studies on zonation of intertidal prosobranch molluscs in the plymouth region

Studies on Zonation of Intertidal Prosobranch Molluscs in the Plymouth RegionAuthor(s): A. J. UnderwoodSource: Journal of Animal Ecology, Vol. 42, No. 2 (Jun., 1973), pp. 353-372Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/3290 .

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353

STUDIES ON ZONATION OF INTERTIDAL PROSOBRANCH MOLLUSCS IN THE PLYMOUTH

REGION*

BY A. J. UNDERWOODt

Department of Zoology, University of Bristol

INTRODUCTION

There have been numerous investigations into the patterns of zonation of intertidal organisms on temperate coasts, and these have been extensively reviewed (Stephenson & Stephenson 1949; Doty 1957; Southward 1958; Lewis 1964; Newell 1970). Earlier surveys which were related to tidal levels on the shore (e.g. Smith & Newell 1955; Wil- liams 1964a, b, 1965) can be compared only with some difficulty. In addition, many earlier surveys were over relatively short periods, population densities were not recorded, and only the extreme vertical limits of the species were accurately determined. A re- investigation of the intertidal zonation of common prosobranchs and intertidal algae in the Plymouth region was therefore carried out to form a basis for studies on larval settlement, histological investigations of annual reproductive cycles and experimental analyses of the behaviour of the adult animals in a laboratory tide model, which have been described elsewhere (Underwood 1971, 1972a, b, c).

It was considered essential that the survey described in this paper should be related to Ordnance Datum (OD) Newlyn, so that the data would be readily available for comparison with subsequent observations on other shores. The present surveys were compared with previously described British transects in an attempt to estimate how far the patterns of zonation discovered could be directly related to tidal rise and fall.

It has been considered in many general treatises on intertidal ecology that the zonation of littoral animals and plants is primarily caused by the tidal cycle (e.g. Southward 1958, p. 161; Lewis 1964, p. 8). Stephenson & Stephenson (1949) have seriously questioned such an idea, pointing out that vertical zonation may be oserved in land-locked lakes remote from typical marine tidal fluctuations and, in fact, wherever there is an interface between a body of water and air. It was hoped that the present observations in the neighbourhood of Plymouth would discover whether the patterns of zonation would show seasonal variations, which might be unrelated to tidal changes.

A weakness of previous detailed investigations of intertidal population structures and growth-rates over long periods has been that large samples have been removed from the shore and counted and measured in the laboratory. Subsequent samples, from the same position on the shore, would therefore not necessarily contain the same proportions of size-classes and would not relate to undisturbed populations.

In the present survey, the numbers of each of three species of trochid, Monodonta lineata (da Costa), Gibbula umbilicalis (da Costa) and G. cineraria (L.), and of two species

* Dedicated to Mr R. Bassindale on his retirement from the Department of Zoology, University of Bristol.

f Present address: Department of Zoology, School of Biological Sciences, University of Sydney, N.S.W. 2006, Australia.



354 Zonation of intertidal prosobranch molluscs

of littorinid, Littorina littorea (L.) and L. littoralis (L.), were recorded in different size classes and at different levels without removing them from the shore. In addition, the presence or absence of L. neritoides (L.), L. saxatilis (Olivi) and Calliostoma zizyphinum (L.), and the seasonal variations in the common intertidal plants were recorded. No attempt was made to distinguish between the sub-species of Littorina saxatilis (James 1968) or between L. littoralis and L. mariae (Sacchi & Rastelli 1966).

METHODS

It was desirable to choose a shore with a reasonably even gradient, so that sampling stations at different levels on the shore would be approximately equidistant both horizontally and vertically. A suitable shore was found at Heybrook Bay, Plymouth which had the further advantage of being near to the Wembury reefs on which investigations were carried out by Colman (1933) and Evans (1947), indicating that the littorinids and trochids studied here have long been present in stable numbers in the area. The shore faced south-west and was sheltered, chiefly by the seaward extension of the Mewstone to the south-east. The lower part of the shore consisted of bedrock, giving way to boulders just below mid-tide. At higher levels these gave way to fine stones and gravel from which the bedrock emerged again at the top of the shore, where it formed the base of a cliff. A transect was chosen to be representative of the area, running down the natural line of the shore rather than at right angles to the sea. This avoided abrupt irregularities due to fissures in the rock substratum, including only such fissures as stretched across the whole of that region of the shore.

Sampling stations were marked with dope paint, which could easily be renewed when required, and their heights measured using a 'Watts Quickset' level. These heights were referred to a pair of metal pegs fastened into solid rock well above the level of Extreme High Water of Spring tides (E.H.W.S.). One of these marked the position of 0 ft (horizontal) in Figs. 1-6, and was at Ordnance Survey reference SX 4987 4836. The heights of these pegs were then related to OD Newlyn at a bench-mark near the top of the cliff.

The sampling stations were at 12 ft (approximately 4 m) horizontally measured from the top of the lower shore bedrock (I 18 ft in Figs. 1-6), except at 322 ft, where there was a 6-ft (2-m) interval to encompass a large block of concrete which served as a readily recognizable reference point. Each station was surveyed at monthly intervals during each period of low spring tides, from September 1969 to July 1971 (except for November 1969 and August 1970). The littorinids and trochids in a 1-m square quadrat at each station were counted and a visual estimate was made of the percentage algal cover of the area enclosed by the quadrat. All the littorinids and trochids were removed and the alga carefully sorted through by hand to ensure that as many as possible of the smaller members of the populations were found. After counting they were immediately returned to the quadrat.

To test the efficiency of this procedure, a bundle of mixed algae, mainly fucoids, was taken to the laboratory at Bristol and washed overnight in tapwater. This removed all tiny gastropods from the plants, which were then soaked in sea water. Fifty very small (less than 3 mm diameter) specimens of Littorina littoralis (the commonest of the species studied) were scattered in the weed which was immersed in sea water. After 24 h, the weed was searched several times by hand in the same manner as was done on the shore. The first search yielded thirty-seven specimens and subsequent searches yielded three and two specimens respectively. This made total yields of 7400 80% and 84% of the total number



A. J. UNDERWOOD 355

of animals present. The inaccuracies of sampling for the other species, which were mostly larger and less camouflaged, would probably have been no greater.

The specimens of the five commonest species fell naturally into three size-classes, which are given in Table 1. The numbers in each size-class were recorded to give some indication of recruitment and growth.

RESULTS

Algal cover

Laminaria digitata (Huds.) Lamour. was the dominant alga on the lower shore, reaching up to a height of 7 0 ft (2 13 m) below OD, i.e. about 1 ft (0 3 m) above Mean Low Water of Spring tides (M.L.W.S.). It extended from 322 ft to the lowest level reached on the shore, a horizontal distance of 54 ft (1 6'8 m). The percentage cover in stations where Lam- inaria was present was nearly always 100% at low tide, when the plants lie flat on the substratum. The area covered by their holdfasts, however, was small, approximately

Table 1. Size-classes (mm) used for various species (height is from the base of the shell to the top of the spire; breadth is across the widest part of the

body-whorl) Species Large Medium Small

Monodonta lineata Height > 11 11-6 6< Breadth >18 18-8 8<

Gibbula umbilicalis Height > 7 7-4 4< Breadth > 13 13-8 8<

G. cineraria Height > 7 7-4 4< Breadth >11 11-8 8<

Littorina littorea Height > 18 18-9 9< Breadth > 14 14-7 7<

L. littoralis Height > 11 11-5 5< Breadth >11 11-6 6<

15%. During the survey, the laminarians were uncovered only during low spring tides. Thus, there were none recorded from May to September 1970 nor from November 1970 to January 1971 (Fig. 1).

There was an abrupt change in the algal cover at 7 0 ft (2 13 m) below OD and no laminarians were found above this level except during May 1970 and 1971, when enor- mous quantities of detached laminarians were cast up on the shore. These covered the entire upper shore from 142 ft to the base of the cliff. This seasonal casting up of L. digitata has important consequences on the shore, particularly in such a sheltered bay. The laminarians lay in dense mats caught in crevices and folds of the substrate, which resulted in large quantities of algal material rotting on the shore throughout May and early June. On less sheltered portions of the neighbouring beaches the cast-up material was present only in landward-facing crevices.

The algal coverage of the eulittoral region was very varied, and particularly dense on the lower shore. Himanthalia elongata Lyngbye, Fucus spp. (L.) and Chondrus crispus Stackh. dominated the lower shore, providing a coverage of between 30 and 9000 up to 5'0 ft (152 m) below OD, somewhat below Mean Low Water of Neap tides (M.L.W.N.). Lithothamnion Philippi was abundant from here downwards, and there were considerable quantities of Himanthalia buttons over this part of the shore. The cover of brown algae




Estimoted % algal cover

+12 6 MHW.S. M.HWN. M.LWN. ML.W.S.

z c 0 0 4'1

-10 0-. 0 50 94 118 376ft

9 6 9

D

9

.7

00nfrrnrha UOteale0Lmir/

Scale |=100%

D (

9 M_

7 _

Enleromorpho Other algae L: G<minG7rl<

FIG. 1. The abundance of algae at different levels on the shore, September 1969 to July 1970.



A. J. UNDERWOOD 357

decreased towards the top of the lower shore, becoming less than 10% for most of the year from October to May, up to the upper part of the bedrock at approximately 4 0 ft (1 22 m) to IP0 ft (0 30 m) below OD. Above the bedrock there was a fairly dense covering of the green alga Enteromorpha intestinalis (L.) Link, on the boulders. This ranged from a cover of 80% at 0 7 ft (0.21 m) below OD, to 10% at 0 4 ft (0 12 m) above OD and was very sparse higher on the shore. The only variance in this cover was found in June 1970 and 1971, when the cast-up Laminaria had been cleared by wave-action and the cover of Enteromorpha was found to be reduced. The alga recovered its normal steady state after about 3 months in 1970 (Fig. 1). Enteromorpha is characteristic of bare substrates which are not absolutely stable (Lewis 1964) such as the boulders described here.

In addition to the species of Fucus, the brown algae included small quantities of Ascophyllum nodosum (L.) Le Jol. and Pelvetia canaliculata (L.) Dcne et Thur. Nearly all the Ascophyllum and Fucus had surface growths of Polysiphonia lanosa (L.) Tandy, especially low down near the hold-fasts.

Above the area of boulders, there was little plant material until the base of the cliff was reached, where there were lichens of various sorts. There were some Verrucaria Schrad. from 1 to 2 ft (0 30 to 0-61 m) below OD, but the quantities were not estimated.

Littorina neritoides and L. saxatilis

These upper shore littorinids were never encountered in any numbers below M.H.W.N. L. saxatilis was found very occasionally with L. littorea in stations from 118 ft to 166 ft, but usually only one specimen was present per m2. On a large slab of rock at 64 ft, beside the transect but higher than it, at 5-5 ft (1 67 m) above OD, there were numerous L. saxatilis and some L. neritoides in crevices. These were present in approximately the same numbers and proportions (80% L. saxatilis) throughout the year. L. saxatilis was found in small numbers in crevices from 50 ft to the base of the cliffs, but from 30 ft upwards L. neritoides was dominant.

These species were not counted every month because they were present in relatively small numbers confined to deep crevices. Their removal for identification and counting would have proved very difficult. Colman (1933) and Evans (1947) showed the distributions of these two species in the Plymouth area to be similar to those found here, with overlapping zones and L. saxatilis extending lower whilst L. neritoides extends higher.

Littorina littoralis

L. littoralis exhibits a pattern of zonation related almost entirely to that of fucoid algae, notably Fucus spp. and Ascophyllum nodosum (Barkman 1955; van Dongen 1956; Bakker 1959). It was found, in the present study, to extend from 118 to 376 ft, i.e. 1 ft (0 30 m) to 10 ft (3 00 m) below OD, but was commonest where the fucoid algae were present (Fig. 2). There was considerable fluctuation in the numbers of Littorina littoralis from month to month, particularly in the smallest size-class (Table 2).

Spawn masses of this species were found during every month from September 1969 to the following July, when very little was present. Large quantities of spawn appeared from November 1970 to July 1971 when they were again decreasing in amount. This indicated a long breeding season, with a resting period in late summer and early autumn. Very small, newly hatched individuals, some with virtually unpigmented shells, could be found at most times of the year, but were particularly common in spring and autumn. This is not evidence for two breeding cycles per year, however, as the decline in numbers during winter can be attributed to heavy storms in December 1969 and 1970, and January




L /tor/na Ait/oral/s 126 MHW.S MH.WR M.LWN. M.LWS.

i \

z 0 o 0 +1

-100.0 0 50 94 118 376ft

S

9 6 9

D

7~~ _ ___

9 7 0

Scale 100

S_

D --

7 _A m

FIG. 2. Distribution of Littorina littoralis.



A. J. UNDERWOOD 359

1970 and 1971, which caused a reduction in the amount of fucoid algae present. Plants were torn off, mostly at the level of the epiphytic Polysiphonia and remained intact only in sheltered crevices. This inevitably led to a reduction in the numbers of Littorina littoralis present.

The dependence on fucoid algae for shelter and food did not seem so complete amongst the smaller specimens. Many of these were found on Chondrus crispus and in coralline pools, where they could be observed grazing on the surface of the algae. If removed to the laboratory and placed in a dish with Chondrus, Corallina or Fucus, these small winkles showed no preference for any particular alga. Probably Chondrus offered better shelter than the larger, broader fronds of the fucoid algae, and certainly there was more protec- tion from wave action as well as from desiccation in many of the Corallina pools. Colman (1940) found many juvenile Littorina littoralis protected by the branching tufts of Lichina pygmaea.

Table 2. Numbers and percentages of total samples in different size-classes: Littorina littoralis

Large % Medium % Small % Total 25 Sept. 1969 41 33-3 21 17-1 61 49-6 123 26 Oct. 54 56.3 13 13-5 29 30-2 96

Nov. - - - - - - - 10 Dec. 14 48.3 4 13.8 11 37.9 29 9 Jan. 1970 24 32.0 26 34-7 25 33-3 75 7 Feb. 24 44.4 16 29-6 14 25-9 54 9 Mar. 18 19.4 18 19-4 57 61P3 93 6 Apr. 22 19.1 36 31-3 57 49-6 115 4 May 11 11P7 19 20-2 64 68-1 94

22 June 60 21-2 148 52-3 75 26&5 283 20 July 47 25-9 75 41P5 59 32-6 181

Aug. - - - - - - -

1 Sept. 39 41P5 26 27-7 29 30-8 94 15 Oct. 60 33.9 44 24-9 73 41P2 177 13 Nov. 80 51-6 69 44-5 6 3*9 155 14 Dec. 70 64-8 34 315 4 3*7 108 29 Jan. 1971 13 54-2 11 45-8 0 0.0 24 26 Feb. 32 64 0 10 20-0 8 16-0 50 29 Mar. 23 76-7 6 20-0 1 3-3 30 26 Apr. 8 3-3 34 14-0 200+ 82-3 242 24 May 16 11.2 14 9-8 113 79 0 143 24 June 19 9 4 27 13-4 156+ 77.2 202 10 July 42 11-6 58 16-1 260+ 72-3 360 Total 717 26-3 709 26-0 1302+ 47-7 2728

Littorina littorea

The pattern of distribution of this winkle on the shore was obviously seasonal. From September to January in both years the majority of the specimens found were in one station, at 130 ft (39 m) below OD. This was on a shelf running across the shore, and the winkles were under stones on the landward side, protected from wave-action and wind. Only occasional specimens could be found elsewhere during these months (Fig. 3). In adjacent areas where the shelf was absent, the only specimens of L. littorea were in deep pools, in much lower numbers than on the transect.

From the end of January to July 1970, the population was much more dispersed, not only downshore, but also horizontally into regions beside the transect. By September




Li/for/no h)'foreG +126 MHWS. MHWN M.LWN. ML.W.S.

C \

I1 0 .. .. .1... . o 0- 0

LL

0 50 94 118 376 ft

I S 9 6 9

D

7 _______-___ 7

ScFlen 100

D_

9 M_

7

FIG. 3. Distribution of Littorina littorea.



A. J. UINDERWOOD 361

1970, however, most of the specimens found were again at 130 ft under stones. They remained there until January 1971 when again they spread laterally and downshore. In June 1971 large numbers were observed in rock pools, particularly a shallow pool at 1- 6 ft (0-48 m) below OD, where the sample counted was 91 /m2, the largest of the survey. Very few of the medium class, and hardly any in the small class were found throughout the survey (Table 3).

Coiman (1933) gave the distribution of L. littorea at Wembury as from 3-4 to 14-7 ft (1.03 to 4*48 m) above E.L.W.S., corresponding in the present survey to levels from 6-3 ft (1 92 m) below to 5*0 ft (1 52 m) above OD, very different from the values reported here. Evans (1947) noted that L. littorea tended to congregate on boulders or in shallow pools,

Table 3. Numbers and percentages of total samples in different size-classes: Littorina littorea

Large % Medium Y. Small % Total

25 Sept. 1969 86 97 7 2 2-3 0 0.0 88 26 Oct. 87 88.8 4 4K1 7 7-1 98

Nov. - - - - - - -

10 Dec. 57 95-0 3 5-0 0 0.0 60 9 Jan. 1970 47 904 5 9.6 0 0.0 52 7 Feb. 9 34-6 17 65.4 0 0.0 26 9 Mar. 29 78-4 8 21-6 0 0.0 37 6 Apr. 12 1000 0 0.0 0 0.0 12 4 May 14 93.3 1 6-7 0 0.0 15

22 June 69 93.2 5 6.8 0 0.0 74 20 July 55 91V6 4 6-7 1 1-7 60

Aug. - - - - - - -

1 Sept. 84 93 3 4 4.4 2 2.2 90 15 Oct. 20 64-5 7 22-6 4 12-9 31 13 Nov. 59 92-2 4 6f2 1 1-6 64 14 Dec. 62 96-9 2 3-1 0 0.0 64 29Jan. 1971 61 98.4 1 1-6 0 0.0 62 26 Feb. 13 76-5 4 23 5 0 0.0 17 29 Mar. 30 96-8 0 0.0 1 3-2 31 26 Apr. 22 95 6 1 4-4 0 00 23 24 May 53 86&9 6 9-8 2 3-3 61 24 June 108 86-4 4 3-2 13 10-4 125 10 July 49 75*3 6 8-1 11 16-6 66

Total 1026 88-7 88 7-6 42 3-7 1156

and gave its distribution in the Plymouth area as similar to that given by Colman (1933). In contrast, its distribution at Craig-yr-Wylfa in Cardigan Bay, where the tidal range is close to that of the Plymouth region, was from E.L.W.S. to E.L.W.N., a total vertical range of approximately 7 5 ft (2-38 m) (Williams 1964a). This represented a very different pattern of zonation from that found previously in the Plymouth region (Fig. 7), but the distribution of L. littorea at Heybrook Bay seems intermediate between these two extremes.

Monodonta lineata

M. lineata (Table 4 and Fig. 4) occurred on the transect at only 1-15/M2 compared with over 30/M2 in Caernarvonshire (Desai 1966) and over 50/M2 in Cardigan Bay (Williams 1965). It usually occupied a somewhat restricted zone, from 1 ft (0 30 m) to 2-6 ft (079 m) below OD, but with occasional specimens below this level, the lower limit




of the zone being rather diffuse. The lowest specimen found on the shore was an isolated one at 5 2 ft (1P58 m) below OD.

It first appeared that the boulder region of the shore might act as a physical barrier against upward movement of the population, but in early summer (June/July) the pattern of zonation changed and the animals were found much higher on the shore, on the Enteromorpha-covered boulders as well as on the solid rock, up to 1 6 ft (048 m) above OD. This represented a horizontal movement of up to 36 ft (1098 m) and a vertical migration of at least 2-6 ft (0 79 m). By September, the animals had returned to their former position.

Very few members of the small size-class were found, and these were nearly all in the upper part of the zone. An additional check of regions of the shore adjacent to the transect revealed no small specimens lower than 1 6 ft (0-48 m) below OD.

Table 4. Numbers and percentages of total samples in diWferent size-classes- Monodonta lineata

Large % Medium % Small % Total

25 Sept. 1969 19 1000 0 00 0 0.0 19 26 Oct. 18 1000 0 0.0 0 00 18

Nov. - - - - - - -

10 Dec. 14 73-7 3 15-8 2 10-5 19 9 Jan. 1970 10 909 1 9.1 0 00 11 7 Feb. 13 100.0 0 0.0 0 00 13 9 Mar. 10 83-3 0 0.0 2 16-7 12 6 Apr. 11 78-6 2 14-3 1 7-1 14 4 May 9 900 1 100 0 0.0 10

22 June 19 63-3 6 20-0 5 16-7 30 20 July 15 78-9 4 2141 0 0.0 19

Aug. - - - - - - - 1 Sept. 10 47-6 6 28-6 5 23-8 21

15 Oct. 7 77-8 1 111 1 11.1 9 13 Nov. 7 53-8 6 46-2 0 0.0 13 14 Dec. 9 750 3 250 0 0.0 12 29 Jan. 1971 13 81-2 3 18.8 0 00 16 26 Feb. 6 75-0 2 250 0 00 8 29 Mar. 12 85 7 2 14-3 0 00 14 26 Apr. 11 84-6 1 7.7 1 7-7 13 24 May 19 95-0 1 5 0 0 00 20 24 June 7 58 3 4 33.3 1 8-3 12 10 July 17 73*9 1 4-4 5 21-7 23

Total 256 78 5 47 14-4 23 741 326

Colman (1933) gave the vertical range of this species as extending about 2 ft downwards from M.H.W.N., which would correspond to 2-3-4-1 ft (0-67 to 1P25 m) above OD, considerably higher than the values obtained here, even during the upshore migration. Evans (1947) gave a much wider range in the Plymouth region, equivalent to 3 5 ft (1 06 m) below to 4d1 ft (1 25 m) above OD in the present survey. Williams (1965), however, recorded a lowly vertical range of approximately 6 ft (1 8 m) upwards from just below M.L.W.S. at Craig-yr-Wylfa. Desai (1966) noted that Monodonta lineata was found 'browsing in the upper half of the intertidal zone', without attempting to define the zonation further.

Gibbula umbilicalis

This species was found in stable numbers from 1-0 to 6-3 ft (0 30 to 1-92 m) below OD,



A. J. UNDERWOOD 363

Monodonto /ineato

+12 6 MHWS MH.W.N MLWN. MLWS

c

to 0- 0 + I

U-C

-100 . . 0 50 94 118 376ft

s + _

9 6 9

D

_

9J 7 0

Scale 20

M

7 _ _ _ _ _ _

D

9 M_

J F

FIG. 4. Distribution of Monodonta lineata.




with a few down to 6-9 ft (2.10 m) below OD (Fig. 5). Most of the large specimens (Table 5) were encrusted with algae and usually in crevices or weed. Small specimens were under stones in damp patches, very small ones being found in Chondrus from June to October 1970 and May to July 1971. At the top of its zone, Gibbula umbilicalis was often found in the same station as Monodonta lineata, and was present with Gibbula cineraria at lower levels.

Colman (1933) gave the extreme range at Wembury for G. umbilicalis as 2-4 to 12-9 ft (0 73 to 3-92 m) above E.L.W.S., which would correspond to 7-3 ft (2.22 m) below to 3-2 ft (0 97 m) above OD, a much higher extension on the shore than was found here. Evans (1947) gave the range as equivalent to 8-1 ft (2-47 m) below to 3'9 ft (1l18 m) above OD, again a greater range and even higher on the shore than was found at Hey-

Table 5. Numbers and percentages of total samples in different size-classes: Gibbula umbilicalis

Large % Medium % Small % Total 25 Sept. 1969 226 87'6 19 7-4 13 5-0 258 26 Oct. 205 87-6 21 9 0 8 3-4 234

Nov. - - - - - - - 10 Dec. 170 97-1 5 2.9 0 0 0 175 9 Jan. 1970 104 77-7 20 14.9 10 7-4 134 7 Feb. 142 92.2 12 7-8 0 0.0 154 9 Mar. 197 93.8 1 0-5 12 5*7 210 6 Apr. 133 91.1 7 4'8 6 4-1 146 4 May 224 94 9 7 3 0 5 2d1 236

22 June 147 78-6 31 16-6 9 4-8 187 20 July 139 83-2 19 11.4 9 5.4 167

Aug. - - - - - - - 1 Sept. 157 77.7 42 20.8 3 1.5 202

15 Oct. 197 73-8 56 20.9 14 5.3 267 13 Nov. 216 86-0 35 14.0 0 00 251 14 Dec. 278 90 5 29 9-5 0 0.0 307 29 Jan. 1971 169 86-7 26 13.3 0 0.0 195 26 Feb. 138 66.3 67 32.2 3 1.5 208 29 Mar. 209 88 9 26 11'1 0 00 235 26 Apr. 195 73-6 60 22.6 10 3.8 265 24 May 180 68.7 67 25-6 15 5-7 262 24 June 117 70.1 39 23-4 11 6 5 167 10 July 127 66-5 47 24-6 17 8-9 191

Total 3670 82.4 636 14-3 145 3-3 4451

brook Bay. Williams (1964b), however, gave the vertical distribution in Cardigan Bay as approximately 1l5-5-0 ft (0'45-152 m) above E.L.W.S., corresponding to 8-2-4-7 ft (2-50-1.43 m) below OD which was a lower and more restricted pattern of zonation than that found at Heybrook Bay.

Gibbula cineraria

The G. cineraria investigated in the present survey were of two distinct varieties, not reported previously. The typical specimens were pigmented, with black bands running round the cephalic and epipodial tentacles. The other variety, which constituted approximately 20% of the population, was lacking in pigmentation, the foot, tentacles and eye- stalks being completely white. The ratio of sexes in both varieties was consistently 1: 1 and no differences were noted in the size composition of the two varieties or in their distribution, so they were considered to be a single population.



A. J. UNDERWOOD 365

Gibb/la umbi///c/is + 12 6M MH WS. M.HW N M.L.W N. M.L.W.S.

0

+1

0 50 94 1 18 376 f t

S

9 6 9

D

9 J 7_ _

Scale |60

o

7 I .

FIG. 5. Distribution of GibbuJla uJmbilicalis.




G. cineraria ranged from sublittoral positions to about 6-4 ft (I 95 m) below OD. Soli- tary specimens were found in pools at higher stations up to 2-6 ft (0'79 m) below OD (Fig. 6). Most were found under fairly large flat stones, or browsing on the fronds of Laminaria at the bottom of the shore. In February 1970 and March 1971, however, the animals collected on the transect and observed in adjacent areas were on the upper surfaces of stones or on the open rock. From February to April 1970 and again early in 1971, there was an upshore movement of nearly 4 ft (1 2 m) vertically, so that the upper limit of the continuous population was only 2-6 ft (0 79 m) below OD. After May 1970 and June 1971 the animals moved back to their position on the shore and their former habit of staying underneath suitable cover. While this upshore migration took place, there was no obvious difference between the behaviour of the- two varieties described above.

Table 6. Numbers and percentages of total samples in different size-classes: Gibbula cineraria

Large ? Medium % Small % Total 25 Sept. 1969 48 26-4 127 69-8 7 3-8 182 26 Oct. 16 94-1 1 5-9 0 0Q0 17

Nov. - - - - - - -

10Dec. 1 9.1 7 63-6 3 27.3 11 9 Jan. 1970 10 100.0 0 0-0 0 0.0 10 7 Feb. 114 77.5 33 22.5 0 00 147 9 Mar. 32 40.5 41 51-9 6 7-6 79 6 Apr. 31 88-6 3 8-6 1 2 8 35 4May 34 61P8 15 27-3 6 10.9 55

22 June 7 58.3 5 41P7 0 00 12 20 July 3 25-0 9 75-0 0 00 12

Aug. - - - - - - - I Sept. 8 80.0 2 20-0 0 0.0 10

15 Oct. 19 20-2 38 40 4 37 39.4 94 13 Nov. 15 25'0 44 73-3 1 1.7 60 14 Dec. 30 61-2 19 38-8 0 0.0 49 29 Jan. 1971 4 33-3 6 500 2 16-7 12 26 Feb. 52 27.9 85 45.7 49 26-4 186 29 Mar. 19 100.0 0 00 0 00 19 26 Apr. 48 57-1 31 36-9 5 6.0 84 24 May 17 51-5 3 91 13 39.4 33 24 June 4 57.1 3 42-9 0 0.0 7 10 July 29 38.2 12 15-8 35 46&0 76

Total 541 45 5 484 40-6 165 13-9 1190

Small individuals occurred sporadically in September and October 1969, March, May and October 1970 and January, February, April and May 1971 (Table 6). Very small, newly settled young were found in samples of Chondrus crispus from the level of the lowest stations in April 1971, adjacent to the transect, at approximately 7-0 ft (2-13 m) below OD. They were 0 25 mm in breadth and unpigmented, with only the beginnings of a body-whorl.

The distribution of this species at Wembury was given by Colman (1933) as from 8-4 ft (2 56 m) above E.L.W.S. down into the sublittoral, i.e. from 1-3 to 9-7 ft (0 39 to 2 95 m) below OD. The upper limit given by Colman corresponded only to the extreme upper limits of isolated specimens of Gibbula cineraria at Heybrook Bay. Evans (1947) gave the upper limit in the Plymouth region as approximately 4-6 ft (1-40 m) above E.L.W.S., which was fairly close to the distribution found here.



A. J. UNDERWOOD 367

Glbbu/a c/nerGriG 126M.H.W.S M HWN. M.L.W.N. M LWS.

-10

z

0 50 94 118 376 ft

S6

9 6 9

-M_

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0_

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S

D

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FIG. 6. Distribution of Gibbula cineraria.




Calliostoma zizyphinum

C. zizyphinum was rarely encountered. A total of nine specimens were found from February to May 1970 and in January, February and April 1971, never more than 1 specimen/m2. They were at various levels on the shore up to 5-2 ft (1 58 m) below OD.

Colman (1933) gave the upper limit of this species at Wembury as 4-2 ft (1P28 m) above E.L.W.S., which was the same as the upper limit found here.

DISCUSSION

Population structure

Moore (1937), Smith & Newell (1955) and Williams (1964a) analysed populations of Littorina littorea and found polymodal frequencies indicative of different age/size- classes, suggesting that small individuals (up to 9 mm) are juveniles up to 6 months old. This conclusion is supported here by the absence of such individuals after November 1969 and 1970 (Table 3), following settlement on the shore during each summer. After 5 or 6 months, the high growth rate recorded by Moore (1937) and Williams (1964a) would have brought these animals into the medium class (9-18 mm). The latter were still not sexually mature (as ascertained by examination of the gonads of specimens adjacent to the transect) and were probably 6-18 months old. The juveniles were found on the shore at the same level as the adults.

The low numbers of the small and medium size-classes of L. littorea made critical analysis of the population structure difficult. The present method of sampling prevented any bias towards under-representation of the smaller animals by not removing all the animals from the shore at each sample. Their removal would possibly have selected for the larger, more motile members of the population which can move more easily into the stations between samples. Despite this, only 3.700 of the total population counted were in the small class and a further 7.6% in the medium class. It must be taken into account, however, that the percentage of the total population is considerably biased towards the large class by the number of samples made during months when there are no small snails present on the shore. When such were present, the percentage of juvenile snails (under 6 months old) ranged from 1 6 in November 1970 to 16&6 in July 1971 and the total percentages due to the two smaller size-classes combined (i.e. animals under about 18 months old) ranged from 666% in September 1970 to 35.500 in October of that year. Although accurate actuarial statistics are not available for this species, there appears to be no reason to suppose that these percentages are insufficient to maintain the recorded size of adult population during those months when the smallest size-class was present on the shore. There is thus no necessity to presume that substantial sublittoral settlement of juveniles (as proposed for Whitstable by Smith & Newell (1955) ) occurred in the Ply- mouth region.

The numbers of members of the large size-class (greater than 11 mm high) of L. littoralis were very variable (Table 2). The population was reduced by winter storms (shown by the changes in numbers found between October and December 1969 and from December 1970 to January 1971) when the cover of fucoid algae was reduced. In addition, the main hatching of young occurred from May to July 1971 when the algal cover increased over the lower part of the shore (Fig. 2 and Table 2). Spawn was present on Fucus from autumn to July, but there was a decrease in quantity from early summer onwards, in contrast to the previously recorded breeding season of March to October (Fretter & Graham 1962). The size-classes reflected age groupings in the population, the numerous



A. J. UNDERWOOD 369

members of the small class being those which hatched that year. No consistent pattern was shown in the variability of numbers in the medium class (0 5-1'1 cm high) but this probably represented animals 6-18 months old. The large class consisted of mature animals of 2 or more years. For most of the sampling period, the percentages of the population in the large and medium classes were very similar. The numbers of Littorina littoralis in the small size-class were greater in the early summer of 1971 than in 1970 (Table 2), and in April, June and July 1971 the numbers were too great for complete counting to be carried out in some stations. Numbers in Table 2 are therefore minimal estimates for the small class.

The numbers of the trochid Monodonta lineata found during the survey were very low, and no accurate estimates of growth rates could be made. The small class, however, was probably animals up to 4 months old (Williams 1965). The few of these which were found occurred mainly in June and September 1970 and July 1971 (Table 4). There were also, however, two in December 1969, possibly retarded specimens from the previous summer's settlement, and three in March and April 1970, possibly early members of the 1970 spawning. The latter were only 10-P 5 mm wide, similar to the newly settled juveniles found by Williams (1965).

Members of the small class of Gibbula umbilicalis were found spasmodically throughout the year and were all from the newly settled young of the previous late summer and early autumn (Underwood 1971). This agreed with the findings of Williams (1964b) who recorded a very low growth-rate during the first year in this species. The medium class contained several sexually mature specimens and probably consisted of animals 1-2 or more years old. Settlement of the young was much higher in 1971 than 1970 (Table 5) but represented a very low percentage of the total population.

G. cineraria showed a probable growth-rate similar to that of G. umbilicalis, as members of the small size-class were found at different times of the year (Table 6). Newly settled young were found in April 1971 with a shell width of 0-25 mm. These presumably grew very rapidly in the first few months and then slowly from autumn onwards. Many members of the medium class (up to 11-mm shell width) were sexually mature, and this class probably included animals 1-2 years old. Larval settlement was possibly predomi- nantly sublittoral as the range of this species extends well below E.L.W.S. (Fretter & Graham 1962).

Patterns of zonation

Although accurate comparative quantitative data about populations of intertidal prosobranchs are lacking from most previous accounts, it is clear that there are differences in the patterns of zonation at different localities. Colman (1933) and Evans (1947) recorded no more than the presence or absence of various organisms at different levels on the shore, and not throughout the year. Inaccuracies would be present in any attempt to compare data with the surveys of Williams (1964a, b, 1965) which were related to predicted low tide levels rather than to more accurately measured reference points. Nevertheless it is interesting to compare the limits of distribution quoted by these authors with the present results, by plotting all heights as feet above E.L.W.S., for those regions with similar mean tidal ranges (Fig. 7).

This shows that, in the Plymouth region, only G. cineraria has a distribution similar to those given by Colman (1933) and Evans (1947). In general, Colman (1933) and Evans 1947) found the zones to be higher or of greater extent than indicated here. In contrast, Williams (1964a, b, 1965) gave lower distributions for species on the coast of Wales. Even




allowing for discrepancies caused by different methods of measurement, it seems clear that the ratio of emersion to submersion and the maximum and minimum periods of emersion are not the major causes of zonation in these species, otherwise there should be closer agreement between the zones, certainly within the Plymouth region.

One pattern which emerged from the present data was consistent with previous observations. Wherever a species has been investigated, it has been found in the same spatial pattern with other species. Thus, Monodonta lineata is higher on the shore than Gibbula cineraria, and does not share the same zone. G. umbilicalis, in contrast, occupies a wider, intermediate zone, overlapping with Monodonta lineata at the top and with Gibbula cineraria lower down. Littorina littorea and L. littoralis have been described in the same zone by Colman (1933) and Evans (1947). In the present survey, this was true when L. littorea was in its dispersed phase (after May), but for most of the year, most of

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culotld DLneta bove littor a, U. shores ar L. ralis. uross-hatching

isoatdicatngcimits ofhro h soeta h mainboyfth populations. Cbut rmClmn(93;E ro vn 14) PMonodonta obserataLitotns;Wa frtome WilandsL a1964b all from Williamges' at95 W3lfomeees

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intertidal molluscs are known to undertake extensive migrations on the shore at certain times of the year. Upshore migrations of Monodonta lineata have been observed in summer (Williams 1965; Desai 1966; and present observations) and explained by Wil- liams (1965) and Desai (1966) as a response to rising temperatures. Desai (1966) considered that they were also related to spawning, but this was denied by Williams (1965) who found that immature specimens also migrated. Lambert & Farley (1968) recorded a seasonal downshore migration of L. littorea in Canada during winter, and laboratory analysis showed this to be a direct response to decreased air temperature. In contrast to this, Fretter & Graham (1962) observed a downshore migration of L. neritoides in Wales at the start of its breeding season. During the present survey, Gibbula cineraria



A. J. UNDERWOOD 371

also undertook seasonal movements up and down the shore, and these coincided with the probable time of spawning in spring (Underwood 1972a). The evidence for linking reproductive cycles and migrations seems strong, but it is unclear whether the stimulus for migration is the result of endogenous physiological changes connected with alterations in the gonads, or whether it is a response to external factors which also control the reproductive cycles. Whatever the mechanism, such migrations occur in Monodonta lineata and Gibbula cineraria without correlated alterations of the tidal cycle.

There thus exists an array of evidence which indicates that further consideration should be given to the proposals of Stephenson & Stephenson (1949) that intertidal zonation is not simply related to tidal factors. Considerable further evidence for this proposition has been gained from laboratory studies of prosobranchs in a tide model (Underwood 1972b, c). These showed that the patterns of zonation were not primarily governed by the rise and fall of the tide, and that the animals can survive under more extreme conditions than those normally encountered on the shore.

ACKNOWLEDGMENTS

This work was carried out while I was in receipt of a Science Research Council Student- ship. I am grateful to Mrs J. E. Milton, Dr T. E. Thompson and to my wife for their assistance with the shore surveys. I am also grateful to my supervisor Dr T. E. Thompson, to Dr C. Little and to Professor D. T. Anderson for critically reading this manuscript.

SUMMARY

(1) Monthly surveys on a transect at Heybrook Bay, from September 1969 to July 1971 recorded the numbers, size-classes and distributions of common motile prosobranchs and related these to algal cover and tidal levels. All individuals sampled were immediately returned to the shore to ensure that normal populations would be present after each survey. The amount of algal cover decreased during winter and increased during the early summer, particularly during the summer of 1971.

(2) Littorina neritoides and L. saxatilis were found in the upper part of the shore (above M.H.W.N.). Monodonta lineata occurred mostly 10-2-6 ft (0 30-0 79 m) below OD New- lyn, with a few specimens down to 5-2 ft (1 58 m) below OD. Littorina littorea had a much more restricted zone, most being found at 0 5 ft (0d15 m) below OD, with a few down to 5-2 ft (1[58 m) below OD. L. littoralis extended from 1-0 to 10-0 ft (0 30-300 m) below OD with a distribution related to that of fucoid algae. Gibbula umbilicalis overlapped with Monodonta lineata and Littorina littorea, extending from 1-0 to 6&3 ft (0 30 to 1 92 m) with a few at 6&9 ft (2- 10 m) below OD. Gibbula cineraria and Calliostoma zizyphinum occurred downwards from 6-4 ft ([ 95 m) and 5-2 ft (1 58 m) respectively, the latter in very small numbers.

(3) Monodonta lineata migrated 2-6 ft (0-78 m) upshore during June and July and returned by September. Gibbula cineraria tended to migrate upshore and back during spring and early summer. Littorina littorea became concentrated just below OD during autumn and winter, but extended downshore during spring and summer.

(4) Juvenile L. littorea grew very quickly during the first 6 months of benthic life and reached sexual maturity at about 18 months. Gibbula umbilicalis and G. cineraria showed a low growth rate during the first year. Juvenile and small members of the populations of Monodonta lineata, Gibbula umbilicalis, G. cineraria and Littorina littorea were scarce,




but were probably present in sufficient numbers to maintain the adult populations. Small specimens of L. littoralis were present throughout the year.

(5) Comparison with previous observations showed considerable variation from shore to shore. The seasonal fluctuations in zonation patterns recorded here occur in the absence of changes in the tidal cycle. These two observations clearly show that the widths and positions of zones are not strictly governed by factors due to the rise and fall of the tide.

REFERENCES

Bakker, K. (1959). Feeding habits and zonation in some intertidal snails. Archs ne'erl. Zool. 13, 230-57. Barkman, J. J. (1955). On the distribution and ecology of Littorina obtusata (L.) and its subspecific units.

Archs neerl. Zool. 11, 22-86. Colman, J. (1933). The nature of the intertidal zonation of plants and animals. J. mar. bibl. Ass. U.K.

18, 435-76. Colman, J. (1940). On the faunas inhabiting intertidal seaweeds. J. mar. biol. Ass. U.K. 24, 129-83. Desai, B. N. (1966). The biology of Monodonta lineata (da Costa). Proc. malac. Soc. Lond. 37, 1-17. Dongen, A. van (1956). The preference of Littorina obtusata for Fucaceae. Archs neerl. Zool. 11, 373-86. Doty, M. S. (1957). Rocky interidal surfaces. Mem. geol. soc. Am. 67(1), 535-85. Evans, R. G. (1947). The intertidal ecology of selected localities in the Plymouth neighbourhood. J.

mar. biol. Ass. U.K. 27, 173-218. Fretter, V. & Graham, A. (1962). British Prosobranch Molluscs. Ray Society, London. James, B. L. (1968). The distribution and keys of species in the family Littorinidae and of their digenean

parasites, in the region of Dale, Pembrokeshire. Fld Stud. 2, 615-50. Lambert, T. C. & Farley, J. (1968). The effect of parasitism by the trematode Cryptocotyle lingua (Creplin)

on zonation and winter migration of the common periwinkle, Littorina littorea (L.). Can. J. Zool. 46 1139-47.

Lewis J. R. (1964). The Ecology of Rocky Shores. English Universities Press, London. Moore, H. B. (1937). The biology of Littorina littorea. Part I. Growth of the shell and tissues, spawning,

length of life and mortality. J. mar. biol. Ass. U.K. 21, 721-42. Newell, R. C. (1970). Biology of Intertidal Animals. Logos, London. Sacchi, C. F. & Rastelli, M. (1966). Littorina mariae, nov. sp.; les differences morphologiques et ecolo-

giques entre "nains" et "normeaux" chez l'esp&ce L. obtusata (L.) (Gastropoda: Prosobranchia). Atti Soc. ital. Sci. nat. 105, 351-69.

Smith, J. E. & Newell, G. E. (1955). The dynamics of the zonation of the common periwinkle (Littorina littorea (L.) ) on a stony beach. J. Anim. Ecol. 24, 35-56.

Southward, A. J. (1958). The zonation of plants and animals on rocky sea shores. Biol. Rev. 33, 137-77. Stephenson, T. A. & Stephenson, A. (1949). The universal features of zonation between tide-marks on

rocky coasts. J. Ecol. 37, 289-305. Underwood, A. J. (1971). Behavioural ecology and reproduction of intertidal prosobranch gastropods.

Unpublished Ph.D. thesis, University of Bristol. Underwood, A. J. (1972a). Observations on the reproductive cycles of Monodonta lineata (da Costa),

Gibbula umbilicalis (da Costa) and Gibbula cineraria (L.) Marine Biol. 17, 333-40. Underwood, A. J. (1972b). Tide model analysis of the zonation of intertidal prosobranchs. I. Four species

of Littorina (L.). J. exp. mar. Biol. Ecol. 9, 239-55. Underwood, A. J. (1972c). Tide model analysis of the zonation of intertidal prosobranchs. II. Four species

of trochid (Gastropoda: Prosobranchia). J. exp. mar. Biol. Ecol. 9, 257-77. Williams, E. E. (1964a). The growth and distribution of Littorina littorea (L.) on a rocky shore in Wales.

J. Anim. Ecol. 33, 413-32. Williams, E. E. (1964b). The growth and distribution of Gibbula umbilicalis (da Costa) on a rocky shore

in Wales. J. Anim. Ecol. 33, 433-42. Williams, E. E. (1965). The growth and distribution of Monodonta lineata (da Costa) on a rocky shore

in Wales. Fld Stud. 2, 189-98.

(Received 8 August 1972)



studies on zonation of intertidal prosobranch molluscs in the plymouth region

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