ORIGINAL PAPER

An assessment of variation in molluscan grazing pressureon Hong Kong rocky shores

Received: 3 June 2002 / Accepted: 24 October 2002 / Published online: 14 December 2002� Springer-Verlag 2002

Abstract Several methods of assessment have been usedto document variation in grazing pressure on temperaterocky shores, although often these methods are appliedwithout consideration of local conditions or species. Inthis study, a comparison was made between abundancecounts of inactive molluscan grazers at low tide, directobservations of grazer activity and distribution through-out day and night tidal cycles, and records of grazingmarks onwax discs, for themid-shore ofHongKong. Theabundance of grazers found during low-tide counts variedamong dates, sites and species. Thismethod, however, didnot record all grazer species that day/night observationsshowed to migrate from the low shore with the rising tide.Low-tide counts, therefore, underestimate grazing pres-sure (number of active grazers per unit area) and grazerguild (number of species). Grazing marks on wax discsalso recorded a greater number of species than the low-tide counts of inactive grazers, and included grazers thatwere seen to migrate up shore during day/night observa-tions. Certain limpet species, however, avoided the waxand did not leave grazing marks, showing this method toalso underestimate grazing pressure. All methods showedgrazing pressure to be variable at spatial scales of tens ofmetres or less and also temporally variable betweensampling dates. The sole use of either low-tide counts orwax discs is likely to underestimate grazing pressure, dueto variation in shore topography and grazer foragingbehaviour, especially on shores with a narrow tidal rangesuch as in Hong Kong. To gain a more accurate assess-ment of total grazing pressure, it is suggested that

recording of grazingmarks onwax discs should be used inconjunction with direct day/night observations.

Introduction

Molluscan herbivores play an important role instructuring intertidal assemblages, and a considerableamount of work has examined their feeding modes andthe impact they have on their food resources (reviewedby Hawkins and Hartnoll 1983; Norton et al. 1990).Numerous studies have examined spatio-temporal vari-ation in grazing pressure, which has traditionally beenachieved by counting inactive grazers at a variety ofscales to give estimates of overall abundance/densities ofherbivores (e.g. Underwood 1975, 1978; Southward andSouthward 1978; Lubchenco et al. 1984; review ofmethods by Baker and Crothers 1991), with the under-lying assumption that these grazers forage within thearea surveyed (Vadas 1985).

Direct observations of grazer foraging activity havealso been used to record grazing pressure (e.g. Cook andCook 1981; Garrity 1984; Little and Stirling 1985; Littleet al. 1988; Evans and Williams 1991), and more novelapproaches using photography or telemetry utilisingsensors of various types (see reviews by Hartnoll 1986;Chelazzi et al. 1994a; Thompson et al. 1997) have beenused to gain more accurate information on time andlocation of foraging activity and, in some cases, a directassessment of active foraging (measurements of raspingrates: Kitting 1980; Petraitis and Sayigh 1987; Chelazziet al. 1994b; recording radula marks on wax discsembedded in the rock surface: Thompson et al. 1997;Forrest et al. 2001).

Much of this work has been developed on temperateshores and, subsequently, used on a wide variety of shoretypes, without questioning how appropriate such tech-niques are for specific shores and the grazers underinvestigation. Differences in species, behaviour, habitat,climatic conditions, etc. may produce conditions that

Marine Biology (2003) 142: 495–507DOI 10.1007/s00227-002-0985-4

N. Hutchinson Æ Gray A. Williams

Communicated by T. Ikeda, Hakodate

N. Hutchinson Æ G.A. Williams (&)The Department of Ecology & Biodiversityand The Swire Institute of Marine Science,The University of Hong Kong,The Kadoorie Biological Sciences Building,Pokfulam Road, Hong Kong

E-mail: hrsbwga@hkucc.hku.hkTel.: +852-22990604Fax: +852-25176082

differ sufficiently from those for which a method was de-veloped, resulting in poor estimates of grazing pressure.Tropical systems, for example, differ from temperatesystems (see review by Brosnan 1992) in that molluscangrazers often forage during different tidal periods (Bert-ness et al. 1981; Garrity 1984) and their behaviour is oftenrestricted to areas adjacent to refuges due to higher levelsof predation and physical stress (Menge and Lubchenco1981; Miller 1983; McKillup and McKillup 1993).Methods used on temperate shores may, therefore, needto be refined or replaced for studies in tropical systems.

Hong Kong has a narrow tidal range (up to a maxi-mum of �2.2 m), and vertical zonation patterns, al-though present, tend to be narrow (Morton and Morton1983; Williams 1993). On steep shores grazers may,therefore, be able to move over a wide tidal gradientwhen feeding. The strong seasonal climate in HongKong also imposes physical constraints on grazermovement (Britton and McMahon 1986; Williams andMorritt 1995), resulting in seasonal migration of grazers(Williams and Morritt 1995; Harper and Williams 2001)and limiting their distribution when inactive duringsummer to refuges such as cracks, crevices and the edgeof rockpools where physical stress is reduced (Williamsand Morritt 1995). Spatial variation in grazing pressureon tropical shores may be exaggerated by topographicfeatures such as natural barriers (Erlandsson et al. 1999),or the distribution and density of refuges used to escapepredation (Menge and Lubchenco 1981; Coull and Wells1983; Gosselin and Chia 1995) and desiccation stress(Kensler 1967; Williams and Morritt 1995). Levings andGarrity (1983), for example, showed that Nerita spp.only forage a short distance from refuges, and grazingactivity is concentrated in a narrow zone around theseareas, creating ‘‘halos’’ of free space around crevices(�10 cm, also see Williams et al. 2000).

Reliable, comparative assessments of grazing pres-sure are, therefore, needed to determine the role ofherbivory in different geographic regions and on variousshore types. This paper uses a variety of techniques toassess spatial and temporal variation in grazing pressureon Hong Kong shores. A comparison is made betweenthese different techniques to identify how specific, localconditions influence the reliability of certain methodsand recommends appropriate techniques for rockyshores with narrow tidal ranges and a diversity of highlymobile, molluscan grazers.

Materials and methods

A comparison of methods to assess grazing pressure

Investigations were carried out at three sites (A–C) on moderatelyexposed stretches of rocky shore (as defined in Kaehler and Wil-liams 1996; Hutchinson and Williams 2001) at Cape d’Aguilar(22�13¢N; 114�12¢E), Hong Kong from August–September 1998.

Grazing pressure was estimated in the mid-shore (1.5 m abovechart datum, C.D.; see Hong Kong Observatory 1998), as grazerspecies richness and abundance are high at this level (Hutchinson

1999). Low-tide counts of grazer density, direct observations ofactive grazers and measurements of grazing marks on the shorewere compared to determine the relative effectiveness of thesetechniques to assess grazing pressure on shores with a limited tidalrange.

Grazing pressure as estimated using low-tide counts

Traditional, quadrat counts of inactive molluscan grazerswere made during day- and night-time low tides. Ten, 50·50 cmquadrats were randomly placed along 10 m long transects at sitesA–C at low tide, and the distribution and abundance of molluscswere recorded. Surveys were conducted on ten randomly chosendates during spring (n=5) and neap (n=5) tide periods. Foranalysis, two random dates out of five were selected for daycounts and two for night counts, to reduce possible problemsassociated with non-independence of samples.

Spatio-temporal variation in grazer abundance was analysedusing a four-factor, nested ANOVA to determine differences be-tween spring and neap tides (two levels: orthogonal and fixed),dates within tidal state (two levels: random and nested within tidalstate), day/night low tides (two levels: fixed and orthogonal) andsite (three levels: random and orthogonal). Separate analyses wereconducted for the total number of grazers and the most abundantspecies (>3 m)2), i.e. Acanthopleura japonica (Lishke), Cellanatoreuma (Reeve), Monodonta labio (Linnaeus), Patelloida saccha-rina (Reeve), Nerita albicilla (Linnaeus) and Siphonaria laciniosa(Linnaeus).

Data for all analyses were checked for homogeneity of vari-ances (Cochran’s C-test) and transformations were performedwhen necessary to satisfy this assumption. Significant differenceswere further examined, when appropriate (i.e. for fixed factors),using SNK (Student–Newman–Keuls) multiple comparison tests(Zar 1996; Underwood 1997).

Grazing pressure as estimated using direct day/night observations

Using the same sampling method, grazer distribution and abun-dance at one site (A) was recorded throughout day and night tidalcycles. Although grazer movement at 1.5 m (C.D.) was of primeinterest, transects were also established at 1.00, 1.25 and 1.75 m, inorder to determine the vertical foraging range of grazers at differenttimes. Counts were conducted every 2 h, on the same samplingdates as the low-tide grazer counts beginning at low tide, throughtwo semi-diurnal tidal cycles (total: �26 h) timed to coincide witheach low tide, high tide and the time at which the animals firstbecame awash on the ebbing and flooding tides. Grazers were re-corded as either active or inactive, defined by whether any move-ment or feeding activity could be seen, in ten random quadrats ateach height. Quadrats were randomly assigned along the transect ateach sampling time to reduce problems of non-independence.Transects were sampled during immersion periods using viewingbuckets or by snorkelling and, at night, using red filtered lightwhich does not appear to disturb molluscan grazers (Little et al.1988).

Temporal variation in grazer abundance, using pooled activeand inactive abundance data, was analysed using a four-factor,nested ANOVA to determine differences between spring andneap tides (two levels: orthogonal and fixed), different tidalstates, i.e. high tide, low tide and the periods when the shore wasawash on the ebb and flood tides (four levels: orthogonal andfixed), night/day (two levels: fixed and orthogonal) or samplingdates (two levels: random and nested within night/day). In orderto reduce possible problems of non-independence only data fromfive random quadrats out of the ten taken during each samplingtime were used in the analysis, and each date was selected atrandom for each combination of factors from a possible poolof five, i.e. five spring-tide sampling dates and five neap-tidesampling dates.

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Assessment of grazing pressure using radula marks on wax discs

Laboratory choice tests

Wax discs have been used on U.K. and Australian shores toestimate molluscan grazing pressure by scoring radula marks lefton the discs (Thompson et al. 1997; Forrest et al. 2001). Thistechnique assumes that the wax is grazed to the same extent as therock substrate, i.e. molluscan grazers are neither attracted nordeterred by the wax. To test this assumption, ten individuals ofmolluscan grazers found at 1.5 m (C.D.) were collected, kept inan aquarium and starved for 14 days. Species included the chitonAcanthopleura japonica, the gastropod limpets Cellana grata(Gould), Cellana toreuma, Patelloida saccharina, the pulmonatelimpet Siphonaria laciniosa, the trochids Monodonta labio, Chlo-rostoma argyrostoma (Lischke), the nerite Nerita albicilla, theplanaxid Planaxis sulcatus (Born) and the turban shell Lunellacoronata (Gmelin).

To test for wax avoidance/preference, the time spent by ananimal on equal areas of wax (Gusswachs, Morsa, Germany; a0.25 mm thick dark blue wax, able to retain clear rasping markseven when rock temperatures exceed 50�C, authors’ personalobservations) and rock over 1 h was scored. Squares of self-ad-hesive tape (3M, Minn., USA) were attached to the underside of5·5 cm wax squares, and these were stuck onto alternate squareareas of a granite rock plate (30·30 cm) in a 20·20 cm grid toform a chessboard pattern. While the wax was raised �0.4 mmabove the surface of the rock due to the thickness of wax andtape, there were no gaps between the rock surface and the edgesof each wax square. This chequered design allowed the grazeraccess to either wax or rock substrates in equal proportions. In-dividuals were placed at the intersection of a wax square and arock square at the plate centre, and their movements were vid-eotaped for 1 h. To enhance feeding behaviour, animals normallyactive underwater (i.e. L. coronata and C. argyrostoma) weresubmerged, whereas those that grazed whilst awash (i.e. A. japo-nica, C. grata, C. toreuma, P. saccharina, S. laciniosa, M. labio, N.albicilla and P. sulcatus) were showered with seawater from aspray-bar.

The plate was then removed, washed, and the dried wax squareschecked for radula marks, to confirm that the animal was feeding,by viewing under a stereomicroscope against a dark background.The relative times spent by the animal on the wax and the rocksubstrate were then scored from the videotape and heterogeneityv2 tests (Zar 1996) used to determine whether species spent an equalperiod of time (i.e. showed an equal preference) on the two sub-strates. Data were pooled after initial analysis to increase the powerof the test (Zar 1996).

Wax disc placement trial

Following Thompson et al. (1997), individually numbered 14 mm(diameter) plastic holders were filled with molten wax and cooledslowly to provide a smooth surface (see also Forrest et al. 2001).Wax discs were placed on the shore at the three sites (A–C) at 1.5 m(C.D.). At each site, three 10-m-long transects were marked andthree, �5·75 cm areas randomly selected along each transect. Ineach area, a grid of 16 holes in which wax discs could be placed wasdrilled, in a 4·4 configuration with 25 cm gaps between each hole.

To determine how long discs should remain on the shore, discswere left on the shore for 13 days. After the first tidal cycle, andthen after every 48 h, the discs were examined at low tide using ahand lens, and any discs lost, damaged or marked by grazers werenoted. Two discs were also taken at random from each grid andviewed under a stereomicroscope in the laboratory. The percentageof the surface marked by grazers was estimated by rotating eachdisc so that all marks could be seen and the species responsibleidentified. To standardise scoring, a marked, clear plastic sheet wasplaced over the discs, and ten disc segments (marked every 36�)were individually scored by eye on a one to ten scale, and combinedfor each disc to give the percentage of area scraped. Discs were then

returned to the shore and replaced in their original holes during thesame low-tide period. The number of discs scraped, percentage areascraped per disc and observations of over-grazing (wherenew grazing marks passed over and obscured another set ofgrazing marks) were scored to determine a suitable duration ofplacement.

Grazing pressure variation

To estimate variation in grazing pressure, four wax discs wererandomly placed in each of the three grids at the three sites andremoved after 7 days. Discs were placed on the shore six times,randomly chosen and overlapping both neap and spring tidal cyclesfrom August–September 1998. Three-factor, nested ANOVA wasused to determine variation in the percentage cover of discs grazed,scored as in the placement trials, with time (six levels: random andorthogonal), site (three levels: random and orthogonal) and grid(three levels: random and nested in site).

Results

Low-tide counts

The total abundance of grazers recorded by low-tidesurveys during both neap and spring tides varied spa-tially and temporally (Figs. 1, 2; Table 1). Variation inabundance was found between night and day counts atthe same sites, as well as between sites (Figs. 1, 2). Usingthis technique, Acanthopleura japonica, Cellana toreuma,Monodonta labio, Nerita albicilla, Patelloida saccharinaand Siphonaria laciniosa were recorded at all sites. Whilemean abundances of individual species varied betweensampling dates (Figs. 1, 2), if species were recorded atone sampling date, then they were generally found at allother dates (Figs. 1, 2). Some exceptions did, however,occur; for example, N. albicilla was found at site Aduring all sampling dates, except on 8 August (Fig. 1).

The abundance of individuals of different speciesvaried between counts conducted during night and daylow tides on the same date (Figs. 1, 2; Table 1). MoreM. labio, for example, were found at site A during theday than in night counts (Fig. 2). Differences could alsobe seen between spring (Fig. 1) and neap tides (Fig. 2),e.g., N. albicilla was recorded on most dates (albeit inlow numbers) during neap tides at site A (Fig. 2), butwas never recorded at the same site during spring tides(Fig. 1). Variation in abundance was species specific, forexample, A. japonica and C. toreuma varied in abun-dance between sites, spring and neap tides, and nightand day low tides; M. labio varied in abundance betweensites, spring and neap tides, and dates. There were nosignificant differences in abundance of P. saccharina orN. albicilla; although abundance of S. laciniosa variedsignificantly at all temporal scales, but not between sites(Table 1). These individual patterns were not apparentwhen species were pooled and abundance of total graz-ers was analysed, as this showed significant differences ingrazer abundance between sites, but not at any of thetemporal scales (Table 1). Estimates of abundance,

497

therefore, varied between sites on the shore and the timeof sampling, whether it was the date, or night or day-time. Whilst abundances of grazers varied between datessurveyed for both the spring and neap tides, there didnot, however, appear to be any obvious pattern of dif-ferences specifically between spring and neap tides(Figs. 1, 2).

Direct day/night observations

Surveys of grazer movements over 26 h (two semi-diurnal tides) showed differences in total grazer abun-dance at 1.5 m (C.D.) with time on all sampling dates(data presented for one date only, Fig. 3), with higherabundances when the shore was awash during bothnight and day tides (Fig. 3). Individual species, how-ever, showed a number of different patterns. A. japonicawas sparsely distributed at this height, and its abun-dance varied significantly over time on some, but not all,dates (Table 2), although it was only active whilst

awash, with some individuals moving up the shore.Individuals continued moving whilst the rock surfacewas still wet, but were inactive when totally immersed(Fig. 3; authors’ personal observations). The abundanceof C. toreuma also varied at 1.5 m (C.D.) within the 26 hstudy period (Fig. 3), at all temporal scales examined(Table 2). C. toreuma started activity as they becameawash, and then continued moving until high tide, whensome individuals appeared to stop. As the tide ebbed,and whilst the shore was still awash, animals com-menced activity until low tide, when they stoppedmoving (Fig. 3; authors’ personal observations).M. labio also became active when awash and moved up-shore with the rising tide (Fig. 3); there were significantdifferences in abundance at all scales at 1.5 m (C.D.;Table 2). Activity decreased when animals wereimmersed, but re-started when they once again becameawash by the ebbing tide (authors’ personal observa-tions), and continued until the rock surface began todry out. It was often difficult to determine whetherS. laciniosa and P. saccharina were active or inactive,

Fig. 1 Mean abundance (+SD,n=10) of molluscan grazers onthe three transects at 1.5 m(C.D.; sites A–C) during springtides at day and night. Notescale change

498

even though they were present on transects at 1.5 m(C.D.) when the shore was awash (Fig. 3). The lowabundance of individuals meant that analysis could notbe performed on S. laciniosa, and while analysis onP. saccharina abundances found significant differences atall scales, this should be viewed with caution as data didnot satisfy Cochran’s test for homogeneity of variances(Table 2).

Chlorostoma argyrostoma and Lunella coronata werenormally found submerged low on the shore, and onlyoccurred at 1.5 m (C.D.) when this height was im-mersed. Both these species became active as the tidestarted to rise, and moved up-shore with the risingtide, remaining submerged. At high tide, animalsappeared to take refuge in crevices and remainedinactive, until the tide began to recede and theybecame awash, when they became active and movedback down to the lower shore (Fig. 3). At night, someanimals were observed moving down-shore on damp,emersed rock surfaces, and, on occasions, individuals

remained in refuges at 1.5 m (C.D.) after the tidehad ebbed and remained inactive until they weresubmerged on the next rising tide (authors’ personalobservations).

Grazing pressure as estimated using radula markson wax discs

Laboratory choice tests

All grazers left distinct marks on the wax, which allowedspecies-specific identification. The majority of specieswere neither attracted or deterred by the wax and spentequal amounts of time on both substrates (v2 testspooled for Yates correction, P>0.05); however, thelimpets C. toreuma and C. grata were reluctant to crossonto the wax (v2 tests, P<0.0001) and only left radulamarks when directly placed on it (authors’ personalobservations).

Fig. 2 Mean abundance(+SD, n=10) of molluscangrazers on the three transects at1.5 m (C.D.; sites A–C) duringneap tides at day and night.Note scale change

499

Disc placement trial

All discs were grazed after 7 days (Fig. 4). At this time,over-grazing of discs (new grazing marks passing overand obscuring older marks) had not yet taken place,while, on average, 35% of the surface of each disc wascovered in marks. Due to limitations in the number ofholes that could be drilled into the rock surface and thedesire to record marks before over-grazing occurred, aperiod of 7 days was chosen as a suitable time framefor subsequent studies using four discs (Fig. 4), whichis a similar time scale as that used by Thompson et al.(1997) and Forrest et al. (2001).

Grazing marks on wax discs

The percentage cover of grazing marks on wax discswas highly variable between sites and, to a lesser ex-tent, between grids within sites (Fig. 5), although therewas no significant variation between grids within sitesor between dates (Table 3). The total percentage coverof discs marked was consistently lower at site B thanat the other sites (up to 50% lower; Fig. 5), althoughthe number of species marking discs at this site wasmore similar to site C than A (Fig. 5). At site A, therewas variation between grids, with the main contribu-tors to grazing pressure being A. japonica (�5–35%),M. labio (�5–25%) and the low-shore grazer, C. ar-gyrostoma (�5–30%). Other species found at this site,such as P. saccharina, S. laciniosa and L. coronatamade smaller, less consistent contributions to theoverall percentage of grazing on discs. Siteo\’e1B hada wider range of species marking the wax discs, ofwhich A. japonica, M. labio, N. albicilla and L. coro-nata made similar contributions (�5–10%). Otherspecies marking wax discs at this site included, atdifferent times and on different grids, P. saccharina, S.laciniosa and C. argyrostoma (�2–5%). All of thesespecies had a greater effect at site C, where the totalpercentage of discs marked was higher than at theother sites (�70%). The main grazers at this site wereA. japonica (�5–35%), M. labio (�10–30%) and N.albicilla (�10–25%). To a lesser extent, P. saccharina,S. laciniosa, L. coronata and C. argyrostoma were alsofound to mark wax discs, accounting for the remain-der of the percentage of wax marked (�2–15% foreach species).

No differences in grazing pattern with time and lo-cation were recorded for C. argyrostoma, P. saccharinaor S. laciniosa (Table 3). Small-scale spatial variation,i.e. variation between grids at different sites [Gr(Si) termin ANOVA], was seen, however, for A. japonica, L.coronata and M. labio (Table 3), suggesting that grazingpressure exerted by these species was variable at a scaleof tens of centimetres. N. albicilla showed a significantinteraction between date and site, but no variation be-tween grids (Table 3), signifying that grazing pressurevaried at a scale of tens of metres on some dates, but noton others for this species.T

able

1Comparisonusingfour-factor,

nestedANOVA

[differencesbetweenspring/neaptides

(Sn),samplingdate

(Da),night/daylow

tide(N

d)andsite

(Si)]ofmolluscangrazer

abundancesat1.5

mC.D

.Data

weresqrt

(x+

1)[totalgrazers],ln

(x+

1)[C.toreuma],ln(x+

0.5)[A.japonica]orln(x+

0.05)[M

.labio,N.albicilla]transform

edwhen

necessary

tohomogenisevariances.Significantdifferencesareshownin

bold

Source

df

Acanthopleura

japonica

Cellanatoreuma

Monodonta

labio

Neritaalbicilla

Patelloida

saccharina

Siphonarialaciniosa

Totalgrazers

Fvs.

MS

FP

MS

FP

MS

FP

MS

FP

MS

FP

MS

FP

MS

FP

Sn

10.1783

0.0323

0.0768

2.1591

0.9375

2.4000

0.0917

Notest

Nd

10.7747

0.3544

0.0009

1.1585

0.0042

0.1500

0.2972

Notest

Da(Sn)

20.12245.39

0.07330.11712.27

0.21924.754427.900.00452.1716

0.870.48484.23753.030.15834.8750

6.72

0.05261.15864.12

0.1067Si·Da(Sn)

Si

22.6613117.170.00031.439627.920.00454.621127.120.004710.53934.230.10294.40423.150.15113.1792

4.39

0.09815.155418.340.0097Si·Da(Sn)

Sn

·Nd

10.0786

0.1386

0.0034

0.0759

0.1042

11.2667

1.0707

Notest

Sn

·Si

20.316913.95

0.01570.13172.56

0.19281.967111.540.02180.0356

0.010.98581.16250.830.49930.2375

0.33

0.73830.43361.54

0.3187Si·Da(Sn)

Nd

·Da(Sn)2

0.11924.90

0.08390.09062.67

0.18352.79904.44

0.09651.0442

0.570.60766.22081.240.38058.5417

39.420.00231.33704.27

0.1018Si·Nd

·Da(Sn)

Nd

·Si

20.13295.47

0.07170.16794.95

0.08290.66721.06

0.42781.1989

0.650.56981.45420.290.76250.9875

4.56

0.09300.08200.26

0.7819Si·Nd

·Da(Sn)

Si·Da(Sn)

40.02270.06

0.99360.05160.21

0.93510.17040.08

0.98952.4890

1.950.10351.40000.400.81130.7250

0.29

0.88500.28110.49

0.7463Residual

Si·Nd

·Sn

20.17997.40

0.04530.371410.950.02392.01073.19

0.14860.3272

0.180.84384.02920.800.50860.0792

0.37

0.71490.76522.44

0.2026Si·Nd

·Da(Sn)

Si·Nd

·Da

(Sn)

40.02430.06

0.99270.03390.14

0.96920.63080.28

0.89021.8458

1.440.22025.00831.420.22920.2167

0.09

0.98660.31320.54

0.7058Residual

Residual

2160.3885

0.2507

2.2463

1.2774

3.5338

2.5102

0.5790

500

Discussion

Suitability of methods

Examination of grazer movement on Hong Kong shoreshighlights particular problems with common methodsused to estimate grazing pressure. The most widely usedmethod of counting grazers in an area at low tide,clearly, does not give an adequate representation ofgrazing pressure. In areas with a large tidal range,grazers observed at low tide may be predominantly re-sponsible for the grazing pressure at that specific heightthroughout the tidal cycle (Hartnoll and Wright 1977;Hawkins and Hartnoll 1982). Direct day/night obser-vations in Hong Kong, with its narrow tidal range and

fast-moving grazers, however, show that a greaternumber of grazer species are active (presumably grazing)at a particular height than are found inactive at thatheight during low tide. In contrast to Forrest et al.(2001), who found that the density of the limpet Cellanatramoserica during low tide gave a good indication ofdensities at high tide (and therefore a good indication ofgrazing pressure), static low-tide counts underestimatedboth species number (Table 4) and abundance of graz-ers, which varied dramatically at different times duringtidal cycles in Hong Kong. Although static low-tidecounts are a widely used method and are easy to per-form, they are likely to underestimate true grazingpressure. Such problems may be common on shores withlimited tidal ranges, short vertical stretches of shore, and

Fig. 3 Example of activity ofgrazers on transects between 1and 2 m (C.D.) over one 26 htime period (black portions ofvertical bars active individuals;grey portions inactiveindividuals, except for plots forP. saccharina, S. laciniosa andtotal molluscan grazers wheredistinctions are not madebetween active and inactiveanimals, see ‘‘Results’’ fordetails). Transect data areshown only when individualsoccurred at that height duringthe survey. The dashed lineindicates tidal flow and,therefore, when organisms wereimmersed or emersed.Horizontal bars represent night(black) and day (white)

501

highly active grazers that may feed outside the zones inwhich they occur at low tide, as has been recordedelsewhere in tropical (e.g. Levings and Garrity 1983;Williams and Morritt 1995) and temperate systems (seereview by Chelazzi et al. 1983).

Day/night observations showed species number andabundance to vary throughout the tidal cycle and pro-vided detailed information on the activity of individualspecies. Intensive observations rather than low-tidecounts are themselves problematic, however, as theyonly record the number of grazers present in an area,without indicating whether animals are actively grazingor simply moving on the shore (see Parpagnoli andChelazzi 1995). Such observations are also time con-suming and difficult where poor weather and sea con-ditions make fieldwork dangerous (e.g. wave-exposedshores; Branch and Branch 1981). It is not possible, evenin Hong Kong’s relatively calm sea conditions (Mortonand Morton 1983), to conduct these surveys duringwinter, or throughout periods of bad weather (Williamsand Morritt 1995). This method also suffers from amajor failing, shared with low-tide counts, as it does notgive any indication of the actual area of shore grazed,merely an indication of the number of grazers and thosespecies actively moving at the shore height of interest(Table 4).

Wax discs provide more accurate information ongrazing intensity in an area (Thompson et al. 1997), andalso some indication of the relative importance of dif-ferent grazer species, as a percentage of wax surfacegrazed on. An underlying assumption of this method isthat animals will graze on the discs in a similar fashionas on the surrounding rock area. Jenkins et al. (2001)found that in some cases limpets on temperate shoresshowed behavioural changes (in direction or speed)when they came into contact with wax discs. As theoccurrence of this was rare, and animals subsequentlymoved over the discs, the method was still deemed to besuitable to estimate grazing pressure. The commoncellanid limpets in Hong Kong, Cellana toreuma and C.grata, however, avoided the wax, and so this techniquealso underestimates grazing pressure. These two speciescommonly move over shore features that project furtherfrom the rock surface than the wax squares stuck to rockplates in the laboratory, and initial tests, using plasticsquares of the same dimensions rather than wax squares,indicated that the height difference between the rocksurface and the surface of the wax was not responsiblefor the avoidance behaviour of these animals towardsthe wax.

The occurrence of over-grazing, i.e. where grazingmarks on the wax surface are obscured by another set oflater grazing marks, is likely to lead to an underesti-mation of grazing pressure using this method (Thomp-son et al. 1997), as the size and depth of radula markscan mean that any sign of previous marks is obliterated.This was certainly the case in the current study as, whileall visible marks were scored, it was not possible to es-timate the percentage cover of grazing marks that wereT

able

2Comparisonusingfour-factor,nestedANOVA

[differencesbetweenspring/neaptides

(Sn),tidalstate,i.e.

high,low

andawash

ontheebbandflood(Ti),night/daysampling

(Nd)andsamplingdate

(Da)]

ofmolluscangrazerabundancesat1.5

mC.D

.Data

wereln(x+

1)[A.japonica,C.toreuma,M

.labio]transform

edwhen

necessary

tohomogenise

variances.Significantdifferencesare

shownin

bold

Source

df

Acanthopleura

japonica

Cellanatoreuma

Monodonta

labio

Patelloidasaccharina

Totalgrazers

Fvs.

MS

FP

MS

FP

MS

FP

MS

FP

MS

FP

Sn

10.1364

0.49

0.5577

4.1051

5.40

0.1458

1.6289

7.63

0.1099

0.4000

0.17

0.7233

15.3828

64.94

0.0151

Sn

·Da(N

d)

Ti

30.0835

0.19

0.9017

0.7598

0.78

0.5451

0.0965

0.02

0.9949

5.4667

22.24

0.0012

1.3150

0.45

0.7272

Ti·Da(N

d)

Nd

10.6789

3.36

0.4628

0.4019

0.32

0.6291

5.0250

2.64

0.2460

0.6250

2.00

0.2929

6.4444

11.13

0.0793

Da(N

d)

Da(N

d)

20.8369

0.29

0.0380

1.2599

3.47

0.0342

1.9066

3.78

0.0253

0.3125

0.53

0.5904

0.5790

1.19

0.3082

Residual

Sn

·Ti

30.1966

0.23

0.8297

2.0952

2.49

0.1575

0.6949

0.35

0.7883

0.5333

0.17

0.9155

4.2397

3.25

0.1020

Sn

·Ti·Da(N

d)

Sn

·Nd

10.0762

1.35

0.6809

0.2274

0.30

0.6394

0.7249

3.39

0.2068

0.0250

0.01

0.9282

1.1631

4.91

0.1570

Sn

·Da(N

d)

Sn

·Da(N

d)

20.3358

0.82

0.2639

0.7606

2.09

0.1276

0.2136

0.42

0.6553

2.4125

4.08

0.0191

0.2369

0.49

0.6163

Residual

Ti·Nd

30.3668

1.79

0.5286

1.4080

1.45

0.3184

4.1386

0.97

0.4666

3.7583

15.29

0.0032

4.0153

1.37

0.3387

Ti·Da(N

d)

Ti·Da(N

d)

60.4474

0.84

0.1054

0.9696

2.67

0.0180

4.2717

8.48

<0.0001

0.2458

0.42

0.8672

2.9292

6.01

<0.0001

Residual

Sn

·Ti·Nd

30.5670

2.69

0.5181

2.9870

3.55

0.0874

0.0551

0.03

0.9930

1.8250

0.57

0.6561

2.2065

1.69

0.2669

Sn

·Ti·Da(N

d)

Sn

·Ti·Da(N

d)

60.6721

0.0170

0.8417

2.32

0.0372

1.9617

3.89

0.0013

3.2125

5.44

<0.0001

1.3039

2.67

0.0177

Residual

Residual

128

0.2494

0.3636

0.5037

0.5906

0.4875

502

Fig. 4 Number of wax discsand mean percentage cover(bars, n=16; +SD) grazed overa 13 day period. Open circlesrepresent the time at whichover-grazing occurred. Arrowindicates the most suitabledeployment time, i.e. maximumnumber of days before over-grazing and time at whichgrazing marks occurred on alldiscs

Fig. 5 Mean percentage cover(n=4; +SD) of grazing markson wax discs left on the shorefor 7 days, in the three grids atsites A–C. Note scale change

503

lost due to over-grazing. When no over-grazing wasobserved, this technique appeared, however, efficient forthe majority of grazers, and so should be used inconjunction with on-shore observations to determinedetailed patterns of total grazing pressure on local semi-exposed shores (see Table 4).

The wax disc method showed that, within a 2 monthperiod, grazing intensity varied little at sampling timesweeks apart. Grazing intensity did, however, vary atspatial scales of meters within sites for some species ofgrazers, with patterns varying from species to species.Variation at this spatial scale is similar to that found intemperate regions (Thompson et al. 1997; Forrest et al.2001) and is likely to be a function of variation in thedistribution patterns of the grazers, their overall size,mobility and heterogeneity of the shore. Grazing pres-sure on more heterogeneous shores, for example, isknown to be patchy (see discussion in Erlandsson et al.1999; Williams et al. 2000).

Low-tide counts severely underestimated the varietyof species found in the grazer guild, as compared toobservations throughout the tidal cycle on Hong Kongshores. Direct day/night observations did not, however,give an indication of whether animals were actuallyfeeding. The wax disc method, while recording physicaldata on the amount of substrate removed by othergrazers, did not record the grazing activity of locallyabundant cellanid limpets, and further work is needed todetermine whether another material may be used as asurrogate for wax to solve this problem. A combinationof techniques is, therefore, needed to adequately assessgrazing pressure on such shores with limited tidal ranges(Table 4).

Spatial and temporal variation in grazing pressure

Grazing pressure on semi-exposed shores in Hong Kongappears to be variable at spatial scales of centimetres tometres, similar to those described on other rocky shores intemperate (e.g. Chelazzi et al. 1994a; Santina et al. 1994;Thompson et al. 1997; Forrest et al. 2001) and also tro-pical systems, where grazing may be concentrated aroundrefuges, producing halos of increased grazing pressure(e.g. Garrity and Levings 1981; Menge and Lubchenco1981; Williams et al. 2000). Consistent high grazingpressure by Acanthopleura japonica, Monodonta labio,Nerita albicilla andChlorostoma argyrostoma, as detectedbywax discs, was recorded at all sites. The contribution tooverall grazing pressure exerted by each species is likely tobe dependant on a variety of factors, such as whether thatspecies is highly mobile and can cover large distancesduring foraging trips (e.g. M. labio), whether it is presentin large numbers (e.g. Patelloida saccharina), whether itsradula is large, enabling individuals to scrape relativelylarge areas of the rock surface (e.g. A. japonica) or amixture of these factors.

The wax disc method was, however, unable to recordmarks left by the limpet Cellana toreuma, and thisT

able

3Comparisonusingthree-factor,nestedANOVA

[differencesbetweensamplingdate

(Da),site

(Si)andgrid(G

r)]ofthepercentagecover

ofgrazingmarksleftonwaxdiscs

onthe

shore.Data

weresqrt(x+

1)[C.argyrostoma,L.coronata]orln(x+

0.015)[P.saccharina,S.laciniosa]transform

edwhen

necessary

tohomogenisevariances.

Significantdifferences

areshownin

bold

Source

df

Acanthopleura

japonica

Monodonta

labio

Neritaalbicilla

Patelloidasaccharina

Fvs.

MS

FP

MS

FP

MS

FP

MS

FP

Da

5214.1824

1.79

0.2035

73.6602

1.39

0.3066

54.5296

0.47

0.7933

2.2011

1.44

0.2899

Da·S

iSi

25171.7269

2816.8380

7881.7269

7.3381

Notest

Gr(Si)

6721.4907

3.27

0.0136

482.2824

3.83

0.0059

50.2269

1.20

0.3347

0.9982

0.63

0.7043

Da

·Gr(Si)

Da

·Si

10

119.9491

0.54

0.8453

52.9602

0.42

0.9252

116.9713

2.79

0.0145

1.5243

0.96

0.4935

Da

·Gr(Si)

Da

·Gr(Si)

30

220.7519

0.65

0.9178

125.8157

0.46

0.9927

41.9546

0.14

1.0000

1.5819

0.70

0.8700

Residual

Residual

162

339.8627

272.8719

289.6883

2.2445

Source

df

Siphonarialaciniosa

Chlorostomaargyrostoma

Lunella

coronata

Totalgrazers

Fvs.

MS

FP

MS

FP

MS

FP

MS

FP

Da

58.6683

2.48

0.1037

2.9927

0.97

0.4809

0.5429

0.38

0.8492

196.2963

1.47

0.2821

Da·S

iSi

27.4000

16.7890

2.9865

36927.0880

Notest

Gr(Si)

64.3432

2.10

0.0833

1.1800

0.63

0.7031

2.6168

2.50

0.0441

29.1806

0.31

0.9267

Da

·Gr(Si)

Da

·Si

10

3.4925

1.69

0.1306

3.0899

1.66

0.1383

1.4163

1.35

0.2486

133.5435

1.42

0.2196

Da·G

r(Si)

Da

·Gr(Si)

30

2.0721

0.55

0.9734

1.8653

0.63

0.9325

1.0463

0.62

0.9360

94.1083

0.31

0.9998

Residual

Residual

162

3.7937

2.9670

1.6787

300.0895

504

species, which moves over vertical distances of ca. 0.5–1 m during foraging trips (authors’ personal observa-tions), and is often abundant on shores (Hutchinson1999; Harper and Williams 2001), is likely to exert rel-atively heavy grazing pressure, as shown for limpets onshores elsewhere in the world (Kitting 1980; Underwood1980; Hawkins 1981; Cubit 1984; Branch 1985; Farrell1988). C. argyrostoma accounted for a considerableproportion of the overall grazing pressure on the shoreat 1.5 m (C.D.), which suggests that species that migrateup-shore to feed play an important, and often over-looked, role. If such species are present low on a shore, itis important that equal emphasis be placed on their rolein shaping assemblage structure at higher shore levels asis placed on non-migratory/resident species. More em-phasis should, in fact, be placed on such species ascompared to some abundant species (such as P. sac-charina), which appear to exert little overall grazingpressure on the shore.

While temporal variation (at a scale of days and be-tween spring and neap tides) was seen in the numbers ofinactive grazers recorded during low tide, there did notappear to be temporal variation in grazing pressure asrecorded using wax discs. As discs were left in situ for aperiod of 7 days, they recorded marks left by animalsforaging during both spring and neap tides. To determinedifferences in grazing pressure between these times, discswould need to be left on the shore for shorter periods oftime, e.g. 2–3 days, although variation in grazing pressureat this temporal scale is probably of little interest, as it isunlikely that this short time period would affect assem-blage structure. Further work, examining variation ingrazing pressure between the winter and summer is,however, likely to be of value, to reveal the relative im-portance of grazing pressure at various shore levels duringtimes of different environmental conditions. Such a studywould show whether grazing pressure remained constantin an area when there was a change in food availability, orwhether the relative importance of different grazer speciesvaries with the time associated with the seasonal migra-tions of specific species (Branch 1975; Chelazzi et al. 1983;Takada 1995, 1996; Williams and Morritt 1995; Harperand Williams 2001).

The various methods of assessment used in the currentstudy showed that grazing pressure varies at a range ofspatial and temporal scales onHongKong shores. The useof different methods, however, results in varying conclu-sions as to the relative importance of the different grazer

species and overall grazing pressure. While all methodsshowed variation in grazing pressure, it was not possibleto inter-calibrate these methods. Thompson et al. (1997),for example, also found no relationship between thenumber of grazers present in an area and the percentagearea of wax discs grazed. Although the wax disc method islikely to underestimate actual grazing pressure, it appearsto be the most useful in as far as it provides an actual unitof measurement of grazing pressure. As these samplingunits (i.e. wax discs) are directly comparable, this methodshould prove most suitable for comparisons at a widevariety of spatial and temporal scales. Caution should beexercised, however, when relying on a single method tomake comparative assessments of grazing pressure with-out initial field trials to investigate the effectiveness of suchmethods, especially when comparing shores from differ-ent areas and tidal regimes.

Acknowledgements The authors wish to thank R. Thompson for adraft of his paper and for showing N.H. his set-up at the DoveMarine Laboratory and to B. Darvell for providing us with variousdental waxes. G.R. Blackmore and Z.Y. Li assisted during 26-hwatches. Many thanks to S.J. Hawkins and the H.K.U. rocky shoreecology group for critical comments on an early form of the textand to an anonymous reviewer, whose suggestions helped to im-prove the manuscript. This research was carried out in partialfulfilment of the requirements for a Ph.D. submitted by N.H., whowas supported by a part-time demonstratorship at The Universityof Hong Kong. Permission to work in the Cape d’Aguilar MarineReserve was granted by the Agriculture, Fisheries and Conserva-tion Department, The Government of Hong Kong SAR.

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