Summary
-
1.
The opposed grasping surfaces of the digits of the chela of the Limulus walking leg have ridge-like pads of pliable cuticle. Receptors are present both on these pads and elsewhere on the surface of the chelae.
-
2.
Mechanoreceptors at the pad are rapidly adapting (Type 1) or slowly adapting (Type 2) (Fig. 1). Both types have thresholds of between 3 and 40 g and receptive fields of 1.2–2.5 mm along the pad (Fig. 3). Response frequency of Type 1 units increases with increasing rate of force change, while the number of spikes increases with increasing force magnitude (Fig. 4, 5). Response frequency and response duration of Type 2 units increase with increasing amplitude of force, but with some movement sensitivity (Fig. 7). Evidence is presented that the receptors involved are the large multipolar cells under the pad and that they have large rapidly conducting axons representing the fast sensory component of the large leg nerve.
-
3.
Chemoreceptor units respond to clam or fish extracts or to glycine, glutamic acid, betaine, or trimethylamine oxide (Fig. 11). Most are tonic, but some units adapt completely within a few seconds, even to constant-flow stimulation. The tonic chemoreceptors are located at the small channel sensilla of the pad and perhaps also of the sides. Their axons are probably the smallest and slowest in the leg nerve.
-
4.
The behavioral response to chemical stimulation of the chelae of intact animals is opening of the stimulated chela (Fig. 12).
-
5.
Other sensory units give phasic or tonic responses to warm or cold sea water, or tonic responses to distilled water and to dilute sea water. The units are inferred to have axons intermediate in size between mechanoreceptors and chemoreceptors, the size decreasing in the order listed.
-
6.
A proprioceptive organ of the tibiotarsal joint contains units responding to closing movement and units responding to closed position. It lacks units responding to opening or to open position.
-
7.
The variety of claw receptors and the large number of sensory cells (300 000–400 000 estimated per claw or 3–4 million total) indicate that the claw sensory apparatus represents a major sensory input into the central nervous system of Limulus. An estimated total of nearly 4 million chemoreceptors (3 million from claws, 1 million from gnathobases) may relate to the very large and well developed corpora pedunculata of the Limulus brain.
Similar content being viewed by others
References
Barber, S. B.: Chemoreception and proprioception in Limulus. J. exp. Zool. 131, 51–74 (1956).
—: Structure and properties of Limulus articular proprioceptors. J. exp. Zool. 143, 283–321 (1960).
—: Responses of Limulus chemoreceptors to amino acid stimulation. Amer. Zoologist 1, 435 (1961 a).
—: Chemoreception and thermoreception. In: The physiology of Crustacea, Vol. II (T. H. Waterman, ed.), pp. 109–131. New York: Academic Press 1961 b.
—, Hayes, W. F.: Properties of Limulus chemoreceptors. Proc. XVI Int. Cong. Zool. Wash. 3, 76–78 (1963).
Bullock, T. H., Horridge, G. A.: Structure and function in the nervous systems of intervertebrates, 2 vols., pp. 1719. San Francisco: W. H. Freeman and Co. 1965.
Bush, B. M. H.: Proprioception by chordotonal organs in the mero-carpopodite and carpo-propodite joints of Carcinus maenas legs. Comp. Biochem. Physiol. 14, 185–199 (1965).
Case, J.: Properties of the dactyl chemoreceptors of Cancer antennarius Stimpson and C. productus Randall. Biol. Bull. 127, 428–446 (1964).
—, Gwilliam, G. F.: Amino acid sensitivity of the dactyl chemoreceptors of Carcini-des maenas. Biol. Bull. 121, 449–455 (1961).
Chapple, W. D.: Sensory modalities and receptive fields in the abdominal nervous system of the hermit Pagurus granosimanus (Stimpson). J. exp. Biol. 44, 209–223 (1966).
Cohen, M. J.: The crustacean myochordotonal organ as a proprioceptive system. Comp. Biochem. Physiol. 8, 223–243 (1963).
Hanström, B.: Das Nervensystem und die Sinnesorgane von Limulus polyphemus. Acta Univ. Lund. Avd. 2, 22 (5), 1–79 (1926).
Hayes, W. F.: Chemoreceptor sensillum structure in Limulus. J. Morph. 119, 121–142 (1966).
—: Fine structure of the chemoreceptor sensillum in Limulus. J. Morph. 133, 205–240 (1971).
—, Barber, S. B.: Proprioceptor distribution and properties in Limulus walking legs. J. exp. Zool. 165, 195–210 (1967).
Hodgson, E. S.: Electrophysiological studies of arthropod chemoreception. III. Chemoreceptors of terrestrial and freshwater arthropods. Biol. Bull. 115, 114–125 (1958).
—: The chemical senses and changing viewpoints in sensory physiology. In: Viewpoints in biology, (J. D. Carthy and C. L. Duddington, eds). vol. 4, p. 83–123. London: Butterworths 1965.
Hoyle, G.: Studies on neuromuscular transmission in Limulus. Biol. Bull. 115, 209–218 (1958).
Krijgsman, B. J., Krijgsman, N. E.: Osmorezeption in Jasus lalandii. Z. vergl. Physiol. 37, 78–81 (1954).
Lacher, V.: Electrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, Kohlendioxyd, Luftfeuchtigkeit, und Temperatur auf den Antennen der Arbeitsbiene und der Drohne (Apis mellifica L.). Z. vergl. Physiol. 48, 587–623 (1964).
Laverack, M. S.: Aspects of chemoreoeption in Crustacea. Comp. Biochem. Physiol. 8, 141–151 (1963).
—: The antennular sense organs of Panulirus argus. Comp. Biochem. Physiol. 13, 301–321 (1964).
Levandowsky, M., Hodgson, E. S.: Amino acid and amine receptors of lobsters. Comp. Biochem. Physiol. 16, 159–161 (1965).
Loewenstein, W. R., Skalak, R.: Mechanical transmission in a Pacinian corpuscle. An analysis and a theory. J. Physiol. (Lond.) 182, 346–378 (1966).
Maynard, D. M.: Organization of central ganglia. In: Invertebrate nervous systems. Their significance for mammalian neurophysiology (C. A. G. Wiersma, ed.), pp. 231–255. Chicago: U. Chicago Press 1967.
McManus, J. J.: Osmotic relations in the horseshoe crab, Limulus polyphemus. Amer. Midl. Natur. 81, 569–573 (1969).
Murray, R. W.: Temperature receptors. In: Advances in comparative physiology and biochemistry. (O. Lowenstein, ed.), vol. 1, pp. 117–175. New York: Academic Press 1962.
Nunnemacher, R. F., Camougis, G., McAlear, J. H.: The fine structure of the crayfish nervous system. Fifth Int. Congr. Electron Microscopy, p. N11. New York: Academic Press 1962.
O'Tanyi, T. J., Jr., Barber, S. B.: Stretch receptors in Limulus limbs. Amer. Zoologist 6, 519–520 (1966).
Patten, W.: On the morphology and physiology of the brain and sense organs of Limulus. Quart. J. micr. Sci. 35, 1–96 (1893).
-Patten, W.: The evolution of the vertebrates and their kin, pp. 486. Philadelphia: Blakiston 1912.
Pringle, J. W. S.: Proprioception in Limulus. J. exp. Biol. 33, 658–667 (1956).
Rathmayer, W.: Electrophysiologische Untersuchungen an Proprioceptoren im Bein einer Vogelspinne (Eurypelma hentzi Chamb.) Z. vergl. Physiol. 54, 438–454 (1967).
Robertson, J. D.: Osmotic and ionic regulation in the horseshoe crab Limulus polyphemus (Linnaeus). Biol. Bull. 138, 157–183 (1970).
Schneider, D., Lacher, V., Kaissling, K. E.: Die Reaktionsweise und das Reaktions-spektrum von Riechzellen bei Anfheraea pernyi (Lepidoptera, Saturniidae). Z. vergl. Physiol. 48, 632–662 (1964).
Shipley, A. E.: Introduction to Arachnida and Xiphosura. In: Cambridge natural history, (S. P. Harmer, ed.), vol. 4, pp. 253–279. New York: Macmillan 1909.
Snodgrass, R. E.: A Textbook of arthropod anatomy, pp. 363. Ithaca: Cornell U. Press 1952.
Sutherland, R.: Fine structure of the crayfish thoracic cord and leg nerves. Amer. Zoologist 6, 520 (1966).
Wyse, G. A.: Functional organization of receptors in the chelae of Limulus polyphemus. Ph.D. Dissertation. The University of Michigan 1967.
—, Maynard, D. M.: Joint receptors in the antennule of Panulirus argus Latreille. J. exp. Biol. 42, 521–535 (1965).
Author information
Authors and Affiliations
Additional information
I am deeply indebted to Dr. Donald M. Maynard for his advice and encouragement. I wish to thank Drs. David R. Bentley, Michael S. Laverack, Gernot Wendler, and Richard Norman for helpful discussion and suggestions.
This work is based on part of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the University of Michigan. The work was carried out under tenure of a Cooperative Graduate Fellowship and a Graduate Fellowship from the National Science Foundation. Much of the equipment used was made available by the National Institutes of Health Graduate Training Grant No. 5 TI GM 989 and by a grant from the Graduate Student Research Fund of The University of Michigan.
Rights and permissions
About this article
Cite this article
Wyse, G.A. Receptor organization and function in Limulus chelae. Z. Vergl. Physiol. 73, 249–273 (1971). https://doi.org/10.1007/BF00297675
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00297675