vertical zonation on rocky shores in the severn estuary

Estuarine and Coastal 2[Iarine Science (x98o) xr, 651-669

Vertical Zonation on Rocky Shores in the Severn Estuar3f

C o l i n Li t t le b a n d L y n d a P. S m i t h c'~ Departments of Zoology b and Botany ~, Bristol University, Bristol BS8 I UG, U.K.

Received x2 November z979 and in revised form I9 February 198o

K e y w o r d s : zonation; estuarine flora; limpets; algae; grazing; wave action ; Bristol Channel

Zonation of algae and invertebrates was examined on rocky shores in the Severn estuary from z975 to I978. These shores were characterised by an absence of macro-algae from M L W S and below. Some littoral algae showed reductions in abundance during the study. In particular, Ascophyllum nodosum and Fucus serratus almost disappeared from the mid shore at one site after z976, and no significant recolonization had occurred by z979. Animal species in general showed predictable and constant zonation patterns, but Littorina ruth's, Patella vulgata and Ehnbffus moclestus all exhibited decreased upper vertical limits in the upper reaches of the estuary.

Three approaches were taken to interpret the zonation patterns and their changes. (i) Exposure to wave action was estimated. Decreasing exposure levels may account for the decline in upper vertical limits of species in the upper estuary. (ii) A sun 'ey of silt, saliniw and temperature was carried out over complete tidal cycles. High silt concentrations may partiaUy explain the absence of macro-algae below MLx, VS. (iii) Preliminary experim, ents compared the effects of grazers in the estuary with those in fully marine conditions. These experiments point to some of the factors which are responsible for the lack of algal recolonization on the shore from which the dominant fucoids disappeared after 1976, but the situation is complex and involves algal reproductive biology as well as grazer activiw.

I n t r o d u c t i o n

On fully marine shores, zonation patterns can often be related to the degree of exposure to wave action (e.g. Moyse & Nelson-Smith, I963; Lewis, x964). In estuaries, however, the factors which affect zonation are not well understood and very little published work is available on the subject. Crothers (z976) has examined zonation patterns in the Bristol Channel and attr ibuted some features of them to exposure, others to estuarine effects. T h e present s tudy was undertaken in the Severn estuary to investigate zonation patterns in situations where estuarine effects are extreme. Initial work employed transects at fixed sites along which the abundance of common invertebrates and algae was estimated at intervals for several years. These studies raised a number of problems, especially concerning the year- to-year changes in zonation. We sought explanations for the zonation patterns

*This paper is dedicated to the late Dr C. R. Boyden who worked for several years on the Severn estuary and who, during the early years of the present study, was a constant source of encouragement and inspiration. dPresent address: Department of Botany, University of Liverpool, Liverpool L69 3BX, U'.K.

65 x o3oz-3524/8o/x2o65x+x9 $oz.oo/o - �9 x98o Academic Press Inc. (London) Ltd.

652 C. Little & L. P. Sndth

and for their changes by three methods. First, we attempted to assess exposure levels, since we felt that these might vary in different parts of the estuary. Exposure levels may be different at different heights on the shore and may, therefore, be important in determining zonation patterns. Second, we conducted surveys of physical and chemical factors over complete tidal cycles, to assess degrees of change in these factors at different levels on the shore. Third, we attempted to assess the importance of grazers in controlling algal distribution at the various sites, since the distribution of grazers in the estuary is regulated by factors peculiar to estuaries as well as by exposure levels. The paper is therefore presented in four sections, describing first the transects, and then the three methods of investigating the possible causes of the zonation patterns described.

GLOUCESTER

CAROIFF " ~ / / ~." !.'X "&'.~J BRISTOt.

~AND PT

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o to zo k m

Figure x. Map of the Severn estuary showing the location of experimental sites.

1. Zonat ion pat terns o f a lgae and invertebrates

Methods and sites Nine rocky shores in the Severn estuary were examined in 1974- 5, from Brean Down to Sharpness (see Figure z). Wherever possible, headlands were used. In z976 seven sites were resurveyed and in z978 a final survey of five sites was made. Detailed results are presented here only for Sand Point, Portishead and Aust, but information from the other sites is used to examine the general trend along the length of the estuary. Results of the initial survey for all nine sites are given in Smith & Little (z98o).

At each site a transect was taken from the top of the shore to low water. Abundance estimates were made at z.o or 0. 5 m vertical intervals, using the abundance scales in Crothers (z976). Abundance levels were estimated not from a narrow belt but from a region about xo m wide so that variations in mosaic patterns were ignored. In the initial survey (i974-5), up to six people were employed at Brean and Sand Point, but thereafter, and at all other

Vertical zonatlon on rocky shores 653

sites, only two people were involved so that the effect of trampling was negligible. From the height of low water, all heights were related to O.D. by reference to the Admiralty Tide Tables. This method of determining height is probably inaccurate, but it was supplemented by reference to the fixed quadrats (see section 4), and was judged never to be in error by more than about 0. 3 m. Nevertheless, some of the minor apparent shifts in zonation may have been caused by deviation of the actual tidal level from the predicted one.

The most seaward site, Sand Point (ST 318659), was a promontory of Carboniferous limestone pointing due west. Our transect was at the end of the point on the south facing side. The shore was steep to O.D., and then consisted of a shallow platform with gullies sloping to low water. Portishead (Battery Point) (ST 464776) was a much smaller headland of Carboniferous limestone; it also pointed west, but on the southern side was a muddy bay. Our transect was on the north facing side, just below the navigation light. The shore consisted of steep cliffs with a short platform towards low water. The most upstream site was Aust (ST 567899) where the upper shore was formed of loose angular boulders which gave way to a region of soft red Keuper marl below MHWN. The main area of the shore was a long platform of Carboniferous limestone just above O.D., which ended in a steep cliff at low water.

Results The results of the transects at three sites are given in Figures 2 and 3- Vertical zonation of algae and invertebrates was apparent at all three sites, although the range and abundance of individual species varied with location. This variation is further shown by Smith & Little (x98o). An outstanding feature of algal zonation at all the estuarine sites was tile absence of macro-algae from MLWS and below, the rock at this level being dominated by the estuarine barnacle Balanus improvlsus. This situation contrasts strongly with typical marine situations, where intertidal algae extend to at least ~ILWS, below which there is a subtidal algal zone.

There were also several cases where species of algae were absent at sites where one might have expected them to be present. Fucus vesiculosus, for example, was almost entirely absent from the transects at Sand Point and Portishead. This is discussed by Smith & Little (x98o) who concluded that a dominant Ascophyllum zone affects the occurrence of F. vesiculosus at many of the estuarine headlands. Blidlngia and Enteromorpha were absent from Sand Point. This is discussed in section 2, since it may be connected with exposure. At Aust, Pelvetla was absent, possibly due to lack of a suitable substrate, since it was found at scattered points further up the estuary. Apart from the mobile shore of loose boulders, there were only the concrete pillars of the Severn road bridge at Aust which might have formed possible substrata for Pelvetia. These were thickly covered by Ulothrlx sp. which could inhibit settlement of fucoid spores (Seshappa, i956 ).

Some species of algae disappeared or suffered reduction in abundance and distribution during the study period. Fucus spiralis and Pelvetia disappeared from the transect at Sand Point after I974. This could be explained partly by the effect of desiccation during the hot dry summers of x975 and I976. Both species also suffered a reduction in abundance at Portishead after I974, but had recovered by x978, and F. spiralis showed a similar pattern at Aust. Failure to recolonize at Sand Point is therefore not understood, but it may be that wave action prevented settlement, since Sand Point was the most exposed site examined. The green algae at Portishead showed a reduction in abundance in 1976, followed by recovery, but no reduction was seen at Aust.

Perhaps the most striking observations on algae were the changes in Fucus serratus and Ascophyllum at Portishead. After x975, the upper limit of F. serratus was reduced from

654 C. Little ~ L. P. Smith

Blidingia and Enteromorpha

Sand Point Portisheod

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MHWS Ascophyllum

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MLWS Abundonce7 75 76 78 75 76 78 75 76 78

Figure z. Vertical distribution of algae at the three transect sites. The abundance scale is that of Crothers (z976). Tidal heights were derived from the Admiralty Tide Tables.

nearly M H W N to well below O.D. After z976 , almost the entire population of Ascophyllum vanished from the mid-shore, leaving small remnants just above M H W N and MLWN. It is possible that F. serratus was ousted by the shading effect of Ascophyllum but, since the dramatic decrease in the latter, no other fucoids have yet colonized the area (December I979). This is contrary to most reports on algal succession following removal of Ascophyllum, in which F. vedculosus is recorded as quickly colonising the cleared area (Burrows, 1948 ).

Vertical =onation oi= rochy shores 655

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Figure 3- Vertical distribution of fauna at the three transect sites.

From the kite diagrams (Figure z) it is evident that many other minor changes were recorded in algal distribution. While some of these recordings may reflect real changes, it is likely that many of them are due to errors in re-locating the transects. On the short steep parts of the beaches it was easy to repeat the original lines but, in the more gently sloping areas such as at Aust and Sand Point below O.D., later transects may have diverged con- siderably from the original and, in spite of the wide area covered in each survey, slight differences in aspect, slope and drainage may have influenced the results.

The most abundant gastropod living on the algae was Littorina littorallr (L.). Littorina marine Sacchi & Rastelli was not present at the three stations examined here, but was found


further seaward at Brean Point (Smith & Little, z98o ). L. littoralis was associated with Ascophyllum and Fueus serratus. Its dependence upon the former is shown strikingly by its distribution in I978, when much of the Ascophyllum had disappeared from Portishead.

The dominant grazing gastropod on rock surfaces was Patella vulgata L. Both its abundance and vertical range at the two seaward stations were very constant, despite changes in algal cover. It penetrated as far as Aust only in 1976, when there was low rainfall in the summer, and saline water presumably penetrated farther than usual up the estuary. At this time a colony was established at Aust, but only at MLWN. Between Aust and Portishead the species was only found at ]MLWN (Smith & Little, x98o ).

The other grazing gastropod on rock surfaces was Littorhta saxatilis agg. At Portishead and Aust, all specimens in this species complex were assigned, after dissection, to L. rudis (Maton). At Sand Point, L. neglecta Bean was also present, but only between ~IHWN and O.D. (see Little, in preparation). All further consideration of the complex is limited to L. rudis. Variation in density of this species was greatest at Aust. Here its vertical range appeared to have been shifted downshore, compared with more seaward stations. The trend was continued at sites further upstream (see Smith & Little, x98o ).

One of the dominant barnacles, Balanus balanoides (L.), showed a tendency to increase its vertical range upwards over the study period. At Portishead this appears to correlate with the decrease in Ascophyllum: over the four years, the shore at Portishead altered from dense cover by Ascophyllum to bare rock covered with a barnacle-limpet community. The other dominant barnacle, Elminius modestus Darwin, showed some tendency for its uppermost vertical limit to be reduced higher up the estuary.

Confinement to low levels on the shore at the head of the estuary therefore seems to be a tendency shown by Patella, L. rudis and Ehninius. This difference in vertical distribution from the more seaward sites might be linked to an increase in desiccation at higher levels on the shore caused by the asymmetrical tide curve in the upper estuary; but this seems unlikely to be the prime cause because the change in distribution was apparent at Aust, whereas the tide curve there shows little change in symmetry from that at Portishead.

Conclusions From this brief description it is evident that there are many points in the distribution of flora and fauna which are difficult to explain. Besides tile reduction in the upper limit of many algal species in z976, which may he explained by increased desiccation that year, there are several minor problems of species distribution, particularly concerning Pelvetia and Fucus vesiculo,us. These may be partly related to substratum requirements, but probably also involve competitive effects. To these may be added the fact that Littorina littoralis showed its greatest abundance at Aust, yet this was actually the site at which this species had its uppermost limit in the estuary. Three further problems may be summarized as follows. First, there was the total lack of macro-algal species low on the shore at all sites. Second, there was the great reduction of Ascophylhtm and Fucus serratus at Portishead. This was particularly striking because it was at this site that Ascophyllum showed its greatest vertical range. Ascophyllum was far from being at its salinity or turbidity limit at Portishead, since it was also common at Aust; at this site it has shown little sign of decrease in abundance during the study period. Third, there was the tendency for some animal species to show decreased upper vertical limits in the estuary. The difficulties of providing explanations for these situations are large because of the interplay of a large number of environmental variables in the estuarine situation: it is likely that any one aspect of change in a community is the result of

Vertical zonation on rocky shores 657

more than one factor. In an attempt to define the effects of some of these factors, we have investigated those that we considered most important: the influences of wave action, high silt loads and variable salinity; and the biological effects due to interactions between species.

2. Effects o n z o n a t i o n o f e x p o s u r e to w a v e a c t i o n

The problems of employing biological exposure scales have been admirably reviewed by Lewis (I964). I t is evident that in estuarine conditions these problems are exaggerated by interactions with the effects of salinity, turbidity and currents. While it is therefore difficult to isolate the effects due to wave action, it is essential to attempt some assessment of the relative importance of wave action at various sites within the estuary. In order to do this, we have estimated the angles over which the shores were open to various lengths of fetch. A similar method was adopted by Baardseth (x97o) for assessing the exposure of rocky shores in Norwegian fjords.

Methods

The angles over which shores were open to fetches of greater than 5 ~ miles, 1o-5o miles, and less than io miles were estimated, for comparison with the data provided by Ballantine (x96i) for shores near Dale, at the mouth of the Bristol Channel. Such a comparison is valid because as at Dale the majority of gales blow from the same direction (SW. to W.), and this is also the direction of greatest fetch.

An effort was also made to determine differences of exposure at different shore levels. It is generally accepted (see, e.g., Lewis, x964) that steeper shores are subjected to greater effects of wave action than are gently sloping shores. The overall slope of the shores was measured from the level of MHWS to O.D., and from O.D. to MLWS.

T~LE x. Some physical characteristics of the sites in relation to exposure

Site

Degrees Degrees Degrees Equivalent Slope of shore open to open to open to exposure (~ from the

> 50 zo-5o < zo on horizontal) miles miles miles Ballantine MHWS O.D. fetch fetch fetch scale -- O.D. - MLWS

Sand Point xz to7 79 5 23 9 Portishead o 56 x45 6 26 x8 Aust o 27 x5o 6 x 9

Results

Results are presented in Table x. One difference between the shores considered in the present survey and those studied by Ballantine (z961) is the predominance in the Severn of fetches between zo and 5 ~ miles, due to the narrowing of the estuary. Despite this difference, however, Sand Point fits well with Ballantine's exposure 5, and Portishead and Aust are both equivalent to exposure 6. Aust is, however, less exposed than Portishead.

The measurements of slope suggest that at Sand Point the top half of the shore is more exposed than the bottom half, whereas the exposure grades are probably uniform at Portis- head and Aust. The gentle slope at Aust reinforces the suggestion made from measurements of fetch that it is less exposed than Portishead.

658 C. Little & L. P. Smith

Conehtsions Perhaps the most marked trend in algal distributions with distance up the estuary was the increase in vertical range of Blidingia and Enteromorpha. Since these existed primarily on the upper shore, where exposure declined from Sand Point to Aust, the inverse correlation with exposure is apparently good. However, while exposure may be relevant in such processes as settlement, it must be emphasized that the actual distribution of green algae is more likely to be controlled by biological interactions such as competition and grazing. Other apparent correlations of exposure with algal density, such as the absence of Pelvetla from upstream sites and the absence of Fucus vesiculosus from downstream ones, are in fact the inverse of those expected. Once again, however, it is likely that direct effects of exposure would be limited to settlement, while survival and growth would be more influenced by the effects of competition and of grazing gastropods.

The decline in the upper vertical limits of Patella, L. rudis and Elmbzhts in the upper estuary also appears to correlate well with the gradual decline of exposure on the upper shore. Here there may well be a direct effect upon survival and distribution, since less exposure will mean less splash and more desiccation at high levels. This will be accentuated by the difference in slope from the steep cliffs at Portishead to the long platform at Aust, as well as by the increasing asymmetry of the tide curve at the upper sites.

The general decrease in barnacle density in the upper reaches of the estuary may also be associated with the reduction of exposure at all levels of the shores in these regions. Barnacles can be excluded by heavy growths of algae, except on vertical faces, although the exact mechanism of this exclusion is not known (Lewis, x964). The general decline in the density of Patella and L. rudis, however, must probably be attributed to changes in salinity and turbidity from the mouth to the head of the estuary, since it is not likely that decrease in exposure would have such a marked effect. The exact site to which a species penetrates is likely to be decided by fortuitous events which oentrol the distribution of larvae, in the ease of barnacles and Patella, or of more mature stages, in the case of L. rudis and L. littoraIin This is exemplified by the settling of Patella at Aust in i976: the colony flourished until x977, but no further settlement occurred and the colony had disappeared again by x978.

In summary, it may be said that there are some effects of exposure which tend to limit the abundance of the fauna at the head of the estuary; but that no direct effect on the algae has been shown. In any case, the majority of exposure effects probably occur via biological interactions by altering the balance between particular species.

3. Effects of other physical and chemical factors on zonation

Methods A survey was undertaken to obtain values of temperature, salinity and silt in waters very close to the shore. Readings were taken over complete tidal cycles of spring and neap tides, in summer and in winter. The study was carried out in collaboration with Dr C. Mettam, and it is hoped to publish the results in full elsewhere. Selected data are given here in an attempt to correlate physical factors with the distribution of organisms in the estuary.

Simultaneous readings were taken at Aust, Portishead and Sand Point, as weU as at stations further upstream and on the Welsh coast (Dr C. Mettam, unpublished data). Samples were taken in glass or polyethylene containers at hourly intervals. Temperature was recorded by mercury bulb thermometer, salinity by an MC 5 Bridge. Silt was measured in i I samples, as dry weight after removal of salts.

Vertical zonation on rocky shores 6 5 9

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660 C. Little r L. P. Smith

Results Mean values of salinity, silt and temperature are given in Table 2.

All temperatures recorded in winter (February,{arch 1977) were between 5 and 9 ~ There were no marked fluctuations over either of the tidal cycles at any of the three stations. In summer (August 1977), the temperature range was 17-2o ~ at Sand Point and Portis- head, and i8-24 ~ at Aust. The increase at Aust was probably due to movement of water over heated sandbanks.

In general, silt levels were higher at Aust than at Portishead, while values at Sand Point were consistently low. At all sites there was a great deal of variation over individual tidal cycles and no consistent pattern was evident (see Figures 4 and 5). On one occasion at Portishead (2 l~Iarch 1977) there were peaks of silt concentration at mid-flood and mid-ebb, but these were not repeated at other times. Values were higher on spring tides than on neaps, as would be expected because spring tides bring large quantities of fluid mud into suspension (Kirby & Parker, 1977).

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Vertical zonation on rocky shores 66x

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Figure 5. Measurements of the salinity and silt content of water samples taken at hourly intervals over a neap tidal cycle in summer (9 August z977). Symbols as in Figure 4.

Large changes in salinity occurred in the course of single tidal cycles at Aust and Portishead, particularly on neap tides (Figures 4 and 5). The patterns of salinity change closely followed those of tidal height, lower salinities occurring at low tidal heights; but there was often a lag phase which meant that there was no direct relation to height. I t was apparent, however, that the greatest fluctuations were experienced on the lower shore, and that above M T L changes over any one tidal cycle were relatively small.

66z C. Little 61 L. P. Smith

Conchlsions None of the temperature values recorded are indicative of a relationship between temperature and the vertical distribution of intertidal species. It is quite possible, however, that extremes of temperature at particular times of year may differ radically at different vertical heights.

The silt measurements help to explain some of the patterns of vertical distribution on the estuarine shores. The absence of macro-algae from IX'ILWS and below is very probably the result of the scouring effect of silt, and to a certain extent of the reduced light penetration affecting the settlement of algal spores. The extent to which the high turbidity of the water affects photosynthesis of the established benthic algae may, however, be offset by the capacity of intertidal algae to photosynthesize effectively during the intertidal period (Brinkhuis et al., x976; Johnson et al., x974). Other anomalies in the distribution of fucoids cannot be explained by silt values alone. In particular, the removal of Ascophyllum from the mid-shore at Portishead was very probably the result of a combination of high turbidity and exceptional current flow in the mid-tide region.

The large cyclical fluctuations in salinity at Aust and Portishead may relate to the absence or scarcity of some of the fauna and flora below MTL, and particularly to the reduced extent of fucoids on the lower shore. They do not explain gaps in the distribution of species at and above MTL, however, as a comparison of the shores at Aust and Portishead illustrates. .4scophyllum was abundant at Aust in a zone subject to greater fluctuations in salinity than the mid-tide region at Portishead where there has been a decrease in tiscophyllum.

Salinity fluctuations over any one tidal cycle were very small at Sand Point and the average fluetuatlon over the year was only approximately 5~o- It is unlikely that this would have a significant effect on the vertical distribution of flora and fauna there.

4. The effects of biological interactions on zonation

The most striking point to remain unexplained after the investigations into the effects of exposure, temperature, silt and salinity, was the virtual disappearance of .4scophyllum and Fueus serratus from the middle of the shore at Portishead, and the lack of any algal recolonization. Because the limpet density was high at Portishead, it seemed possible that algal settlement was prevented by the grazing action of limpets. The following experiments were designed to test this hypothesis. Although they are only preliminary, we feel that it is appropriate to describe them here because they throw considerable light upon the complexi- ties of biological interactions in the Severn.

Methods At Sand Point and at Portishead permanent x m ~ quadrats were marked out with brass bolts in the region of O.D. to ML~,VN. Control quadrats were also established there, in which no experimental interference took place. In order to cheek the efficacy of our techniques in the estuary, we also set up experimental quadrats, with controls, at Porlock where conditions were sufficiently marine that the results of limpet removal would be expected to follow those reported in the literature. The first site was at Hurlstone Point (SS 898493) and a second was later established at Yellow Rocks (SS 855484) (see Figure x) where the degree of exposure was less. Details of all the quadrats at the start of the experiments are given in Table 3. Unfortunately, both the sites at Porloek were more exposed than those in the estuary; but we could find no other local site where bedrock was present at O.D. Initial clearance of the experimental quadrats took place in the summer of x978. All Patella were removed, counted and biomasses determined (see Table 3). At intervals of 2- 4 weeks, the


TABLE 3. Biological and physical characteristics of experimental sites

Porlock Porlock Experimental sites Portishead Sand Point Hurlstone Point Yellow Rocks

Tidal level: rel. to O . D . rel. to C.D.

- x . 2 m - x ' 7 m - x ' 4 m +o.8 m +5"3 m +4"3 m +3"8 m +6"o m

(MLWN/ (MLWN/ (MLWN/ (MTL) MTL) hlTL) MTL)

Angle of slope 5 ~ xo* 4 ~ 45 ~ Aspect o *(N) z5 o~ (WSW) 34 ~ (NNW) 40* (NE) Rock type Carboniferous Carboniferous Old Red Old Red

limestone limestone Sandstone Sandstone Exposure on scale of Ballantlne ca. 6 5-6 z-3 3-4 Date of initial x m ~ survey (all 4 Aug. x978 7 Aug. x978 6 Aug. x978 x8 Nov. x978

limpets removed). Date of application of antifouling 9 Apr. x979 3x Mar. x979 30 Mar. x979 3o Mar. x979

paint Initial survey: Limpet density (nos. m -z) 76 xo3 x64 58 Limpet biomass (g dry wt m -z) 5"47 5"9z 4"5z x'9z Flora:

Verrucarla spp. (% cover) ao o x5 2o Diatoms (% cover) 7 ~ 80 o o Fucus spp. (% cover) o o o Io Ascop.~yllum (% cover) o 4 o o Ulva sp. o trace o o Red algae (% cover) o o trace z

sites were revisited, all l impets which had entered the areas were removed and the density of algal growth, if any, was assessed. At the Porlock sites it soon became apparent that l impets migrated into the cleared quadrats too rapidly for their removal every 2 - 4 weeks to be effective. In the autumn of x978, therefore, larger areas (6-- 9 m 2) were cleared at Porlock. This to some degree reduced the number of l impets reaching the centre of the quadrats before the next clearance. In order to reduce the entrance of l impets even further, the r m e quadrats were surrounded by a line of anti-fouling paint (International T .B.T. Antifouling) approximately xo cm wide in the spring of I979. This t reatment was very effective, bu t we suspected that runoff at low tide from the upper lines of anti-fouling paint influenced conditions within the quadrat. In the summer of x979, therefore, a final modification was made to the x m e areas. The bot tom and side lines were repainted and the side lines were continued up the rock face until a line across could be placed so that drainage down the slope did not run into the quadrat; or, if this was not possible, the lines were continued up tlle rock face as far as practicable.

T h e effectiveness of the anti-fouling paint may be judged from the following figures. Dur ing the period March to August I979, average biomasses of l impets recorded in the i m e quadrats at the end of each month were: for Portishead, o.ooI g dry wt.; for Sand Point, 0"034 g; for Yellow Rocks, 0.005 g; and for Hurlstone Point, 0.o97 g. T h e maximum figure was o .29z g, recorded at Hurlstone Point, i.e. 6.5% of the biomass of the initial l impet population. This figure was exceptional and was caused by the growth of diatoms over the anti-fouling paint, thus providing an entrance for the limpets. T h e highest figures apart from this were o . i i o g at Sand Point and at Hurlstone Point. These were equivalent to x. 9 and 2.4% of the initial biomasses respectively. Some of this amount was made up by spat which settled in the quadrats.


At the two estuarine sites, the density of grazers apart from Patella was very low. A few Littorina rttdis were occasionally present, but it is most unlikely that these could have any significant effect upon algal growth. At Porlock, Littorina neglecta was common in the Hurlstone Point quadrat, and at Yellow Rocks other grazers such as Monodonta lineata, Gibbula umbillcalis and Littorina littorea were frequent. Anti-fouling paint did not deter

Porlock HP

A

Diatoms

Green sp.

Fucus

1978 1979

A S O N D J F M A M d J A S t~

Porphyro B Diatoms Green sp. Fucus Porphyro

Porlock YR

A

Diatoms

Green sp.

1978 1979

A S 0 N D d F M A M d J A S N

_l

Pot.oh)ira B

Diatoms Green sp. Fucus Porphyro

Figure 6. Effect of limpet removal on the abundance of algae at Porlock. HP, Hurlstone Point; YR, Yellow Rocks. A, limpets removed; B, control area. The areas involved were 6 m = at Yellow Rocks, and 9 m s at Hurlstone Point, except that at the latter site data for z m 2 were used up to April z979. Limpets were initially removed on 6 August t978 at Hurlstone Point and z8 November z978 at Yellow Rocks. Abundances are given on a 4 point scale: x, less than 5% cover; 2.5-2o% cover; 3, 2o-60% cover; 4, greater than 6o% cover. Diatoms were not classified. Green sp. comprised Ulothrix speciosa at Hurlstone Point, with the addition of Enteromorpha intestinalis and Ulca lactuca at Yellow Rocks. Fucus sp. were not classified. Porphyra was P. umbilicalis.

their movements at all, so that further efforts to restrict the access of aH grazers were made using wire mesh fences. Unfortunately, for a variety of technical reasons these were not effective; but the combination of anti-fouling paint strips and wire fences offers exciting possibilities in future work for separating the effects of Patella from those of trochids and littorinids.

Vertical :onation on rocky shores 665

Porlishead 1978 1979

A S 0 N D J F A

M A M d J A S 0 r] D

Diatoms

Green sp.

Fu~Js Porphyro

Diatoms Green sp. Fucus Porph.vro

Sand Point 1978 1979

A S O N D J F M A

A M J d A S 0 N D

Diatoms

Green sp.

Fucus

Porphyro

B

Diatoms Green sp. II I

Porphyro ~ I

Figure 7. Effect of limpet removal on the abundance of algae at Portishead and Sand Point. A, limpets removed; B, control areas. The areas involved were x m% Limpets were initially removed on 4 August I978 at Portishead and 7 August x978 at Sand Point. Diatoms were not classified. Green sp. were Ulva lactuca at Portis- head, with the addition of Enteromorpha intestinalis at Sand Point. Fucus sp. w e r e

not classified. Porphyra was P. umbilicalis. Abundances as in Figure 6.

Results The results of these experiments are summarized in Figures 6 and 7. At Porlock, there was some lag in the development of the flora following removal of limpets, but by April z979 there had been significant changes in the flora compared with that of the control area. At Hurlstone Point a thick cover of diatoms was accompanied by the settlement of Ulothrlx speciosa, and was followed by Porphyra umbilicalis and Fucur sp., together with scattered patches of Laurencia pinnatifida, Lomentaria articulata and Palmaria palmata. At Yellow Rocks the dominant green alga to develop was also Ulothrix, but here it was accompanied by Enteromorpha intestinalis, Ulva laetuca and Cladophora sp. Fueus sp. settled at the same time, and a settlement of Porphyra occurred later, as at Hurlstone Point. The development of the flora at both these experimental sites was not paralleled by settlement of algae on the rest of the shore, and must therefore be attributed to lack of grazing activity by Patella.

In contrast, the experimental and control areas at the two estuarine sites did not produce such striking results. Apart from an increase in diatom cover (not evident from Figure 7

666 C. Little s L. P. Smith

because the cover remained within abundance 4), there were no significant changes in the flora at Portishead until the autumn of 1979, at which time a dense settlement of Fucus sporetings was recorded. Settlement was apparent in both experimental and control areas, but there was greater survival of the settled sporelings in the llmpet-free area. At the time of the Fucus settlement an increase in the green alga Enteromorpha bztestinalis was also recorded.

At Sand Point there was a resident flora when the area was originally cleared of limpets, and the cover of this had increased--together with the addition of some Fucus and Porphyra sporelings--by late 1978. Similar settlement was, however, also observed outside the experimental area. There was no further settlement of algae (although an increase in the size of those already present caused an increase in percentage cover by February 1979) until September 1979. At this time a further settlement of Fucus sporelings occurred, but once again this was also recorded outside the experimental area.

Conclusions The clearance experiments at Porlock produced a succession typical of those described for marine rocky shores: settlement of green algae and Porphyra was followed or accompanied by settlement of fucoids. At the estuarine sites no equivalent settlement of green algae took place, and, although fucoids did settle, their settlement was not only patchy and much delayed, but was recorded outside the limpet-free areas as well as within them. Since the limpet biomass at the estuarine sites was equivalent to that at the marine sites (Table 3), it appears that the grazers were less active in the estuary. The reasons for lack of algal re-colonization of the bare mid-shore at Portishead therefore appear to be linked to factors which affect the biology of both the algae and the giazers. These factors are further considered in the Discussion.

Discussion

Several peculiarities of vertical zonation in the Severn estuary can be attributed to the effects of physical and chemical variables. Decrease in exposure towards the head of the estuary appears to be at least partly responsible for the decrease in the upper vertical limit of ,animal species, but has no obvious direct effect upon algal distribution. Silt levels probably act mainly in combination with the effects of tidal scour, and prevent the colonization by macro-algae of levels at MLWS and below. Silt may also aid scour at MTL, where current flow is greatest, and the mass removal of algae from M T L may be due to this effect. The influence of salinity, however, appears to be upon horizontal distribution along the estuary and not upon vertical distribution. Desiccation on the upper shore increases in the upper estuary because of the decrease in exposure and possibly because of the asymmetry of the tide curve. In some years it can have serious effects upon algal survival.

The experiments in which grazers were removed have suggested that grazing effects are very different in the estuary from those on marine shores. The results at Porlock are in accordance with most others recorded after removal of grazers from purely marine habitats such as those of Jones (1948), Lodge (I948), Jones &. Kain (1967) and Southward (I964; 1978 ). At Sand Point and Portishead, in contrast, removal of grazers was not followed by any settlement of green algae, and the settlement of fucoids was much delayed. I t appears also that the limpets were not as effective in removing sporelings as they were in marine conditions. There appear to be few observations in the literature which report a lack of effect of grazers on the flora. The work of Raffaelli (1979) in New Zealand showed that at one site the removal of grazers had no effect upon algal diversity, ,and this was attributed to the harsh

Vertical .7onation on rocky shores 667

conditions of the physical environment. This argument cannot apply to the Severn, where at times macro-algae can flourish in the mid shore. In any case, settlement of fucoids has been observed in the Severn, both in areas containing limpets and in those without. The factors which underlie algal colonisation in the Severn can therefore only be understood when two approaches are combined: the differences in the biology of grazers inside the estuary and outside must be assessed; and the factors affecting algal reproduction, settlement and growth in the estuary must be known. We are not yet in a position to be able to make final conclusions on these two subjects, but some preliminary considerations can be made.

Limpet biology. Over the five months April-August x979, it appeared that the limpets at Hurlstone Point were much more mobile than those in the estuary. During this period, 48 individuals were taken from the i m ~ quadrat, compared with xo at Sand Point and only one at Portlshead. The initial density and biomass of limpets differed somewhat at the four sites, with more limpets of smaller size at Hurlstone Point (see Table z); but this difference does not seem large enough to explain the enormous apparent difference in mobility. Two explanations may be suggested. The first is that the Old Red Sandstone at Porlock is very hard and smooth compared with the jagged Carboniferous limestone at Portishead; this may affect homing, since it is not possible for the limpets to form scars at Hurlstone Point. Several authors have commented upon the fact that Patella shows most movement on smooth rock (Orton, x9z9; Jones, x948; Lewis & Bowman, x975). The second point concerns food supply. At Portishead there was usually a thick layer of diatoms covering the rock except in high summer; the feeding areas of Patella were often clearly defined and left large ungrazed areas between individuals. At Hurlstone Point, in contrast, the rock was normally devoid of obvious diatom cover. At the estuarine sites, therefore, it may be that algal settlement can, at some times of year, occur in the presence of limpets because these can obtain an adequate food supply almost without moving. If this is the case, potential settlement of algae must often be determined by factors which more directly affect the reproductive biology of the algal species concerned.

Algal reproductive biology. Although estuarine algal populations have in some cases been shown to have a high incidence of asexual reproduction (Russell, x97z), sexual reproduction of fucold algae has been observed throughout the Severn estuary (Smith, x978 ). Salinity is known to affect the onset of reproduction of some marine algae in estuaries (Russell, z97z), and it must be admitted that the production of viable spores/gametes has not been ascertained. The importance of understanding the effects of environmental variables on the settlement of spores has been stressed by many workers (e.g. Charters et al.., x973). It is possible that fluctuations in the production of viable spores could affect successful settlement. Spore density has been shown to affect settlement of algae (Hruby & Norton, r979). The reproductive season of fucoids is known to vary with locality (Rees, x93z; Knight & Parke, x95o; Blaekler, i956 ) and this may also be further affected by an estuarine r~gime.

Even if there is abundant production of viable spores, successful settlement is not guaranteed. Fucus eggs are free floating, once released, until they are fertilized. The zygote then quickly settles on the shore where, if conditions are favourable, it adheres and rapidly germinates (Hardy & Moss, I979). Silt inhibits the settlement of spores in Himanthalia (Moss et aL, z973), but it is not known if Fucus is affected. Thick diatom films may affect Fucus, since Sehonbeck & Norton (x979) have shown that, in culture, diatoms inhibit the growth and survival of germlings of Fucus spiralis. It may be, then, that some clearance of diatom films by Patella is necessary before ~'uctts can settle.

668 C. Little & L. P. Smith

Growth and development of spores subsequent to settlement are dependent upon several factors. Density of spore settlement helps to protect the young colony, but may also have the inhibitory effect of over-crowding. The resistance of young algae to desiccation and exposure is often different from that of older plants. For example, young ttscophylhtm plants only establish successfully under a canopy of Fucus spp. (Burrows, x948 ), and certain Fucus spp. are known to establish more successfully when there is a good growth of filamentous green

algae (Lodge, i948 ). The two points which are likely to be the critical ones determining the reeolonlzation of

bare rock in the Severn are therefore the viability of spores, both over the yearly cycle and from year to year; and the physical factors which affect the settlement of Fucus spores. An examination of these two aspects is essential to art understanding of algal colonization and succession.

Acknowledgements

Part of the initial survey work reported in this paper involved the help of students from Bristol University. In addition to them, we would like to thank Ms P. E. Stirling) ~Iiss C. S. Blow and Miss N. ~I. Ford for considerable help in the experimental investigations involving limpet removal. The survey of physical and chemical factors was planned in collaboration with Dr C. blettam, and we are grateful to him and to Dr A. E. Dorey, Dr D. J. Patterson, Dr R. ~f. Crawford, Mrs A. J. Williams, Mr D. Home, Dr D. G. ~Iann and Miss L. A. Edgar for assisting us by taking samples. During part of the study, L. P. S. was supported by a N.E.R.C. research grant.

Finally, we would like to acknowledge our indebtedness to the late Dr C. R. Boyden, who often assisted us in the early stages of the work, and to whom this paper is dedicated.

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