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Responses of cuticular sense organs of the lobster, Homarus vulgaris (crustacea)—I. Hair-peg organs as water current receptors
Comp. Biochem. Physiol., 1962, Vol. 5, pp. 319 to 325. Pergamon Press Ltd., London. Printed in Great Britain
RESPONSES OF CUTICULAR SENSE ORGANS OF THE LOBSTER, H O MA R U S VULGARIS (CRUSTACEA)--I. HAIR-PEG ORGANS AS WATER CURRENT RECEPTORS M. S. LAVERACK The Gatty Marine Laboratory, St. Andrews, Fife, Scotland
(Received 15 January 1962) A b s t r a c t - - 1 . A short description is given of hair-peg organs which are present
in large numbers on the anterior part of the body and appendages in Homarus. 2. Observations have shown that these sense organs respond to a water current by deflexion about a hinge at their base. 3. Electrophysiological studies reveal that impulses are generated by the sense organs when they are deflected by a water current. 4. Action potentials occur at a water flow of about 0-30 cm/sec and above. 5. It is suggested that this represents a "distant touch" mechanism. INTRODUCTION SENSE organs associated with the cuticle of lower crustaceans, often in the form of projecting hairs or tufts of hairs, have been described for a number of species, e.g. Argulus (Debaisieux, 1953) and Caprella (Wetzel, 1935). Few studies have been made on decapods, however, and information is only available for Praunus and Crangon (Debaisieux, 1949), Carcinus (Luther, 1930) and a report of slit sensiUa in Homarus (Wiersma, 1959). Behavioural studies have indicated that sense organs responding to water currents, pressure waves, chemicals, vibration and other stimuli are probably present on the crustacean body and appendages (Luther, 1930; Brock, 1930). Varied functions have been postulated for certain specific structures (figures by Luther, 1930; Balss, 1944), but these proposals rely upon a theoretical analysis of the possible actions of the sense organs based on anatomical data alone. Electrophysiological experiments designed to discover and distinguish the functions of such organs have been carried out in only a few cases. Hodgson (1958), (Cohen & Dijkgraaf, 1961) has shown that the median antennule of Cambarus bartonii is sensitive to chemical stimuli. Wiersma (1959) reports that the slit sensillae carried on the walking legs of the lobster Homarusare sensitive to touch, but is not sure whether this is the normal physiological response. The present work on single fibre or few-unit preparations, in which differences between sensillae have been distinguished, supports at least some of the suggestions of earlier workers that decapods are sensitive to water currents. 319
320
M.S. LAWRACK THE SENSE ORGAN
Study of the external surface and of histological sections of the chelae of Homarus (Laverack, 1962) reveals that the surface is covered with many hair-like projections. Externally the most obvious of these are the bunches and rows of hairs that are particularly prominent near the cutting edge of the chela. Less obvious, but present in great number, are small depressions each containing a
FIG. I. A hair-peg organ. These lie in depressions on the exterior surface of the cuticle. Note the solid central rod surrounded by fine hairs. The organ is seen here from the broad face.
small hair sensillum arranged like a fan in one plane. T h e sensillum consists of a plate carrying a rod which is surrounded by fifty to one hundred hairs; the hairs are arranged in a fan-shaped manner around the base of the rod (Fig. 1). The plate is hinged along the broad axis of its base, and the sensillum as a whole deflects
_• Movement of organA W a t e r ~ k _ ~ . i/2 the cup Woter'~7"~
FIa. 2. Diagram to show how the hair-peg organ is deflected in its cup by a water current passing across the surface of the cuticle. The diagram shows the innervation which consists of fibres from three to five sensory cells lying in the epidermis. when a water current acts upon the broad surface of the fan (Fig. 2). The rod from tip to base measures approximately 50~; its base is 15b~in breadth. The structures are permanent and not easily broken off, and are replaced at moulting since they have been seen fully developed on newly moulted animals. These organs, which will hereafter be called hair-peg organs , are distributed over large areas of the exoskeleton of the lobster. T h e y are most concentrated on the inner and outer faces of the chelae where .they number about 75/cm 2. The hair-pegs are also found on the walking legs (30/cm ~) and anterior parts of
WATER CURRENT RECEPTORS I N HOMARU~ VULGARLS
321
the body. They have been observed at 25/cm = on the carapace. They are infrequent in distribution on the posterior parts of the body such as the rear appendages and the telson, and are notably absent from the antennae and antennules. MATERIALS AND METHOD Experiments were carried out on isolated claws of Homarus. The upper, movable joint and the lower fixed joint 'of the chela were both found suitable for investigation; thus each animal provides four preparations. The length of each preparation was about 1 in.
gxoskeleton
Ner~
bundles
FIG. 3. Diagram showing the experimental situation. The exoskeleton is removed for about ½ in. along the claw and the internal tissues teased to expose the nerve bundles within. The chela joint was cut from the cheliped and by careful manipulation with a needle the fine nervous connexions to the sense organs of the proximal portion of the claw were broken. The needle was passed between the internal tissues and the exoskeleton for this purpose. The exoskeleton was then removed with bone forceps for a distance of about ½ in. along the claw (Fig. 3), to expose the internal tissues.
,o,ap I
it-c-7 il I_
I /
!
oo,,,o.
// Preparation Rubber diaphragm FIG. 4. T h e claw as it is placed in the expe~mental flow chamber. W a t e r flows from left to right across the surface of the claw.
After this preliminary exposure of tissue at its base the tip of the claw was pushed through a small hole in a rubber diaphragm in the experimental chamber, as shown in Fig. 4. If the hole in the diaphragm is small it is completely occluded by the chela, which thus prevents escape of water from the chamber. If water did tend to leak from the hole this was prevented by applying Vaseline to its edges. The intact distal end of the claw now protruded into the experimental flow chamber,
322
M.S. LAVERACK
whilst the exposed part was available for further dissection under a binocular microscope. The flow chamber was then filled with sea water and connected to a reservoir containing sea water. Careful teasing of the exposed tissues reveals that the nervous supply of this region consists of numerous stout bundles of fibres, the majority of which must presumably be sensory in function. Selection of an appropriate fibre bundle connected to a sense organ lying within the experimental chamber was done by trial and error as the innervation pattern is not constant. It is not possible to draw a map of the fibres and state that a particular sense-organ response can be monitored from a fibre in a given region. However, the hair-peg organs are so numerous on the surface of the chelae that chances are high that functional units can be found. Impulses were monitored with a conventional amplifier and oscilloscope display, with concurrent recording on tape for later analysis. Recordings were made through fine platinum electrodes held by a micromanipulator. Two methods of stimulation were used. First, an electrically controlled inlet valve was used to start and stop a flow of water through a chamber from a reservoir. The opening and closing of the valve was recorded on the second beam of the oscilloscope in some experiments, but it was found that an artefact, produced at the moment of opening and also at the shutting of the valve, often appeared on the first beam and this was used to indicate the stimulation period in such records. Water flowing through the valve passed through a tap which could be turned so as to vary the volume of water passing across the chamber in a given period of time. Flow rates between 0.20 and 1.02 cm/sec could be obtained, and these were satisfactory for stimulation purposes. Secondly the tap itself was attached to the spindle of a 1~ potentiometer (variable) energized by a 120 V d.c. battery. As the tap was turned, deflexion of the second beam provided a record of the varying rate of flow through the chamber. RESULTS Water current receptor organs of the lobster, when placed in the experimental bath as described above, are not normally active. No background discharge of potentials is recorded when the water covering the preparation is still. It is essential that the tip of the claw be completely immersed beneath the surface of the water, because spurious discharges are observed if the water surface laps over the exoskeleton. When water is allowed to flow over the claw surface, action potentials are observed in the nerve fibres. At low rates of flow there is no response until the speed of flow reaches about 0-25 cm/sec. The initial response then consists of one or two action potentials at intervals of many seconds until the valve is closed. With increasing rates of flow the response recorded from these fibres becomes more pronounced and the activity more prolonged, with action potentials occurring at irregular intervals. The initial response, lasting about ~ - ~ sec, is a short burst of spikes that are of high frequency. At the fastest flow rate used (1.02 cm/sec) action potentials were obtained throughout the period that the valve was open
(d]
C)
(b)
(o)
ma
W Ul
~ G ~ J t J i
F SeC
m B U !
O ~ l i
FIG. 5. E x p e r i m e n t a l results showing the response of a single organ to water fl0w. T h e water current starts at the stimulus artefact and continues until the second artefact. T h e top line (a) shows the response to a flow of 1-02 cm/sec, (b) at 0"92 cm/sec, (c) 0.55 cm/sec and (d) the threshold response at a flow of 0"25 cm/sec.
~ I
|ncreoslnQ
Flow rote increQsinq
role
Flow
rate
decreasing
Fro. 6. Response of a h a i r - p e g o r g a n to a gradually increasing rate o f w a t e r flow. T h e s e c o n d b e a m indicates an increasing rate o f flow w h e n deflected d o w n ; a d e c r e a s i n g rate w h e n m o v i n g up.
I second
Flow
WATER CURRENT RECEPTORS I N H O M ARU S VULG.4RIS
323
and the maintained frequency was between 5/sec and 30/sec depending on the preparation, When the valve was closed a small burst of potentials was noted immediately following closure, the strength of the burst being dependent on the previous flow rate (Fig. 5). The "off" response is not so pronounced as the "on" response, the number of impulses seen being small. It is uncertain whether this "off" response is correlated with the hair-peg returning to its original position. Experiments involving tactile stimulation of these organs indicate that spikes occur only when the hair-peg is bent away from the normal plane, and not when it returns to the resting position. Some adaptation may occur during the passage of a water current over the chela surface, but experiments in which stimulation was prolonged for periods of 30--40 sec show that complete adaptation does not occur and that frequency of impulses remains fairly regular during this time. All records show that a postexcitatory period of depression follows after the first burst of action potentials. Experiments where the water current velocity was changed progressively also indicate that when water flows slowly the activity of the sense organ is low, rising as the water flow increases and then falling again when the water flow decreases (Fig. 6). When the velocity of water flow is changed rapidly and continuously the organ does not fire in a manner that closely follows the curve of the velocity of water, but only in an intermittent way. DISCUSSION
Cohen & Dijkgraaf (1961) have recently remarked on the lack of knowledge of the functions of the many described types of crustacean sense organ. Information which is available stems almost entirely from behavioural studies, where the reactions of intact animals have been compared with the reactions of other specimens from which the organ under consideration has been removed. Prosser (1935) and Wiersma, Ripley & Christensen (1955) have described action potentials in the central nervous system of the crayfish Procambarus resulting from tactile stimulation by bending of hairs. Wiersma (1959) has also described spikes occurring upon touch stimulation of "slit-sensillae" of Homarus, though touch sensitivity may not be their true function. Hughes & Wiersma (1960) investigated the synaptic connexions between sensory neurones and interneurones in the abdominal nerve cord of Procambarus clarkii, by stimulation of hairs carried on the abdominal segments. They noted that localization of stimulus was made difficult by the high sensitivity of certain end organs responding to any disturbance of the water covering the preparation. Analysis of this sensory function was not carried further. The suggestion that Cardnus maenas possesses sense organs responding to small water currents seems a possible explanation of the resuks of Bethe's experiments (1895), results which were attributed by Bethe to chemoreception. Blind animals were said to be able to distinguish the direction of attractant chemical stimuli, but may in fact have responded to minute water currents arising from the food source. Brock (1930), working on the same species, showed by behaviour
324
M.S. LAVERACK
experiments that the antennules carry organs which are sensitive to water currents, and this observation was extended by Luther (1930), who showed that water current sensitivity provided the basis for rheotactic orientation. That fine, delicate, tufted sense organs are present on the cuticle of decapod Crustacea has been remarked by a number of observers. In his review Balss (1944) suggested that these organs might be structures sensitive to water currents. Luther (1930) indicated that "B/Jschelorgane", similar to those shown in Fig. 1, are present on many surfaces of Carcinus maenas including the carapace, abdomen, dactylopodite of the periopods etc., but he suggested that they are chemosensory organs. In H o m a r u s vulgaris (Laverack, 1962), the distribution of hair-peg organs agrees with the findings of Luther, but observations of living examples shows that each hair-peg organ is hinged at its base and moves in response to water movements. When the organs move, impulses can be recorded in the nervous system. I have found that chemical stimuli do not cause responses above noise level. The hair-peg organs are sensitive to water velocities of the order of 0.30 cm/sec. Faster velocities evoke greater responses, and these appear to be non-adapting since the organs continue to fire throughout prolonged periods of stimulation without any noticeable decrease in frequency. They respond to suddenly changing water velocities, and also to currents that rise gradually over a period of seconds. I suggest that the hair-peg organs represent a " t o u c h " mechanism for reception of stimuli originating some distance away and which set up water currents. Lobsters kept in aquaria and provided with rock cover are often to be found sitting in crevices or holes with the large chelae held across in front of the body and with the antennae protruding into the water in front of the hole. It can now be appreciated that this stance presented a large sensory surface to the environment, including as it does the eyes, antennae, antennules and chelae. One interesting outcome of this investigation is the contradiction of the classical view that the antennae or antennules carry all the current-detecting mechanism of the animal. The hair-peg organs discussed in this paper have not been found either on the antennae or on antennules, though they are present in great numbers elsewhere on the body surface. Antennae and antennules may carry other current receptors and electrophysiological studies are in hand to ascertain whether or not such receptors are present. Descriptions of various sensory structures from the appendages of H o m a r u s are available (Laverack, 1962), but physiological functions have as yet been ascribed to few of them. Acknowledgements--I am deeply indebted to Professor H. G. Callan and to Dr. G. A. Horridge for their comments on the preparation of this manuscript.
REFERENCES
BALSSH. (1944) mecapoda. In BRONN'STierrichs, Bd. 5, Abt. 1, pp. 321-480. Akademisches Verlag, Leipzig. BETHE A. (1897) Das Nervensystem yon Carcinus rnaenas. Arch. Mikroskop Anat. u. Entwicklungsmechanik. 50, 460-546.
WATER CURRENT RECEPTORS IN ttOM~4RUS V U L G A R I S
325
BROCK F. (1930) Der verhalten der ersten Antennen von Brachyuren und Anomuren in bezug attf das ungebende Medium. Z. vergl. Physiol. 11, 774--790. COHEN M. J. & DIIKOZAAFS. (1961) Mechanoreception. In Physiology of Crustacea, Vol. 2, pp. 65-108. Academic Press, New York. DEBAISXEUXP. (1949) Les poils sensoriels d'arthropodes et l'histologie nerveuse. 1. Praunus flex'uosus MtiU., et Crangon crangon L. Cellule 52, 311-360. DEBAISmUXP. (1953) Histologie et histogenese chez Argulus foliaeeus L. (Crustace, Branchiure). Cellule 55, 245-290. HUGH~S G. A. & WI]~ZSMAC. A. G. (1960) Neuronal pathways and synaptic connexions in the abdominal cord of the crayfish..7. Exp. Biol. 37, 291-307. LAW~CK M. S. (1962) The cuticular sense organs of Homarus vulgaris, and their occurrence on the antennae, chelae and first walking leg. (In preparation.) LUTI~R W. (1930) Versuche tiber die chemorezeption der Brachyuren. Z. vergl. Physiol. 12, 177-205. PaossEs C. L. (1935) Action potentials in the nervous system of the crayfish. III. Central responses to proprioceptive and tactile stimuli..7. Comp. Neurol. 62, 495-505. WImaSMA C. A. G. (1959) Movement receptors in decapod Crustacea..7. Mar. Biol. Ass. U.K. 38, 143-152. WIEaSMA C. A. G., RIPLEY S. H. & CHaXSTENSENE. (1955) The central representation of sensory stimulation in the crayfish..7. Cell. Comp. Physiol. 46, 307-326.
RESPONSES OF CUTICULAR SENSE ORGANS OF THE LOBSTER, H O MA R U S VULGARIS (CRUSTACEA)--I. HAIR-PEG ORGANS AS WATER CURRENT RECEPTORS M. S. LAVERACK The Gatty Marine Laboratory, St. Andrews, Fife, Scotland
(Received 15 January 1962) A b s t r a c t - - 1 . A short description is given of hair-peg organs which are present
in large numbers on the anterior part of the body and appendages in Homarus. 2. Observations have shown that these sense organs respond to a water current by deflexion about a hinge at their base. 3. Electrophysiological studies reveal that impulses are generated by the sense organs when they are deflected by a water current. 4. Action potentials occur at a water flow of about 0-30 cm/sec and above. 5. It is suggested that this represents a "distant touch" mechanism. INTRODUCTION SENSE organs associated with the cuticle of lower crustaceans, often in the form of projecting hairs or tufts of hairs, have been described for a number of species, e.g. Argulus (Debaisieux, 1953) and Caprella (Wetzel, 1935). Few studies have been made on decapods, however, and information is only available for Praunus and Crangon (Debaisieux, 1949), Carcinus (Luther, 1930) and a report of slit sensiUa in Homarus (Wiersma, 1959). Behavioural studies have indicated that sense organs responding to water currents, pressure waves, chemicals, vibration and other stimuli are probably present on the crustacean body and appendages (Luther, 1930; Brock, 1930). Varied functions have been postulated for certain specific structures (figures by Luther, 1930; Balss, 1944), but these proposals rely upon a theoretical analysis of the possible actions of the sense organs based on anatomical data alone. Electrophysiological experiments designed to discover and distinguish the functions of such organs have been carried out in only a few cases. Hodgson (1958), (Cohen & Dijkgraaf, 1961) has shown that the median antennule of Cambarus bartonii is sensitive to chemical stimuli. Wiersma (1959) reports that the slit sensillae carried on the walking legs of the lobster Homarusare sensitive to touch, but is not sure whether this is the normal physiological response. The present work on single fibre or few-unit preparations, in which differences between sensillae have been distinguished, supports at least some of the suggestions of earlier workers that decapods are sensitive to water currents. 319
320
M.S. LAWRACK THE SENSE ORGAN
Study of the external surface and of histological sections of the chelae of Homarus (Laverack, 1962) reveals that the surface is covered with many hair-like projections. Externally the most obvious of these are the bunches and rows of hairs that are particularly prominent near the cutting edge of the chela. Less obvious, but present in great number, are small depressions each containing a
FIG. I. A hair-peg organ. These lie in depressions on the exterior surface of the cuticle. Note the solid central rod surrounded by fine hairs. The organ is seen here from the broad face.
small hair sensillum arranged like a fan in one plane. T h e sensillum consists of a plate carrying a rod which is surrounded by fifty to one hundred hairs; the hairs are arranged in a fan-shaped manner around the base of the rod (Fig. 1). The plate is hinged along the broad axis of its base, and the sensillum as a whole deflects
_• Movement of organA W a t e r ~ k _ ~ . i/2 the cup Woter'~7"~
FIa. 2. Diagram to show how the hair-peg organ is deflected in its cup by a water current passing across the surface of the cuticle. The diagram shows the innervation which consists of fibres from three to five sensory cells lying in the epidermis. when a water current acts upon the broad surface of the fan (Fig. 2). The rod from tip to base measures approximately 50~; its base is 15b~in breadth. The structures are permanent and not easily broken off, and are replaced at moulting since they have been seen fully developed on newly moulted animals. These organs, which will hereafter be called hair-peg organs , are distributed over large areas of the exoskeleton of the lobster. T h e y are most concentrated on the inner and outer faces of the chelae where .they number about 75/cm 2. The hair-pegs are also found on the walking legs (30/cm ~) and anterior parts of
WATER CURRENT RECEPTORS I N HOMARU~ VULGARLS
321
the body. They have been observed at 25/cm = on the carapace. They are infrequent in distribution on the posterior parts of the body such as the rear appendages and the telson, and are notably absent from the antennae and antennules. MATERIALS AND METHOD Experiments were carried out on isolated claws of Homarus. The upper, movable joint and the lower fixed joint 'of the chela were both found suitable for investigation; thus each animal provides four preparations. The length of each preparation was about 1 in.
gxoskeleton
Ner~
bundles
FIG. 3. Diagram showing the experimental situation. The exoskeleton is removed for about ½ in. along the claw and the internal tissues teased to expose the nerve bundles within. The chela joint was cut from the cheliped and by careful manipulation with a needle the fine nervous connexions to the sense organs of the proximal portion of the claw were broken. The needle was passed between the internal tissues and the exoskeleton for this purpose. The exoskeleton was then removed with bone forceps for a distance of about ½ in. along the claw (Fig. 3), to expose the internal tissues.
,o,ap I
it-c-7 il I_
I /
!
oo,,,o.
// Preparation Rubber diaphragm FIG. 4. T h e claw as it is placed in the expe~mental flow chamber. W a t e r flows from left to right across the surface of the claw.
After this preliminary exposure of tissue at its base the tip of the claw was pushed through a small hole in a rubber diaphragm in the experimental chamber, as shown in Fig. 4. If the hole in the diaphragm is small it is completely occluded by the chela, which thus prevents escape of water from the chamber. If water did tend to leak from the hole this was prevented by applying Vaseline to its edges. The intact distal end of the claw now protruded into the experimental flow chamber,
322
M.S. LAVERACK
whilst the exposed part was available for further dissection under a binocular microscope. The flow chamber was then filled with sea water and connected to a reservoir containing sea water. Careful teasing of the exposed tissues reveals that the nervous supply of this region consists of numerous stout bundles of fibres, the majority of which must presumably be sensory in function. Selection of an appropriate fibre bundle connected to a sense organ lying within the experimental chamber was done by trial and error as the innervation pattern is not constant. It is not possible to draw a map of the fibres and state that a particular sense-organ response can be monitored from a fibre in a given region. However, the hair-peg organs are so numerous on the surface of the chelae that chances are high that functional units can be found. Impulses were monitored with a conventional amplifier and oscilloscope display, with concurrent recording on tape for later analysis. Recordings were made through fine platinum electrodes held by a micromanipulator. Two methods of stimulation were used. First, an electrically controlled inlet valve was used to start and stop a flow of water through a chamber from a reservoir. The opening and closing of the valve was recorded on the second beam of the oscilloscope in some experiments, but it was found that an artefact, produced at the moment of opening and also at the shutting of the valve, often appeared on the first beam and this was used to indicate the stimulation period in such records. Water flowing through the valve passed through a tap which could be turned so as to vary the volume of water passing across the chamber in a given period of time. Flow rates between 0.20 and 1.02 cm/sec could be obtained, and these were satisfactory for stimulation purposes. Secondly the tap itself was attached to the spindle of a 1~ potentiometer (variable) energized by a 120 V d.c. battery. As the tap was turned, deflexion of the second beam provided a record of the varying rate of flow through the chamber. RESULTS Water current receptor organs of the lobster, when placed in the experimental bath as described above, are not normally active. No background discharge of potentials is recorded when the water covering the preparation is still. It is essential that the tip of the claw be completely immersed beneath the surface of the water, because spurious discharges are observed if the water surface laps over the exoskeleton. When water is allowed to flow over the claw surface, action potentials are observed in the nerve fibres. At low rates of flow there is no response until the speed of flow reaches about 0-25 cm/sec. The initial response then consists of one or two action potentials at intervals of many seconds until the valve is closed. With increasing rates of flow the response recorded from these fibres becomes more pronounced and the activity more prolonged, with action potentials occurring at irregular intervals. The initial response, lasting about ~ - ~ sec, is a short burst of spikes that are of high frequency. At the fastest flow rate used (1.02 cm/sec) action potentials were obtained throughout the period that the valve was open
(d]
C)
(b)
(o)
ma
W Ul
~ G ~ J t J i
F SeC
m B U !
O ~ l i
FIG. 5. E x p e r i m e n t a l results showing the response of a single organ to water fl0w. T h e water current starts at the stimulus artefact and continues until the second artefact. T h e top line (a) shows the response to a flow of 1-02 cm/sec, (b) at 0"92 cm/sec, (c) 0.55 cm/sec and (d) the threshold response at a flow of 0"25 cm/sec.
~ I
|ncreoslnQ
Flow rote increQsinq
role
Flow
rate
decreasing
Fro. 6. Response of a h a i r - p e g o r g a n to a gradually increasing rate o f w a t e r flow. T h e s e c o n d b e a m indicates an increasing rate o f flow w h e n deflected d o w n ; a d e c r e a s i n g rate w h e n m o v i n g up.
I second
Flow
WATER CURRENT RECEPTORS I N H O M ARU S VULG.4RIS
323
and the maintained frequency was between 5/sec and 30/sec depending on the preparation, When the valve was closed a small burst of potentials was noted immediately following closure, the strength of the burst being dependent on the previous flow rate (Fig. 5). The "off" response is not so pronounced as the "on" response, the number of impulses seen being small. It is uncertain whether this "off" response is correlated with the hair-peg returning to its original position. Experiments involving tactile stimulation of these organs indicate that spikes occur only when the hair-peg is bent away from the normal plane, and not when it returns to the resting position. Some adaptation may occur during the passage of a water current over the chela surface, but experiments in which stimulation was prolonged for periods of 30--40 sec show that complete adaptation does not occur and that frequency of impulses remains fairly regular during this time. All records show that a postexcitatory period of depression follows after the first burst of action potentials. Experiments where the water current velocity was changed progressively also indicate that when water flows slowly the activity of the sense organ is low, rising as the water flow increases and then falling again when the water flow decreases (Fig. 6). When the velocity of water flow is changed rapidly and continuously the organ does not fire in a manner that closely follows the curve of the velocity of water, but only in an intermittent way. DISCUSSION
Cohen & Dijkgraaf (1961) have recently remarked on the lack of knowledge of the functions of the many described types of crustacean sense organ. Information which is available stems almost entirely from behavioural studies, where the reactions of intact animals have been compared with the reactions of other specimens from which the organ under consideration has been removed. Prosser (1935) and Wiersma, Ripley & Christensen (1955) have described action potentials in the central nervous system of the crayfish Procambarus resulting from tactile stimulation by bending of hairs. Wiersma (1959) has also described spikes occurring upon touch stimulation of "slit-sensillae" of Homarus, though touch sensitivity may not be their true function. Hughes & Wiersma (1960) investigated the synaptic connexions between sensory neurones and interneurones in the abdominal nerve cord of Procambarus clarkii, by stimulation of hairs carried on the abdominal segments. They noted that localization of stimulus was made difficult by the high sensitivity of certain end organs responding to any disturbance of the water covering the preparation. Analysis of this sensory function was not carried further. The suggestion that Cardnus maenas possesses sense organs responding to small water currents seems a possible explanation of the resuks of Bethe's experiments (1895), results which were attributed by Bethe to chemoreception. Blind animals were said to be able to distinguish the direction of attractant chemical stimuli, but may in fact have responded to minute water currents arising from the food source. Brock (1930), working on the same species, showed by behaviour
324
M.S. LAVERACK
experiments that the antennules carry organs which are sensitive to water currents, and this observation was extended by Luther (1930), who showed that water current sensitivity provided the basis for rheotactic orientation. That fine, delicate, tufted sense organs are present on the cuticle of decapod Crustacea has been remarked by a number of observers. In his review Balss (1944) suggested that these organs might be structures sensitive to water currents. Luther (1930) indicated that "B/Jschelorgane", similar to those shown in Fig. 1, are present on many surfaces of Carcinus maenas including the carapace, abdomen, dactylopodite of the periopods etc., but he suggested that they are chemosensory organs. In H o m a r u s vulgaris (Laverack, 1962), the distribution of hair-peg organs agrees with the findings of Luther, but observations of living examples shows that each hair-peg organ is hinged at its base and moves in response to water movements. When the organs move, impulses can be recorded in the nervous system. I have found that chemical stimuli do not cause responses above noise level. The hair-peg organs are sensitive to water velocities of the order of 0.30 cm/sec. Faster velocities evoke greater responses, and these appear to be non-adapting since the organs continue to fire throughout prolonged periods of stimulation without any noticeable decrease in frequency. They respond to suddenly changing water velocities, and also to currents that rise gradually over a period of seconds. I suggest that the hair-peg organs represent a " t o u c h " mechanism for reception of stimuli originating some distance away and which set up water currents. Lobsters kept in aquaria and provided with rock cover are often to be found sitting in crevices or holes with the large chelae held across in front of the body and with the antennae protruding into the water in front of the hole. It can now be appreciated that this stance presented a large sensory surface to the environment, including as it does the eyes, antennae, antennules and chelae. One interesting outcome of this investigation is the contradiction of the classical view that the antennae or antennules carry all the current-detecting mechanism of the animal. The hair-peg organs discussed in this paper have not been found either on the antennae or on antennules, though they are present in great numbers elsewhere on the body surface. Antennae and antennules may carry other current receptors and electrophysiological studies are in hand to ascertain whether or not such receptors are present. Descriptions of various sensory structures from the appendages of H o m a r u s are available (Laverack, 1962), but physiological functions have as yet been ascribed to few of them. Acknowledgements--I am deeply indebted to Professor H. G. Callan and to Dr. G. A. Horridge for their comments on the preparation of this manuscript.
REFERENCES
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