Tide-model analysis of the zonation of intertidal prosobranches. II. Four species of trochids (Gastropoda: Prosobranchia)

d. exp. mar. BioL EcoL, 1972, Vol. 9, pp. 257-277; ~) North-Holland Publishing Company

TIDE-MODEL ANALYSIS OF THE ZONATION OF INTERTIDAL PROSOBRANCHS. H. FOUR SPECIES OF TROCHIDS (GASTROPODA: PROSOBRANCHIA). A . J. UNDERWOOD t

Department of Zoology, UniverMty of Bristol, Bristol, England Abstract: Experiments were carried out in a tide model to determine the patterns of zonation of four species of trochids under laboratory conditions. Calliostoma zizyphinum (L.), Gibbula cinerar a (L.) and G. umbilicalis (da Costa) did not show a constant pattern of zonation. Monodonta lineata (da Costa) adopted the same zonation in the model as that previously described for Littoriua littorea (L.), i.e. at and just below high tide level, but this was higher than normally found on the shore. Time-lapse monitoring of the movements of the four species showed that, except for Monodonta lineata, they were influenced by the rise and fall of the water level in the tank and tended to move up and down with it. Under conditions of reduced tidal period Calliostoma zizyphinum, Gibbula cineraria, and G. umbilicalis showed, however, a pattern of zonation more like that on the shore. Movement mainly occurred during periods of submersion and the number of animals moving at any one time was very low. Monodonta lineata, ano to a lesser extent, Gibbula umbilicalis could compensate for the increased rate of movement of water level during the 3-h tidal period by increased rates of movement and greater levels of activity. Thus, not only does the moving water level bring about the initiation of movement of the animals, but it also governs their rate of movement. None of the four species showed any differences in their patterns of movement or distribution whether in complete darkness, or continuous light. When under continuously damp conditions Monodonta lineata adopted a lower position in the model, possibly because of the movemer t of a layer of water over the substratum. Negative geotaxis was less strong in Calliostoma zizyphinum and Gibbula cineraria in the absence of a moving water level. The results indicate that, with th.e possible exception of Calliostoma zizyphinum, the physical stresses due to emersion were unlikel3~ to be the major control of zonation. It is considered possible that differential zonation shown on the sea shore by British littorinids and trochids might be governed by the different requirement~ of the species for food.

INTRODUCTION

As described in a previous paper (Underwood, 1972b), the use of a laboratory tidemodel has made possible a re-appraisal of the r61e of physical factors in the control of intertidal zonation. The validity of such laboratory regimes has been examined in the four British species of Littorina (L.) and in the present paper has been extended to an examination of the common British trochids, Monodo, 'ta lineata (da Costa), Gibbula umbilicalis (da Costa), G. cineraria (L.) and Calliostoma zizyphinum

{L.). t Present address: Departme.nt of Zoology, School of Biological Sciences, University of Sydney, N.S.W., Australia. 257

258

A.J. UNDERWOOD MATERIAL AND METHODS

The construction and mode of operation of the tide model used in this investigation have previously been described (Underwood, 1972a) as well as the method of analysis of the time-lapse films of movement of Littorina (Underwood, 1972b). Animals were collected from the shore et Heybrook Bay, Plymouth and maintained in an aquarium at Bristol: p.one was kept for more than one month before being used and Gibbula cineraria was used within one week of collection since they showed some mortality after two weeks in the laboratory. RESULTS PRELIMINARY EXPERIMENTS

Initially, experiments were conducted without time-lapse monitoring of the movement of the animals to determine the basic responses to the laboratory tidal regime. All four species could be observed on the vertical front and sides of the tank throughout experiments and it was considered unlikely, therefore, that the slope of the shore could have much influence on the distribution of animals in the experimental tank. Monodonota lineata showed a marked similarity to the zonation described for Littorina littorea (Underwood, 1972b): it congregated at and below high tide level (in Bands 8-11, with a few individuals above high water level in Band 12). Monodonta lineata also showed the crevice effect found in Littorina littorea, where the animals tended to remain at the lateral margins of the tank. As with L. littorea, this was investigated by the insertion of a wall down the centre of the experiment~! shore, in Band E (Underwood, 1972b). This caused aggregations of Monodonta lineata in bands A, D, F and J, with a few individuals in Bands B and I. The crevice effect is again due to the physical presence of a vertical surface on the sloping shore rather than a biotic attraction to other animals. Calliostoma zizyphinum, Gibbula cineraria and G. umbtTicalis did not adopt a permanent pattern of zonation in the tank, but tended to follow movements of the water level. Further analysis of these patterns of movement will be described later (p. 261) G. cineraria, in contrast, tended to be abundant in the lower regions of the tank, especially under the reduced (3 h) tidal period. TIME-LAPSE MONITORED EXPERIMENTS

Normal (12.5 h) tidal period Calliostoma zizyphinum showed no tendency to adopt any zone in the model, nor to remain subtidal in Band 1. Throughout the tidal period there was a fairly high Activity Index (A.I.) (Underwood, 1972b), ranging up to nearly 40. Usually, the animals tended to move with the water level, i.e. upwards during the rising phase of

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TIDE-MODEL ANALYSIS OF ZONATION IN TROCHIDS

261

the tide and downwards during the ebb. There was a fairly high rate of movement per animal (between 2.0 and 3.0 units/h) of which a considerable proportion was lateral. Although the tendency to follow the water level was quite marked, there was some downward movement during the rising tide and upward movement during the ebb (Fig. 1). Animals often crawled above high water level and on several occasions remained emersed for a period of hours. When animals were stranded by the falling tide, they remained motionless until the next tide reached them. There was thus very little movement whilst emersed, except some downward movement at the end of each tidal cycle due to animals passively sliding down the shore or falling off the substratum and rolling to the bottom of the tank. Whilst submersed, animals tended to move for periods of up to one hour and then remain motionless for varying periods before continuing. Occasional individuals remained motionless throughout whole tidal cycles, but during subsequent cycles these moved while others remained motionless, at the bottom of the tank. For the first two cycles, there was an increase in lateral movement per animal during the falling tide. In many cases the animals would move very quickly for short periods, as if unwilling to be left emersed by the falling water level. They were never seen to move actively downshore, but upon reaching the sides of the shore, turned round and retraced their horizantal movement so that the resultant movement was downshore in a series of zig-zags. After two tidal cycles this was less common. In general, the pattern of movement of any individual was random. Many moved onto the vertical sides of the experimental tank. There was an increase in the number present on the sloping shore at the end of each tidal cycle when some fell or slid to the bottom of the tank and re-attached to the sloping surface. There were major differences from the foregoing in the pattern of movement shown by Gibbula cineraria. None moved above high tide level and none fell off the substratum du~-';',~ low tide. Animals left uncovered remained completely motionless until the next tide reached them, resulting in several individuals remaining at quite high levels in the tank (Bands 9 and 10) throughout periods of emersion. There was, therefor'e, less upward movement in subsequent cycles than during the first two when animals were becoming established. During the ebb tide, however, there was considerably greater active downward movement involving animals moving directly downshore with the water level, rather than from side to side as in Caliiostoma zizyphinum, resulting in greater numbers of Gibbula cineraria being found in the subtidal region (Band 1) than in the slightly higher levels (Bands 2-4) as in Calliostoma zizyphinum. Thus, the peaks of numbers present in Band 1 at low tide were greater than for C. zizyphinum (Fig. 2). Emersed animals did not move and the slight movement during periods of emersion was due to a few individuals slipping downwards a few cm and occasionally (passively) crossing one of the grid-lines~ Gibbula umbilicalis also tended to follow the water level throughout the tidal cycle, but in general showed less movement. They did not move whilst emerged and showed no passive downward movement. Those which climbed above mid-tidal level

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Fig. 3. Analysis of movement of Gibbula umbilicalis in the tide model with a 12.5-h tidal period and continuous light.

TIDE-MODEL ANALYSIS OF ZONATION IN TROCHIDS

263

were not the same ones in each tidal cycle. Vertical movement on the sloping shore during periods of submersion was considerably more direct (i.e. up and down shore) than in the previously described species. As with G. cineraria, the animals on the vertical surfaces of the tank moved downwards during the falling tide and thus increased the low tide numbers in Band 1: again none was observed above the level of high tide (Fig. 3). There was a marked contrast between the behaviour of Monodonta lineata and the other three troehids. M. lineata adopted a pattern of distribution and movement in the tank much more like that described for Littorina iittorea (Underwood, 1972b). They moved upwards for several cm at the start of an experiment, sometimes ahead of the water leve! befole coming to rest. There was thus some upward movement in air during the first tidal cycle (Fig. 4). The animals continued upwards until they reached the highest levels of the tide, a few going into Band 12 and then remained motionless. Most moved upwards at the edge of the tank, i.e. they crawled along the rising water level until they reached the side of the shore, when they moved vertically upwards. Others, however, at first moved directly upwards and then laterally at high tide of the first cycle, and eventually arrived at the edges of the shore. The vertical spread down the side of the shore (i.e. throughout their zone, Bands 8-11) may have been due to a greater response due to the 'crevice effect', than to the negative geotaxis. Because the Monodonta lineata were fairly large, they would have to be distributed up and down the edge of the shore to keep in contact with a vertical surface. During the ebb of the tide most of the animals remained motionless and did not follow the water down. Very occasionally a solitary individual on a vertical surface would move downwards with the water level, appearing on the slope just before low tide: none on the sloping shore actively moved downwards during the ebb of the tide, although occasional individuals slipped downwards passively during periods of emersion, but never more than one grid-line was crossed by any an'~mal. This did result in an individual being present infrequently in the region between the zone and low tide (in Band 7). During subsequent periods of submersion there was little movement, a few animals moved up or dow,a one vertical unit and one or two crossed the tank from side to side. Movement began as soon as the water reached the animals. Any lateral movement ceased as soon as the animals reached the lateral margins of the shore, there being very few occasions when animals moved onto or off the shore; the number present throughout the tidal cycle remained, therefore, more constant. No pattern of direction of movement could be discerned for any individual; any which slipped downwards were seen to move up again during the uext rising tide. Movement of M. lineata was usually in bursts of 20--30 min (4-6 ~'ames of film) between periods of inactivity of approximately the same length.

Reduced (3 h) tidal period The rate of inllow of sea water into the experimental tank was increased to the appropriate rate for a 3-h tide (Underwood, 1972a) and the aml~litude mainta.ined

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TIDE-MODEL ANALYSIS OF ZONATION IN TROCHIDS

265

at 50 cm. Under these conditions Calliostoma zizyphinum showed an increased A.I. because fewer ani.~als were stimulated to move. There was an increase in the upward rate of movement during the first cycle at the start of an experiment (from a mean hourly rate of 1.04 units/animal/h during a 12.5-h period to 1.58 units~animal~ h) but this increase was insufficient to allow them to keep up with the more rapidly rising water level so that there were far fewer animals in the upper half of the tank and never any above high tide level (Fig. 5). Subsequent movement was random and there were no major changes of position. There were occasional periods when the amount of movement was negligible as the falling water level moved over the animals during the ebb tide; presumably the rate of water movement was too great to allow them to undergo the zig-zc.g movements described earlier. No animals ever dropped off the sabstratum during periods of emersion and all passive downward movement was abolished. Similar trends were shown by Gibbula cineraria to those described for Calliostoma zizyphinum when under the 3-h period. A.I. and total movement/animal were reduced. The tendency to follow the water level was maintained, but less obviously as a result of the increased rate of movement of the water and reduced movement of the animals, so that the number in any region of the tank tended to remain more constant throughout the tidal cycle than during the 12.5-h period. There was little or no movement whilst emersed. In contrast, Gibbula umbilicalis showed an increased A.I. under the new experimental conditions (to 19 at high tide compared with 7 before). The total movement/ animal was also increased and these two factors made the overall distribution of animals in the different bands more like that of a normal tidal period than shown by Calliostoma zizyphinum or Gibbula cineraria. The cycle of following the water level up and down was maintained, but by fewer individuals and there were, therefore, no high tide peaks of numbers in the region above mid-tidal level. There was also less tendency for animals to move onto the sloping shore at the start of each experiment and this caused less fluctuation in the numbers recorded in Band 1. Upward movement at the start of each experiment was greater than that shown in the 12.5-h period, and the increase was greater than that shown by Calliostoma zizyphinum. This increase, from 0.62-0.94 units/animal was, however, insuf~cient to enable the animals to keep up with the rising water level. Monodonta lineata showed a pattern of distribution in the tank under the 3-h tidal period which was virtually identical to that described for the normal period. During the first rising tide the animals moved upwards much more quickly than in the 12.5-h period (4.81 units/animal/h compared with 1.08 units in the normal period) and this increase was more than sufficient to compensate for the fourfold increase in rate of movement of the water level. The animals were able to reach their zone (Bands 8-11) within 2 tidal cycles as before. During subsequent periods of emersion, there was a small amount of random movement as in the normal tidal period, but the slight passive downward movement during emersion was abolished.

TIDAL CYCLE 3

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Fig. 5. Analysis of movement of Calliostoma zizyphinum in the tide model with a 3-h tidal period and continuous light. Movement parameters multiplied by 4 to give units/h. Figures above histograms give the values whore greater than the scale.

TIDE-MODEL ANALYSIS OF ZONATION IN TROCHIDS

267

Increased (20 h) tidal period During successive increased tidal periods of 20 h, Calliostoma zizyphinum showed very marked cyclical up and down movements with the water level. Many individual~, however, remained in the subtidal region, and the A.I. was ~ow (about 3 at high tide): none ever went above the level of high water and few (about 5 out of 30) were usually to be found above mid-tidal level during high water. The animals were virtually always submersed, except a t the end of the first cycle when a few could be found emersed; these always fell off the substratum and rolled to the bottom of the tank after 4-9 h emersion. In Gibbul~ cineraria the A.I., lateral and vertical movements]animal were all reduced. The only movement observed in air was of a few that became detached from the substratum and rolled to the bottom of the tank after 4-6 h emersion. The tendency to move up and down with the water level throughout the tidal cycle was maintained. The reduced A.I. and activity/animal, however, resulted in a lower overall dispersi,.)n in the tank. G. umbilicalis showed some of the trends described for the former two species. There was no movement in air, except for a few which became deta,~hed from the substratum after 7-11 h emersion: some remained above mid-tidal level throughout the entire cycle. The te,~dency to follow the water level up and down was maintained, but only 3 or 4 animals moved above mid-tidal level during each cycle compared with 8 or 9 during the 12.5-h period. During tidal cycles of increased period, Menodonta lineata exhibited a very different distribution in the tide model. Animals began to climb up the shore during the first rising tide at a slower speed than during a 12.5-h tide, but did not reach so high, leaving many animals in the region between the zone and low tide. Some of these climbed up and down during each tidal cycle. Many remained emersed for long periods during the tidal cycle, although none went above high-tide level. None of those emersed became detached from the substratum during emersion, although severa' of them slid passively downshore after several hours of emersion, but only 1 or 2 ur.its before the next rising tide reached them. The total movement]h]animal during the prolonged tidal cycle wss very similar to that during a normal cycle but, because the animals were lower in the shore, movement occurred during a greater proportion of the tidal cycle. No tidal period As described for Littorina littorea (Underwood, 1972b), experiments were carried out to see if there were rhythms of activity in the absence of the tidal cyle. After allowing the animals to establish their pattern of zonation in two 12.5-h tid~ cycles, the motor was stopped with the water at high tide level and the rate of inflow maintained to prevent stagnant water f~'om being present. Calliostoma zizyphinum and Gibbula cineraria showed very little and only a random movement, with a very low A.1. (about half the value for a normal ti0al period),

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Fig. o. Analysis of movement of Gibbula umbilicalis in the tide model with no tidal puriod and the water maintained at high-tide level.

TIDE-MODEL ANALYSIS OF ZONATION IN TROCHIDS

269

so that the overall pattern of distribution was maintained: no cyclic or directional rhythms of activity could be observeJ. G. umbilicalis, in contrast, exhibited a far greater A.I. (16) and total movement/ animal than as show rt, during the 12.5-h tidal period (A.I. was 16 compared to 7 during the normal tide). The number of animals on the sloping shore increased as those on the vertical surfaces gradually moved in from the sides of the tank. The immigrants were either already above mid-tidal level, or gradually moved there, so that the number in the regions below mid-tidal level remained constant, giving a gradual increase in the numbers above mid-tide level (Fig. 6); otherwise, movement was random. Monodonta lineata maintained the high-tide distribution throughout the period of observation with no tidal cycle. The A.I. was very low compared with that under the 12.5-h tidal period (2 compared with 10). Total movement/animal was low; individuals did move up and down, but never more than 1 unit, thus maintaining a position in the normal zone (Bands 8-11). There were constantly 1 or 2 animals above the water level, but these did not move except to return below the surface of the water after 3-6 h emersion. This represer.ted the only movement in air.

Darkness Experiments were conducted with 3-h and 12.5-h tidal periods with the tank in complete darkness, except for the electronic flash at 5-min intervals. The flash was never seen to disrupt the movement of any animal previously moving, nor to stimulate movement. Comparison of the analyses of these experiments with their counterparts under continuous light showed that, as with Littorina iittorea (Underwood, 1972b), the absence of light made no discernible difference to the distribution or pattern of movement of any of the top-shells tested.

Lack of desiccation in the tide model o~ series of experiments was carried out to determine the responses of animals in the tide model (12.5-h tidal period) when the substratum remained permanently wet throughout the tidal cycle. The apparatus used to cause a stream of sea water down the sloping shore has been described in an earlier paper (Underwood, 1972b). The cyclic movement to follow the water level was maintained in Calliostoma zizyphinum despite the changed conditions. The A.I. was reduced to less than half the normal value (13 compared with 28, at high tide, under the 12.5-h period). The total activity/animal was the same. There were fewer animals moving upshore during each tidal cycle and the rate of upward movement during the first cycle was somewhat less than in the previously described experiments at this tidal period. The up and down movements were much more direct than p.eviously described, and animals which were left emersed by the falling tide no longer fell off after a period of exposure, but continued to wander randomly. Some were able to remain above high-tide level for considerable periods, others remained subtidal for whole tidal cycles.

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272

A.J. UNDERWOOD

In Gibbula cineraria the absence of desiccation during emersion caused a complete disappearance of the tendency to follow the moving water level. The animals moved upwards with the water level at the start of the first tidal cycle and in some cases continued upwards until they were above high-tide level (Fig. 7). They did not, however, follow the water level down again during the ebb and many remained at the higher le:'eis and continued to move about, whilst emersed. The total movement/animal and ~mounts of vertical movement were in general h/gher than during a normal tidal cycle, but the vertical movement was equal up and down throughout the tidal cycle. The absence of desiccation made little difference to the distribution and pattern of movement of G. umbilicalis. There were, however, fewer animals moving downwards with the falling tide and some remained for very long periods above the level of high water. Superimposed on the normal pattern of movement for a 12.5-h period was random wandering of emersed animals. Monodonta lineata showed a peculiar difference in pattern of zonation compared with the normal. The A.I. was enhanced (15 at high tide compared with 10) and the total movement/animal was also raised slightly. During the first tidal cycle at the start of an experiment, M. lineata did not ascend the shore as quickly as under the normal 12.5-h tidal conditions, so that by high tide many had not reached the zone, but were in ttle region between the zone and low-tide level (in Bands 2-7). Some never left the subtidal regions (Band 1), but others reached positions above high tide level (Fig. 8). As a result of this, some animals were submersed throughout all of the tidal cycle and consequently there was continuous movement. There was quite considerable random lateral and vertical movement when emersed, and the amount of vertical movement whilst submersed was greater than during a normal tidal cycle. This movement was equally upwards and downwards throughout the tidal c~cle and was not related to the direction of movement of the water level. DISCUSSION

There have ~,~cn only two previous experimental investigations into the patterns of distribution and behaviour of intertidal trochids using laboratory tide models (Thompson, 1968; Micallef, 1969). In both of these the responses of the animals to different regimes of tidal rise and fall were not investigated, and the pattern of behaviour in relation to the tidal cycle was not described. Thompson (1968) reported that the two species of Gibbula were able to adopt eqmvalent zones to those on the shore at Porlock, Somerset, but Monodonta lineata was unable ~Loshow significant zonation in a tide model. There are several differences in ThoT~pson's account from the results obtained here. In the Thompson (1968) tide model the positions of animals in the experimenta~ tank could only be recorded at low tide. i.e. when the shore was out of the water. This caused considerable bias in the recording of the positions of the species of Gibbtda. which the present investigation has shown '~to have a marked

TIDE-MODEL ANALYSIS OF ZONATION IN TROCHIDS

273

tendency to follow the moving water level. Thus, zonation at low tide in the Thompson model was not representative of the real situation. The non-significance of position displayed by Monodonta lineata as described by Thompson (1968) can be explained in two ways. Very small samples were used (only 8 or 9 animals) and the zonation was described in terms of the percentage of the shore at Porlock normally occupied by each species, Significant variation from a random distribution would be very difficult to detect by a statistical test such as the Poisson distribution used by Thompson (1968). Thompson also mentioned other experiments in which M. lineata was found to give a highly significant zonation when tested in the absence of other species. It was suggested, therefore, that the absence of zonation in his first experiments was due to some form of interspecific interference. The difference, in fact, represents the increase in significance demonstrable when using samples of 40 rather than 8 or 9 individuals in each experiment (Underwood, unpublished observations). Micallef (1969) used a tide model with an experimental tank of such small size that the maximal tidal amplitude obtained was only 22.5 cm. The tank was divided into 2.5 cm horizontal zones and experiments were conducted using 4 or 5 individuals of each of the four species of trochid under a much reduced (3 h) tidal period. He claimed that all four species adopted a pattern of zonation similar to that found on the shore. There were, however, several unsatisfactory aspects of his method of experimentation. Gibbula cineraria and Calliostoma zizyphinum were said to be unable to withstand emersion for more than a few minutes (Micallef, 1969), but the filmed pattern of movements of these species in the present series of experiments showed that they could withstand far longer periods of emersion. The difference may be partly due to the fact that in Micallef's tank only vertical surfaces were available. The effects of a 3-h tidal period (as used by Micallef, 1969) on the distribution of Gibbula cineraria, G. umbilicalis and Calliostoma zizyphinum in the Bristol tide model have been described in the present work. All three species showed a distribution in the tank different flora that shown under a normal tidal period. Only Monodonta lineata showed the same distribution during 3-h and 12.5-h periods. Micallef (1969), without any observations on the distribution of animals in a tide model under a normal tidal period, attempted to correlate their patterns of distribution under natural and laboratory conditions: he also carried out many of his experiments with the air and sea water temperatures the same, either at 13 °C (which represented spring) or 15-20 °C (which represented summer). These temperatures are far too high for comparison with natural conditions at Plymouth, where the mean sea water temperature does not rise above approximately 16 °C (Cooper, 1958). The present experiments in the tide model have the same short-comings as those on Littorina littorea (Underwood, 1972b), but serve, to show the main features of distribution of the different species of trochid. Field observations (Underwood, 1971) have slaown that the pattern of distribution on the shore is not absolutely constant in relation to the tidal cycle. Only the rela.tive zonation of different species in relation to each other appears to be immutable: Monodonta lineata was found in the model

274

A. J U N D E R W O O D

at the same level as Littorina littorea (Underwood, 1972b) and these two species were found to share the same zone on the shore at Heybrook Bay (Underwood, 197!). Gibbula umbilicalis and G. cineraria, however, were much lower on the shore than the two former species and also took up lower positions in the model. TABLE 1 Comparative data from tide-model experiments. For 3 and 12.5 h tidal periods, the A.I. and total ~novement/animal are the means of four tidal cycles (after the first two) recorded at high tide and ~,¢rtical movement/animal is the mean upward movement/h from low to high tide of the first tidal cycle at the start o f an experiment. For "0-h tidal periods, the A.I. and total movement/animal are the means of three tidal cycles (after the ,rst one) recorded at high tide. A.I. and total movement/ animal in the absence of a tidal cycle are the means of recordings at the 6th, 18th, 30th and 42nd hours o f observation.

3h

12.5 h

Tidal period 12.5 h

20 h

None

(no desiccation)

Cailiostoma zizyphinam A.I. Total movement/animal Vertical movement/animal

5 0.81 1.58

28 2.50 1.04

13 2.50 0.62

4 1.00 0.25

15 3.00 --

Gibbula cineraria A.I. Total movement/animal Vertical movement/animal

2 0.37 !.21

16 2.50 !.46

19 4. ! 2 1.25

4 0.67 O. 17

7 1. ! 2 --

Gibbula unJbilicalis A.I. Total movement/animal Vertical movement/animal

19 2.44 0.96

7 1.00 0.62

9 1.12 0.58

11 1.50 0.32

- !6 2.87 --

Monodonta lineata A.I. Total movement]animal Vertical movement/animal

9 1.44 4.81

10 1.69 1.08

15 2.06 0.54

14 !.34 0.45

2 0.31 --

The major differences in the patterns of movement of the four species of trochid in the time-lapse monitored experiments are summarized in Table I. All four species showed strong negative geotaxis, but Calliostoma zizyphinum, Gibbula cineraria, and to a lesser extent G. umbilicalis, all also showed a tendency tc, follow the movements of the water level. When the water level was stationary at high tide level, there was a marked decrease in both the amount of movement and the A.I. in all the species except G. t~mbi!icalis; such movement as occurred was random, except in G. umbilic~lis, wl~ch showed a slight tendency to move upwards. In general, the number of animals moving (as reflected by the value of the A.I.) was low under all the

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275

experimental conditions. Predictably, Calliostoma zizyphinum and Gibbula cineraria showed less movement under conditions of increased tidal period, when there was a 11, t~utg~ --I. decreased rate of change of water |evei" animals following L"I L-G watei-'lt~Vg;, .... ' :- .i,-alJLa.. would perforce climb up and down more slowly unless they were capable of movi,g ahead of the rising water. G. umbilicalis increased its rate of movement and its A.I. during a reduced tidal period, but was not able to compensate completely for the ~hange6 rate of water level movement. Calliostoma zizyphinum, Gibbula cineraria and G. u,nbilicalis were capable of movement in air when the substratum was continually moist and the active avoidance of desiccation obviously played a r61e in the control of their patterns of behaviour. It must be emphasized, however, that the detachment from the substratum shown during emersion by Callh~stoma zizyphimlm and Gibbula cineraria during a 12.5-h tidal cycle only occurred in animals in the upper levels of the tank where the length of the period of emersion in each tide was very much greater than that which would be experienced in the normal positions occupied on the shore. Monodonta lineata was able to compensate for the increased rate of rise of water level during the 3-h tidal period, the moving water level not only acting as a stimulus for the initiation of movement of the animals, but also for its rate. When under conditions of constant flowing sea water over the substratum, M. lineata tended to adopt a lower position in the tank than normal. This seemed to be due to decreased rates of ascent of the tank during the first tidal cycle at the start of the experiment. It was considered possible that upward movement while the water on the substratum flowed downwards might have been influenced by some form of rheo~axis, but rheotaxis could not be demonstrated. It seems possible that the downward movement of the water on the substratum during a rising tide may prevent the animals from distinguishing the position of the moving water level. During prolonged tidal periods, M. lineata did not reach such high levels in the tank as during a 12.5-h period. This may have been partly due to a disinclination to move for more than about 10-h in the first tidal cycle and a tendency to remain in any position after once being exposed to the air at that level. Each subs¢quent emersion resulted in a net movement which retained the original zonation of the animals at the start of the tidal period. The tendency of M. lineata to adopt positions at the lateral borders of the shore was not shown by the other trochids. As described for Littorina (Underwood, 1972b), there were no differences in ~iotrl':~ " bution oc movement of the trochids when in complete darkness compared with those shown in light. The major conclusion from these results must be that all the species of trochid were abi~ to withstand far greater periods of emersion in the tide model than would normally be encountered in their normal pattern of distribution on the shore, a similar conclusion to that reached after analysis of the distribution and movement of L. litwrea in the same tide model (Underwood, 1972b). Exactly the same patterns of distribution were shown in the model at all times of the year and, therefore, at all

276

A.J. UNDERWOOD

air and water temperatures in the range tested. Thus the tidal rise and fall is not necessarily the major controlling factor in zonation in the model; if it were, it should have resulted in much closer agreement between the pattern of zonation in the model and that found on the seashore. Even allowing for errors in the pattern of zonation on the tide model as a result of the reduced tidal ,m:~,!itude ~:nd the absence of waves, the supposed close control of distribution by the tidal cycle should have been detectable. The supposition that the rise and fall of the tide is the only factor governing all intertidal zonation is further discredited by the fact that several species of intertidal molluscs are known to undertake extensive migrations on the shore at certain times of the year, but without any correlated alterations in the tidal cycle. Such migrations have been observed in several British species of prosobranch, e.g. Littorina neritoides (Fretter & Graham, 1962), Monodonta lineata (Williams, 1965; Underwood, 1971), Gibbula cineraria (Underwood, 1971) and any explanation of the factors governing intertidal zonation must take these into account. In the present series of experiments, the two majo:" environmental features which were lacking in the tide model were the physical factors caused by waves and the biological influence of the preseace of food and competition for it. It appears unlikely that wave action is the primary controlling factor in intertidal zonation because zonation is found on virtually all British shores regardless of the degree of exposure or shelter: wave action acts as a modifier to basic zonation patterns (Ballantine, 1961; Lewis, 1964). It has been recognized in Littorina littoralis that zonation is dependent on the distributiop of fucoid algae, in the absence of which this species appears to be incapable of establishing any pattern of zonation in a tide model (Evans, 1965; Thompson, 196,$; Underwood, 1972b) or on the shore (EbbingeWubben, quoted by Barkman, 1955). There is little information in the literature on the feed,ing habits of the differer~t species of intertidal littorinids and trochids beyond general observations that they f~ed on algal detrius and diatoms (Fretter & Graham, 1962) and it seems possible that the type, quantity and quality of algal food could be very different from one part of the shore to 8aother, and differences in the pattern of zonation from shore to shore may well be the result of difli~rences in the physical characteristics of diflbrent shores which would affect the distribution of diatoms and algae. ACKNOWLEDGEMENTS

I grateNllly acknowledge the technical advice and assistance of Mr P. Bull, Mr K. Wood and Mr A. P. W. Makepeace in the time-lapse photography. Thanks are due also to my wife and to Mrs J. Milton for their assistance with the tide model experiments and to my supervisor Dr T. E. Thompson for his considerable help and encouragement and for critically reading the manuscript of this paper. This study was carried out while I w,~ in receipt of a Science Research Council Studentship.

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REFERENCES

BALLANTINE,W. J., 1961. A biologically-defined exposure scale for the comparative description of rocky shores. Fid Stud., Vol. l, pp. 1-19. BARKMAN,J. J., 1955. Or the distribution and ecology ofLittorina obtusata (L.) and its subspecific units. Archs nderl. ZooL, Vol. 11, pp. 22-86. COOPER, L. H. N., 1958. Mean sea temperatures in Plymouth Sound. J. mar. biol. Ass. U.K., Vol. 37, pp. 1-~. EVANS, F., 1965. The effect of light on zonation of the four periwinkles Littorina iittorea (L.), L. obtusata (L.), L.saxatilis (Olivi) and Melaraphe neritoides (L.)in an experimental tidal tank. Neth. J! Sea Res., Vol. 2, pp. 556-565. FRETTi~R, V. & A. GRAHAM, 1962. British prosobranch molluscs. Ray Society, London, 755 pp. LEw,s, J. R., 1964. The ecology of rocky shores. English Universities Press, London, 323 pp. MICALLEF, H., 1969. The zonation of certain trochids under an artificial tidal regime. Neth. Yl Sea Res., Vol. 4, pp. 380-393. THOMPSON, T. E., 1968. Experiments with molluscs on the shore and in a laboratory tide model. Sch. Sci. Ret,., Voi. 149, pp. 97-102. UNDERWOOD, A. J., 1971, Behavioural ecology and reproduction of intertidal prosobranch gastropods. Ph.D. Thesis, University of Bristol, 214 pp. UNDERWOOD,A. J., 1972a. Sinusoidal tide models: design, construction and laboratory performance. J. exp. mar. BioL Ecol., Vol. 8, pp. 101-11 I. UNDERWOOD, A. J., 1972b. Tide model analysis of the zonation of intertidal prosobranchs. I. Four species of Littorina (L.) J. exp. mar. BioL Ecol., Voi. 9, pp. 239-255. WILUAMS, E. E., 1965. The growth and distribution of Monodonta lineata (da Costa) on a rocky shore in Wales. Fld Stud., Vol. 2, pp. 189-198.