Journal of comparative physiology

, Volume 141, Issue 1, pp 67–75 | Cite as

Limulus gill cleaning behavior

  • Winsor H. WatsonIII
Article

Summary

  1. 1.

    The gill cleaning movements ofLimulus occur in definite periods (bouts). The sequence of movements in a bout, and the movements themselves, are highly stereotyped.

     
  2. 2.

    In a bout of gill cleaning the paired gill plates are adducted across the midline so that opposite gill plates can interact. The interaction consists of rhythmic flicking of the inner lobe of a gill plate between the book gill lamellae of the contralateral gill.

     
  3. 3.

    Each bout of cleaning lasts for approximately one minute and can be divided into four basic phases: pairing, crossing over, lateral cleaning, and medial cleaning (Fig. 2).

     
  4. 4.

    There are two distinct pairing arrangements of the gill plates during cleaning. During left leading (LL) cleaning all the gill plates are paired with an adjacent gill plate, except L1 and R5. During right leading (RL) cleaning, which is the mirror image of LL cleaning, all the gills are paired except for R1 and L5 (Fig. 3).

     
  5. 5.

    Cleaning bouts are further organized into long-term patterns which last for hours (Fig. 4).

     
  6. 6.

    There are four major muscle groups involved in gill cleaning. Muscles 48/115 adduct the gill plate across the midline; muscles 113/114 flick the inner lobe, and muscles 20 (remotor) and 22 (promotor) control the anterior-posterior position of the gill plate during cleaning. The patterns of activity of these muscles are reliably different during RL and LL cleaning (Fig. 5).

     
  7. 7.

    Each abdominal ganglion controls the movements of a pair of gill plates. During a bout of cleaning one member of the pair is being cleaned (subprogram A) and the other is not being cleaned (subprogram B). It is suggested that there are higher-order interganglionic neurons which control the expression of either the RL or LL patterns of cleaning. This is accomplished by dictating which gill plate of a pair uses subprogram A and which subprogram B, for all five ganglia.

     
  8. 8.

    It is concluded that a gill cleaning bout constitutes a moderately complex fixed action pattern, meeting the criteria of stereotypy within and between animals, intricacy of appendage movements, involvement of more than one effector system, and tendency to occur in its entirety in the absence of apparent stimuli (vacuum activity).

     

Keywords

Abdominal Ganglion Gill Lamella Definite Period Appendage Movement Major Muscle Group 

Abbreviations

CNS

central nervous system

L1–5

left gill plates 1–5

LL

left leading pattern of gill cleaning

R1–5

right gill plates 1–5

RL

right leading pattern of gill cleaning

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References

  1. Carlson, J.R., Bentley, D.R.: Ecdysis: neural orchestration of a complex behavioral performance. Science195, 1006–1008 (1977)Google Scholar
  2. Davis, W.J.: The neural control of swimmeret beating in the lobster. J. Exp. Biol.50, 99–118 (1969)Google Scholar
  3. Davis, W.J., Kennedy, D.: Organization of invertebrate motor systems. In: Handbook of physiology, Sect. 1, Vol. 1, Part 2. Geiger, S.R., Kandel, E.R., Brookhart, J.M., Mountcastle, V.B. (eds.), pp. 1023–1087. Bethesda: American Physiological Society 1977Google Scholar
  4. Dorsett, D.A., Willows, A.O.D., Hoyle, G.: Neuronal basis of behavior inTritonia. IV. Central origin of a fixed action pattern. J. Neurobiol.4, 287–300 (1973)Google Scholar
  5. Fourtner, C.R., Drewes, C.D., Pax, R.A.: Rhythmic outputs coordinating the respiratory movement of the gill plates ofLimulus polyphemus. Comp. Biochem. Physiol.38 A, 751–762 (1971)Google Scholar
  6. Grillner, S.: Locomotion in vertebrates: central mechanisms and reflex interactions. Physiol. Rev.55, 304–347 (1975)Google Scholar
  7. Hyde, I.H.: The nervous mechanism of respiratory movements inLimulus polyphemus. J. Morphol.9, 431–448 (1893)Google Scholar
  8. Hyman, L.H.: The invertebrates: Platyhelminthes and Rhyncocoela. The acoelomate bilateria, Vol. II. New York: McGraw-Hill 1951Google Scholar
  9. Jennings, J.B.: Symbiosis in the Turbellaria and their implications in studies on the evolution of parasitism. In: Symbiosis in the sea. Vernberg, W.B. (ed.). Columbia: South Carolina Press 1974Google Scholar
  10. Koester, J., Mayeri, E., Liebeswar, G., Kandel, E.R.: Neural control of circulation inAplysia. II. Interneurons. J. Neurophysiol.37, 476–496 (1974)Google Scholar
  11. Lankester, E.R., Benham, W.B.S., Beck, E.J.: On the muscular and endoskeletal systems ofLimulus andScorpio, with some notes on the generic characteristics of scorpions. II. Description of the muscular and endoskeletal systems ofLimulus. Trans. Zool. Soc. (London)11, 314–338 (1885)Google Scholar
  12. Moffett, S.: Neuronal events underlying rhythmic behavior in invertebrates. Comp. Biochem. Physiol.57 A, 187–195 (1977)Google Scholar
  13. Patten, W.: The evolution of vertebrates and their kin. Philadelphia: Blakiston 1912Google Scholar
  14. Patten, W., Redenbaugh, W.A.: Studies onLimulus. II. The nervous system ofLimulus polyphemus. with observations upon the general anatomy. J. Morphol.16, 91–180 (1900)Google Scholar
  15. Stein, P.S.: Intersegmental coordination of swimmeret motoneuron activity in crayfish. J. Neurophysiol.34, 310–318 (1971)Google Scholar
  16. Truman, J.W., Sokolove, P.G.: Silk moth eclosion: hormonal triggering of a centrally programmed pattern of behavior. Science175, 1491–1493 (1972)Google Scholar
  17. Watson, W.H. III: Long-term patterns of gill cleaning, ventilation and swimming inLimulus. J. Comp. Physiol.141, 77–85 (1980)Google Scholar
  18. Watson, W.H. III, Wyse, G.A.: Coordination of heart and gill rhythms inLimulus. J. Comp. Physiol.124, 267–275 (1978)Google Scholar
  19. Willows, A.O.D., Dorsett, D.A., Hoyle, G.: The neuronal basis of behavior inTritonia. III. Neuronal mechanism of a fixed action pattern. J. Neurobiol.4, 255–285 (1973)Google Scholar
  20. Wyse, G.A.: Intracellular and extracellular motor neuron activity underlying rhythmic respiration inLimulus. J. Comp. Physiol.81, 259–276 (1972)Google Scholar
  21. Wyse, G.A., Page, C.H.: Sensory and central nervous control of gill ventilation inLimulus. Fed. Proc.35, 2007–2012 (1976)Google Scholar
  22. Wyse, G.A., Sanes, D.H., Watson, W.H. III: Central neural motor programs underlying short- and long-term patterns ofLimulus respiratory activity. J. Comp. Physiol.141, 87–92 (1980)Google Scholar

Copyright information

© Springer-Verlag 1980

Authors and Affiliations

  • Winsor H. WatsonIII
    • 1
    • 2
  1. 1.Department of ZoologyUniversity of MassachusettsAmherstUSA
  2. 2.Marine Biological LaboratoryWoods HoleUSA

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