J. comp. Physiol. 126, 287-291 (1978)
Journal
of Comparative
Physiology. A
9 by Springer-Verlag 1978Leg-to-Body Geometry Determines Eyestalk Reactions to Substrate Tilt
Substrate Orientation in Spiny Lobsters IV
Felicita Scapini*, Douglas M. Neil**, H e r m a n n Sch6ne
Max-Planck-Institut ffir Verhaltensphysiologie, D-8131 Seewiesen, Federal Republic of Germany Accepted May 31, 1978
Summary. The effect o f oscillatory m o v e m e n t of sin- gle legs (about C-B axis) on c o m p e n s a t o r y eyestalk reactions and on leg counterforce as normally produced by substrate tilt has been investigated with the legs at different states of flexion (M-C joint) and leg-to-body orientation (T-C joint). Eye response and force reaction released by standard C-B m o v e m e n t increase with increasing angle of M - C (Figs. 2, 4) and decrease with decrease of T-C angle (Fig. 3). The effects d e m o n s t r a t e a multiplying influence o f M - C signal and T-C signal on C-B signals. The stump of an a u t o t o m i z e d leg releases eye responses of similar magnitude to unimpaired single legs (Fig. 5).
The data are discussed in relation to neurophys- iological findings and with respect to the geometrical implications for the mechanism o f substrate orienta- tion (Fig. 6).
Introduction
D e c a p o d crustacea show c o m p e n s a t o r y eyestalk m o v e m e n t s and equilibrium reactions in response to stimulation o f leg proprioceptors on a tilting substrate (Sch6ne et al., 1976). The basic elements of the sen- sory system involved are the individual legs which have different effects on the eye response (Sch6ne and Neff, 1977) and which contribute accordingly to the interaction .of leg receptor input and statocyst input (Sch6ne et al., 1978). We are n o w in a position to consider h o w each leg operates to produce a biolog- ically meaningful output. Available evidence suggests
* Permanent address: Istituto di Zoologia, Universit5 di Firenze, Italy
** Permanent address: Department of Zoology, University of Glasgow, Scotland
Please address requests for offprints to H. Sch6ne
that m o v e m e n t s of the C-B joint are of particular im- portance in producing the observed responses (Sch6ne et al., 1976; Clarac et al., 1976). Here we report exper- iments which investigate geometrical relationships at other joints within the leg and between leg and body in relation to the c o m p e n s a t o r y eyestalk response.
Materials and Methods
Spiny lobsters (Palinurus vulgaris) from the Thyrrenian coast were kept under seminatural conditions. Apparatus and general experi- mental procedure have been described in a previous paper (Sch6ne et al., 1976; Neil and Sch6ne, 1978). Special techniques concern the moving device for single legs (Fig. 1). Plexiglas cradles were
Fig. 1. Setup for moving single legs or groups of legs and recording displacement, eye response and the force exerted by the legs. The animal is shown in a stylised frontview with eyestalks and legs. The same holds true for the inset drawings in the other figures
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26,27,
P4 L E G S L 2+3+4 ~ @o
AMPL.• ~ 0.065 H z ] R LEGS MC e ,, +16 ~ ' ,, } ' O F F ~ | " . . . . , 0.0/-,3 HzJ B O A R D ,, +15 ~ 0 . 0 6 5 H z - O N /,,_ .| 0 I I I I 1 I I I 1 1 I I 6 0 90 120 150 M C - A N G L E ( d e g )Fig. 2. Eyestalk response to oscillatory movement of left meri of legs 2, 3, 4 at various fixed positions of M-C joint. Open circles refer to experiments with right legs strung up, filled circles to those with right legs touching stationary substrate. Note that eye responses are reduced in the latter case (due to interaction of b o t h sides; cf. Sch6ne and Neff, 1977)
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/ 0 / 0 0 0 I I I I I I I I I I 30 6 0 9 0 1 2 0 I i M C - A N G L E ( d e g )Fig. 3. Eye response to oscillatory movement of left merus (leg 4) at various fixed M-C angles, and at two settings of T-C angle (cf. left inset figure representing a dorsal view)
F. Scapini et al. : Eye Response to Substrate Tilt in Spiny Lobsters 289 <
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Fig. 4. Eyestalk response (open symbols) and force response (filled symbols) to oscillatory movement of left legs 2, 3, 4 at various fixed M-C angles. Eye response and force response have been recorded simultaneously, they refer to the same experiments; numbers denote sequence of measurements
Cl EXP. 1014, P5 MC 135 ~ , TC 90 ~ [ 7. 5 o " ~ . . . / / ~ / ~ E Y E b EXP. 29/15, P7
BASIS OF AUTOT. LEG [3
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Fig. 5a and b. Eye response to oscillatory movement(a) of a single leg and(b) of the base of an autotomized leg; the basis was provided with a prothesis stick
constructed which fitted neatly over the merus and carpus leg segments of 1 or 3 legs. A fixable joint made it possible to set the carpus at any position in its normal angular range. An extension from the cradle was connected to the drive transmission into which a strain gauge (Grass force displacement transducer FT 0.3 C) was inserted.
Thus the counterforcing response of the legs to the imposed stimulus could be continuously monitored. Eye movements were measured using a miniature angle transducing device (Marrelli and Hsiao, 1976) and recorded on a chart recorder (Philips Oscillo- script).
Data points were derived from the original records by averag- ing peak-to-peak values of 6-10 cycles, the variability of response amplitude being small.
R e s u l t s
Eye Responses
F o r a c o n s t a n t a m p l i t u d e o f m o v e m e n t o f t h e C - B j o i n t , c h a n g e s in t h e s t a t i c a n g u l a r s e t t i n g o f t h e M - C j o i n t h a v e a s y s t e m a t i c e f f e c t o n t h e e v o k e d e y e s t a l k m o v e m e n t (Fig. 2), L a r g e r r e s p o n s e s o c c u r w h e n t h e M - C j o i n t is e x t e n d e d t h a n w h e n it is f l e x e d . I n a d d i t i o n to this i n f l u e n c e o f t h e r e l a t i o n s b e - t w e e n l e g s e g m e n t s a n o t h e r a s p e c t o f l e g - t o - b o d y g e o -metry is also of importance. The setting of the T-C angle was changed, so that the leg m o v e d out of the transverse plane of the body into a plane directed 45 ~ to the front. This systematically reduced the eye- stalk response over the whole range of M - C settings (Fig. 3).
Force Responses
A new aspect concerns the counterforce produced by the m o v e d leg itself (Fig. 4) (cf. Neil et al., 1978). The settings of the M - C angles m o d u l a t e the force of the legs involved. F o r the same angular m o v e m e n t of the leg with respect to b o d y (at C-B joint) the counterforce generated by the basal muscles is larger when the M - C joint is open (170 ~ than when it is closed (90~
Autotomized Leg
Although MC-joint is of influence, the CB-joint nev- ertheless works in the absence of the input f r o m the distal segments. This was d e m o n s t r a t e d by applying sinusoidal m o v e m e n t s to a prothesis firmly cemented to the stump of an a u t o t o m i z e d leg (i.e. to the basis- segment) (Fig. 5). The reaction is of the same order of magnitude as that of the experiments with single legs.
Discussion
The results d e m o n s t r a t e that inputs f r o m propriocep- tors at the M - C and T-C joints interact with the signal f r o m the C-B joint receptors as multiplying factors. The relationship between the results and the " d i s t r i b u t e d reflexes" recently described in crustacean legs (Clarac et al., 1978; Ayers and Davis, 1977) re- mains at present unclear. The observed effects on leg force output (Fig. 4) m a y indeed reflect such interseg- mental reflexes. Our results on the eye response imply, however, that receptors at one joint can influence the output effect o f receptors at a n o t h e r joint, an interaction which falls outside our current concept of distributed reflexes (Bush et al., 1978).
F o r an understanding of the functional signifi- cance of o u r results, the geometry of the leg-to-body relations m u s t be taken into account. The M - C joint permits m o v e m e n t in a vertical plane, so that flexion and extension a b o u t the joint cause the leg to stand at different distances f r o m the b o d y long axis. The M - C setting is thus an i m p o r t a n t p a r a m e t e r determin- ing the angular displacement of the C-B joint caused
f \
, r , , , , , , . . V / / / ' ,
Fig. 6. Scheme of experimental situation as transferred to natural conditions. Note that same merus lift releases small eye response, when leg touches small step at close distance (M-C flexed) and larger eye response when leg touches higher step at larger distance (M-C extended)
by substrate tilt. The leg articulates horizontally a b o u t T-C joint and thus a m o v e m e n t here b o t h changes the standing distance f r o m the body midline, and in addition moves the plane of action of the distal leg segments relative to the transverse body plane. The following explanation is in accordance with these geometrical relations and our experimental find- ings. If we suppose that the eye m o v e m e n t s compen- sate for the shift of the (visual) surroundings as caused by the substrate-to-body movements, then our results imply that leg m o v e m e n t s with an open MC-angle correspond to a greater shift of the surrounding than those with a m o r e closed one. Such a situation is demonstrated in Figure 6. The same merus lift is produced by a low step at a small distance f r o m b o d y (i.e. flexed MC-angle) and by a higher step of a larger distance (extended M - C joint). The latter situation corresponds to a larger change of surround- ings and thus should lead, and does, to a larger eye- stalk reaction than the first one. A similar line of argument fits the observed effects of changing the T-C joint angle.
Thus our findings indicate that the geometrical relations of the legs with respect to body affect the c o m p e n s a t o r y eye movement. The question, however, if in addition the individual legs act differently also because of specific intrinsic weighting factors is still open.
We wish to give thanks to the Max-Planck-Institut (FS, DMN) and to the Carnegie Trust (DMN) for financial support. We thank Renate Alton for technical assistance and Dorothee Maier for her help with the data analysis. Particular thanks should be expressed to the Istituto di Zoologia, Universita di Firenze (Direc- tor: Prof. Dr. L. Pardi) for promoting this research.
References
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F. Scapini et al. : Eye Response to Substrate Tilt in Spiny Lobsters 291
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