The Response of A Hydroid to Weak Water-Borne Disturbances

The ability to detect moving objects in an aqueous medium by the mechanical disturbance they produce is known for a number of animal groups ; leeches (Whitman, 1898; Herter, 1929), amphibians (Whitman, 1898; Kramer, 1933), fish (see recent review by Lowenstein, 1957), and even amoebae (Schaeffer, 1916). Most coelenterates, however, appear able to respond to the presence of a predator or to prey only when such objects actually touch some part of their surface. This is probably true even for those forms such as Gonionemus and Corymorpha which behave as though they were actively seeking food (Yerkes, 1902; Torrey, 1904). Although hydroid medusae are able to locate accurately a tactually stimulated portion of their subumbrella surface with their manubrium (Romanes, 1885; Horridge, 1955), there is no evidence that they are able to react to objects at some distance. Hardy (1958), however, described capture of Balanus nauplii by ‘accurate deft twists of the manubrium’ in a scyphozoan ephyra and suggests that vibration perception by statocysts may be involved. Hydroid polyps have been shown to be able to bend toward sources of chemicals diffusing in the water (Loomis, 1955), but this response probably occurs normally only following capture of a suitable prey. The great sensitivity of Calliactis to movement above the oral disk (Passano & Pantin, 1955) suggests that this species might react to the proximity of moving animals.

It was observed that polyps of the hydroid Syncoryne mirabilis would bend toward a vibrating glass rod placed in their vicinity in a dish of sea water (Fig. 1). This was most easily shown by mounting a fine-tipped rod in a manipulator and, after moving the tip near a polyp, lightly tapping the manipulator. The polyp would immediately bend toward the rod unless it were placed directly above the mouth of a polyp, in which case the polyp would respond by contracting.

The present paper describes some of the characteristics of stimuli effective in evoking this response, gives evidence that such polyp bending plays an important role in the life of the animal, and attempts to explain the mechanisms of detection of stimuli and determination of the direction of bending.

Colonies of Syncoryne were maintained in running sea water at approximately 16°C. Syncoryne polyps are about 1-5 mm. in length. Individual polyps were removed from a colony and pinned by the stalk to a piece of cork mounted on the bottom of a dish of sea water. All such dishes were kept in running sea water until used in an experiment and were returned to this sea water whenever their temperature rose much above 16⁰ C. In experiments involving ablation of tentacles, one-fourth of the sea water in the dish was replaced by isotonic magnesium chloride and the polyps were left in this solution until they no longer responded to touch. After removal of the desired parts, the dishes were restored to running sea water until the animals recovered their sensitivity.

Controlled stimuli were given to the polyps by means of a prodder attached to a speaker cone driven electrically by square pulses from a Grass S4 stimulator. The prodder consisted of a glass rod with a 1 cm. piece of cover-slip cemented to its end, perpendicular to the direction of prodder movement. The speaker and prodder were mounted in a manipulator. In an experiment the prodder was positioned with the cover-slip parallel to the long axis of a hydroid polyp. It was hoped that by using a vibrating area many times larger than the polyp, differences between experiments due to slightly different lateral placement of the prodder would be minimized.

The prodder movement was calibrated by putting the flat surface under a compound microscope and measuring its movement with an ocular micrometer when the speaker was energized by various d.c. voltages. The displacement of the prodder was a linear function of the applied voltage in the range of strengths used in the experiments. As the usual input to the speaker was not a constant current, but a brief pulse (most often 5 msec, in duration), and since the prodder was placed in sea water which would impede its movement, it is felt that the displacement in air as measured by the microscope represented the maximum possible excursion of the prodder.

In all experiments the polyp response measured was a bending of the hydranth. In some cases one tentacle, or a few, alone twitched toward the source of stimulus without movement of the whole polyp. This response was most often seen when using a prodder with a fine tip; when using a prodder with a large surface, the bending response of the whole polyp almost always had a lower threshold than the individual tentacle twitches, and the latter could, for the most part, be ignored. Occasionally one or more polyps in a dish would show continued spontaneous tentacle twitching. Examination of such polyps always revealed the presence of a hypotrichous ciliate crawling about their surface. This indicates that small local disturbances are sufficient to cause polyp reactions.

Responses were best seen in hydroids which had been held in the laboratory for several days. Possibly due to the disturbances involved, freshly collected polyps were relatively unreactive. Once in the laboratory, polyps would show responsiveness for several weeks, even though they were not intentionally fed and the average polyp size decreased greatly.

By using stimuli caused by a stepwise increase or decrease in the current energizing the speaker, it was shown that the polyp response did not depend upon the direction of polyp displacement; a sudden advance of the prodder or a sudden retreat were equally able to evoke bending of the polyp towards the prodder. A square-wave input to the prodder system was somewhat more effective than a step increase or decrease (about 20 % less voltage required) if the duration of the pulse was 5 msec, or more. At durations less than 5 msec., the threshold voltage to square pulses increased with decreasing duration. This was probably due to mechanical damping of the stimulating system.

The most obvious demonstration of the independence of the bending response on the direction of polyp displacement was given by an experiment in which the prodder was placed between two polyps growing from a common branch. Here the directionality of the stimuli delivered to each polyp was exactly reversed; whenever the prodder moved toward one polyp it moved away from the other. Even in this case, however, both polyps bent toward the prodder when the stimulus exceeded threshold.

In a number of trials, each involving many measurements on a single polyp, the strength of stimulus required to cause polyp bending was found to be an exponential function of the distance of the prodder from the polyp (Fig. 2). This indicates a drop in the stimulus strength with increasing distance from the prodder. The threshold intensity at different distances may be in part affected by greater damping of the prodder on larger excursions, and the intensity-distance curve may also be influenced by ‘focusing’ of the disturbance by the large flat prodder surface. Noteworthy was the sensitivity of the polyps. At a distance of 0·5 mm. from the centre of a polyp, responses were obtained with a prodder displacement of from 2·5 to 3 μ.

Because Syncoryne will respond to a single excursion of the prodder, bending toward a prodder vibrating at any frequency does not mean that the polyp is sensitive to this frequency. The polyp may only be responding to the first pulse in the series.

To test the effect of frequency on the response, a polyp was stimulated by a prodder vibrating at a given frequency, while the amplitude of the pulsations was increased until the polyp responded. The rate of amplitude increase was 20 % per pulse at frequencies less than one per second, and 20 % per second at frequencies greater than this. This method gave the surprising result that animals would not respond at all to frequencies greater than five per second. The average maximum frequency which would cause polyp bending was three per second (range 1-5 per second, fourteen trials on six different polyps). The threshold intensity for bending remained rather constant at frequencies from one per 10 sec. to the maximum frequency to which the polyp would respond.

These results show that pulses which cause no overt response can still modify the animal’s future behaviour, somehow inhibiting the bending response to normally supra-threshold stimuli arriving in the immediate future.

Because of the small distances involved, it is difficult to decide if Syncoryne responds to pressure waves, or to currents set up by the prodder movement. To distinguish between these possibilities, the reactions of Syncoryne to stimuli consisting mainly of water currents were observed.

A glass pipette was mounted in a manipulator, and a rubber bulb attached to the pipette by a flexible tube. The end of the pipette was then brought near to a polyp, and, by squeezing the bulb, the polyp could be subjected to water currents.

A polyp could be bent by the water jet until it was perpendicular to its stalk without responding. If the manipulator holding the pipette was tapped while the polyp was so displaced, it would often respond by bending toward the pipette.

By repeatedly squeezing and releasing the rubber bulb, a polyp could be made to oscillate about its stalk at frequencies up to three per second without responding by bending. If, however, the rubber bulb was compressed sharply, causing a sudden jet of water to strike the polyp (and probably also causing the system including the pipette to vibrate), the polyp usually bent toward the pipette.

These results indicate that Syncoryne polyps are quite inert to all but possibly suddenly changing water currents. Whether the polyps are sensitive to sudden changes in water currents streaming past them, or only to water-borne vibrations cannot yet be stated.

For an animal to detect a mechanical disturbance, one portion of its structure must be moved by the stimulus with respect to some other portion. Syncoryne, unlike free-living animals, has a fixed position in space because of the attachment of its stolons to the substrate. It was thought possible that vibration perception in this hydroid involved displacement of the flexible hydranth about the more rigid, fixed, stalk. The following experiment was performed to test this hypothesis.

A viscous solution of methyl cellulose dissolved in sea water was placed in a dish. A layer of sea water was carefully poured over this solution and the two liquids slightly mixed, creating a liquid column of increasing viscosity and density. When a detached hydroid polyp was placed in this solution, it soon nearly stopped sinking. The polyp’s vibration threshold could then be measured while it was thus suspended in a liquid and lacking a fixed point in space. Following such measurements, the cut end of the polyp stalk was grasped in a pair of forceps mounted in a manipulator, the polyp held at the same depth in the column, and the threshold again measured In the latter measurements, the polyps again had a fixed reference point. Table 1 gives the results of this experiment. Accuracy is defined as the number of times the polyp bent toward the plane of the prodder out of the total number of responses. If the polyp bent parallel to the prodder, away from the prodder, or contracted, the response was counted as negative.

The results indicate that possession of a fixed reference point does not play a decisive role in Syncoryne vibration perception.

In order to determine the role, if any, of the capitate tentacles of Syncoryne in perception of a near-by disturbance, vibration thresholds of a number of polyps lacking tentacles were determined. Two polyps were pinned to a mounted piece of cork in each of several dishes. Both were anaesthetized with magnesium chloride and the tentacles of one were removed with a pair of fine scissors. After the polyps had recovered, an equal number of threshold determinations was made on each member of the pair, the intact polyp serving as a control. The results of this experiment are summarized in Table 2.

The average threshold of polyps without tentacles was statistically significantly higher than those with tentacles (P < 0·001).

In a second series of trials, all the tentacles were removed from one side of a number of polyps. A comparison of the thresholds when the prodder was on the side with tentacles and when it was on the side without tentacles was made. The results of this experiment are presented in Table 3.

The average threshold when the prodder was on the side with tentacles was significantly lower than when the prodder was on the side without tentacles (P < 0·05). Most striking, however, was the difference in accuracy, 100 % in the first case, 17·4% in the second. This compares with a normal accuracy in intact animals of about 80%. The lower average threshold between the groups in the last study and the controls in the previous series might be due to different states of nutrition, different degrees of laboratory acclimatization, or possibly, a general heightened excitability due to the operation itself.

Further evidence of an increased tendency to bend toward the tentacle side was seen when a dish containing four such half denuded polyps was jarred. All four polyps immediately bent toward the side with tentacles.

In a further attempt to identify structures responsible for vibration perception, selected points on the polyp surface were subjected to discrete prods. The stimulating apparatus used was the same as described above, except that the prodder ending in a large flat surface was replaced by one which ended in a narrow blunt tip. This prodder was moved toward the desired portion of the hydroid until it touched and caused a small displacement of the hydranth. The threshold voltages of pulses activating the prodder system were then determined.

Three measurements were made at different times for each of the selected points on the polyp surface and tentacles, and these were averaged to get the threshold for this area. All measurements were made on a single polyp. The results of this experiment are presented in Table 4.

The average threshold of the tentacles was significantly lower than that of the points on the hydranth tested (P < 0·05).

The direction of polyp bending was found to depend not on the direction of tentacle displacement, but only on the particular tentacle stimulated. The polyp bent toward the stimulated tentacle whether it was displaced toward the polyp body or in any direction perpendicular to the tentacle axis.

That such polyp responses are not only interesting laboratory phenomena, but may also play an important role in the life of the animal, was shown by experiments in which a small living copepod was held by the abdomen in a pair of forceps attached to a manipulator and brought near but not touching a Syncoryne polyp. As long as the copepod remained still, the Syncoryne was also motionless ; as soon as the copepod began to struggle it was quickly seized and eaten by the polyp. A Syncoryne polyp can, then, detect and suitably respond to the presence of a small moving crustacean in its immediate environment. Even after having eaten a copepod (and being distended from the presence of such a relatively large object in its gastric cavity), a polyp would continue to respond to a vibrating rod.

With the information at hand, it is possible to set up a hypothetical model which would explain the bending behaviour in Syncoryne. This model can serve as a first approximation, and will certainly be subject to later revision.

It has been shown that the intensity of the disturbance caused by the prodder falls off with increasing distance (Fig. 2). If the prodder is set at a given distance and the intensity of the stimulus gradually increased, when the disturbance is just above threshold on the side of the polyp closest to the prodder it may still be below threshold on the far side. It is postulated that the longitudinal muscles of the polyp are functionally divided into a number of parallel fields, each responding to disturbance only of its own periphery. In such a case, when the disturbance is above threshold on only one side of the hydroid, the polyp will bend toward that side (Fig. 3). If the polyp response is not all-or-none, but graded with the stimulus intensity (evidence of this is given below), the polyp will bend towards the prodder as long as the stimulus strength and degree of muscular contraction are greater on the prodder side than on the far side of the polyp, even if the stimulus intensity is above threshold on both sides.

The stiff polyp tentacles have been shown to be either directly sensitive to displacement or able to transmit a disturbance to sensory elements elsewhere on the polyp body. Since they project out from the polyp in all directions, one or more of them will be closer to the source of disturbance and hence subject to greater displacement than any other portion of the polyp. This, coupled with the greater sensitivity of tentacles than other areas on the polyp surface to displacement, makes it seem probable that it is movement of the tentacles which normally initiates the bending response. The lateral projection of the tentacles would also tend to increase the range of stimulus intensity over which only one side of the polyp is activated (see Fig. 3).

For such a mechanism to be a reasonably accurate control of the direction of bending, the stimulus intensity difference across the polyp must be significant when compared to the natural variation in sensitivity of either side of the polyp. The stimulus intensity at that part of the polyp closest to the prodder can be expected to be about 33 % higher than at the polyp midline (from Fig. 3). In the experiment shown in Fig. 2, 73 % of the threshold measurements fell between 16 % below and 16% above the least squares regression line, showing that, indeed, the intensity difference across a polyp is significant when compared to the variability in sensitivity.

This model would explain the increased threshold when all the tentacles are removed from a polyp or when the prodder is on the tentacle side of a polyp from which half the tentacles have been removed. It also accounts for the decreased accuracy in polyps without tentacles (the width is decreased, hence there is smaller intensity difference on the two sides of the polyp and greater probability of exciting the far side or both sides simultaneously with near-threshold stimuli). A lower threshold for tentacle displacement than for displacement of other polyp parts would explain the tendency of half tentacled-polyps to bend towards the tentacle side and the great difference in the accuracy of such polyps with different prodder positions.

Further evidence that it is stimulus intensity difference on the two sides of the polyp which governs the direction of bending is given by experiments in which the stimulus intensity was increased above threshold with the prodder at a set distance from the polyp mid-line. Although there was too much variation in polyp response to give quantitative results, in general the degree of polyp bending increased with increasing stimulus intensity until about twice threshold strength. Above this, the angle to which the polyps bent decreased with increasing stimulus intensity. This decreased bending was associated with polyp shortening. At very high intensities the only response which could be produced was polyp contraction.

The interpretation given these results is that the degree of muscular contraction is a function of the stimulus strength. Increasing the stimulus strength leads to a greater contraction of the muscles on the side of the polyp towards the prodder. With further intensity increase, however, the displacement threshold for receptors activating the muscles on the far side of the polyp is surpassed. The degree of bending to still stronger stimuli will depend on the difference in the degree of contraction of the two sides of the polyp, until, with maximum stimuli and maximum muscle contraction, the only response is a shortening of the hydroid. When both sides of the polyp are stimulated equally, as when the prodder is directly above the polyp, the response seen is equal contraction of all longitudinal muscles and polyp shortening.

The bending response of Syncoryne suggests an advantage gained from possession of short, stiff, tentacles and, hence, their raison d’être from an evolutionary point of view. The long slender tentacles of most hydroids. would tend to drag behind a bending hydranth and be of little value in prey capture of this sort. The tentacles of Syncoryne, on the other hand, can be moved through the water rapidly and make effective weapons.

I wish to thank Dr T. H. Bullock and Dr G. A. Horridge for reading the manuscript and Dr G. Hoyle for helpful advice offered during the course of this investigation. The work was performed during the tenure of a National Science Foundation predoctoral Fellowship. Additional aid was given by a grant (B 21) to Dr T. H. Bullock from the National Institute of Neurological Diseases and Blindness.