Primary Research Paper

Spatial patchiness of epilithic biofilm caused by refuge-inhabiting high shore

gastropods

Richard Stafford1,2,* & Mark S. Davies11Ecology CentreUniversity of Sunderland, SR1 3SD, Sunderland, UK2Present address: School of Biology, Ridley Building, University of Newcastle upon Tyne, NE1 7RU, Newcastle upon

Tyne, UK(*Author for correspondence: Tel.: +44-(0)191-222 7820; E-mail: richard.stafford@ncl.ac.uk)

Received 9 September 2004; in revised form 3 March 2005; accepted 5 March 2005

Key words: Melarhaphe neritoides, Littorina saxatilis, epilithic biofilm, grazing halo, spatial patchiness

Abstract

Aggregations of Melarhaphe neritoides and Littorina saxatilis are common on the high shore in north-eastEngland. These aggregations are frequently found in crevices which act as a refuge from desiccation. Theaggregations are surrounded by patches of epilithic biofilm which are visibly lighter in colour than thebiofilm present on the remainder of the high shore. Chlorophyll a levels were lower in regions of closeproximity to aggregated littorinids (mean=4.9 lg cm)2) as compared to areas >5 cm away from the edgeof the visible colour change (mean=15.9 lg cm)2). Manipulations of littorinid density showed that areasof high density had significantly lower levels of chlorophyll a than those where littorinids were excluded.This difference was mainly due to the presence of higher numbers of small grazed areas or an increase in sizeof grazed areas rather than a homogenous change in chlorophyll a levels across the entire manipulated area.These results are supported by observations showing that only 7% of the total foraging time of littorinidswas spent outside visibly lighter patches of biofilm suggesting littorinids only control local biofilm levelsthrough grazing.

Introduction

The abundance of epilithic biofilm on rockyshores is regulated by a combination of physicalfactors, growth, recruitment and grazing (-Underwood & Denley, 1984; Menge & Suther-land, 1987; Underwood & Jernakoff, 1984) Theimportance of gastropod grazing on biofilmregulation has been extensively studied (reviewedby Underwood, 1979; Hawkins & Hartnoll,1983; Norton et al., 1990). However, most ofthis work has concentrated on the mid to lowshore where grazer biomass and grazer diversityare often greater than higher on the shore. Formarine grazers occupying the high shore, theperiods in which foraging can take place are

limited to during wave splash and immersion byspring tides (Little, 1989; Stafford, 2002). Thishas lead to hypotheses predicting that in con-trolling the distribution and abundance of bio-film the importance of biotic factors, includinggrazing, decreases with increasing shore height(Connell, 1972; Underwood, 1979). Despite this,numerous studies have shown that grazing onthe high shore can play a significant role in theregulation of the biofilm (Nicotri, 1977; Branch& Branch, 1981; Mak & Williams, 1999; Kaehler& Froneman, 2002; Thompson et al., 2004).

Littorinid gastropods are the most commongrazers high on rocky intertidal shores (Stephenson& Stephenson, 1972; McMahon, 1990). Two highshore species are found throughout most of

Hydrobiologia (2005) 545:279–287 � Springer 2005DOI 10.1007/s10750-005-3320-5

Britain: Littorina saxatilis (Olivi) and Melarhapheneritoides (L.) (Fretter & Graham, 1994; see Reid,1996 for revised taxonomy of the L. saxatilisspecies complex). M. neritoides generally reacheshigher levels on the shore but the vertical distri-bution of the two species overlaps (Fretter &Graham, 1994). Both species of littorinid feed onthe epilithic biofilm (Norton et al., 1990) which is ablack/green covering of the rock, mainly consistingof the lichen Verrucaria maura (Fletcher, 1980;personal observations), and preferentially inhabitcrevices when inactive at low water, often formingdense aggregations (Emson & Faller-Fritsch, 1976;Raffaelli & Hughes, 1978). Grazing appears to beconcentrated around these aggregations in patchesof visibly reduced biofilm, herein referred to asgrazing halos, a few centimetres in diameter, centredon the aggregations (Hawkins & Hartnoll, 1983).Halos appear to be caused by grazers retreating to asafe position, such as a crevice or aggregation toavoid the risk of predation, desiccation or dis-lodgement during emersion (Menge, 1978; Garrity& Levings, 1983; Fairweather, 1988; Johnson et al.,1998; Jones & Boulding, 1999). This safe positionmay be more simple to relocate if the organism onlyforages a short distance away from it.

The presence of grazing halos appears to resultin a spatially patchy biofilm on the high shore,with some areas highly grazed and some with littleor no grazing. To determine accurately the meanbiofilm abundance of such an area would requirea high number of samples (Krebs, 1989). A pre-vious study into biofilm regulation by littorinidson the high shore in the UK used only a lownumber of samples and failed to detect any sig-nificant relationship between grazer pressure andbiofilm abundance (Mak, 1996). Here a highernumber of samples are used to more accuratelyassess the spatial patterns present on the highshore.

This study will investigate whether high shorelittorinids reduce their potential food intake toforage close to suitable refuges and will examinethe extent to which they regulate the biofilmpresent on the high shore. The following specifichypotheses will be tested:

1. Chlorophyll a will be significantly lower insidethe visibly lighter grazing halos than over theremainder of the high shore.

2. Grazers will spend a greater proportion oftheir foraging time within grazing halos thanoutside.

3. Grazing pressure does regulate biofilm densityand manipulations of grazer pressure will alterthe mean biofilm density present on the shore.

4. Grazing pressure influences the proportion ofthe shore covered by grazing halos and thisproportion will change with manipulations ofgrazer pressure.

Materials and methods

Site and study organisms

A disused harbour at Sunderland in north-eastEngland (grid reference: 54:54:22 N, 1:21:07 W)was used for the study. The high shore is man-madefrom concrete blocks forming a vertical surfacewith crevices and refuges formed by the erosion ofcement between the blocks and erosion of sandparticles on the face of the blocks. The surface ofthe rock is generally covered in an epilithic biofilmdominated by the lichen Verrucaria maura.Melarhaphe neritoides and Littorina saxatilis arecommon from �5 m above chart datum (+C.D.)with densities of �300 and �250 m)2, respectively.Although the density of littorinids was higher atthis site than the average shore in north-eastEngland the pattern of visible grazing halos wasclearly present on other natural and man madehigh shores (personal observations). The presentstudy was conducted at 5.6 m + C.D., the level ofmean high water spring tides (MHWS) betweenFebruary and July 2001, when the study wasundertaken.

Chlorophyll a levels within and outside of grazinghalos

Ten, approximately circular, visible grazing haloseach containing 10–20 littorinids were randomlyselected during February 2001. Each halo wascleared of all littorinids and the radius of the halomeasured as the maximum distance from thecentre to where a visible colour change in theepilithic biofilm occurred. Rock chips (<0.5 cm2)were taken from the centre of the grazing halos

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and at 25, 50, 75, 100 and 150% of the distance ofthe radius. Because the size of the halos varied itwas not possible to take replicate chips at the samedistances within each halo. Ten chips were alsotaken haphazardly from outside (>50 mm fromthe edge of the colour change) the grazing halos.Rock chip areas were determined from digitalphotographs using image analysis software (OSI-RIS 353, University of Geneva, Switzerland) andchlorophyll a levels were determined using the coldmethanol method (Nagarkar & Williams, 1997).Differences in chlorophyll a between differentdistances from the centre of the halo and outsideof the halo were compared using a single factorANOVA with the percentage distance from thecentre of the halo a fixed factor.

The proportion of littorinid foraging activitywithin halos

In order to determine the foraging time spentwithin the grazing halo, ten halos containingbetween 8 and 11 littorinids in an approximateratio of fiveMelarhaphe neritoides to four Littorinasaxatilis were selected at 5.6 m + C.D. Freshseawater was sprayed at the littorinids to initiatemovement and spraying was continued for a periodof 2 h, approximately equal to the period of wet-ting during a high tide with moderate wave action(waves <1 m in height). The number of littorinidsleaving each halo and the proportion of time spentoutside the halo was recorded. Foraging intensitywas assumed to be equal per unit time both insideand outside halos as no large changes in the speedof littorinid movement were detected during theforaging period, suggesting that grazing occurredimmediately once the littorinid began moving.

Effects of manipulation of littorinid densityon chlorophyll a levels and the proportion of grazinghalos

Twenty five, 250 · 250 mm areas were randomlylocated along a horizontal transect at5.6 m + C.D. and cleared of littorinids. Noattempt was made to standardise the number ofhalos present in the areas or the topographiccomplexity of the areas. Fifteen of these areas,selected at random, had a border placed aroundthem to form an enclosure. The border comprised

silicon sealant with Gem organic snail repellent(Gem gardening, Lancashire, UK) imbedded intothe sealant. Melarhaphe neritoides and Littorinasaxatilis were unable to cross these borders inpreliminary laboratory and field experiments. Fiverandomly selected areas had half a border, madeup from two L-shaped sections in opposite cornersas a procedural control, and five areas were leftwithout borders (Open).

Littorinids of natural density (19 Melarhapheneritoides and 16 Littorina saxatilis) and approxi-mately mean size (M. neritoides �2.1 mm;L. saxatilis �2.8 mm in length) were placed withinfive randomly selected areas with borders to createenclosures of natural density (N.D. Enclosed).Natural densities of littorinids were also placed inthe open and half border areas (L-Barrier). Doublethe natural densities of littorinids (38 M. neritoidesand 32 L. saxatilis) were placed in five, randomlyselected areas (double density) and the fiveremaining areas were left empty of littorinids(Exclusion). All areas were sprayed with seawaterto stimulate movement of littorinids and sprayingwas continued for 2 h until all the littorinids hadfirmly attached to the rock surface. Some dis-lodgement of littorinids occurred over the first fewdays. Areas were checked daily and new littorinidsadded, when needed, to maintain densities. Den-sities remained relatively constant after five dayswith the maximum reduction in numbers being<10% in any individual area.

Experimental areas were checked weekly, afterdaily checks during the first week, and anypotential breaks or thin areas of the bordersrepaired. The study was conducted over 3 months,between March and May 2001. This study dura-tion was used as preliminary studies indicated thatareas of ungrazed bare rock (with biofilmremoved) would develop a biofilm visually indis-tinguishable to that present outside of grazinghalos after three months. At the end of the three-month period the experimental areas were digitallyphotographed and the percentage of visible graz-ing halos present for each area was calculatedusing an image analysis program (OSIRIS 353,University of Geneva). A single factor ANOVAwas conducted to investigate variation in thepercentage of grazing halos between treatments (afixed factor) to determine if the percentage ofvisibly lighter grazing halos varied with changes in

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littorinid density. Fifteen rock chips (<0.5 cm2)were also taken from each area. The positions ofthe rock chips were determined using random,computer generated coordinates. Chlorophyll awas extracted using the cold methanol method(Nagarkar & Williams, 1997). Variation in chlor-ophyll a levels between and within treatments werecompared using a nested ANOVA design withindividual rock chips as replicates from eachexperimental area and individual experimentalareas (a random factor) nested within treatmenttype (a fixed factor). Histograms of the frequencyof chips from each treatment type having differentchlorophyll a concentrations (rounded to thenearest lg cm)2) were plotted to investigate howthe spatial patchiness of the biofilm varied withmanipulations of littorinid density.

Results

Chlorophyll a levels within and outside of grazinghalos

Grazing halos examined in the study had a meandiameter of 62±16 (SD) mm, n = 10, and con-tained a mean of 13.2±4.4 (SD) littorinids,n=10. The variance of chlorophyll a was nothomogeneous between the different distances fromthe centre of the grazing halo (Cochran�sC=0.428, p<0.05) with the highest variancebelonging to the distance of 100% of the radius ofthe halo, possibly because these chips contained abiofilm both from inside and outside the halo

(S2=33.4 at 100% radius, as compared to a meanvariance of 11.5). Because both the number ofreplicate chips (10 per distance) and number ofdistances (7 groups) investigated is large theANOVA test is considered robust to the effects ofheterogeneity of variance (Underwood, 1997).Chlorophyll a levels were significantly lower withinthe grazing halos (distances of 0, 25, 50 and 75% ofradius) than open areas of rock (F6,63=23.41,p<0.001; Fig. 1). The levels immediately outsidethe halo, at 150% of the distance of the radius, werenot significantly different to those from the chipstaken>50 mm from the grazing halos. Chips takenat 100% of the radius distance (i.e. on the edge ofthe halo) showed a value of chlorophyll a signifi-cantly different those inside and outside the halo,with the mean value falling between the mean valueinside and outside of the halos (Fig. 1).

The proportion of littorinid foraging activitywithin halos

Most littorinids moved exclusively within the ha-los, however, in all but two halos at least one lit-torinid left the halo. A mean of 16.5%±7.6 (95%confidence interval) of littorinids per halo left ha-los at some point. Time spent moving variedgreatly between individuals. Some littorinids didnot move during the study, whereas others movedfor as little as 15 min and some for as long as 2.5 h(continuing to move after spraying of the haloshad stopped). The mean time spent moving out-side of grazing halos, for those littorinids thatmoved outside grazing halos, was 24.3% ± 11.0

Figure 1. Mean (±95% C.I. n=10) chlorophyll a levels of rock chips taken at relative distances of the visible radius of grazing halos.

Outside halo indicates chip taken >50 mm from the edge of a grazing halo. Asterisks represent homogeneous groups as tested by SNK

tests with p<0.05 for differences between groups (*=0, 25, 50 and 75 < **=100 < ***=150 and Outside).

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(95% confidence interval) of the individual�s totaltime in movement. Movement time outside grazinghalos as a percentage of the total movement timefor all littorinids associated with a halo was6.8%±1.3 (95% confidence interval).

Effects of manipulation of littorinid densityon chlorophyll a levels and the proportion of grazinghalos

Significant differences occurred in the percentageof grazing halos present in different treatments(Table 1). Exclusion areas had significantly higherpercentage of grazing halos than the L-Barrier,N.D. Enclosed, Open and double density areas. Inaddition the double density areas had a signifi-cantly higher percentage of grazing halos than anyof the natural density treatments.

Differences in chlorophyll a concentrationbetween treatments of different littorinid densityalso occurred (Table 2), however, there was nodifference between replicate areas of the sametreatment (Table 2). Differences between naturaldensity treatments (Open, N.D. Enclosed andL-Barrier) did not occur, but chlorophyll a con-centration was significantly higher in the littorinidExclusion treatment compared to those of thedouble density and the Open control treatments.

Since there were no significant differences betweenreplicate areas nested in treatments the factor canbe pooled, which may increase the power of boththe ANOVA and SNK tests (Table 2). Pooling the�treatment� factor lowered the error mean squareestimate from 29.25 to 28.99 giving F4,370 = 3.91,p=0.004 for the factor �treatment�. The reductionin the mean square estimate, however, was notsufficient to modify the result of the SNK tests.

In treatments with grazers present the distribu-tion of biofilm (measured using chlorophyll a) wasbimodal withmode values between 4–7 lg cm)2 and14–19 lg cm)2 (Fig. 2). The peak in the distributionrepresented by lower chlorophyll a values was morepronounced for the double density treatment (with31% of chips having a chlorophyll a concentration<7.5 lg cm)2) than for the natural density treat-ments (L-Barrier 19%, Natural Density Enclosed19%, Open 16% of chips having <7.5 lg cm)2 ofchlorophyll a). The exclusion treatment showed apossible multimodal distribution but the peak in thedistribution represented by lower chlorophyll a val-ueswasmuch less pronouncedwith only 5%of chipshaving <7.5 lg cm)2 of chlorophyll a.

Discussion

Chlorophyll a concentration was much lowerwithin grazing halos, and outside of the visibleboundaries of the halos chlorophyll a levels

Table 1. ANOVA to investigate variation in the percentage

area of grazing halos with different treatments of littorinid

density

d.f. SS MS F p

Treatment 4 1338.2 334.5 23.4 <0.001

Error 20 286.0 14.3

Total 24 1624.2

S.N.K. tests

Exclusion L-Barrier N.D.

Enclosed

Open Double

Density

(3.4) (15.6) (17.4) (20.4) (25.4)

Unbroken lines show no significant differences in mean values

(shown in brackets) of the treatments as defined by SNK tests.

Exclusion = all littorinids removed and exclusion barriers put

in place, L-barrier = natural density of littorinids with two

corners of exclusion barrier present, N.D. enclosed = natural

density of littorinids but enclosed by a full barrier,

Open = natural density of littorinids and no barrier, double

density = twice the natural density enclosed by a full barrier.

Cochran�s Test C = 0.249 not significant.

Table 2. ANOVA to investigate variation in the standing stock

of chlorophyll a between treatments and between replicate

treatments (Areas)

d.f. SS MS F p

Treatment 4 453.1238 113.2809 4.66 0.0081

Area

(Treatment)

20 486.6381 24.3319 0.83 0.6745

Error 350 10238.7230 29.2535

Total 374 11178.4849

S.N.K. tests

Exclusion N.D.

Enclosed

L-Barrier Open Double

Density

(15.9) (14.2) (14.0) (13.7) (12.5)

Unbroken lines show no significant differences in mean values

(in lg cm)2, shown in brackets) of the treatments as defined by

SNK tests. Details of treatment types are given in the text or

legend to Table 1. Cochran�s Test C = 0.063 not significant.

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increase significantly within distances of a fewcentimetres. The percentage of littorinids movingoutside of the boundaries of the grazing halowhilst foraging were small and these foragingpatterns resulted in a spatially patchy distribution

of primary producers on the high shore. Spatiallypatchy patterns of littorinids and epilithic biofilmhave previously been identified, e.g. for UK lit-torinids (Hawkins & Hartnoll, 1983) and for highshore littorinids in Australia (Branch & Branch,

Figure 2. The frequency of rock chips with different values of chlorophyll a taken from experimental areas with different littorinid

density treatments. Exclusion = all littorinids removed and exclusion barriers put in place, L-barrier = natural density of littorinids

with two corners of exclusion barrier present, N.D. enclosed = natural density of littorinids but enclosed by a full barrier,

Open = natural density of littorinids and no barrier, double density = twice the natural density enclosed by a full barrier. n = 75 for

each treatment.

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1981). Similar patterns also exist in other com-munities (e.g. grazing halos around urchins,Benedetticecchi & Cinelli, 1995, and predationhalos around dog whelks Menge, 1978; Johnsonet al., 1998). All these examples are related by thefact that the centre of the halo contains a refugefor the organism to protect itself against physicalstress or predation. If littorinids organised theirforaging so as to maximise food intake then theyshould forage primarily outside of the halo as thiswould allow a greater intake of food per unit timeor radula rasp (Chelazzi et al., 1994). Melarharpheneritoides has been shown to move an averagedistance of 255 mm in 75 min on artificial sub-stratum suggesting it could move to the edge of thehalo to begin grazing and return to the centre ofthe halo within its foraging time (Stafford, 2002).They do not, however, operate such a strategy,appearing to begin grazing as soon as movement isinitiated as no change in speed of movement isnoticed during the course of a foraging excursion(personal observations). It is possible that the lit-torinids may consume all the food they require byforaging solely within the grazing halos, as thechlorophyll a analysis clearly demonstrates thatfood is present within the halo. Further workmeasuring growth rates of littorinids feeding insidehalos and outside halos or work on gut contents ofthe littorinids feeding on different densities of foodwould be necessary to test this hypothesis. How-ever, this study demonstrates that the benefits ofbeing able to locate a crevice or aggregation ofother individuals to reduce physical stress duringemersion or to reduce the chance of predation ismore important than the potential maximisationof food intake for these organisms.

Manipulation of littorinid density affects theproportion of grazing halos present supporting thehypothesis that grazing by littorinids does controlbiofilm on the shore. Increases in littorinid densityresulted in a greater total area of the shore beingcovered by grazing halos and the mean density ofbiofilm, as measured by chlorophyll a concentra-tion, being reduced. Similarly, excluding littorinidsresulted in a significantly smaller area of the shorebeing covered by grazing halos and a higher meanchlorophyll a level. The changes in chlorophyll awith littorinid density appeared to be mainly be-cause of the change in the area covered by grazinghalos rather than because of a homogeneous de-

crease in chlorophyll a. This can be seen from thefrequency of chips collected from different valuesof chlorophyll a. In all treatments most chips hadchlorophyll a values between 13 and 19 lg cm)2,however, as grazer density increased from zero tonatural density and double density the percentageof chips with these values fell and the percentage ofchips with chlorophyll a values <7.5 lg cm)2

rose. The lower chlorophyll a values are in therange of values found from chips inside grazinghalos and it is likely that it is the increase in fre-quency of chips taken from inside halos thatreduces the overall mean value of chlorophyll a intreatments with higher grazer density.

The results of this study show conformity withmost previous work on littorinid grazing, showingan increase in standing stock of biofilm with areduction of the littorinid number (e.g. Branch &Branch, 1981; Potter & Schleyer, 1991; Kaehler &Froneman, 2002; Thompson et al., 2004). Mak(1996), however, did not show any significantrelationship between standing stock of biofilm andhigh shore littorinid density in the UK. His studytook a single rock chip from each of grazed areasand exclusion areas at a given time. If rock chipsdid not fall within a grazing halo then it would belikely that little difference in standing stock ofbiofilm would occur between the grazed andungrazed treatments and significant differenceswould be unlikely to occur. The same experimentaldesign, using a single rock chip from each littorinidexclusion or inclusion area, however, has been usedto demonstrate significant differences in biofilmstanding stock on shores in Hong Kong (Mak &Williams, 1999). This may indicate that the spatialvariability of biofilm standing stock in Hong Kongis far lower than in north-east England.

Even when double the natural density of lit-torinids were placed in experimental areas on theshore, only one quarter of the treatment area wascovered by grazing halos and little change in thestanding stock of biofilm outside the halosoccurred. As such the results suggest that littorinidsare only able to locally control the high shorebiofilm (over distances of centimetres) in north-eastEngland. The results of the current study indicatethat a far greater littorinid density could be sup-ported by the food available, but that refuges are soimportant to these organisms that large areas ofshore are unexploited by them.

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Acknowledgements

We would like to thank Dr Gray Williams andpast and present staff and students at the HardRock Marine Laboratory (University of HongKong) and the anonymous referees for commentson the manuscript. This work was supported by aUniversity of Sunderland studentship to R.S.

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