J. comp. Physiol. 129, 217-221 (1979)
of Comparative
Physiology. A
9 by Springer-Verlag 1979Leg Resistance Reaction as an Output and an Input
Reactions of the Spiny Lobster,Palinurus vulgaris,
to Substrate Tilt VID o u g l a s M . N e l l * , H e r m a n n S c h 6 n e , a n d F e l i c i t a S c a p i n i * *
Max-Planck-Institut ftir Verhaltensphysiologie, D-8131 Seewiesen, Federal Republic of Germany Accepted September 27, 1978
Summary. 1. S u b s t r a t e tilting c o n s i s t e n t l y elicits b o t h a n e y e s t a l k r e s p o n s e a n d a r e s i s t a n c e r e a c t i o n b y the legs in the s p i n y l o b s t e r Palinurus vulgaris.
2. T h e s e two r e s p o n s e s differ f r o m e a c h o t h e r in t e r m s o f t h e i r p h a s o - t o n i c f o r m , f r e q u e n c y r e s p o n s e a n d s t r e n g t h o f b i l a t e r a l linkage.
3. C h a n g i n g t h e r e l a t i o n s h i p b e t w e e n i m p o s e d leg m o v e m e n t a n d the force o f leg resistance d e m o n - strates t h a t f o r c e c h a n g e s a l o n e l e a d to e y e s t a l k m o v e - m e n t s . H o w e v e r this e y e s t a l k r e s p o n s e is g r e a t l y en- h a n c e d w h e n leg d i s p l a c e m e n t also t a k e s place.
4. I t a p p e a r s t h a t the d e t e c t i o n o f s u b s t r a t e o r i e n t a t i o n h a s a m u l t i s e n s o r y basis d i s t r i b u t e d be- t w e e n d i f f e r e n t leg p r o p r i o c e p t o r s .
mental procedures are described elsewhere (Sch6ne et al., 1976; Neil and Sch6ne, 1979). The footboard mass was in most cases brought into balance about its turning axis, and in all cases the forces during lifts without the animal present were subtracted from the values obtained during the experiment. The forces in the system were measured using the arrangement shown in Fig. 1. A strain gauge (Grass type FT.03C) was incorporated in the drive system which operated either directly onto the footboard, or through an interposed spring. The springs employed had the following com- pliances:
Spring No. Compliance (g. cm- 1)
37 50 38 11 39 4 42 125 Introduction T h e r i g h t i n g r e s p o n s e s w h i c h serve to r e s t o r e a n d m a i n t a i n n o r m a l p o s t u r e are i m p o r t a n t c o m p o n e n t s o f the r e a c t i o n s i n d u c e d b y s u b s t r a t e tilt in the s p i n y l o b s t e r , Palinurus vulgaris ( S c h 6 n e et al., 1976). The r e s i s t a n c e r e a c t i o n s o f the legs a g a i n s t the s u b s t r a t e fall i n t o this c a t e g o r y , a n d h a v e b e e n m e a s u r e d u n d e r a v a r i e t y o f e x p e r i m e n t a l c o n d i t i o n s ( S c a p i n i et al., 1978 ; S c h 6 n e et al., 1978). H e r e we p r e s e n t a n anal- ysis o f the r e s i s t a n c e r e a c t i o n s o f the legs as a n o u t p u t o f the e q u i l i b r i u m system, a n d r e p o r t t h a t in the ab- sence o f m o v e m e n t itself c h a n g e s in the forces a c t i n g o n the legs p r o v i d e a n a d e q u a t e i n p u t to the leg r e c e p - t o r s y s t e m c o n t r o l l i n g e y e s t a l k m o v e m e n t .
Material and Methods
Spiny lobsters (Palinurus vulgaris) from the Tyrrhenian coast were kept under semi-natural conditions. Apparatus and general experi- * Permanent address: Department of Zoology, University of Glasgow, Glasgow G12 8QQ, Scotland
** Permanent address : Istituto di Zoologia, Universit~t di Firenze, Firenze, Italy
BOARD i H
" 7 1
{()RCE
i
bl I!!ANGI
Fig. 1. Apparatus used to tilt footboard and to record leg resistance reaction and eyestalk response. A strain gauge is incorporated in the drive system, and when necessary springs can be inserted below the gauge. Outputs from the strain gauge, the board angle potentiometer and the eyestalk angle transducer are converted to analog signals and fed to a pen recorder
218 D.M. Neil et al. : Reactions o f the Spiny Lobster to Substrate Tilt FORCE [200g EXR 3/3/1, P3 = ~ l EYE c 2 0 ~ BOARD ! 20 ~ , , ,,h 1 , , ,
o
6'
'
'4
21
EXP. M l t 1-2,P 3 ' Z 'r C a ' FORCE [200g / EYE [20 ~ B OAR D_~[_20 ~ 2 ' 2 ' ' ' 2 6 ' ' f ~ EXP. 3/2/2, P3 i o 4T I M E
' 6
FORCE [200g EYE r20~ ' ' I~2 s e c )BOARD [20 ~
, + LI'6
Fig. 2. Effect of changing angular velocity of footboard tilt on leg resistance reaction and eyestalk response. Outputs were moni- tored on left side o f the animal (see inset figure), tn each record upper trace is a force measurement (increasing force upwards), middle trace is movement o f the left eyestalk (dorsal movement is downwards) and lower trace is board movement (lift is upwards).
Arrows: starting values; dashed lines: horizontal position of the
board and the average initial force and eyestalk values. Velocity of footboard tilt: top record, 15.0 ~ s - 1 ; middle record, 8.3 ~ s - t ; b o t t o m record, 3.3 ~ s -1
]=-
.Lift Stop Down Stop
t
t
1
l
/ ~ LEFT],+~
Io) WHOLE ]14 ~ L up I R down j f ~ BOARD _14 ~ L down / R up I I I t I I [ I I I I I I I i [ 4 8 12 16 20 24 28 32Lift Stop Down Stop
t
t
1
l
J
I I I I I I I t I I I I 4 8 12 16 20 24 (b) +250g FORCE -250g 16 LEFT EYE~
14 ~ Left up LEFT 14 = Lef! down H.BOARD=- FORCE {c)
500 g LEFT
, . ~ " ~ - - - ~ 2 2 o +
~ . ~ RIGHT "315 ~ Right down
. ~ ~ ~. u~n J~.~ARD_]15= Right up [ i I I I I [ I I I 1 I I I I I I l
; 8 12 16 20 24 28 32 36
TIME (sec]
Fig. 3 a-e. Leg and eyestalk responses with different footboard con- figurations, a Whole footboard, ramp movements, b F o o t b o a r d split along long axis and hallTooard ipsitateral to monitored outputs moved (ramp tilts), e F o o t b o a r d split and halfboard contralateral to monitored outputs moved (sinusoidal tilts)
For a given lift o f the drive arm (routinely 10 cm, but in some cases 20 cm) the force acting on the board was a function of the strength of the spring. The lobster's leg reaction, by extending the spring, was capable of reducing board movement or preventing it completely. Eyestalk movements were measured using a minia- ture angle transducer (Marrelli and I-Isiao, 1976) and recorded on a Philips Oscilloscript pen recorder.
R e s u l t s
1. Force as an Output
During ramp movements of the footboard with rigid drive (Fig. 1) the righting force of the legs increases
with displacement and can reach values exceeding 500 g (Figs. 2, 3 a). When the imposed board move- ment stops the force exerted by the animal declines from this peak, but is still maintained at high values. The form of this response was found to be consistent over a range of tilt velocities (Fig. 2). The eyestalk response to these trapezoid board movements is of a phaso-tonic form, although the phasic peak which is reached before the end of the lift is not as distinct as previously found (Sch6ne et al., 1976).
When only the halfboard ipsilateral to the moni- tored eye is moved both the leg reaction and the eyestalk response are reduced to approximately half the values for whole board movement (Figs. 3 a, b).
60-- p
/,0
\'d x
\
< m20
~ ~ :
..R\b
Force
E_ 0 - - - o - 2 0 ~ Left Eye .z -/,0, I I I I I l l l l 1 I I I I l l l l 0.01 0.1 1 FRE&UE NCY (Hz)Fig. 4. Phase relationships of eyestalk and leg responses to sinusoi- dal movements of a whole footboard over a restricted range of frequencies (0.02-0.2 Hz)
When legs contralateral to b o t h m o n i t o r e d outputs are m o v e d on a halfboard the eyestalk m o v e m e n t is reduced by a further 25%, while the resistance reaction of the legs (standing on a stationary half- board) almost completely disappears (Fig. 3c).
The phase angles of eyestalk responses relative to oscillatory whole b o a r d m o v e m e n t s are consistent with previous measures (Neil and Sch6ne, 1978) but the phase of the leg reaction leads the eyestalk re- sponse over the range o f frequencies tested (Fig. 4).
2. F o r c e as an I n p u t
The above results demonstrate that leg resistance reactions always a c c o m p a n y f o o t b o a r d movements, and thus the possibility exists that it is in fact these force changes rather than changes in leg joint angles which underlie the measured eyestalk movements. In an a t t e m p t to investigate this possibility the re- lationship between the imposed b o a r d m o v e m e n t and the resulting leg righting force was altered by inserting different springs into the driving system (see Material and Methods). The profile of the leg reaction is essentially unchanged during lifts with an interposed spring c o m p a r e d with the rigid drive, but the magnitude of b o a r d m o v e m e n t is reduced to a small drift which continues beyond the lifting phase (Fig. 5). The eyestalks respond strongly during the lift, which corresponds to the period of increasing leg force, but continue to m o v e when the lift is completed and the force is declining, as long as the f o o t b o a r d continues to drift (Fig. 5 a). Similar results were obtained during the return phase (drive m o t o r reversed).
In m a n y experiments, and with different stimulus configurations (whole board, half board, three-leg
Lift Stop Down (a}
i i
11
. . . . BOARD ]6o
1 I I I I l ////1__ I I I I [ I A 8 12 16 20 2/, 60 64. 68 72 76 80 8A
Lift Stop Down (b)
. . . . , d '~176 FORCE ]sog
. . . .
1, ~
BOARD I i I I I I Ill// I I I ..I I I I 0 4 8 12 16 20 24 28 60 6/. 68 72 76 8084. TIME (sec) 3Fig. 5a and b. Typical examples of experiments with interposed springs in the drive system. In each case the drive arm moves the upper end of the spring through ca. 10 cm. Periods when the drive motor is operating indicated by arrows. In a (spring 38) both spring extension (lift) and release (down) result in a leg resis- tance reaction, although in each case there is an accompanying board movement. In b (spring 39) leg reaction is again present, but here almost completely prevents board movement during the lift. On return the leg reaction subsides but no board movement occurs. However, a clear eyestalk response is still present
group) eyestalk m o v e m e n t s of up to 4 ~ were measured in the complete absence of f o o t b o a r d m o v e m e n t s (Figs. 5b, 6). In each case, however, leg righting forces in the range 10-130 g were recorded (Fig. 6). This indicates that force alone, in the absence of leg move- ment, is an input p a r a m e t e r to the eyestalk control system. Nevertheless, m o v e m e n t o f the leg joints is an additional and more powerful input, as is demon- strated in Fig. 6. F o r a given force of leg reaction the eyestalk response increases with increasing foot- b o a r d displacement, and reaches values which greatly exceed those recorded with force changes alone.
D i s c u s s i o n
Several differences emerge between the responses of" legs and eyestalks to stimulation o f leg receptors on a moving substrate. The leg resistance reaction con- tinues as long as there is an imposed force, whereas
220 D.M. Neil et al. : Reactions of the Spiny Lobster to Substrate Tilt 16
T
/ EYESTALK t2~ I MOVEMENT I0 [Degrees) ... 6-...T
o 2O0 26 80 FORCE (g) 0 0Fig. 6. The relationship of the eyestalk response to leg displacement and leg resistance force, plotted in 3 dimensions. Data from 3 experimental arrangements: 9 =whole footboard (springs 37, 38); o = h a l f b o a r d (springs 37, 38, 39, 42); 9 = group of three legs held in cradle spanning meri (springs 38, 39). When no leg displacement occurs the eyestalk response appears to be a function of the force generated by the leg reaction. However, for a given force eyestalk response increases in ,proportion to amount of leg displacement
the eye response reaches peak values before the end of board movement (Fig. 2). The different phase rela- tionships with sinusoidal inputs (Fig. 4) are also indi- cative of different input-output transformations. A clear difference exists in the strength of the contra- lateral effect, the eyestalk response being a little less than the ipsilateral value while the leg reaction is effectively absent (Fig. 3). Such differences may be related to the natural functions of these output sys- tems. The eyestalk reaction compensates for the shift of the visual surroundings, and is therefore expressed by both eyes. The leg reactions contribute to righting and may be organised mainly in terms of reflexes within individual appendages which react to particu- lar external forces and movements acting upon them. The finding that eyestalk movements accompany changes in the leg resistance reactions in the absence of leg movement itself raises questions about the sen-
sory basis of this effect. Candidates as receptors in- clude stress detectors in the cuticle (e.g. campaniform sensilla, CSD's)(Laverack, 1976; Clarac, 1976)and muscle tension organs (Macmillan, 1976). The effect of such force detecting systems acting alone is limited, however, resulting in eyestalk displacements of less than 5 ~ This compares with eyestalk responses of greater than 20 ~ when changes in particular leg joint angles (especially at C-B, see Sch6ne et al., 1976) also occur (Fig. 6). It therefore seems probable that a compound sensory input from force detectors and position detec- tors (e.g. chordotonal organs, strand organs) nor- mally drives the eyestalk response to forced changes in leg-to-body position. Although the nature of this interaction is at present unknown, it is becoming in- creasingly clear that intra- and inter-segmental leg reflexes in Palinurus are based on multiple pro- prioceptive effects rather than on simple reflex re-
s p o n s e s t o t h e s t i m u l a t i o n o f i n d i v i d u a l s e n s o r y r e c e p - t o r s ( C l a r a c e t a l . , 1 9 7 6 ; B u s h e t a l . , 1 9 7 8 ; C l a r a c e t al., 1 9 7 8 ; S c a p i n i e t al., 1978).
F.S. and D.M.N. received financial support from the Max-Planck- Gesellschaft. D.M.N. was also supported by a grant from the Carnegie Trust. We want to express our thanks to Renate Alton for her co-operative help.
References
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Clarac, F., Neil, D.M., Vedel, J.P. : The control of antennal move- ments by leg proprioceptors in the rock lobster, PaIinurus vul- garis. J. comp. Physiol. 107, 275-292 (1976)
Clarac, F., Vedel, J.P., Bush, B.M.H.: Intersegmental reflex co- ordination by a single joint receptor organ (CB) in rock lobster walking legs. J. Exp. Biol. 73, 29 46 (1978)
Laverack, M.S. : External proprioceptors. In: Structure and function ofproprioceptors in the invertebrates. Mill, P.J. (ed.), pp. 1 63. London: Chapman and Hall 1976
Macmillan, D.L. : Arthropod apodeme tension receptors. In: Struc- ture and function of proprioceptors in the invertebrates. Mill, P.J. (ed.), pp. 427442. London: Chapman and Hall 1976 Marrelli, J.D., Hsiao, H.S. : Miniature angle transducer for marine
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responses. J. Exp. Biolf(in press ) (1979)
Scapini, F., Neil, D.M., Sch6ne, H. : Leg-to-body geometry deter- mines eyestalk reactions to substrate tilt. Substrate orientation in spiny lobsters IV. J. comp. Physiol. 126, 287-291 (1978) Sch6ne, H., Neil, D.M., Stein, A., Carlstead, M.K.: Reactions of the spiny lobster, Palinurus vulgaris, to substrate tilt (I).
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Sch6ne, H., Neil, D.M., Scapini, F.: The influence of substrate contact on the gravity orientation. Substrate orientation in spiny lobsters V. J. comp. Physiol. 126, 293-295 (1978)
