem de l’Académie des Sciences, Tom V d Sav étr ParisGoogle Scholar
  14. Bullock TH, Hofmann MH, New JG, Nahm FK (1991) Dynamic properties of visual evoked potentials in the tectum of cartilaginous and bony fishes, with neuroethological implications. J Exp Zool (Suppl 5):142–155Google Scholar
  15. Cailliet GM, Goldman KJ (2004) Age determination and validation in chondrichthyan fishes. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 399–448Google Scholar
  16. Cailliet GM, Musick JA, Simpfendorfer CA, Stevens JD (2005) Ecology and life history characteristics of chondrichthyan fish. In: Fowler SL, Cavanagh RD, Camhi M, Burgess GH, Cailliet GM, Fordham SV, Simpefendorfer CA, Musick JA (eds) Sharks, rays and chimaeras: the status of the chondrichthyan fishes. IUCN Shark Specialist Group. IUCN, Gland, pp 12–18Google Scholar
  17. Calis E, Jackson EH, Nolan CP, Jeal F (2005) Preliminary age and growth estimates of the rabbitfsh, Chimaera monstrosa, with implications for future resource management. J Northw Atl Fish Sci 35:15–26CrossRefGoogle Scholar
  18. Casper BM, Mann DA (2006) Evoked potential audiograms of the nurse sahrk (Ginglymostoma cirratum) and the yellow stingray (Urobatis jamaicensis). Environ Biol Fishes 76:101–108CrossRefGoogle Scholar
  19. Casper BM, Mann DA (2007a) Dipole hearing measurements in elasmobranch fishes. J Exp Biol 210:75–81PubMedCrossRefGoogle Scholar
  20. Casper BM, Mann DA (2007b) The directional hearing abilities of two species of bamboo sharks. J Exp Biol 210:505–511PubMedCrossRefGoogle Scholar
  21. Casper BM, Mann DA (2009) Field hearing measurements of the Atlantic sharpnose shark Rhizoprionodon terraenovae. J Fish Biol 75:2768–2776PubMedCrossRefGoogle Scholar
  22. Casper BM, Lobel PS, Yan YH (2003) The hearing sensitivity of the little skate, Raja erinacea: a comparison of two methods. Environ Biol Fishes 68:371–379CrossRefGoogle Scholar
  23. Cavanagh RD, Kyne PM (2005) The conservation status of deep-sea chondrichthyan fishes. In: Shotton R (ed) Deep sea 2003: conference on the governance and management of deep-sea fisheries. Part 2: conference poster papers and workshop papers, Queenstown, 1–5 Dec 2003 and 27–29 Nov 2003, Dunedin. FAO Fisheries Proceedings No. 3/2. FAO, Rome, pp 366–380Google Scholar
  24. Chu YT, Wen MC (1979) A study of the lateral-line canals system and that of Lorenzini ampullae and tubules of elasmboranchiate fishes of China. Academic Press, ShanghaiGoogle Scholar
  25. Collin SP (1988) The retina of the shovel-nosed ray, Rhinobatos batillum (Rhinobatidae): morphology and quantitative analysis of the ganglion, amacrine and bipolar cell populations. Exp Biol 47:195–207PubMedGoogle Scholar
  26. Collin SP (1999) Behavioural ecology and retinal cell topography. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) Adaptive mechanisms in the ecology of vision. Kluwer, Dordrecht, pp 509–535Google Scholar
  27. Collin SP, Whitehead D (2004) The functional roles of passive electroreception in non-electric fishes. Anim Biol 54:1–25CrossRefGoogle Scholar
  28. Compagno LJV (1990) Alternative life-history styles of cartilaginous fishes in time and space. Environ Biol Fishes 28:33–75CrossRefGoogle Scholar
  29. Compagno LJV (1999) Systematics and body form. In: Hamlett WC (ed) Sharks, skates and rays: the biology of elasmobranch fishes. Johns Hopkins University Press, Baltimore, pp 1–42Google Scholar
  30. Compagno LJV, Musick JA (2005) Deepwater species. In: Fowler SL, Cavanagh RD, Camhi M, Burgess GH, Cailliet GM, Fordham SV, Simpefendorfer CA, Musick JA (eds) Sharks, rays and chimaeras: the status of the chondrichthyan fishes. IUCN Shark Specialist Group, IUCN, Gland, pp 216–217Google Scholar
  31. Compagno LJV, Didier DA, Burgess GH (2005) Classification of chondrichthyan fish. In: Fowler SL, Cavanagh RD, Camhi M, Burgess GH, Cailliet GM, Fordham SV, Simpefendorfer CA, Musick JA (eds) Sharks, rays and chimaeras: the status of the chondrichthyan fishes. IUCN Shark Specialist Group, IUCN, Gland, pp 4–11Google Scholar
  32. Condit R, Le Boeuf BJ (1984) Feeding habits and feeding grounds of the northern elephant seal. J Mamm 65:281–290CrossRefGoogle Scholar
  33. Coombs S, Montgomery JC (1999) The enigmatic lateral line system. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, Berlin, pp 319–362Google Scholar
  34. Corwin JT (1978) The relation of inner ear structure to feeding behavior in sharks and rays. In: Johari O (ed) Scanning electron microscopy. S.E.M. Inc., Chicago, pp 1105–1112Google Scholar
  35. Corwin JT (1989) Functional anatomy of the auditory system in sharks and rays. J Exp Zool 252(Suppl 2):62–74CrossRefGoogle Scholar
  36. Crescitelli F (1969) The visual pigment of a chimaeroid fish. Vis Res 9:1407–1414PubMedCrossRefGoogle Scholar
  37. Crescitelli F (1991) Adaptations of visual pigments to the photic environment of the deep-sea. J Exp Zool 256(Suppl 5):66–75Google Scholar
  38. Crescitelli F, McFall-Ngai M, Horwitz J (1985) The visual pigment sensitivity hypothesis: further evidence from fishes of varying habitats. J Comp Physiol A 157:323–333PubMedCrossRefGoogle Scholar
  39. Dangles O, Irschick D, Chittka L, Casas J (2009) Variability in sensory ecology: expanding the bridge between physiology and evolutionary biology. Q Rev Biol 84:51–74PubMedCrossRefGoogle Scholar
  40. Davies WL, Carvalho LS, Tay B-H, Brenner S, Hunt DM, Venkatesh B (2009) Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res 19:415–426PubMedCrossRefGoogle Scholar
  41. Dean B (1906) Chimaeroid fishes and their development. Carnegie Institute Publication, Washington DCGoogle Scholar
  42. Denton EJ, Gray JAB (1988) Mechanical factors in the excitation of the lateral lines of fishes. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, Berlin, pp 595–617Google Scholar
  43. Denton EJ, Nicol JAC (1964) The choroidal tapeta of some cartilaginous fishes. J Mar Biol Assoc UK 44:219–258CrossRefGoogle Scholar
  44. Di Giácomo E, Perier M (1996) Feeding habits of cockfish, Callorhinchus callorhynchus (Holocephali: Callorhynchidae), in Patagonian waters (Argentina). Mar Freshw Res 47:801–808CrossRefGoogle Scholar
  45. Didier DA (1995) Phylogenetic systematics of extant chimaeroid fishes (Holocephali, Chimaeroidei). Am Mus Nat Hist Novit 3119:1–86Google Scholar
  46. Didier DA (2002) Two new species of chimaeroid fishes from the southwestern Pacific Ocean (Holocephali, Chimaeridae). Ichthyol Res 459:299–306CrossRefGoogle Scholar
  47. Didier DA (2004) Phylogeny and classification of extant Holocephali. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 115–136Google Scholar
  48. Didier DA (2008) Two new species of the genus Hydrolagus Gill (Holocephali: Chimaeridae) from Australia. In: Last PR, White WT, Pogonoski JJ (eds) Descriptions of new Australian chondrichthyans. CSIRO Marine and Atmospheric Research Paper No. 022, pp 349–356Google Scholar
  49. Didier DA, Séret B (2002) Chimaeroid fishes of New Caledonia with description of a new species of Hydrolagus (Chondrichthyes, Holocephali). Cybium 26:225–233Google Scholar
  50. Didier DA, Leclair EE, Vanbuskirk DR (1998) Embryonic staging and external features of development of the chimaeroid fish, Callorhinchus milli (Holocephali, Callorhinchidae). J Morphol 236:25–47CrossRefGoogle Scholar
  51. Didier DA, Last PR, White WT (2008) Three new species of the genus Chimaera Linneaus (Chimaeriformes: Chimaeridae) from Australia. In: Last PR, White WT, Pogonoski JJ (eds) Descriptions of new Australian chondrichthyans. CSIRO Marine and Atmospheric Research Paper No. 022, pp 327–339Google Scholar
  52. Dijkgraaf S (1962) The functioning and significance of the lateral-line organs. Biol Rev 38:51–105CrossRefGoogle Scholar
  53. Douglas RH, Partridge JC, Hope AJ (1995) Visual and lenticular pigments in the eyes of demersal deep-sea fishes. J Comp Physiol A 177:111–122CrossRefGoogle Scholar
  54. Douglas RH, Partridge JC, Marshall NJ (1998) The eyes of deep-sea fish I: lens pigmentation, tapeta and visual pigments. Prog Ret Eye Res 17:597–636CrossRefGoogle Scholar
  55. Ekström von Lubitz DK (1981) Ultrastructure of the lateral-line sense organs of the ratfish, Chimaera monstrosa. Cell Tissue Res 215:651–665PubMedGoogle Scholar
  56. Evangelista C, Mills M, Siebeck UE, Collin SP (2010) A comparison of the external morphology of the membranous inner ear in elasmobranchs. J Morphol. doi: 10.1002/jmor.10812 PubMedGoogle Scholar
  57. Fänge R (1982) Exogenous otoliths in elasmobranchs. J Mar Biol Assoc UK 62:225CrossRefGoogle Scholar
  58. Faucette JR (1969) The olfactory bulb and medial hemisphere wall of the rat-fish, Chimaera. J Comp Neurol 137:377–406PubMedCrossRefGoogle Scholar
  59. Fay RR, Kendall JI, Popper AN, Tester AL (1974) Vibration detection by the macula neglecta of sharks. Comp Biochem Physiol 47A:1235–1240CrossRefGoogle Scholar
  60. Fernald RD (1990) The optical system of fishes. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, London, pp 45–61Google Scholar
  61. Fields RD, Lange GD (1980) Electroreception in the ratfish (Hydrolagus colliei). Science 207:547–548PubMedCrossRefGoogle Scholar
  62. Fields RD, Bullock TH, Lange GD (1993) Ampullary sense organs, peripheral, central and behavioral electroreception in chimeras (Hydrolagus, Holocephali, Chondrichthyes). Brain Behav Evol 41:269–289PubMedCrossRefGoogle Scholar
  63. Franz V (1905) Zur anatomie, Histologie und Funktionellen Gestaltung des Selachierauges. Jena Z Naturw 40:697–840Google Scholar
  64. Fröhlich E, Negishi K, Wagner H-J (1995) Patterns of rod proliferation in deep-sea fish retinae. Vis Res 35:1799–1811PubMedCrossRefGoogle Scholar
  65. Gačić Z, Damjanović I, Mićković B, Hegedis A, Nikčević M (2007) Spectral sensitivity of the dogfish shark (Scyliorhinus canicula). Fish Physiol Biochem 33:21–27CrossRefGoogle Scholar
  66. Gardiner JM, Atema J (2007) Sharks need the lateral line to locate odor sources: rheotaxis and eddy chemotaxis. J Exp Biol 210:1925–1934PubMedCrossRefGoogle Scholar
  67. Garman S (1904) The chimaeroids especially Rhinochimaera and its allies. Bull Mus Comp Zool 41:243–271Google Scholar
  68. Gordon JDM (1999) Management considerations of deep-water shark fisheries. In: Shotton R (ed) Case studies of the management of elasmobranch fisheries. FAO Fisheries Technical Paper, No. 378, pp 774–818Google Scholar
  69. Grogan ED, Lund R (2004) The origin and relationships of early Chondrichthyes. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 3–32Google Scholar
  70. Haine OS, Ridd PV, Rowe RJ (2001) Range of electrosensory detection of prey by Carcharhinus melanopterus and Himantura granulata. Mar Freshw Res 52:291–296CrossRefGoogle Scholar
  71. Hara TJ (1975) Olfaction in fish. Prog Neurobiol 5:271–335PubMedCrossRefGoogle Scholar
  72. Harahush BK, Hart NS, Green K, Collin SP (2009) Retinal neurogenesis and ontogenetic changes in the visual system of the brown banded bamboo shark, Chiloscyllium punctatum (Hemiscyllidae, Elasmobranchii). J Comp Neurol 513:83–97PubMedCrossRefGoogle Scholar
  73. Hart NS, Lisney TJ, Marshall NJ, Collin SP (2004) Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch. J Exp Biol 207:4587–4594PubMedCrossRefGoogle Scholar
  74. Hart NS, Lisney TJ, Collin SP (2006) Visual communication in elasmobranchs. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers Inc., Enfield, pp 337–392Google Scholar
  75. Helfman GS (2007) Fish conservation: a guide to understanding and restoring global aquatic biodiversity and fishery resources. Island Press, Washington DCGoogle Scholar
  76. Hodgson ES, Mathewson RF (1978) Electrophysiological studies of chemoreception in elasmobranchs. In: Hodgson ES, Mathewson RF (eds) Sensory biology of sharks, skates and rays. Office of Naval Research, Arlington, pp 227–267Google Scholar
  77. Holl A (1973a) Funktionsmorphologie der Nase von Chimaera monstrosa (Holocephali). Z Morph Tiere 74:271–296CrossRefGoogle Scholar
  78. Holl A (1973b) Feinstruktur des Riechepithels von Chimaera monstrosa (Holocephali). Mar Biol 23:59–72CrossRefGoogle Scholar
  79. Hueter RE (1991) Adaptations for spatial vision in sharks. J Exp Zool 256(Suppl 5):130–141Google Scholar
  80. Hueter RE, Murphy CJ, Howland M, Sivak JG, Paul-Murphy JR, Howland HC (2001) Refractive state and accommodation in the eyes of free-swimming versus restrained juvenile lemon sharks (Negaprion brevirostris). Vis Res 41:1885–1889PubMedCrossRefGoogle Scholar
  81. Hueter RE, Mann DA, Maruska KP, Sisneros JA, Demski LS (2004) Sensory biology of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 325–368Google Scholar
  82. Hughes A (1977) The topography of vision in mammals of contrasting lifestyles: comparative optics and retinal organization. In: Crescitelli F (ed) Handbook of sensory physiology, vol VIII/5. Springer, Berlin, pp 613–756Google Scholar
  83. James KC, Ebert DA, Long DJ, Didier DA (2009) A new species of chimaera, Hydrolagus melanophasma sp. nov. (Chondrichthyes: Chimaeriformes: Chimaeridae), from the eastern North Pacific. Zootaxa 2218:59–68Google Scholar
  84. Johnson RH, Nelson DR (1978) Copulation and possible olfaction-mediated pair formation in two species of carcharhinid sharks. Copeia 1978:76–84Google Scholar
  85. Jollie M (1962) Chordate morphology. Reinhold, New YorkGoogle Scholar
  86. Jordan LK (2008) Comparative morphology of stingray lateral line canal and electrosensory systems. J Morphol 269:1325–1339PubMedCrossRefGoogle Scholar
  87. Jordan LK, Kajiura SM, Gordon MS (2009a) Functional consequences of structural differences in stingray sensory systems. Part I: mechanosensory lateral line canals. J Exp Biol 212:3037–3043PubMedCrossRefGoogle Scholar
  88. Jordan LK, Kajiura SM, Gordon MS (2009b) Functional consequences of structural differences in stingray sensory systems. Part II: electrosensory system. J Exp Biol 212:3044–3050PubMedCrossRefGoogle Scholar
  89. Kajiura SM (2001) Head morphology and electrosensory pore distribution of carcharhinid and sphyrnid sharks. Environ Biol Fishes 61:125–133CrossRefGoogle Scholar
  90. Kajiura SM (2003) Electroreception in neonatal bonnethead sharks, Sphyrna tiburo. Mar Biol 143:603–611CrossRefGoogle Scholar
  91. Kajiura SM, Fitzgerald TP (2009) Response of juvenile scalloped hammerhead sharks to electric stimuli. Zoology 112:241–250PubMedCrossRefGoogle Scholar
  92. Kajiura SM, Holland KN (2002) Electroreception in juvenile scalloped hammerhead and sandbar sharks. J Exp Biol 205:3609–3621PubMedGoogle Scholar
  93. Kajiura SM, Forni JB, Summers AP (2005) Olfactory morphology of carcharhinid and sphyrnid sharks: does the cephalofoil confer a sensory advantage? J Morphol 264:253–263PubMedCrossRefGoogle Scholar
  94. Kalmijn AJ (1971) The electric sense of sharks and rays. J Exp Biol 55:371–383PubMedGoogle Scholar
  95. Kalmijn AJ (1982) Electric and magnetic field detection in elasmobranch fishes. Science 218:916–918PubMedCrossRefGoogle Scholar
  96. Kalmijn AJ (2003) Physical principles of electric, magnetic, and near-field acoustic orientation in early orientation in early aquatic vertebrates. In: Collin SP, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, Berlin, pp 77–91CrossRefGoogle Scholar
  97. Kelly JC, Nelson DR (1975) Hearing thresholds of the horn shark, Heterodontus francisci. J Acoust Soc Am 58:905–909PubMedCrossRefGoogle Scholar
  98. Kimber JA, Sims DW, Bellamy PH, Gill AB (2009) Male–female interactions affect foraging behaviour within groups of small-spotted catshark, Scyliorhinus canicula. Anim Behav 77:1435–1440CrossRefGoogle Scholar
  99. Kleerekoper H (1978) Chemoreception and the role of its interaction with flow and light perception in the locomotion and orientation of some elasmobranchs. In: Hodgson ES, Mathewson RF (eds) Sensory biology of sharks, skates and rays. Office of Naval Research, Arlington, pp 269–329Google Scholar
  100. Kokuho T, Nakaya K, Kitagawa D (2003) Distribution and reproductive biology of the nine-spot ratfish Hydrolagus barbouri (Holocephali; Chimaeridae). Mem Grad Sci Fish Sci Hokkaido Univ 50:63–87Google Scholar
  101. Kotrschal K, van Staaden MJ, Huber R (1998) Fish brains: evolution and environmental relationships. Rev Fish Biol Fish 8:373–408CrossRefGoogle Scholar
  102. Kretz R, Ishida AT, Stell WK (1982) Ratfish retina-intercellular recordings and HRP injections in an isolated, superfused all-rod retina. Vis Res 22:857–861PubMedCrossRefGoogle Scholar
  103. Kritzler H, Wood L (1961) Provisional audiogram for the shark, Carcharhinus leucas. Science 133:1402–1482CrossRefGoogle Scholar
  104. Kuchnow KP (1971) The elasmobranch pupillary response. Vis Res 11:1395–1406PubMedCrossRefGoogle Scholar
  105. Kuhlenbeck H, Niimi K (1969) Further observations on the morphology of the brain in the holocephalian elasmobranchs Chimaera and Callorhynchus. J Hirnforsch 11:267–314PubMedGoogle Scholar
  106. Ladlich F (2000) Acoustic communication and the evolution of hearing in fishes. Philos Trans R Soc Lond B 355:1285–1288CrossRefGoogle Scholar
  107. Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, OxfordGoogle Scholar
  108. Last PR, Stevens JD (2009) Sharks and rays of Australia, 2nd edn. CSIRO Marine and Atmospheric Research, MelbourneGoogle Scholar
  109. Last PR, White WT, Pogonoski JJ (2008) Chimaera argiloba sp. nov. a new species of chimaeroid (Chimaeriformes: Chimaeridae) from northwestern Australia. In: Last PR, White WT, Pogonoski JJ (eds) Descriptions of new Australian chondrichthyans. CSIRO Marine and Atmospheric Research Paper No. 022, pp 341–348Google Scholar
  110. Lisney TJ, Collin SP (2006) Brain morphology in large pelagic fishes: a comparison between sharks and teleosts. J Fish Biol 68:532–554CrossRefGoogle Scholar
  111. Lisney TJ, Collin SP (2007) Relative eye size in elasmobranchs. Brain Behav Evol 67:266–279CrossRefGoogle Scholar
  112. Lisney TJ, Collin SP (2008) Retinal ganglion cell distribution and spatial resolving power in elasmobranchs. Brain Behav Evol 72:59–77PubMedCrossRefGoogle Scholar
  113. Lisney TJ, Bennett MB, Collin SP (2007) Volumetric analysis of sensory brain areas indicates ontogenetic shifts in the relative importance of sensory systems in elasmobranchs. Raff Bull Zool (Suppl 14):7–15Google Scholar
  114. Litherland L, Collin SP (2008) Comparative visual function in elasmobranchs: spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions. Vis Neurosci 25:549–561PubMedCrossRefGoogle Scholar
  115. Litherland L, Collin SP, Fritsches KA (2009a) Visual optics and ecomorphology of the growing shark eye: a comparison between deep and shallow water species. J Exp Biol 212:3583–3594PubMedCrossRefGoogle Scholar
  116. Litherland L, Collin SP, Fritsches KA (2009b) Eye growth in sharks: ecological implications for changes in retinal topography and visual resolution. Vis Neurosci 26:397–409PubMedCrossRefGoogle Scholar
  117. Liu Z (2001) Phylogenetic relationships of the living chimaeroid fishes based on characters of the brain and cranial nerves. New Mexico J Sci 41:1–24Google Scholar
  118. López HL, San Román NA, Di Di Giácomo EE (2000) On the south Atlantic distribution of Callorhinchus callorhynchus (Holocephali: Callorhynchidae). J Appl Ichthyol 16:39CrossRefGoogle Scholar
  119. Lowenstein O, Roberts TDM (1951) The localization and analysis of the responses to vibration from the isolated elasmobranch labyrinth. A contribution to the problem of hearing in vertebrates. J Physiol (Lond) 114:471–489Google Scholar
  120. Lychakov DV, Boyadzhieva-Mikhailova A, Christov I, Evdokimov II (2000) Otolithic apparatus in Black Sea elasmobranchs. Fish Res 46:27–38CrossRefGoogle Scholar
  121. Maddock RG, Nicol JAC (1978) Studies on the eyes of Hydrolagus (Pisces: Chimaeridae). Contrib Mar Sci 21:77–87Google Scholar
  122. Maisey JG (2001) Remarks on the inner ear of elasmobranchs and its interpretation from skeletal labyrinth morphology. J Morphol 250:236–264PubMedCrossRefGoogle Scholar
  123. Maruska KR (2001) Morphology of the mechanosensory lateral line system in elasmobranch fishes: ecological and behavioral considerations. Environ Biol Fishes 60:47–75CrossRefGoogle Scholar
  124. Maruska KR, Tricas TC (2004) Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray. J Exp Biol 207:3463–3476PubMedCrossRefGoogle Scholar
  125. Mauchline J, Gordon JDM (1983) Diets of sharks and chimaeroids of the Rockall Trough, northeastern Atlantic Ocean. Mar Biol 75:269–278CrossRefGoogle Scholar
  126. McComb DM, Kajiura SM (2008) Visual fields of four batoid fishes: a comparative study. J Exp Biol 211:482–490PubMedCrossRefGoogle Scholar
  127. McComb DM, Tricas TC, Kajiura SM (2009) Enhanced visual fields in hammerhead sharks. J Exp Biol 212:4010–4018PubMedCrossRefGoogle Scholar
  128. McComb DM, Frank TM, Hueter RE, Kajiura SM (2010) Temporal resolution and spectral sensitivity of the visual system of three coastal shark species from different light environments. Physiol Biochem Zool 83:299–307PubMedGoogle Scholar
  129. McFarland WN (1970) Visual pigments of Callorhinchus callorynchus, a southern hemisphere chimaeroid fish. Vis Res 10:939–942PubMedCrossRefGoogle Scholar
  130. McGowan DW, Kajiura SM (2009) Electroreception in the euryhaline stingray, Dasyatis sabina. J Exp Biol 212:1544–1552PubMedCrossRefGoogle Scholar
  131. Meng Q, Yin M (1981a) A study on the olfactory organ of skates, rays and chimaeras. J Fish China 5:209–228Google Scholar
  132. Meng Q, Yin M (1981b) A study on the olfactory organ of sharks. Trans Chinese Ichthyol Soc 2:1–24Google Scholar
  133. Montgomery JC, Skipworth E (1997) Detection of weak water jets by the short-tailed stingray Dasyatis brevicaudata (Pisces: Dasyatidae). Copiea 1997:881–883CrossRefGoogle Scholar
  134. Moura T, Figueiredo I, Bordalo-Machado P, Almeida C, Gordo LS (2005) A new deep-water chimaerid species, Hydrolagus lusitanicus n. sp. from off mainland Portugal with a proposal of a new identification key for the genus Hydrolagus (Holocephali: Chimaeridae) in the north-east Atlantic. J Fish Biol 67:742–751CrossRefGoogle Scholar
  135. Myrberg AA (2001) The acoustical biology of elasmobranchs. Environ Biol Fishes 60:31–45CrossRefGoogle Scholar
  136. Northcutt RG (1978) Brain organization in the cartilaginous fishes. In: Hodgson ES, Mathewson RF (eds) Sensory biology of sharks, skates and rays. Office of Naval Research, Arlington, pp 117–193Google Scholar
  137. Northcutt RG (1989) The phylogenetic distribution and innervation of craniate mechanoreceptive lateral lines. In: Coombs S, Gorner P, Munz H (eds) The mechanosensory lateral line: neurobiology and evolution. Springer, Berlin, pp 17–78Google Scholar
  138. Parker GH (1909) The influence of the eyes, ears and other allied sense organs on the movements of the dogfish Mustelus canis (Mitchill). Bull US Bur Fish 29:43–57Google Scholar
  139. Partridge JC, Shand J, Archer SN, Lythgoe JN, van Groiningen-Luyben WAHM (1989) Interspecific variation in the visual pigments of deep-sea fishes. J Comp Physiol A 164:513–529PubMedCrossRefGoogle Scholar
  140. Patterson C (1965) The phylogeny of chimaeroids. Philos Trans Roy Soc Lond B 249:101–219CrossRefGoogle Scholar
  141. Paulin MG (1995) Electroreception and the compass sense of sharks. J Theor Biol 174:325–339CrossRefGoogle Scholar
  142. Peach MB (2001) The dorso-lateral pit organs of the Port Jackson shark contribute sensory information for rheotaxis. J Fish Biol 59:696–704CrossRefGoogle Scholar
  143. Peach MB (2003) Inter-and intraspecific variation in the distribution and number of pit organs (free neuromasts) of sharks and rays. J Morphol 256:89–102PubMedCrossRefGoogle Scholar
  144. Peach MB, Marshall NJ (2000) The pit organs of elasmobranchs: a review. Philos Trans R Soc Lond B 355:1131–1134CrossRefGoogle Scholar
  145. Peach MB, Marshall NJ (2009) The comparative morphology of pit organs in elasmobranchs. J Morphol 270:688–701PubMedCrossRefGoogle Scholar
  146. Peach MB, Rouse GW (2000) The morphology of the pit organs and lateral line canal neuromasts of Mustelus antarcticus (Chondrichthyes: Triakidae). J Mar Biol Assoc UK 80:155–162CrossRefGoogle Scholar
  147. Peach MB, Rouse GW (2004) Phylogenetic trends in the abundance and distribution of pit organs of elasmobranchs. Acta Zool (Stockh) 85:233–244CrossRefGoogle Scholar
  148. Peterson EH, Rowe MH (1980) Different regional specializations of neurons in the ganglion cell layer and inner plexiform layer of the California horned shark, Heterodontus francisci. Brain Res 201:195–201PubMedCrossRefGoogle Scholar
  149. Popper AN, Ramcharitar J, Campana SE (2005) Why otoliths? Insights from inner ear physiology and fisheries biology. Mar Freshw Res 56:497–504CrossRefGoogle Scholar
  150. Quaranta KL, Didier DA, Long DJ, Ebert DA (2006) A new species of chimaeroid, Hydrolagus alphus sp. nov. (Chimaeriformes: Chimaeridae) from the Galapagos Islands. Zootaxa 1377:33–45Google Scholar
  151. Quinn TP, Miller BS, Wingert RC (1980) Depth distribution and seasonal and diel movements of ratfish, Hydrolagus colliei, in Puget Sound, Washington. Fish Bull 78:816–821Google Scholar
  152. Raschi W (1986) A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei). J Morphol 189:225–247CrossRefGoogle Scholar
  153. Raschi W, Aadlond C, Keithar ED (2001) A morphological and functional analysis of the ampullae of Lorenzini in selected galeoid sharks. In: Kapoor BG, Hara TJ (eds) Sensory biology of jawed fishes—new insights. Science Publishers Inc., Enfield, pp 297–316Google Scholar
  154. Retzius G (1881) Das Gehörorgan der Wirbelthiere, vol 1. Samson and Wallin, StockholmGoogle Scholar
  155. Roberts BL, Ryan KP (1971) The fine structure of the lateral-line sense organs of dogfish. Proc R Soc Lond B 179:157–169CrossRefGoogle Scholar
  156. Schluessel V, Bennett MB, Bleckmann H, Blomberg S, Collin SP (2008) Morphometric and ultrastructural comparison of the olfactory system in elasmobranchs: the significance of structure–function relationships based on phylogeny and ecology. J Morphol 269:1365–1386PubMedCrossRefGoogle Scholar
  157. Schluessel V, Bennett MB, Bleckmann H, Collin SP (2010) The role of olfaction throughout development: functional adaptations in elasmobranchs. J Morphol. doi: 10.1002/jmor.10809 PubMedGoogle Scholar
  158. Sedberry GR, Musick JA (1978) Feeding strategies of some demersal fishes of the continental slope and rise off the Mid-Atlantic Coast of the USA. Mar Biol 44:357–375CrossRefGoogle Scholar
  159. Sisneros JA, Tricas TC (2002) Ontogenetic changes in the response properties of the peripheral electrosensory system in the Atlantic stingray (Dasyatis sabina). Brain Behav Evol 59:130–140PubMedCrossRefGoogle Scholar
  160. Sivak JG (1978) Optical characteristics of the eye of the spiny dogfish (Squalus acanthias). Rev Can Biol 37:209–217PubMedGoogle Scholar
  161. Smeets WJAJ, Nieuwenhuys R, Roberts BL (1983) The central nervous system of cartilaginous fishes. Springer, BerlinGoogle Scholar
  162. Soto JMR, Vooren CM (2004) Hydrolagus matallanasi sp. nov. (Holocephali, Chimaeridae) a new species of rabbitfish from southern Brazil. Zootaxa 687:1–10Google Scholar
  163. Southwood A, Fritsches K, Brill R, Swimmer Y (2008) Sound, chemical and light detection in sea turtles and pelagic fishes: sensory-based approaches to bycatch reduction in longline fisheries. Endanger Species Res 5:225–238CrossRefGoogle Scholar
  164. Tester AL (1963a) Olfaction, gustation and the common chemical sense in sharks. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates and rays. John Hopkins University Press, Baltimore, pp 503–531Google Scholar
  165. Tester AL (1963b) The role of olfaction in shark predation. Pac Sci 17:145–170Google Scholar
  166. Tester AL, Kendall JI, Milisen WB (1972) Morphology of the ear of the genus Carcharhinus, with particular reference to the macula neglecta. Pac Sci 26:264–274Google Scholar
  167. Theisen B, Zeiske E, Breucker H (1986) Functional morphology of the olfactory organs in the spiny dogfish (Squalus acanthias L.) and the small-spotted catshark (Scyliorhinus canicula (L.)). Acta Zool (Stockh) 67:73–86CrossRefGoogle Scholar
  168. Theiss SM, Lisney TJ, Collin SP, Nart NS (2007) Colour vision and visual ecology of the blue-spotted maskray Dasyatis kuhlii Müller & Henle, 1814. J Comp Physiol A 193:67–79CrossRefGoogle Scholar
  169. Theiss SM, Hart NS, Collin SP (2009) Morphological indicators of olfactory capability in wobbegong sharks (Orectolobidae, Elasmobranchii). Brain Behav Evol 73:91–101PubMedCrossRefGoogle Scholar
  170. Tozer H, Dagit DD (2004) Husbandry of spotted ratfish, Hydrolagus colliei. In: Smith M, Warmolts D, Thoney D, Hueter R (eds) The elasmobranch husbandry manual: captive care of sharks, rays and their relatives. Special Publication of the Ohio Biological Survey, Columbus, pp 488–491Google Scholar
  171. Tricas TC (1982) Bioelectric-mediated predation by swell sharks Cephaloscyllium ventriosum. Copeia 1982:948–952CrossRefGoogle Scholar
  172. Tricas TC (2001) The neuroecology of the elasmobranch electrosensory world: why peripheral morphology shapes behavior. Environ Biol Fishes 60:77–92CrossRefGoogle Scholar
  173. Tricas TC, Gruber SH (eds) (2001) The behavior and sensory biology of elasmobranch fishes: an anthology in memory of Donald Richard Nelson. Kluwer, DordrechtGoogle Scholar
  174. Tricas TC, Sisneros JA (2004) Ecological functions and adaptations of the elasmobranch electrosense. In: von der Emde G, Mogdans J, Kapoor BG (eds) The senses of fish: adaptations for the reception of natural stimuli. Narosa Publishing House, New Delhi, pp 308–329Google Scholar
  175. Tricas TC, Kajiura SM, Summers AP (2009) Response of the hammerhead shark olfactory epithelium to amino acid stimuli. J Comp Physiol A 195:947–954CrossRefGoogle Scholar
  176. Turner JR, White EM, Collins MA, Partridge JC, Douglas RH (2009) Vision in lanternfish (Myctophidae): adaptations for viewing bioluminescence in the deep-sea. Deep-Sea Res 56(1):1003–1017Google Scholar
  177. Vigh-Teichmann I, Szel A, Rohlich P, Vigh B (1990) A comparison of the ultrastructure and opsin immunocytochemisyty of the pineal organ and retina of the deep-sea fish Chimaera monstrosa. Exp Biol 48:361–371PubMedGoogle Scholar
  178. Wagner H-J (2001) Brain areas in abyssal demersal fishes. Brain Behav Evol 57:301–316PubMedCrossRefGoogle Scholar
  179. Wagner H-J, Fröhlich E, Negishi K, Collin SP (1998) The eyes of deep-sea fish. II. Functional morphology of the retina. Prog Retin Eye Res 17:637–685PubMedCrossRefGoogle Scholar
  180. Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science, Bloomfield HillsGoogle Scholar
  181. Waltman B (1966) Electrical properties and fine structure of the ampullary canals of Lorenzini. Acta Physiol Scand 66(Suppl 262):1–60Google Scholar
  182. Warrant EJ, Locket NA (2004) Vision in the deep sea. Biol Rev 79:671–712PubMedCrossRefGoogle Scholar
  183. Webb JF (1989) Gross morphology and evolution of the mechanoreceptive lateral-line system in teleost fishes. Brain Behav Evol 33:34–53PubMedCrossRefGoogle Scholar
  184. Whitear M, Moate RM (1994) Microanatomy of the taste buds in the dogfish, Scyliorhinus canicula. J Submicrosc Cytol Pathol 29:357–367Google Scholar
  185. Whitehead DL (2002) Ampullary organs and electroreception in freshwater Carcharhinus leucas. J Physiol (Paris) 96:391–395CrossRefGoogle Scholar
  186. Wueringer BE, Tibbetts IR (2008) Comparison of the lateral line and ampullary system of two species of shovelnose ray. Rev Fish Biol Fish 18:47–64CrossRefGoogle Scholar
  187. Yopak KE, Frank LR (2009) Brain size and brain organization of the whale shark, Rhincodon typus, using magnetic resonance imaging. Brain Behav Evol 74:121–142PubMedCrossRefGoogle Scholar
  188. Yopak KE, Montgomery JC (2008) Brain organization and specialization in deep-sea chondrichthyans. Brain Behav Evol 71:287–304PubMedCrossRefGoogle Scholar
  189. Zeiske E, Theisen B, Gruber SH (1987) Functional morphology of the olfactory organ of two carcharhinid shark species. Can J Zool 65:2406–2412CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Animal Ecology, Evolutionary Biology CentreUppsala UniversityUppsalaSweden

Personalised recommendations