Environmental Biology of Fishes

, Volume 44, Issue 1–3, pp 143–155 | Cite as

Ecomorphology of solitary chemosensory cell systems in fish: a review

  • Kurt Kotrschal
Article

Synopsis

Solitary chemosensory cells (SCCs) are present in the skin of a wide spectrum of lower vertebrates, such as lampreys, elasmobranchs, teleost fishes and some amphibians (Kotrschal 1991, Whitear 1992). However, due to the difficulties studying them, virtually all our present knowledge on SCCs stems from the anterior dorsal fin of two species of rocklings (Gadidae). This fin is a peculiar chemosensory organ, carrying approximately 5 million SCCs (Kotrschal et al. 1984, Kotrschal & Whitear 1988). The evidence derived from this model on the structure of SCCs, on their innervation and brain representation, on the flow dynamics at the receptors, on their electrophysiological responses and behavioral relevance indicates that this fin is actively sampling for substances leaked from other fish, such as body mucus and bile components. Possibly, the rockling anterior dorsal fin aids in predators avoidance. To generate hypotheses on the functions and biological roles of the generalized., scattered SCC systems present in most fishes, their structural parameters are put in perspective to taste bud structure and function and to the rockling results. Ecomorphological reasoning serves to establish testable hypotheses: in essence, SCC systems spread over the body surface may be designed as general water samplers, but not for the exact localization of a stimulus source. If the function of the latter is equally dependent on water flow, as the rockling fin organ, fish would have to rely either on the ambient water flow, or speed up their own swimming to optimize SCC input. If SCCs are indeed evolved in the context of predator avoidance, a comparison between life history intervals and between species should reveal, that the system varies in accordance with predation pressure. It is concluded, that in fish, SCCs are certainly an important source of environmental information. If we do not understand functions and biological roles of SCCs, it will not be possible to explain fish behavior and ecology. Evidently, further investigations are urgently needed.

Key words

Chemoreception, Cyprinidae, Gadidae, Facial nerve, Skin, Taste, Teleosts, Rocklings 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Atema, J. 1971. Structures and functions of the sense of taste in fish (Ictalurus natalis). Brain Behav. Evolut. 4: 273–294.Google Scholar
  2. Baatrup, E. & K.B. Doving. 1985. Physiological studies on solitary receptors of the oral disk papillae in adult brook lamprey, Lampetra planeri (Bloch). Chem. Sens. 10: 559–566.Google Scholar
  3. Bardach, J.E. & J. Atema. 1971. The sense of taste in fishes.Google Scholar
  4. Essler, H. & K. Kotrschal. 1994. Effects of chemo-stimulation on swim path patterns in minnows (Phoxinus phoxinus). J. Fish Biol. 45: 555–567.Google Scholar
  5. Finger, T.E. 1982. Somatotopy of the representation of the pectoral fin and free fin rays in the spinal cord of the sea robin, Prionotus carolinus. Biol. Bull. Mar. Biol. Lab., Woods Hole 163: 154–161.Google Scholar
  6. Finger, T.E. & B. Böttger. 1990. Transcellular labeling of taste bud cells by carbocyanine dye (DiI) applied to peripheral nerves in the barbels of catfish, Ictalurus punctatus. J. Comp. Neurol. 302: 884–892.Google Scholar
  7. Gerhardt, G.A., A.F. Oke, G. Nagy, B. Moghaddam & R.N. Adams. 1984 Nafion-coated electrodes with high selectivity for CNS electrochemistry. Brain Res. 290: 390–395.Google Scholar
  8. Godement, P., J. Vanselow, S. Thanos & F. Bonhoeffer. 1987. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101: 697–713.Google Scholar
  9. Gomahr, A., M. Palzenberger & K. Kotrschal. 1992. Density and distribution of external taste buds in cyprinids. Env. Biol. Fish. 33: 125–134.Google Scholar
  10. Honig, M.G. & R.I. Hume. 1989. DiI and DiO: versatile fluorescent dyes for neuronal labelling and pathway tracing. Trends Neurosci. 12: 333–336.Google Scholar
  11. Jakubowski, M. & M. Whitear. 1990. Comparative morphology and cytology of taste buds in teleosts. Z. mikrosk.-anat. Forsch. 104: 529–560.Google Scholar
  12. Kinnamon, J.C. 1987. Organization and innervation of taste buds. pp. 277–297. In: T.E. Finger & W.L. Silver (ed.) Neurobiology of Taste and Smell, Wiley, New York.Google Scholar
  13. Kotrschal, K. 1991. Solitary chemosensory cells — taste, common chemical sense or what? Rev. Fish Biol. Fisheries 1: 3–22.Google Scholar
  14. Kotrschal, K. 1992. Quantitative scanning electron microscopy of solitary chemoreceptor cells in cyprinids and other teleosts. Env. Biol. Fish. 35: 273–282.Google Scholar
  15. Kotrschal, K. & M. Whitear. 1988. Chemosensory anterior dorsal fin in rocklings (Gaidropsarus and Ciliata, Teleostei, Gadidae): somatetopic representation of the ramus recurrens facialis as revi,,aled by transganglionic transport of HRP J. Comp. Neurol. 268: 109–120.Google Scholar
  16. Kotrschal, K., M. Whitear & A. Adam, 1984. Morphology and histology of the anterior dorsal fin of Gaidropsarus mediterraneus (Pisces. Teleostei), a specialized sensory organ. Zoomorphol. 104: 365–372.Google Scholar
  17. Kotrschal, K., R. Peters & J. Atema. 1989. A novel chemosensory system in fish: do rocklings (Ciliata mustela, Gadidae) use their solitary chemoreceptor cells as fish detectors? Biol. Bull. 177: 328.Google Scholar
  18. Kotrschal, K., J.C. Kinnamon & S.M. Royer. 1990. High-voltage electron microscopy and 3-D reconstruction of solitary chemosensory cells and DiI labeling of primary afferent nerves. pp. 412–413. In: Proc. XIIth Int. Congr. Electron Microsc., San Francisco.Google Scholar
  19. Kotrschal, K., M. Whitear & T. Finger. 1993a. Spinal and facial innervation of the skin in the gadid fish Ciliata mustela (Teleostei). J. Comp. Neurol. 331: 407–417.Google Scholar
  20. Kotrschal, K., R. Peters & J. Atema. 1993b. Sampling and behavioral evidence for mucus detection in a unique chemosensory organ: the anterior dorsal fin of rocklings (Ciliata mustela: Gadidae: Teleostei). Zool. Jahrb. Physiol. 97: 47–67.Google Scholar
  21. Motta, P.J. & K. Kotrschal. 1991. Correlative, experimental, and comparative evolutionary approaches in ecomorphology. Neth. J. Zool. 42: 400–415.Google Scholar
  22. Moore, P.A., G.A. Gerhardt & J. Atema. 1989. High resolution spatio-temporal analysis of aquatic chemical signals using microelectrochemical electrodes. Chem. Sens. 14: 829–840.Google Scholar
  23. Parker, G.H. 1912. The relation of smell, taste and the common chemical sense in vertebrates. J. Acad. Nat. Sci. Philadelphia 15: 219–234.Google Scholar
  24. Peters, R.C., G.W. van Steenderen & K. Kotrschal. 1987. A chemoreceptive function for the anterior dorsal fin in rocklings (Gaidropsarus and Ciliata: Teleostei: Gadidae): electrophysiological evidence. J. Mar. Biol. Ass. U.K. 67: 819–823.Google Scholar
  25. Peters, R.C., K. Kotrschal, W.-D. Krautgartner & J. Atema. 1989. A novel chemosensory sytem in fish: electrophysiological evidence for mucus detection by solitary chemoreceptor cells in rocklings (Ciliata mustela, Gadidae). Biol. Bull. 177: 329.Google Scholar
  26. Peters, R.C., K. Kotrschal & W.-D. Krautgartner. 1991. Solitary chemoreceptor cells of Ciliata mustela (Gadidae, Teleostei) are tuned to mucoid stimuli. Chem. Sens. 16: 31–42.Google Scholar
  27. Silver, W.L. 1987. The common chemical sense, pp. 65–87. In: T.E. Finger & W.L. Silver (ed.) Neurobiology of Taste and Smell, Wiley, New York.Google Scholar
  28. Whitear, M. 1965. Presumed sensory cells in fish epidermis. Nature 208: 703–704.Google Scholar
  29. Whitear, M. 1971. Cell specialization and sensory function in fish epidermis. J. Zool. (Lond.) 163: 237–264.Google Scholar
  30. Whitear, M. 1992. Solitary chemoreceptor cells. pp. 103–125. In: T.J. Hara (ed.) Chemoreception in Fishes, Chapman and Hall, London.Google Scholar
  31. Whitear, M. & K. Kotrschal. 1988. The chemosensory anterior dorsal fin in rocklings (Gaidropsarus and Ciliata, Teleostei, Gadidae): activity, fine structure and innervation. J. Zool. (Lond.) 216: 339–366.Google Scholar
  32. Whitear, M. & R.M. Moate. 1994. Chemosensory cells in the oral epithelium of Raja clavata (Chondrichthyes). J. Zool. (Lond.) 232: 295–312.Google Scholar

Copyright information

© Kluwer Academic Publishers 1995

Authors and Affiliations

  • Kurt Kotrschal
    • 1
  1. 1.Zoologisches Institut der Universität Wien and Konrad Lorenz ForschungsstelleGrünau IIAustria

Personalised recommendations