exp. Biol. (1976). 6S, 381-393 381ith 6 figures

Printed in Great Britain

AN ELECTROPHYSIOLOGICAL STUDY OFMECHANISMS CONTROLLING POLYP RETRACTION

IN COLONIES OF THE SCLERACTINIAN CORALGONIOPORA LOB AT A

BY PETER A. V. ANDERSON*

Department of Biological Sciences, University of California,Santa Barbara, California 93106, U.S.A.

(Received 1 March 1976)

SUMMARY

1. Electrical or mechanical stimulation of Goniopora lobata producescoordinated retraction of polyps in the colony. With repetitive stimulation,the response spreads in linear, radial increments which become successivelysmaller with each stimulus.

2. Electrical activity recorded from these colonies is interpreted asoriginating in a conduction system responsible for effecting the colonialretraction response. The electrical activity spreads incrementally throughthe colony in a similar manner to the behavioural response.

3. Various hypotheses have been proposed to account for such a spreadof electrical activity. Of these, only interneural facilitation is of appreciableimportance to Goniopora.

4. Temporary termination of a pathway, by the passage of an impulsethrough it, was found and interpreted as being an additional and importantproperty of the colonial conduction system.

INTRODUCTION

In colonial anthozoans, a colonial response can either be through-conducted orspread incrementally (Horridge, 1956, 1957). Through-conducted waves of polypretraction are characteristic of the colonial responses of alcyonarians, and it hasrecently been shown that such behaviour is controlled by through-conduction systemsin these colonies (Shelton, 1975 c; Anderson & Case, 1975; Anderson, 1976). In coralswhere the spread of the response is incremental, the first stimulus affects only alimited number of polyps around the stimulating site but each subsequent stimulusincreases the size of the responding area. The amount by which each stimulus increasesthe distance over which polyps are affected is a criterion for dividing these corals intothree groups (Horridge, 1957): those in which the increments continually increase insize (e.g. Sarcophyton), those in which the increments get successively smaller(e.g. Goniopora, Porites) and those in which the size of the increments remains constant(e.g. Palythoa). In the cases where the increments decrease in size, a finite maximumarea of response is eventually attained.

• Present address: Department of Biology, University of Victoria, Victoria, B.C., Canada V8W 2Y2.

382 PETER A. V. ANDERSON

To explain incremental spread in a conduction system suspected of being a nervenet, with neurones operating in an all-or-nothing manner, Horridge (1957) proposedtwo models. The first, a mechanical one, consisted of a network of units connected bytransmissive and non-transmissive junctions in such a manner that prior activitywould convert a non-transmissive junction into a transmissive one. This model wasrejected because of excessive variation in the results obtained from it and because itfailed to explain all observed types of behaviour. The second, a mathematical approach,attempted to explain the increasing response as being a consequence of an increaseddensity of units initially activated by each stimulus. Although able to explain muchof the observed behaviour, this model incorporated unsupported assumptionsunacceptable to Josephson, Reiss & Worthy (1961). Using computer simulations,these investigators were able to study the effect of several variables, amongst them thefacilitatory effect of prior activity, on the spread of activity through a network ofunits. The simple interpretation of interneural facilitation used in Horridge's modelwas extended by incorporating an additional variable, decay of facilitation with time.As a consequence, these investigators were able to apply trains of 'stimuli' of differentfrequencies to the model and have different numbers of junctions remaining facilitatedby the previous 'impulse'. The results gave spreads similar to those displayed byliving corals.

The above three models are similar in that they assumed that the observed spreadof the colonial response was a consequence of incremental spread of activity through aconduction system responsible for its control. This assumption was questioned byShelton (1975 a, d) who was able to record through-conducted electrical activityfrom a scleractinian in which the colonial behavioural response spread in decreasingincrements. To explain the difference between the behaviour of the conductionsystem and the colonial response it effects, Shelton (1975*2) proposed a model that wasbased on the observation that the latency from stimulus to recording of consecutiveimpulses increased. He suggested that such changes in conduction delay would haveappreciable effects on the facilitatory state of the polyp muscles and could, ifsufficiently great, result in incremental spread of the colonial responses of some corals.

Goniopora is a scleractinian coral in which the colonial response spreads in decreas-ing increments (Horridge, 1957). As such, it was selected for study during an investi-gation of colonial conduction systems in the Anthozoa. The results obtained from thisstudy are at variance with those obtained by Shelton (1975 a, d) and show that con-duction systems which operate incrementally are present in the Anthozoa. As aconsequence, models for incremental spread, such as those of Horridge (1957) andJosephson et al. (1961), require reconsideration.

MATERIALS AND METHODS

Specimens of Goniopora lobata Milne-Edwards and Haime (Family, Poritidae)were collected by skin diving from the reefs surrounding the Banda Islands, Indonesia.For reasons given in the Results, all collections were made from one population foundin approximately 20 feet of water. They were maintained on shore in aquaria asdescribed previously (Anderson, 1976). Electrical recordings were made with suctionelectrodes (tip diameter, 200-400/tm) and the signals amplified and displayed by

Polyp retraction in G. lobata 383

conventional means (for details see Anderson & Case, 1975). Electrical stimuli wereapplied through either a suction electrode similar to those used for recording orthrough two closely apposed silver wires, insulated except for their tips. Where longterm records were required, a Lockheed Store 4 FM tape recorder was used. Allexperiments were conducted at 28 °C, the ambient water temperature.

RESULTSBehavioural observations

Many species of Goniopora are available in a variety of habitats in the Banda area.Colonies of the same species have similar maximum areas of response. The maximumarea of response is a parameter that can be measured underwater and consequently itwas possible to collect only specimens of one kind. Uniformity was further insuredby the use of one large population for all collections. These two safeguards preventedmorphologically similar species from being mistakenly studied as one, as waseventually proven by examination of the skeletons of the specimens used. The maxi-mum area of response was also used to determine the condition of specimens used inthe experiments because it was found that changes in this parameter invariablypreceded decay of the colonies.

The polyps of Goniopora are large, 3 cm long and 3 mm wide; expanded theycompletely conceal the surface of the corallum. Expanded colonies exhibited infre-quent and irregular movements, the most common being bending of the column ofsome polyps. The tentacles were somewhat more active and often twitched, eithersingly or in groups, towards or away from the oral disk. Occasionally, a group of3-4 polyps would suddenly twitch or writhe once or twice in unison.

If a tentacle were touched lightly with a probe, it and its immediate neighbourson a polyp shortened rapidly. A second effective stimulus invariably affected the wholepolyp which withdrew by means of a series of discrete twitches. A single light touchapplied to the column of a polyp had no apparent effect, but if touched again thecolumn wall would indent at the point of contact and occasionally bend towards theside being stimulated. Withdrawal followed the third or fourth stimulus. With electricalstimulation the effect was similar with at least two suprathreshold stimuli beingnecessary before polyp retraction occurred. If a polyp was stimulated, either elec-trically or mechanically, after it had begun to withdraw, a colonial response was evoked.

The spread of polyp retraction during a colonial response was always found to beincremental. Although mechanical stimuli were used for the underwater observations,electrical ones were preferred for the laboratory studies because of the more precisecontrol available with electrical stimuli. The stimuli were applied through a suctionelectrode attached to the base of a polyp, which invariably withdrew as a result ofelectrode attachment. After a delay to allow any colonial effects of electrode attach-ment to subside, electrical shocks were given at different frequencies. Each supra-threshold stimulus produced a partial retraction of polyps. The first affected the 3 or4 polyps immediately surrounding the stimulating electrode, and each subsequentstimulus increased the size of the responding area. Recruitment of a polyp into thecolonial response always occurred suddenly. Polyps not involved in the colonialresponse remained relatively motionless, displaying only the occasional spontaneous

384 PETER A. V. ANDERSON

y\

50 ms

Fig. 1. A single impulse ( • ) recorded with a suction electrode from the colonial nerve net aftera single suprathreshold electrical stimulus (5 V, 1 ms). The stimulus artifact is marked • .

movement described earlier. When the border of the area involved in the colonialresponse reached them, they suddenly twitched once. Thereafter, they responded toalmost every subsequent stimulus by partially retracting. Each stimulus increasedthe area over which the response was evoked, with successive increases diminishing insize, until a maximum area of response was attained - there was a decreasing incre-mental spread. The final size of the responding area was a function of the frequencyand number of stimuli. At frequencies greater than 2/second, 40-50 polyps within anarea approximately 3x3 cm eventually retracted. This area is the same size as thatattained by the multiple waves of polyp retraction that followed a strong mechanicalstimulus. The final shape of the area affected by electrical stimulation, and to asomewhat lesser extent the numbers of polyps involved, differed a great deal evenwith the same colony.

Close observation revealed that at least one polyp within a responding area did notnecessarily respond to every stimulus. For instance, a polyp might begin twitchingafter the fifth stimulus of a series, continue twitching after a further three, not twitchafter the next, and then resume twitching after all subsequent ones until it had totallywithdrawn.

Electrical activity

Electrical activity associated with colonial responses was recorded with suctionelectrodes attached to the colonies. To avoid movement artifacts caused by the twitchesof the large polyps, the electrodes were attached to the coenosarc, or 'ridges' betweenthe polyps. For most experiments two recording electrodes and one stimulatingelectrode were used. These were placed in a straight line with the stimulating electrodeat one end.

Recorded electrical activity consisted of multiphasic impulses that were typicallyof 20 /iY amplitude and 70 ms duration (Fig. 1). Recordings with two electrodes ofthe response to a series of suprathreshold stimuli showed that the evoked electricalactivity spread away from the stimulating site but was not through-conducted(Fig. 2). Initially, no evoked potentials could be recorded but after several stimulihad been applied, impulses would be recorded from the nearer recording site. Withfurther stimulation impulses would also be recorded from the more distant site.

Polyp retraction in G. lobata 385

I>WM.|!>W>I

20

25"\ T »!

30 35

1

40 45

1

20

500 ms

Fig. 2. Electrical activity evoked by a train of 46 electrical stimuli (see numbers). Impulseswere first recorded regularly from a recording site O-66 cm from the point of stimulation(upper traces) and later spread to a more distant recording site, 1-34 cm from the stimulatingsite (lower traces). The first stimulus artifact is marked • and the first potential recordedon the upper trace is marked T.

The relationship between the distance of an electrode from the point of stimulationand the number of stimuli necessary before activity could be recorded is given inFig. 3 for two stimulus frequencies. At a frequency of 3/s, fewer stimuli wereneeded, and more activity was recorded, than when the frequency was i/s. Atthe lower frequency, activity never spread as far as at the higher frequency. Noevoked potentials were ever recorded from points more than 1-5 cm from the stimulat-ing site. The results from these experiments suggest that the spread of electricalactivity is incremental. Occasionally, impulses would be recorded that were apparentlyout of sequence from stimuli that would not be expected to evoke potentials (Fig. 2,lower trace, stimulus number 10). These impulses appeared irregularly and in-frequently and were probably a consequence of spontaneous activity.

During a train of stimuli there was an increase in the interval between stimulation(signified by the stimulus artifact) and the recording of a potential. This is apparentto a limited extent in Fig. 2. To see if this was a result of a change in conductionvelocity or a change in the delay between stimulation and generation of the impulse

PETER A. V. ANDERSON

30

•5 20

.0

I 10

0-5 1-0Distance (cm)

1-5

Fig. 3. Relationship between the distance of an electrode from the stimulating site andthe mean number of stimuli (A, frequency 3/s; # i/s) required to spread activity to thatpoint. The interval between stimulus trains was determined by the time necessary for re-expansion of retracted polyps. Each distance was tested an average of 4-5 times. The barsillustrate the range of the values obtained.

at the stimulating site, use was made of the arrangement of three electrodes describedearlier. This made it possible to measure the delay between stimulation of a potentialand its appearance at the two recording sites and hence the conduction velocitybetween those points, as in Fig. 4. At a stimulus frequency of 3 pulses/s (Fig. 4A)the interval between artifact and impulse increased continually until the 24th stimuluswhen it diminished. At 2 pulses/s (Fig. 4B) the same trends were apparentalthough the values of the delays were less and resembled those that occurred with astimulus frequency of 1 pulse/s (Fig. 4C). At all three frequencies there is aslight increase in the conduction velocity of the first few impulses before the conduc-tion velocity decreases or, in the case of the 1 pulse/s data, levels off. This trendis most apparent in the data displayed in Fig. 4 A where the first four impulses areconducted at successively faster velocities. While these increases in conductionvelocity may not appear significant when compared with the remainder of the graphs,their regular appearance in all other instances where conduction velocities wererecorded would argue for their validity.

Since it would be expected that the retractor muscles of a polyp would be sensitiveto the interval between arriving impulses rather than the stimulation to recordinginterval, the data from Fig. 4A, B were replotted to display the interval (Fig. 5).When consecutive stimuli successfully evoked potentials there were no significantdifferences in the interpulse interval; when impulses were not recorded, the intervalchanged significantly. Interpulse intervals with a range of 330-1300 ms could occur(depending on the stimulus frequency and number of 'unsuccessful* stimuli) withoutapparently affecting the spread of subsequent impulses across the colony.

Single impulses followed light mechanical stimulation. If strong stimuli were used,bursts were recorded (Fig. 6A). There were never more than 7 impulses in any one

Polyp retraction in G. lobata 387

-112

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8.

3

a12 18 24 30 36

210

180

150

J, 120

•1 90Q

60

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-

-

-

-

1

6

,1

-

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12 18 24 30 36

Stimulus number.

- 9 - 2

- 6u

3 |o

Fig. 4. Effect of stimulus number upon the delay between the stimulus artifact and theappearance of the impulse evoked by each stimulus of a series applied at frequencies of3/s (A), 2/s (B) and i/s (C). Each graph gives the delay for points 0-7 cm ( • ) and 1-15 cm(A) from the stimulating site, and the conduction velocity for propagation between thosetwo recording sites (O).

burst, with the minimum interpulse interval being 60 ms. During a burst, the amplitudeof the impulses changed, often increasing slightly at first and later decreasing. Thismight indicate operation of a facilitation-antifacilitation mechanism. Bursts ofimpulses were never observed after electrical stimulation.

During the course of this investigation, well in excess of 100 stimulus trains wereapplied to the colonies. In approximately 6% of these, a single, 'early', impulse wasrecorded after the first stimulus (Fig. 6B). Thereafter, the result was as usual: nofurther impulses were recorded until a number of stimuli had been applied. Thisnumber corresponded with that usually found for the stimulus frequency and distancesinvolved (Fig. 3). The 'early' impulse did not appear to be propagated very farthrough the colony since it could only be recorded from the electrode nearer thestimulating site. The interval between the stimulus artifact and the 'early' impulsewas frequently longer than that for the impulses evoked by later stimuli. This

PETER A. V. ANDERSON

•--»

1000

3

c 500

12 18 24 30Stimulus number

36 42

Fig. 5. Interpulse interval (msec) for the 3/s (A) and 2/s (O) data from the 0-7 cmelectrode of Fig. 4. Appreciable changes in interpulse interval only occurred when stimulifailed to evoke recordable impulses.

increased interval is not apparent in Fig. 6B. 'Early' impulses never followed thesecond or third stimulus of a series, yet appeared after the first stimulus. Conse-quently, they appear to be a feature of the conduction system rather than artifacts.

Because the spread of activity was incremental and somewhat variable, the re-fractory period of the conduction system could not be measured electrophysiologically.Instead, behavioural observations were used, with twitches of the polyps serving asthe indicator of activity. The interstimulus interval was reduced until a value wasreached at which the second stimulus of a pair had no effect. This interval, 75-80 ms,can be interpreted as the refractory period of the conduction system if it is assumedthat the refractory period of the conduction system is shorter than that of the muscles.Such a relationship appears to be a feature of many coelenterate neuroeffectorprocesses (Bullock, 1943). This value for the refractory period compares well withthe minimum interpulse interval (60 ms) of the burst of impulses evoked by a singlestrong mechanical stimulus (Fig. 6A). Attempts to find the refractory period of themuscles failed because it proved difficult to categorise which polyps responded towhich stimulus with the small interstimulus intervals involved.

A facilitatory period for the coral was found by increasing the interval between twostimuli until the second stimulus produced no further spread of the response effectedby the first shock. This interval was found to be of the order of 6-7 s and was inter-preted as the facilitatory period of the conduction system.

The colonial conduction system was sensitive to excess magnesium. All colonialbehavioural responses were completely abolished after 10 min exposure to a 50%solution of isosmotic MgCl2. 6H2O in sea water. This effect was reversed when thecolony was returned to normal sea water.

Polyp retraction in G. lobata 389

V(A) in fr (pJ^

, l250 ms

(B) A

500 ms

Fig. 6. (A) A burst of impulses evoked by a single, strong, mechanical stimulus (V). (B) Record-ing of an ' early' impulse (A). These were occasionally found to be evoked by the first stimulus(0) of a stimulus train. Note that an additional 7 stimuli had to be applied before anyadditional impulses were recorded. Both traces are part of a single continuous recording.

DISCUSSION

The behaviour of Goniopora lobata is similar to that described by Horridge (1957)for a Red Sea species, G. planulata. Colonial activity spread away from the point ofstimulation in increments that became successively smaller with each stimulus until,eventually, a maximum area of response was attained. The electrical activity whichcontrols the colonial response in G. lobata also spread in increments and only overdistances equivalent to those over which polyp retraction occurred.

The nature of the recorded impulses is uncertain. They may be true records ofactivity originating in elements of the colonial conduction system, or potentials fromoverlying epithelial or muscular tissue. Either type of impulse would, however,accurately reflect the spread of activity in the colonial conduction system. Themorphological basis of this colonial conduction system is not clear although theall-or-nothing nature of the impulses suggests that it is an ensemble of all-or-nothingelements which may be neural, judging by the effectiveness of excess Mg2+ in suppres-sing activity. The all-or-nothing nature of the impulses may also argue against thepossibility that the recorded impulses are epithelial or muscle action potentials sincesuch potentials show variations in amplitude and duration resulting from neuro-effector facilitation (Robson & Josephson, 1969; Anderson & Case, 1975). Shelton(1975 a, d) has termed the colonial conduction systems of other corals nerve nets, onaccount of similarities between them and the conduction system responsible formuscle activation and polyp withdrawal in sea anemones. However, a distinctionshould be made between the known nerve net in solitary anthozoans and thosepostulated for colonial anthozoans. Individual polyps can behave independently ofthe remainder of the colony (Horridge, 1957; Anderson & Case, 1975; Anderson,1976) by means of a conduction system restricted to individual polyps (Anderson &Case, 1975; Anderson, 1976). This conduction system may be similar to the nerve net

39° PETER A. V. ANDERSON

in solitary anthozoans. However, colonial responses are effected by activity in asecond, purely colonial, conduction system which activates the conduction systems inall the polyps. The colonial conduction system does not appear to activate the retractormuscles of the polyps directly (Anderson & Case, 1975) so should not be associatedwith the nerve net in sea anemones. Assuming both are nervous, a better classificationfor the two conduction systems would be: the polyp nerve net and the colonial nervenet. This distinction will be used in future discussions.

Since the activity spreads in increments, the question of how electrical activity canspread incrementally through a conduction system composed of all-or-nothing unitsmust, once again, be considered. Of the earlier models proposed as explanations, two(Horridge, 1957, mechanical model and Josephson et al. 1961) are based on the conceptof interneural facilitation* The pertinent details of each have been described earlier.While Horridge's first model has been rejected, the results obtained by Josephsonet al. indicate that interneural facilitation may be an important factor in conductingsystems which operate in an incremental manner.

The exact contribution of interneural facilitation to the operation of the Gonioporacolonial nerve net could not, however, be ascertained in this study. Any effectiveinvestigation into the role of interneural facilitation in the transmission of activitybetween two units of a conduction system must be so designed that the interactionsbetween a few, and perhaps ultimately only two, nerves be studied. Suction electrodesof the type used in this study do not make this possible since they undoubtedly includemany active elements within their receptive fields. Consequently, no more can besaid about the role of interneural facilitation in Goniopora other than, being the onlyknown mechanism which could produce the observed spread of impulses, it wouldappear to be necessarily present; but it is still a theory awaiting physiological con-firmation. None the less, until shown otherwise or replaced by other theories, inter-neural facilitation requires inclusion in models for incremental spread.

In addition to interneural facilitation, other variables appear to influence themanner in which impulses spread. The appearance on many records (e.g. Fig. 6B)of an impulse after the first stimulus of a series presents two interesting problems.First, how can a conduction system in which activity normally spreads incrementallybecome through-conducting and, secondly, once that conduction system has becomethrough-conducting, why do all subsequent stimuli not evoke recordable impulses ?One possible mechanism by which an impulse could appear after a single stimulus,is suggested by the observation that the colony is spontaneously active. In severalrecordings (e.g. Fig. 2) spontaneous impulses were observed. While such spontaneousimpulses may be a result of mechanical stress induced by the electrodes, the observa-tion that 3-4 neighbouring polyps would occasionally writhe and twitch indicatesthat spontaneous impulses are also probably a feature of undisturbed colonies.

Any spontaneous impulses would have a facilitatory effect on junctions they reach,with the number of facilitated junctions increasing with the frequency of spontaneousactivity. Depending on the origin of the spontaneous activity, and therefore, thelocation of the facilitated junctions, electrical stimulation of the nerve net wouldproduce responses which deviate from concentric circles to ones distorted towards thelocus of the spontaneous activity. This was commonly found in Goniopora. Anadditional result of spontaneous activity could be the formation of a pathway of

Polyp retraction in G. lobata 391

facilitated junctions between the recording site and the stimulating electrode. This isparticularly likely, if, as a result of mechanical stress, the electrodes themselvesgenerate much of the spontaneous activity. Long pathways are formed only by largenumbers of impulses (Fig. 2) so the pathways produced by the few spontaneousimpulses generated in Goniopora would be relatively short. Furthermore, the routeformed would probably not be the most direct one possible between the stimulatingand recording sites with the result that the conduction velocity would be relativelyslow. These features of a pathway formed by spontaneous activity are consistentwith the properties of the ' early' impulses which were only recorded from sites nearto the stimulating electrode, and after delays longer than those for subsequentimpulses.

To explain the absence of impulses following stimuli subsequent to that whichevoked the 'early' potential, factors in addition to spontaneous activity must beconsidered. Since the 'early' impulse has no apparent effect on propagation ofsubsequent electrical activity through the colony, it would appear that the pathwaythrough which that first potential travelled is unavailable to subsequent potentials,i.e. some factor or factors have terminated the pathway. It is unlikely that any ter-minating factor could distinguish between an impulse evoked by the first stimulus of aseries and those evoked by subsequent stimuli so the terminating factor wouldprobably operate after each impulse. However, if activity is to be propagated acrossthe colony, the duration of the terminating influence would have to be shorter than thefacilitatory period of junction between the nerves, 6-7 s, or else facilitation could notoccur. Two factors which could play a part in terminating a conduction pathway arerefractoriness of the conducting units and fatigue of the junctions between those units.The refractory period for the conduction system was estimated to be 75-80 ms. Thisfigure corresponds with both the minimum interval between the pulses in the burststriggered by mechanical stimuli and figures found for other coelenterates. However,it appears that in coelenterates refractory period measurements have been made onlyon whole networks of conducting units. So far as can be ascertained, there are nopublished figures for the refractory period of the individual units of conduction incoelenterates, be they nerves, epithelial cells or muscles. The refractory period of theseunits may be far greater than that of a whole net and of sufficient duration to effectivelyterminate an otherwise available pathway. It is, however, doubtful whether thisrefractory period could attain values of 500 and 1000 ms so as to effectively exclude apathway to impulses evoked at frequencies of 1 and 2/s respectively.

The relatively long intervals over which pathways are unavailable for propagationsuggest that fatigue of the junctions between conducting units may be the morelikely explanation of the pathway termination. Further evidence for fatigue of thejunctions is that in many of the records (e.g. Figs. 2, 4), impulse frequency diminishesas the number of applied stimuli increases. This can be explained by an increase inthe number of junctions used in propagation, and hence fatigued, with the result thatfewer pathways would be available and less activity transmitted across the colony. Inother anthozoan conduction systems, the nerve net in the coral Isophyllia and the SSIin the anemone Calliactis, a breakdown in conduction with repetitive stimulation hasbeen attributed to fatigue (Shelton, 1975 b, d).

The phenomena of fatigue and interneural facilitation can effectively explain the

392 PETER A. V. ANDERSON

changes in conduction velocity described here (Fig. 4). At the beginning of a train ofimpulses, the conduction velocity increased slightly. This is not entirely apparentfrom these results but was found to be a consistent feature of this organism. It hasalso been observed in a far more pronounced manner in some pennatulids (Anderson,unpublished). In any diffuse conducting system, there are a great many pathwaysavailable to an evoked impulse and the pathway chosen will determine to a very greatextent the conduction velocity of an impulse. At the beginning of a train of impulses,the first potential might be expected to travel by the fastest route but if the conductionsystem requires interneural facilitation, the first pathway chosen, rather than beingthe fastest, would probably be the most accessible or one requiring least facilitation.Passage of the first impulse would, however, facilitate other, more direct pathwaysfor subsequent impulses and the conduction velocity would increase. If the passageof an impulse through a pathway terminates that pathway, the routes used at thebeginning of a burst would not be available for subsequent impulses so other slowerpathways would have to be used. In this manner both the increases and subsequentdecreases in conduction velocity can be explained.

If the system suggested here does operate, each stimulus would have to activatedifferent groups of nerves. Depending on the rate at which the different groups ofnerves are activated (stimulus frequency), the rate at which the facilitatory effect ofprior activity decays, and the rate at which the pathways become available aftertermination by fatigue and refractoriness, different patterns of spread of activitythrough the colony, and hence different colonial responses, would be produced. Thissystem is similar to that of Josephson et al. (1961) except for the additional variable,temporary termination of pathways by prior activity.

Electrical activity has been recorded from the colonial nerve nets of other corals(Shelton, 1975 a, d). In these cases, however, the conduction system is through-conducting over large areas of the colony, e.g. Porites. In Porites the colonial responsespreads in decreasing increments (Horridge, 1957; Shelton, 1975 d) but, since itpossesses a through-conducting system, models describing incremental spread ofelectrical activity through systems composed of all-or-nothing units are unnecessary.Instead Shelton (1975 d) suggests that the observed behaviour is a result of changesin the conduction delay of consecutive impulses. These delays, which increasedwith stimulus number and were greatest in the area immediately surrounding thestimulating electrode, would lead to an increased separation of impulses arriving atpolyps with a resulting absence of muscle activation when the interpulse intervalexceeded the facilitatory period of the muscles. The results of similar experimentsdescribed here indicate that while the propagation of a series of impulses across acolony results in an increased delay from stimulus artifact to impulse recording(Fig. 4), that increased delay does not produce any significant increase in the inter-pulse interval of consecutive impulses (Fig. 5). It remains to be seen whether theapparent non-linear nature of the imposed conduction delays (Shelton, igy$d) issufficient in itself to control the behaviour of corals such as Porites.

One of the features of the computer simulation of Josephson et al. (1961) was thatsmall changes in the value of parameters such as the ratio of transmissive to non-transmissive junctions, the facilitatory decay rate and the average length of conductingunits could produce large changes in the distance over which each 'stimulus' is

Polyp retraction in G. lobata 393

effective. The changes in the maximum areas of response of the different speciesobserved during the course of this study may be a consequence of changes in thevalues of similar parameters in the different Goniopora species.

This study of the ALPHA HELIX South East Asian Bioluminescence Expedition wassupported by the National Science Foundation under grants OFS 74 01830 and OFS74 02888 to the Scripps Institute of Oceanography and NSF grant BMS 74 23242to the University of California, Santa Barbara. Part of the travel cost of the authorwas met by an award from the Alumni Association of the University of California.Additional support was afforded by Office of Naval Research Contract N00014-75-C-0242 and NSF grant BMS 72-01971 to Dr James F. Case.

I would like to thank Dr James F. Case for allowing me to participate on the expedi-tion and for his valuable comments on the manuscript. My sincere thanks also toDrs G. Adrian Horridge and Robert K. Josephson for their many useful suggestionsand discussions. Finally I would like to thank Dr John Wells who identified the corals.

This paper is part of a thesis to be submitted by the author to the Department ofBiological Sciences, University of California, Santa Barbara in partial fulfilment ofthe requirements for the Ph.D.

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ANDERSON, P. A. V. & CASE, J. F. (1975). Electrical activity associated with luminescence and othercolonial behavior in the pennatulid Renilla kollikeri. Biol. Bull. mar. biol. Lab. Woods Hole 149, 80—95.

ANDERSON, P. A. V. (1976). Electrophysiology of the Organ-Pipe coral, Ttibipora musica. Biol. Bull. mar.biol. Lab. Woods Hole (In Press).

BULLOCK, T. H. (1943). Neuromuscular facilitation in scyphomedusae. J. Cell. Comp. Physiol. 22,251-72.

HORRIDGE, G. A. (1956). A through-conducting system co-ordinating the protective retraction ofAlyconium (Coelenterata). Nature, Land. 178, 1476-7.

HORRIDGE, G. A. (1957). The co-ordination of the protective retraction of coral polyps. Phil. Trans.R. Soc. Lond. B 240, 495-528.

JOSEPHSON, R. K., REISS, R. F. & WORTHY, R. M. (1961). A simulation study of a diffuse conductingsystem based on coelenterate nerve nets. J. Theoret. Biol. 1, 460-87.

ROBSON, E. A. & JOSEPHSON, R. K. (1969). Neuromuscular properties of mesenteries from the sea-anemone Metridium.J. exp. Biol. 50, 151-68.

SHELTON, G. A. B. (1975a). Electrical activity and colonial behaviour in Anthozoan hard corals.Nature, Lond. 253, 558-60.

SHELTON, G. A. B. (19756). The transmission of impulses in the ectodermal slow system of the seaanemone Calliactis parasitica (Couch). J. exp. Biol. 62, 421—32.

SHELTON, G. A. B. (1975c). Colonial conduction systems in the Anthozoa: Octocorallia. J. exp. Biol. 62,571-8.

SHELTON, G. A. B. (1975 d). Colonial behaviour and electrical activity in the Hexacorallia. Proc. R. Soc.Lond. B 190, 239-56.

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