grazing dynamics in intertidal rockpools: connectivity of microhabitats

Journal of Experimental Marine Biology and Ecology 370 (2009) 9–17

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Journal of Experimental Marine Biology and Ecology

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Grazing dynamics in intertidal rockpools: Connectivity of microhabitats

Laure M.-L.J. Noël a,b,⁎, Steve J. Hawkins a,d, Stuart R. Jenkins a,c, Richard C. Thompson b

a The Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UKb Marine Biology and Ecology Research Centre, School of Biological Sciences, Marine Institute, University of Plymouth, Plymouth, PL4 8AA, UKc School of Ocean Sciences, University of Wales, Bangor, Menai Bridge, Anglesey, LL59 5AB, UKd College of Natural Sciences, University of Wales, Bangor, Gwynedd, LL57 2UW, UK

⁎ Corresponding author. The Marine Biological AssocPlymouth, PL1 2PB, UK. Tel.: +44 1752 633332; fax: +44

E-mail address: [email protected] (L.M.-L.J. Noël)

0022-0981/$ – see front matter © 2008 Elsevier B.V. Aldoi:10.1016/j.jembe.2008.11.005

a b s t r a c t
a r t i c l e i n f o
Article history:
Differences between rockp Received 6 February 2008Received in revised form 11 November 2008Accepted 18 November 2008
Keywords:Foraging behaviourHerbivoryPatellidsRocky intertidalTidepool

ool and emergent rock communities are often attributed to their contrastingphysical conditions. However, differences in grazing pressure between rockpools and open rock could alsoexert an important structuring role. Greater densities and/or the lack of tidal constraints on foraging mayallow grazing intensity to be greater in rockpools. Here, wax discs were deployed to compare grazingintensity between rockpool and emergent rock habitats at each of three tidal heights on a moderatelyexposed shore in SW England. Grazing intensity was then examined in relation to herbivore density. Grazingintensity in pools was twice that on emergent rock, despite a lower density of herbivores in the rockpools. Ofthese herbivores, patellid limpets are the dominant grazers on rocky shores throughout the NE Atlantic andare recognised to have a major role in structuring intertidal communities. Thus, subsequent experimentsfocussed on the influence of limpets in determining the differences in consumer pressure between rockpoolsand emergent rock. Three alternative explanations were considered: (1) the effect of continuous immersionon grazing intensity in rockpools; (2) differences in limpet species abundance between the two habitats; (3)movement of limpets from emergent rock into pools to feed. The level of grazing pressure exerted by Patellaulyssiponensis (Gmelin), the predominant species living constantly immersed in rockpools, was similar to thatof P. vulgata (Linnaeus) which is predominantly found on emergent rock. P. vulgata were observed movingfrom emergent rock into rockpools during high tide. Manipulative experiments confirmed that these foragingexcursions resulted in a 2-fold increase in grazing intensity in the pools. Grazing activity of P. vulgata inrockpools was not consistent between sites and may be influenced by differences in wave exposure and/orthe abundance of microbial resources. Elevated consumer pressure in rockpools may be an important factorinfluencing algal assemblages and probably explains the predominance of grazer resistant-species in thesepools.

© 2008 Elsevier B.V. All rights reserved.

1. Introduction

Rockpool habitats are markedly different from emergent freely-draining rock (Metaxas and Scheibling, 1993). Protection fromdesiccation by constant immersion is generally assumed to be themain controlling factor (Femino and Mathieson, 1980). As aconsequence, rockpools have been considered as distinct habitatsfrom the rest of the intertidal (e.g. Underwood, 1981). Connectivityof pools with the surrounding emergent rock and the influence ofmobile consumers on the rockpool ecosystems have not beenexamined (but see Delany et al., 2002). Although grazers can play animportant role in determining the composition and biomass of algalassemblages in pools (e.g. Lubchenco, 1982; Benedetti-Cecchi, 2000),

iation of the UK, Citadel Hill,1752 633102..

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little attention has been given to the level of grazing activity in thishabitat (but see Wai and Williams, 2006a).

Herbivores have an important role in structuring communitieson rocky shores (Benedetti-Cecchi, 2000) and their feeding patternsand behaviour have been extensively studied (Hawkins andHartnoll, 1983; Norton et al., 1990, for reviews). A range ofmolluscan grazers are present on rocky shores in the NE Atlanticincluding patellid limpets, littorinids and trochids. Littorinids andtrochids can be abundant and contribute to overall grazing pressure.However, manipulative experiments have indicated that theirinfluence in structuring macroalgal assemblages is relatively lowcompared to that of patellid limpets (e.g. Jenkins et al., 2005;Coleman et al., 2006). Limpets are the dominant grazers on theseshores (Hawkins and Hartnoll, 1983; Jenkins et al., 2005). Theytypically feed on microbial films of diatoms, cyanobacteria, andfilamentous algae by scraping the rock surface using deep radulastrokes and they can also remove macroalgal germlings, smallgastropods and barnacles from the substratum by bulldozing

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10 L.M.-L.J. Noël et al. / Journal of Experimental Marine Biology and Ecology 370 (2009) 9–17

(Hawkins et al., 1989; Hill and Hawkins, 1991). Limpets are alsoeffective consumers of macroalgae (e.g. Le Roux, 2005; Davies et al.,2007; Lorenzen, 2007). During their foraging excursions, limpetscomplete a loop centred on a resting point (home scar) (Hartnolland Wright, 1977; Evans and Williams, 1991). The timing of foragingactivity varies among localities in relation to the tidal (emersed/immersed) and day/night cycles (e.g. Little, 1989; Santini et al.,2004) and is dictated by a combination of endogenous rhythms andexogenous factors (e.g. Della Santina et al., 1994). Foraging activity ispartitioned in order to limit the risk of predation by starfish andcrabs at high water (Little et al., 1990; Williams et al., 1999),dislodgement by wave action during immersion (Hawkins andHartnoll, 1982), predation by birds at low tide (Coleman et al., 1999)and heat and desiccation stress during emersion (Branch, 1981).

One of the most common methods to determine the level ofconsumer pressure in intertidal habitats is to quantify grazer densityduring low tide. This may not accurately reflect grazing intensity(e.g. Forrest et al., 2001), since estimates of grazer abundance duringlow tide (when limpets are on their home scars) do not take intoaccount foraging excursions at high tide (e.g. Hutchinson andWilliams, 2003; Davies et al., 2006). An alternative and more directmethod of assessing grazing intensity relies on quantifying theradula scrapes left on the surface of wax discs placed flush with thesubstratum (Thompson et al., 1997; Forrest et al., 2001). These discsdo not affect the behaviour of limpets in the NE Atlantic as shownby video recordings for Patella vulgata (Jenkins et al., 2001) andobservations for P. ulyssiponensis (Jenkins, unpub. data, Hawkinset al., 1989; but see Hutchinson and Williams, 2003 for contrastingeffects with cellanid limpets in Hong Kong). Wax discs have beensuccessfully used to demonstrate spatial and temporal patterns inthe grazing activity of patellid limpets in Europe (e.g. Jenkins et al.,2001; Jenkins and Hartnoll, 2001) but failed to do so for the Asiaticcellanid limpets (Hutchinson and Williams, 2003).

The relative distribution of grazing pressure between rock-pools and emergent rocks has not previously been quantified.Most studies on limpet activity have been on emergent rock (seeHawkins and Hartnoll, 1983 for review) and the rockpoolenvironment has been relatively overlooked (but see Wai andWilliams, 2006a). It as been suggested that grazing intensity isgreater in rockpools than on emergent rock due to the ability ofgrazers to forage constantly in pools because these habitats arecontinuously submerged, and/or because of greater herbivoredensity in the pools (Dethier, 1982; Lubchenco, 1982; Chapman,1990). Limpet species distribution on rocky shores may also drivedifferences in grazing intensity between rockpools (where P.ulyssiponensis predominates) and emergent rock (where P.vulgata predominates) (Davies, 1969; Delany et al., 2002). Incontrast, trochids and littorinids do not appear to have markeddifferences in their distribution between pool and emergent rockhabitats (Underwood, 1973; Hawkins and Hartnoll, 1983).

The overall aim of this study was to test whether grazingintensity differed between rockpools and emergent rock habitatsand if so to investigate the possible causes of these patterns.Although rockpool and emergent rock habitats experiencediffering physical conditions (e.g. desiccation), developing ourunderstanding of the importance of grazing pressure can provideinsights into factors determining community structure of rock-pools (e.g. Wai and Williams, 2006b). Patellid limpets were themain focus of the present study because of their recognised keyrole in structuring assemblages on emergent rock. Limpet grazingactivity was examined in rockpools and on emergent rock usingthe indirect wax disc method of Thompson et al. (1997) togetherwith direct observations at both high and low tide. Possibleexplanations of the grazing patterns observed were examined:(1) differences in herbivore density; (2) the absence of tidalconstraints on limpet foraging in pools; (3) differences in limpet

species distribution between the two habitats and (4) move-ments of limpets from emergent rock into pools to feed there.

2. Material and methods

2.1. Study sites

Experimental work and direct observations were predominantlyconducted at Wembury Bay (Southwest England; 50° 18′ N, 4° 5′ W),which is a moderately exposed shore with flat and smooth slopingbedrock interrupted by rockpools and has assemblages typical ofshores in the NE Atlantic (Lewis, 1964). An additional site wasestablished at Downderry (50° 21′N, 4° 22′W), which is 32 kmwest ofWembury with similar bedrock and pools. The most commonherbivores at both sites are the limpets Patella vulgata, P. ulyssiponensisand P. depressa (Pennant), the topshells (named as such hereafter)including the trochids Gibbula umbilicalis (da Costa), Osilinus lineatus(da Costa), and the littorinids Littorina littorea (Linnaeus), L. obtusata(Linnaeus) and L. saxatilis (Olivi) (Lewis, 1964; Hawkins and Hartnoll,1983). P. ulyssiponensis is predominantly found in pools colonized bycalcareous encrusting coralline such as Phymatolithon spp. (Foslie)(Lewis, 1964; Fretter and Graham, 1976). Predators such as thedogwhelk Nucella lapillus (Linnaeus), the shore crab Carcinus maenas(Linnaeus) and, during low tide, the oystercatcher Haematopusostralegus, are also present at these locations.

2.2. Comparison of foraging activity between rockpools and emergentrock

To establish whether there are differences in grazing intensitybetween pools and emergent substrata and to test if grazing intensityis related to herbivore density, a multifactorial experiment was set upat Wembury. Six rockpools (depth 8-15 cm, surface area 0.35-1 m2)and six emergent rock areas were randomly selected at each of threeshore levels: high-shore (3 to 4 m above Chart Datum), mid-shore(1 to 3 m above Chart Datum) and low-shore (0.5 to 1 m above ChartDatum). An array of nine wax discs (diameter 14 mm, spacing:185 mm) was deployed in 3×3 organisation in haphazardly selectedareas of similar grazeable substrata (40×40 cm) in each pools and oneach area of emergent rock (n=6) (Thompson et al., 1997; Forrest et al.,2001). Wax disc holes were made with a drill bit long enough (60 cm)to avoid the need to empty the pools. Discs were deployed for periodsof 15 days every three months (from June 2002 to March 2003) toassess the patterns of grazing pressure through time. Previous work inSW England has shown a 2 week deployment to be appropriate andthat discs were not overgrazed in this time frame (Jenkins et al., 2001;Moore et al., 2007). The percentage area of each disc scraped byradulae was estimated under a dissecting microscope with the help ofa circular acetate grid with twenty-five evenly spaced holes. Allradular marks encountered under these holes were recorded and thepercentage cover of grazing marks estimated. To allow easierdistinction of the marks, a fine layer of printer toner powder wasapplied to the discs with a paint brush. Grazer density (limpet andtopshell) was recorded in three replicate 20×20 cm quadrats in eachpool and on each area of emergent rock at the time of each wax-discdeployment. Grazer density recorded using this approach wasconsidered representative of populations observed in the entirerockpool. This was tested by comparing limpet densities obtainedwith this protocol with total limpet counts from additional rockpools(n=4). These rockpools, sampled during the same time period(September), were selected for their similarity in location, size andshore height (high and low). No significant differences were foundbetween sampling approaches in both high and low shore (ANOVA,F1,12=2.58, PN0.05).

Estimates of total grazing intensity per experimental unit,including both limpets and topshells, were calculated over the areas

11L.M.-L.J. Noël et al. / Journal of Experimental Marine Biology and Ecology 370 (2009) 9–17

studied by averaging the percentage cover of grazing marks on thediscs deployed for each sampling date (rockpools and emergent rock,n=6). Cochran's test was used prior to analysis to check thehomoscedasticity of data and if necessary data were transformed(Winer, 1971). The influence of habitat (Rockpool and Emergent rock)and shore level (High, Mid and Low shore) on grazing intensity wasdetermined using a two factor ANOVA with both factors fixed andorthogonal on each sampling date. The influence of these factors ongrazer density was considered separately for the two main grazergroups (limpet, topshell) using an ANOVA with two fixed andorthogonal factors (habitat, shore level) at each sampling date.When there were significant differences (Pb0.05), post-hoc multiplecomparisons were undertaken using Student-Newman-Keuls tests(SNK) (Underwood, 1997). Analyses were carried out using WinG-MAV5 (EICC, University of Sydney). Pearson's correlation coefficientwas used to examine the relationship between grazer density andgrazing intensity using all of the data in each habitat (rockpools oremergent rock, n=72).

2.3. Role of limpets in determining differences in grazing intensitybetween rockpools and emergent rock

The grazing intensity of the species of limpets typically found inrockpools (Patella ulyssiponensis) and those typically found onemergent rock (P. vulgata) was compared on the upper shore only.Six replicate pools (for P. ulyssiponensis) and six replicate areas ofemergent rock (for P. vulgata)were randomly chosen. In each replicatearea, five similar-sized limpets (average length 42 mm±1 SE) of eachspecies were enclosed by fences in their respective environments(pools and emergent rocks). Fences were circular (perimeter: 2 m),made of L-folded wire mesh (diameter 13 mm) of 5 cm height andfixed on the rock with screws and washers. Holes were made with adrill bit long enough to avoid emptying the pools. Ten wax discs weredeployed in each fenced area for 15 days on each of two dates inwinter 2004 and summer 2005. The discs were evenly interspacedand their number increased from the previous experiment tomaintain

Fig. 1. Overall grazing intensity (%) in rockpools and on emergent rock at each of three shorpercentages of surface area scraped by limpets and topshells on nine replicate wax discs av

the same density of discs per surface of grazable substrata studied.Limpet grazing marks were counted in the laboratory to estimategrazing intensity. Grazing intensity was compared using an ANOVAwith three factors: species (P. ulyssiponensis, P. vulgata) and season(Winter, Summer) were fixed and orthogonal and trial (2 trials) wasrandom and nested within season.

Direct observationsweremade at high tide by snorkelling and at lowtide to establish spatial patterns of grazer distribution during immer-sion. These observations quantified any movement of limpets at hightide between pools and the surrounding rock that is emergent duringlow tide. At the beginning of September 2003, six rockpools wereselected on the upper shore (3-4mabove Chart Datum) to allow reliableobservations to be made by snorkelling during high neap tides. Thedensity of grazerswas recorded in three replicate 20×20 cmquadrats ineach habitat. Preliminary observations showed that no P. ulyssiponensismoved from the pools onto the emergent rock, but that P. vulgatamovedfrom the emergent rock into the pools, someasurements focused on thelatter. Quantitative observations of P. vulgata distribution were made ataround the time of highwater. Additional snorkelling observationsweremade throughout the high tide period to examine activity patterns oflimpets. During low tide, all P. vulgata situated on emergent rock within12.5 cm of the edges of the rockpools (86 limpets in total) were tagged(Helagrip PVC cable markers, HellermannTyton) using Subcoat S epoxy(Veneziani). Coding allowed the limpets to be identified and thepositions of their home scars in relation to the borders of the pools to berecorded. The border of the pools was defined as the limit of theencrusting Phymatolithon spp.. Two distance categories were definedbased on the average limpet's original home scar position in relation tothe pool border: ‘Close’ - those within 3.5 cm of the pool border (54limpets tagged for this category) and ‘Far’ - those between 3.5 and12.5 cm of the pool (32 limpets tagged for this category). Positions of P.vulgata, relative to theedgesof thepool,were recordedduringhighneaptides by snorkelling and during the following low tide on four dates bydaylight, and ononeoccasion at night. For eachobservation, the positionof each limpet wasmeasured by taking theminimum distance from thecentre of their shell to the edge of the Phymatolithon spp. which

e levels (High, Mid, Low) on four sampling occasions over a year. Data are mean (±SE)eraged per plot (n=6).

Table 12-way ANOVA comparing overall grazing intensity estimated in the two habitats (rockpool and emergent rock) at each of the three shore levels studied on each sampling occasion

June September December March

DF MS F P MS F P MS F P MS F P

Habitat (Ha) 1 3994 83.9 ⁎⁎⁎ 4980 1525 ⁎⁎⁎ 8012 178.4 ⁎⁎⁎ 9073 243.5 ⁎⁎⁎

Level (Le) 2 172.6 3.6 ⁎ 264.1 8.1 ⁎⁎ 23.5 0.5 0.5 73.7 1.9 nsHa×Le 2 35.8 0.75 ns 14.7 05 ns 143.3 3.2 3.2 25.3 0.7 nsResidual 30 47.6 32.6 44.9 37.3SNK (Le) High b Mid=Low Low b Mid=High

Habitat: Ha (Rockpool, Emergent rock); Shore level: Le (High, Mid, Low); (n=6). Data were ArcSin transformed. (Cochran's test non significant for each sampling occasion aftertransformation). ⁎⁎⁎: Pb0.001; ⁎⁎: Pb0.01; ⁎: Pb0.05; ns: non significant. SNK: “=”: factor levels of the same rank, “b”: factor levels with significant differences according to theirrank order (see Fig. 1).


demarked the pool boundary. Positive values were attributed to limpetsthat remained on emergent rock and negative values for those thatentered the rockpool. Limpetswere classified in three activity states: notmoving (Inactive), active on emergent rock (Active) and active enteringthe pool (Entering). The percentage of each activity state per rockpoolwas calculated for each tidal observation. For those entering the pool,proportions were compared using an ANOVA with two fixed andorthogonal factors: tide (High and Low tide), distance from the poolborder (Close and Far) for each of the sampling dates.

The extent to which movement of P. vulgata from the surroundingrock into pools could have caused greater grazing intensity withinpools was then examined experimentally over the intertidal gradient.Rockpools were fenced and compared to similar pools left open inorder to assess the net effect of limpet foraging excursions on grazingintensity due to (1) limpets moving into the pools, resulting in highergrazing levels in open pools; (2) limpets moving out of the pools,inducing elevated grazing in fenced pools or (3) at an equal rate ofentry and exit leading to similar grazing in both treatments. Sixrockpools of similar size (depth 8-15 cm, area 0.35-1 m2) andcommunity composition were randomly selected at each of three

Fig. 2. Limpet and topshell densities (m2) in rockpools and on emergent rock at each of threegrazer count (±SE) in three replicate 20×20 cm quadrats averaged per plot (n=6).

shore levels: high (3-4m above Chart Datum), mid (1-3 m above ChartDatum) and low (0.5-1 m above Chart Datum). At each shore level,three pools were fenced to block any movement of limpets into or outof the pools, and threewere left open to allow freemovement. Twentywax discs were deployed in each pool at the beginning of November2003 and left for 15 days. The discs were evenly interspaced and theirnumber set to cover the whole area of grazable surface present in thepools. Limpet density was recorded at low tide in each pool in threereplicate 20×20 cm quadrats. Limpet grazing intensity and densitywere compared using an ANOVA with two fixed and orthogonalfactors: shore level (High, Mid, Low), and fence (Open and Fencedpool). Topshell grazing was not considered as fences did not blocktheir movement.

A further experiment was conducted to confirm whether limpetsmoved into pools in order to graze. This experiment was set up atWembury and Downderry in order to examine the generality of theeffect. P. vulgata of similar biomass (length 34 mm±1 SE, dry weight0.27 g±0.03 SE) situated on emergent rock at the edge of six rockpoolswere selected at natural densities on the upper shore (6 P. vulgata±0.4SE per 25×25 cm) (see Moore et al., 2007 for method). They were

shore levels (High, Mid, Low) on four sampling occasions over a year. Data are mean of

Table 22-way ANOVA comparing limpet and topshell densities counted in the two habitats (rockpool and emergent rock) at each of the three shore levels studied in each sampling occasion

Limpet June September December March


Habitat (Ha) 1 447.8 59.42 ⁎⁎⁎ 334.5 97.09 ⁎⁎⁎ 440.5 82.12 ⁎⁎⁎ 776.1 161.8 ⁎⁎⁎

Level (Le) 2 80.88 10.06 ⁎⁎⁎ 73.84 21.43 ⁎⁎⁎ 82.75 15.43 ⁎⁎⁎ 46.62 9.72 ⁎⁎⁎

Ha×Le 2 35.57 4.42 ⁎ 12.72 3.69 ⁎ 15.01 2.8 ns 5.18 1.08 nsResidual 30 8.04 3.44 5.36 4.80SNK (Ha×Le) (Ha×Le) Le Le

High: In=Out High: In b Out Low b High b Mid High=Mid b LowMid: In b Out Mid: In b OutLow: In b Out Low: In b Out

Topshell June September December March


Habitat (Ha) 1 326.2 55.04 ⁎⁎⁎ 484.3 143.2 ⁎⁎⁎ 166.7 31.62 ⁎⁎⁎ 153.6 33.20 ⁎⁎⁎

Level (Le) 2 12.82 2.16 ns 60.15 17.79 ⁎⁎⁎ 62.72 11.90 ⁎⁎⁎ 27.92 6.04 ⁎⁎

Ha×Le 2 0.31 0.05 ns 4.25 1.26 ns 92.30 17.51 ⁎⁎⁎ 46.53 10.06 ⁎⁎⁎

Residual 30 5.93 3.38 5.27 4.63SNK Le (Ha×Le) (Ha×Le)

Low=High N Mid High: In b Out High: In b OutMid: In b Out Mid: In b OutLow: In=Out Low: In=Out

Habitat: Ha (In: inside pool, Out: emergent rock); Shore level: Le (High,Mid, Low); (n=6). Datawere square root transformed. (Cochran's test non significant after transformation). ⁎⁎⁎:Pb0.001; ⁎⁎: Pb0.01; ⁎: Pb0.05; ns: non significant. SNK: “=”: factor levels of the same rank, “b” or “N”: factor levelswith significant differences according to their rank order (see Fig. 2).


enclosed (perimeter: 1 m) such that fences covered an area half in thepool and half on the emergent rock and that limpets were located atthe interface between these two habitats. Other grazers were removedfromwithin the fenced areas. An array of nine wax discs was deployedin each sector of these cages (pool or emergent rock), for 15 days oneach of three replicate dates in summer 2005. Grazing intensityrecorded on the discs was used to compare habitat feedingpreferences between pools and emergent rock using an ANOVA withthree orthogonal factors: habitat (Rockpool and Emergent rock) wasfixed, site (Downderry, Wembury) and trial (3 trial periods) were bothrandom.

3. Results

3.1. Comparison of grazing intensity between rockpools and emergentrock

Grazing intensity was significantly greater in rockpools than onemergent rock (Fig. 1). This pattern was consistent on all samplingoccasions and across all three tidal heights (Table 1). Overall grazing inrockpools was twice that on emergent rock with an annual mean of83%±3 SE in pools compared to 42%±4 SE on emergent rock. Limpetgrazingmarks were often from a single individual. They never covered

Fig. 3. Patella vulgata activity at the edges of rockpools and inside high shore pools during connot moving (Inact.), active on emergent rock (Act.), active and entering in the rockpool (Ent.home scar within 3.5 cm of the pool border; “Far”: limpet home scar 3.5-12.5 cm from the

more than 50% of the discs surface and were rarely seen overlapping.On some occasions, topshell radulae marks were recorded covering upto 60% of the discs and some overlapping marks suggested there mayhave been a small underestimation in grazing intensity for thisspecies.

There was no correlation between total grazer density and totalgrazing intensity in rockpools or on emergent rock (rockpools: r=0.22,PN0.05; emergent rock: r=-0.06, PN0.05). In general, the total grazerdensity (including limpets and topshells) was greater on emergentrock than in rockpools on all sampling dates, except September(Fig. 2). Limpets were significantly more abundant on emergent rockat all shore levels and on all sampling occasions, except on thesampling date of June on the high shore where equal numbers oflimpets were recorded in each habitat (Table 2, Fig. 2). The density oftopshells varied between sampling dates. In June and September,topshells were significantlymore abundant in pools than on emergentrock (Table 2, Fig. 2). This pattern was reversed in December andMarchwith significantly lower density in pools than on emergent rockexcept on the low shore where densities were equal (Table 2, Fig. 2). Insummary, the overall grazing intensity was twice as high in rockpoolscompared to emergent rock. The overall grazer density was sig-nificantly greater on emergent rock than in pools (except for oneoccasion) and was not correlated with grazing intensity.

secutive high and low tides at day and night. Limpets were classified in three categories:). Data are mean of percentage (±SE) of estimated limpet activity (n=6). “Close”: limpetedge of the pool.

Table 32-way ANOVA comparing position of limpets entering the rockpools between high tide and low tide according to their initial distance from the pool borders

Day 1 Day 2 Day 3 Day 4 Night

DF MS F P MS F P MS F P MS F P MS F P

Tide (Ti) 1 1193 9.01 ⁎⁎ 443.5 4.61 ⁎ 917.1 9.25 ⁎⁎ 826 14.6 ⁎⁎ 286.4 5.56 ⁎

Distance (Di) 1 405.5 3.06 ns 17.49 0.18 ns 25.42 0.26 ns 320.2 5.27 ⁎ 80.53 1.56 nsTi×Di 1 405.5 3.06 ns 17.49 0.18 ns 25.42 0.26 ns 320.2 5.27 ⁎ 80.53 1.56 nsResidual 20 132.4 96.18 99.15 56.47 51.53SNK Day 4 (Ti xDi) High tide: Close N Far, Low tide: Close = Far

Tide: Ti (High tide, Low tide); Distance from the pool border: Di (Close, Far); (n=6). Data were ArcSin transformed. (Cochran's test still significant after transformation except for Day4). ⁎⁎: Pb0.01; ⁎: Pb0.05; ns: non significant. SNK: “=”: factor levels of the same rank, “N”: factor levels with significant differences according to their rank order (see Fig. 3).


3.2. Role of limpets in determining differences in grazing intensitybetween rockpools and emergent rock

The experiment that examined the grazing activity of the twomainlimpet species showed that there was no difference in grazingpressure exerted by Patella ulyssiponensis in rockpools and P. vulgataon emergent rock. This effect was consistent across all samplingoccasions with no interactions with seasons nor trial dates (ANOVA,F1,40=2.92, non significant).

During snorkellingobservations, a small number of P. vulgata (10%±2SE)were recordedmoving fromemergent rock into the pools during dayand night time high tide (Fig. 3). This movement increased the limpetdensity in the pool by around 7%±1 SE at the time of the observation.This pattern was significant and occurred regardless of initial distancesof P. vulgata from the pool edge (Close or Far) for most of the samplingdates except for day 4 where more P. vulgata close to the pool borderentered the pools (Table 3). P. vulgata was seen entering the poolsrapidly during theflooding tideanddeparting just before the ebbing tideuncovered thepools.Noneof the tagged limpetswere observed enteringthe rockpools during low tide (Fig. 3). A similar patternwas observed atnight although samplingwas only possible on one occasion so itwas notpossible to generalise from this result (Fig. 3). For those limpets that didnot enter pools, the percentage of P. vulgata away from their home scar(Active) or inactive were similar between high and low tide except forlimpets situated far from the pool (Fig. 3). P. vulgata far from the poolwere less active at low tide during both day and night and were mostactive at high tide especially during night time (Fig. 3). P. ulyssiponensiswas never observed leaving the pools during the snorkellingobservations.

The experiment that examined the influence of limpet movementon grazing activity in rockpools confirmed that grazing intensity wassignificantly greater in openpools than fenced ones (Fig. 4 and Table 4).There were no differences in limpet density between fenced and opentreatments during low water observations (Table 4). This result wasin agreement with snorkelling observations indicating movement ofP. vulgata from the emergent substrata into the pool occurring at hightide only. This limpet movement significantly increased grazing

Fig. 4. Limpet grazing intensity (%) and density (m2) in fenced (Fence) and non-fenced (Openscraped wax disc area (±SE) and mean of limpet count (±SE) in three replicate 20×20 cm q

pressure in pools left open compared to fenced ones with a 5-foldincrease on the upper shore, a 1.25-fold increase on themid shore and a2-fold increase in lower shore (Fig. 4). Overall grazing intensity fromlimpets (in fenced and open pools) was greater on the mid and lowershore than the upper shore (Table 4, SNK). Limpet density was greatestat the mid shore level (Table 4, SNK).

Comparisons of the limpet feeding preference between emergentrock and rockpools showed that at both Wembury and Downderry, P.vulgatawith home scars at the edge of pools moved inside the pools tograze (Fig. 5). However, there were differences between these shoresas indicated by the significant interaction between the sites andhabitats (Table 5). At Wembury, there was a trend of preferentialgrazing inside pools shown by a significant increase in grazingintensity (Table 5, SNK, Fig. 5). At Downderry, grazing activity wassignificantly greater on emergent substrata (Table 5, SNK, Fig. 5).Although limpet biomass was selected to be similar between shores,individual P. vulgata sizes were smaller at Downderry and as aconsequence more limpets were enclosed than at Wembury (ANOVA,F1,60=53.4, Pb0.001). This difference may have been responsible forthe lower grazing intensity at Downderry (Fig. 5).

4. Discussion

Grazing intensity in rockpools was twice that recorded on emergentsubstrata, despite a lowerdensity of herbivores in the pools. This greatergrazing intensity in rockpools was not caused by differences in grazerabundance or by species-specific differences in grazing activity (Patellaulyssiponensis vs P. vulgata) between the two habitats. However, therewas a small but consistent movement of limpets into the pools at hightide which significantly increased the amount of grazing in the pools.These observations confirm the speculations of Lubchenco (1982) andDethier (1982) regarding the balance of grazing pressure between thetwo habitats, but contrast with the predictions of Lubchenco (1982) of apositive relationship between the density of grazers and grazingintensity, both inside pools and on emergent rock.

Grazing pressure was similar between P. ulyssiponensis and P.vulgata when measured in the habitats they predominate, rockpools

) rockpools at each of three shore levels (High, Mid, Low). Data are mean percentage ofuadrats averaged per pool (n=3).

Table 42-way ANOVA comparing limpet grazing activity and density in fenced and openrockpools at each of the three shore levels studied

Grazing Density

DF MS F P MS F P

Level(Le) 2 979.3 19.02 ⁎⁎⁎ 6909.72 20.59 ⁎⁎⁎

Fence (Fe) 1 354.19 6.88 ⁎ 61.72 0.18 nsLe x Fe 2 21.36 0.41 ns 281.63 0.84 nsResidual 12 51.49 335.64SNK(Le) Low = Mid N High Low = High b Mid

Fence treatment: Fe (Fenced, Open); Shore level: Le (High, Mid, Low); (n=3). Grazingdata were ArcSin transformed. (Cochran's test non significant after transformation).⁎⁎⁎: Pb0.001; ⁎: Pb0.05; ns: non significant. SNK: “=”: factor levels of the same rank, “b”or “N”: factor levels with significant differences according to their rank order (see Fig. 4).

Table 5ANOVA comparing the grazing preference for rockpools or emergent rock of P vulgatasituated at the pool border during three trials at the two shores studied

DF SS MS F P

Site (Si) 1 1310.07 1310.07 11.21 ⁎⁎

Habitat(Ha) 1 181.24 181.24 1.55 nsTrial(Tr) 2 56.71 28.36 0.24 nsSi×Ha 1 2414.72 2414.72 20.66 ⁎⁎⁎

Si×Tr 2 84.56 42.28 0.36 nsHa×Tr 2 91.67 45.84 0.39 nsSi×Ha×Tr 2 135.81 67.91 0.58 nsResidual 60 7011.65 116.86SNK (Si×Ha) Downderry: Pool b Emergent, Wembury: Pool N Emergent

Site: Si (Downderry, Wembury); Habitat: Ha (Rockpool: Pool, Emergent rock:Emergent); Trial: Tr (Trial 1, Trial 2, Trial 3); (n=6). (Cochran's test non significant).⁎⁎⁎: Pb0.001; ⁎⁎: Pb0.01; ns: non significant. SNK: “b”or “N”: factor levels withsignificant differences according to their rank order (see Fig. 5).


and emergent rock respectively. Constant immersion of limpets inrockpools might be expected to enhance their ability to forage(Dethier, 1982). Whilst no firm conclusions can be drawn on theinfluence of constant immersion on grazing intensity since no directcomparisonwasmade for either species, observations suggest that theextra time window provided by constant immersion was not utilisedfor foraging by P. ulyssiponensis. Snorkelling observations showed thatgrazing by P. ulyssiponensis was restricted to the pools during highwater. This restriction of foraging activity to high tide could beinfluenced by the threat of predation from oystercatchers and otherbirds previously observed feeding on Wembury shore (Coleman et al.,1999). Since the pools used in this study were relatively shallow,limpets may be at risk of predation from birds at low tide in both pooland emergent rock habitats. Given the distribution of limpet species,enhanced grazing in rockpools cannot be explained solely on the basisof lower desiccation stress due to constant immersion, or on thegrounds of differences in grazing intensity between species.

Limpet movement from emergent rock into pools at high tideincreased consumer pressure in the rockpool habitat. The entry of P.vulgata whose home scars were aggregated at pool edges occurredjust at the time of pool immersion and exit coincided with the fallingtide, which may act as a cue to return to their scars (e.g. Hawkins andHartnoll, 1983; Davies et al., 2006). This restriction of foraging to hightide is most likely a response to escape predation from birds (Colemanet al., 1999), and was previously reported in Plymouth (Orton, 1929)and at other locations (Hartnoll and Wright, 1977; Hawkins andHartnoll, 1983). When P. vulgata movement into pools was preventedby fences, the difference in grazing pressure compared with openpools was sufficient to explain why the grazing intensity in rockpoolswas twice that than on emergent rock. This was consistent at all threetidal levels examined. The increase in grazing intensity as aconsequence of P. vulgata migration at high tide was not consistentwith the small number of individuals observed moving into pools bysnorkelling (10% of total limpets aggregated around the pools at each

Fig. 5. Grazing intensity of Patella vulgata (%) situated at the edge of high shore levelrockpools showing grazing preferences either in pools or on emergent rock at two sites:Downderry andWembury. Data are mean percentage of wax disc area scraped (±SE) for9 wax discs averaged per rockpool or emergent rock plot (n=6).

high tide). Snorkelling observations corresponded to a snapshot of fewminutes of the foraging activity in the pools and probably under-estimated the number of P. vulgata entering the pools during hightide. When considered in relation to the time scale of the grazingintensity measurements (15 days), the number of limpets grazing inthe pools at high tide appears to have been sufficient to explain thehigher grazing intensity recorded in open pools compared to fencedones.

All P. vulgata recorded in pools at high tide, during the snorkellingobservations, returned to emergent rock on the falling tide. Adult P.vulgata can tolerate continual immersion in pools for at least 6 monthswithout mortality (Noël, 2007). Juvenile P. vulgata are often found inpools but they typicallymigrate out as they become adults (Delany et al.,2002). P. ulyssiponensis is considered aggressive compared to P. vulgataand interference competition has been observed between these species(Hawkins, pers. obs.). However, the relative absence of P. vulgata in poolsat low tide ismore likely explained at long-termbya lower physiologicaltolerance to fluctuating rockpool conditions when disconnected fromthe sea than by competition with P. ulyssiponensis (Firth and Crowe,2008). By remaining at the pool interface, P. vulgata appears to benefit tosome extent from protection against thermal stress because of theevaporative cooling effect of the pools (Williams andMorritt,1995). Thiswould be especially true on the upper shore which experiences thelongest emersion. At this shore level, limpet migration from the poolborder resulted in the greatest increase of grazing activity in the pools.The rockpool interfacemayalsooffer proximity to greatermicrobial-filmresources to feed on by protecting the pool biofilm from thermal andinsolation stress (Jenkins et al., 2001; Thompson et al., 2004). Biofilmsare recognised to influence limpet foraging (Mackay and Underwood,1977; Thompsonet al., 2004, 2005) anddifferences in qualityor quantityofmicrobial resources could influence thedistributionof grazing activitybetween pools and emergent rock. The substantially greater grazingactivity inpools, especially at the upper shore level, may inpart also be aconsequence of sparsermicrobial resources on emergent rock owning tosever physical conditions.

In terms of preferred foraging microhabitat by P. vulgata, thecontrasting results between Wembury and Downderry were unex-pected. Although both shores are moderately exposed, Wembury isprotected from wave action by an island, the Mewstone, just off shore.On emergent rock of moderately exposed shores, the abundance ofmicroalgae is higher than on sheltered ones (Thompson et al., 2005). P.vulgata is also known to spend more time foraging when exposed togreater wave action (Della Santina et al., 1994). At the slightly moresheltered site ofWembury, sparser food resources combinedwith lowerwave action could have induced P. vulgata to feed preferentially inrockpools. To confirm this, further investigations would be required tomeasure microalgal abundance in rockpools and on adjacent emergentrock and to compare grazing intensity in pools on both exposed andsheltered shores.


Grazing dynamics observed at the pool-emergent rock interfaceemphasise the importance of herbivory for the rockpool ecosystem.Foraging excursions of P. vulgata at the pool edge increased grazingpressure in the rockpools at high tide but this would not have beendetected if observations had been based on the abundance of limpets atlow tide alone. This outcomewasobserved at all tidal levels atWemburybut was more pronounced on the upper shore. Preferential foraging inpools does not appear to be a general phenomenon as itwas not evidentat Downderry. None the less, it is evident that limpet grazing inrockpools can play amajor role in structuring pool assemblages over theentire intertidal gradient, at least at some locations. This could have animportant influence on the composition of algal assemblages (e.g. WaiandWilliams, 2006b). Although biota living in rockpools escape some ofthe environmental stress typical of the intertidal (e.g. desiccation), thepresent study showed that they are under high consumer pressure. Inbenign environments such as rockpools, elevated herbivory can lead toswitch the nature of interactions between species from competition atlow consumer stress to facilitation at high consumer pressure (Bertnessand Callaway, 1994). For example, an association can occur betweenpalatable and unpalatable species, with the latter serving as protectionfor the former against grazing (Pfister and Hay, 1988; Bertness andCallaway, 1994). These associations were evident in rockpools atWembury (Noël, 2007). Heavy consumer pressure can be predicted tolead to grazer-resistant speciespredominating fromearly colonisation ofpools (Benedetti-Cecchi, 2000; Wai andWilliams, 2006b) and acting asfoundation species (sensu Dayton, 1972). These species may hostpalatable epiphytes which would otherwise be grazed away on thepool bedrock (Benedetti-Cecchi, 2000; Noël, 2007). Rockpools aretherefore not only a shelter for species sensitive to desiccation buttheir community structure appears also to be shaped by the strongconsumer pressure recorded there. The influence of grazing on rockpoolcommunity composition may be an even more profound structuringforce than the widely reported effect of grazing on emergent rock.Limpet foraging appears to be an important factor connecting adjacentmicrohabitats such as rockpools and emergent rock. It is important toour understanding of ecological interactions in the intertidal that poolsand emergent rock are considered as being connected rather thandistinct, isolated habitats.

Acknowledgement

This work was supported by a NERC grant-in-aid funded fellowshipat the Marine Biological Association of the UK and the NERC standardgrant NE/B504649/1 (to SRJ, RCT and SJH). Thanks to M. Wagner, A.Smith, E. Navas and M. Lilley for assistance for the experimental set upand sampling. We are also grateful to the Wembury Voluntary MarineConservation Area for their assistance in using this site. [RH]

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