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LJournal of Experimental Marine Biology and Ecology,233 (1999) 81–94

Littorinids control high intertidal biofilm abundance ontropical, Hong Kong rocky shores

*Y.M. Mak , Gray A. WilliamsThe Department of Ecology and Biodiversity and The Swire Institute of Marine Science,

The University of Hong Kong, Hong Kong

Received 4 March 1997; received in revised form 20 July 1998; accepted 21 July 1998

Abstract

Biotic interactions in the high shore are assumed to be of little importance as compared to therole of adverse physical factors, despite the fact that these shore levels support dense numbers ofgrazing littorinids worldwide. In Hong Kong, three species, Nodilittorina trochoides, N. radiataand N. vidua, are abundant in the high shore and graze the epilithic biofilm, which is primarilycomposed of cyanobacteria (mostly Gloeocapsa and Dermocarpa species). When littorinids wereexcluded from the high shore (2.00–2.25 m above C.D.) using gum barriers, growth of the biofilmas measured by chlorophyll a levels was enhanced after 42 days at three different sites. Whilst theoverall pattern of increasing chlorophyll a levels in exclusion areas was the same for all threesites, there was between-site variation possibly due to different littorinid densities and/or rocktypes. Exclusion of grazers, however, revealed that even at high shore levels on tropical shoresbiotic factors can control biofilm development. It is suggested that this influence acts in synergywith physical factors such as tidal inundation and frequency of wave splash and storms which candirectly control littorinid grazing activity and presumably biofilm growth. 1999 ElsevierScience B.V. All rights reserved.

Keywords: Nodilittorina trochoides; N. radiata; N. vidua; Littorinidae; Biofilm; Hong Kong;Tropical shore

1. Introduction

The importance of biotic factors, including competitive interactions for resources andherbivory, in controlling the distribution and abundance of marine organisms is generally

*Corresponding author. Present address: Agriculture and Fisheries Department, 13 /F Canton Road Govern-ment Offices, 393 Canton Road, Kowloon, Hong Kong.

0022-0981/99/$ – see front matter 1999 Elsevier Science B.V. All rights reserved.PI I : S0022-0981( 98 )00122-1

82 Y.M. Mak, G.A. Williams / J. Exp. Mar. Biol. Ecol. 233 (1999) 81 –94

thought to decrease with increasing height on rocky shores (Connell, 1972; Underwood,1979). Consistent with this perspective, algal abundance has been shown to beinfluenced by competition and herbivory at lower tidal levels, whilst at upper levelsabundance appears governed principally by physical stresses, such as thermal anddesiccation stresses associated with tidal inundation (Norton, 1985; Underwood, 1985;however, see Underwood, 1991). Gastropods are among the most numerous andsuccessful aquatic herbivores and their influence on rocky intertidal community structurehas been widely documented (reviewed by Underwood, 1979; Hawkins and Hartnoll,1983; Vadas, 1985). As there are substantial populations of benthic-feeding, herbivorousgastropods and arthropods at high shore levels on most rocky shores (Lewis, 1964;Stephenson and Stephenson, 1972; Newell, 1979), it is unlikely that algal abundance atthese heights is unaffected by biotic factors.

Previous experiments on the effects of grazing and physical factors indicate that theupper limits of some algae may be caused by grazing gastropods removing algal spores(Cubit, 1984; Underwood and Jernakoff, 1981). This is thought to be a dynamic balancebetween whether the algae can recruit and survive at certain levels, and whether grazerscan check algal growth rates. Physical factors associated with emersion during low tidecan determine the growth, abundance and sometimes the survival of these algae if theybecome established above their normal upper limit when grazers are removed (Under-wood, 1980), and some species of algae are apparently restricted to low shore byphysical factors, and do not colonize higher levels even when grazers are removed(Underwood, 1980; Norton, 1985). The relative roles of grazers and physical conditionsin the high shore can be separated by removal of the dominant grazers to examinewhether predation accounts for the apparent bare condition of this region or whetherphysical factors are of primary importance.

The high intertidal often appears bare of algae and yet supports dense numbers ofgrazing snails of the family Littorinidae throughout the world (Stephenson andStephenson, 1972; McMahon, 1990). Most Littorinidae feed on the epilithic biofilm ofdiatoms, cyanobacteria and bacteria (Norton et al., 1990). There have been many studieson the effects of littorinid grazing in the high shore (reviewed by Norton et al., 1990;McQuaid, 1996); influencing primary production in mainly temperate regions, forexample, Littorina scutulata (Castenholz, 1961; Nicotri, 1977), Littorina planaxis andLittorina scutulata (Foster, 1964), Nodilittorina unifasciata (Branch and Branch, 1981);and overall community structure, for example, Littorina keenae (Castenholz, 1961;Foster, 1964), Littorina sitkana (Behrens, 1976), Littorina plena (Chow, 1989),Littorina kraussi, Nodilittorina africana and N. natalensis (Potter and Schleyer, 1991).

Algae–herbivore interactions have been extensively examined in temperate intertidalhabitats (reviewed by Lubchenco and Gaines, 1981; Hawkins and Hartnoll, 1983; Vadas,1985) but few studies have been conducted on tropical shores (reviewed by Brosnan,1992). On tropical shores, physical stress in the high shore is great (Moore, 1972); rocktemperatures can exceed 508C (Williams and Morritt, 1995). The diatoms whichdominate epilithic biofilms on temperate shores are replaced by the more temperaturetolerant cyanobacteria as the dominant primary producers on tropical shores. Given thespeculation concerning latitudinal patterns in algae (including cyanobacteria)–herbivoreinteractions (e.g., Lubchenco and Gaines, 1981; Brosnan, 1992) and the influence of

Y.M. Mak, G.A. Williams / J. Exp. Mar. Biol. Ecol. 233 (1999) 81 –94 83

gradients in consumer pressure on community organization (Menge and Lubchenco,1981; Menge and Sutherland, 1987), it is clear that more comparative work is needed intropical habitats. The current study focuses on the relative impact of grazing bylittorinids on the abundance of the cyanobacteria-dominated epilithic biofilm in the highintertidal on rocky shores in Hong Kong.

2. Materials and methods

2.1. Sites and littorinid densities

Three sites (Fig. 1) were selected around Cape d’Aguilar, Hong Kong Island (228209

N, 1148109 E). Sites had similar exposure to wave action but different rock types (Sites

Fig. 1. The three selected sites at Cape d’Aguilar, Hong Kong.


1 and 3 are granodiorite; Site 2 is coarsely crystalline tuff, see Morton and Harper,1995). The dominant high shore grazing gastropods are the three littorinid species,Nodilittorina trochoides (Gray, 1839), N. radiata (Eydoux and Souleyet, 1852) and N.vidua (Gould, 1859) (Ohgaki, 1985; Reid, 1992), the major epilithic biofilm species arecyanobacteria (year-round) and diatoms (seasonally, Nagarkar, 1996).

On 28 March 1994, five quadrats (25 3 25 cm) were randomly located between2.00–2.25 m above Chart Datum (C.D.), above the ‘Kyrtuthrix-zone’ (see Kaehler andWilliams, 1996). To estimate grazer density, all littorinids were counted and removedfrom the quadrats. Twenty individuals of each species were randomly selected and shelllength (maximum length from apex to base) was measured (60.1 mm) using amicrometer on a stereomicroscope in the laboratory. Dissections were made of the gutcontents of some animals, which were prepared for cryo-stage SEM (Leica CambridgeS440). The remaining animals were released back to the same collection point.Nodilittorinids in Hong Kong feed on the epilithic biofilm, primarily cyanobacteriaspecies, in the high shore (Williams, 1994). To quantitatively assess the epilithic biofilm,

2chlorophyll a levels were measured from ten random rock chips ( | 2 cm ) removed ateach site and chlorophyll extracted using the hot methanol method (HMSO, 1986;Nagarkar and Williams, 1997).

2.2. Exclusion experiment

The influence of grazing on bioflm assemblages in the high shore was investigated bythe manipulative exclusion of littorinids. Experimental areas were established on 30March 1994 at the three selected sites between 2.00–2.25 m above C.D. and theexperiment was concluded on 23 May 1994 after 52 days. This period represents thetransition between the cool, dry and hot, wet monsoon seasons in Hong Kong and is alsothe time of maximal growth of the epilithic biofilm (Nagarkar, 1996). The maximumtidal range, air temperature range and sunshine hours were 1 0.7–2.2 m C.D., 18.9–32.98C and 0–11.4 h, respectively, within the experimental period (Fig. 2). Mean airtemperature generally increased during the course of experiment and tidal immersionwas limited to 3.5 h of the experimental period (as calculated from hourly tidal data,Hong Kong Observatory).

Sites were replicated to examine the generality of the results to high intertidal areaswithin the Cape d’Aguilar area. Exclusion areas were constructed using ‘Tree tanglegum’ pest barrier (The Tanglefoot Co., Michigan, USA) which effectively excludeslittorinids (Williams, 1994). Five replicates were established at each site. In eachreplicate set of treatments, there was one exclusion area with a complete barrier, onehalf-barrier (as a control for the presence of the gum) and one un-manipulated open area(corners marked on the shore, Fig. 3). The control treatment for the possible effect of thegum barrier was broken-strips of pest barrier accounting for an overall length of 50%barrier and 50% rock (Fig. 3). A propane blow torch was used to dry the rock surface ofthe outer edge of the area before the barrier ( | 1 cm in width) was applied. Thedimension of all the treatments was 27 3 27 cm allowing a 2 cm area to control for edgeeffects. Treatments were placed parallel to the sea at the appropriate tidal height in areasof relatively homogeneous rock. Treatments were randomly allocated at each height, but


Fig. 2. Variation in the maximum air temperature and sunshine hours at the 10 sampling dates (meterologicaldata from the Hong Kong Observatory).

within a sequence of the three treatments, therefore producing an unplanned blockingeffect.

All sampling was performed during low tide when the experimental sites wereemersed and the rock surface was dry. Any littorinids, or other gastropods, found in theexclusion treatments were removed and damaged barriers repaired. To assess biofilm

2abundance, chlorophyll a was extracted from rock chips ( | 2 cm ), taken from each areaevery six days, using hot methanol. Overall , 3.5% of the surface area of each replicate

2was removed. Small rock chips ( | 0.5 cm ) were removed at Day 0 and Day 36 fromexclusion areas, fixed in 2.5% Glutaraldehyde, air dried, coated with a gold /palladiummixture and then examined under the SEM to view the epilithic biofilm (see Nagarkarand Williams, 1997, for details).

Chlorophyll data were analyzed by a 2-way analysis of variance (ANOVA) with thetwo factors, site (Sites 1, 2 and 3) and treatment (exclusion area, control or open area).Time was not included as a factor in the analysis as samples would be temporallynon-independent. Temporal data are graphically displayed and data are analyzed for Day42, which showed the greatest difference between treatments. The unplanned blockingeffect causes problems with spatial non-independence between treatments. To overcomethis flaw in the design and analyze independent replicates, random pairs of replicatesfrom treatments were chosen for analysis (from separate ‘blocks’). Due to the limitednumber of replicates, only pairwise comparisons of treatments (e.g. Exclusion vs.Control) could be compared (i.e. using 2 replicates for each treatment of the possible 5available). Three random sets of replicates were chosen for each comparison to removeany bias in this procedure; resulting in three ANOVAs, each repeated 3 times.Homogeneity of variances was assessed using Bartlett’s test and normality tested using aresidual normal plot (SAS Vers. 6.08, SAS Institute Inc., USA). Heteroscedasticity was


Fig. 3. Experimental design. Experimental areas were 27 3 27 cm and were randomly distributed withinblocks. The lines represent barriers constructed using pest barrier, Tree tangle gum.

observed in the data which were subsequently ln (x 1 1) transformed. Significant resultswere further separated using SNK tests (Zar, 1996).

3. Results

3.1. Sites and littorinid densities

Nodilittorina trochoides, N. radiata and N. vidua were abundant at the three selected


Table 1Combined mean density /25 3 25 cm (6S.D., n 5 5) and mean size (mm6S.D.) of the littorinid species andmean chlorophyll a concentration (6S.D., n 5 10) at three sites around Cape d’Aguilar

Site Littorinid species Mean density6S.D. Mean size6S.D.

1 Nodilittorina trochoides 8.5361.79Nodilittorina radiata 18.2563.27 7.9861.57Nodilittorina vidua 6.6361.08

22Chlorophyll a 0.95360.56 gg cm2 Nodilittorina trochoides 4.5561.68

Nodilittorina radiata 69.82624.5 3.8361.53Nodilittorina vidua 3.6961.27

22Chlorophyll a 0.72260.25 gg cm3 Nodilittorina trochoides 8.2061.54

Nodilittorina radiata 20.8165.12 7.6561.19Nodilittorina vidua 8.3261.34

22Chlorophyll a 1.4460.71 gg cm

sites. A higher density of, relatively small, littorinids was found at Site 2 as compared toSites 1 and 3 (Table 1). The distribution of littorinids at Site 2 was also more patchythan at the other sites (high S.D., Table 1). The mean density and size of the threelittorinids were similar at Sites 1 and 3, except for N. vidua which were relativelysmaller at Site 1. Chlorophyll a concentrations were much higher at Site 3 than the othertwo sites which were similar (One-way ANOVA, df 5 2, 27, F 5 4.54, P 5 0.02; SNKmultiple comparison, Site 3 . Site 1 5 Site 2).

3.2. Exclusion experiment

During the course of the experiment, grazers only invaded the exclusion area twice.These species (Monodonta labio and Acanthopleura japonica) were removed duringroutine sampling. The crustacean scavenger, Ligia exotica, was able to enter theexclusion areas and did not appear to be hindered by the pest barrier.

The overall pattern of chlorophyll a abundance showed a similar temporal change atall three sites. Chlorophyll a concentration was, in general, lowest at Site 2 anddecreased at all sites from the start of the experiment until Day 24, when treatmentsreached their lowest chlorophyll concentration (Fig. 4, Table 2). This pattern wasinversely related with physical factors, air temperature and sunshine hours, especially onDays 24 and 30, when the decrease in chlorophyll a levels coincided with an increase inair temperature and sunshine hours (Fig. 2). On Day 24, however, a dark brown colourwas observed in all exclusion areas at the three sites. After 42 days, there was asignificant increase in chlorophyll a concentration in the exclusion areas as compared tothe control and open areas, which were similar, in all analyses (Fig. 4, Table 2). Therewas also a significant difference between the sites in all combinations, and in onesequence for the Exclusion vs. Open comparison there was a significant two-wayinteraction which showed that exclusion areas had consistently higher chlorophyll levelsthan open areas, however, levels did vary between sites. In general, Site 3 had the


Fig. 4. Variation in mean chlorophyll a concentration ( 1 S.D., n 5 5) with different experimental treatments atthe three sites over the 10 sampling dates.


Table 2Two-way ANOVA to investigate the relationship between chlorophyll a concentration with treatment (Ex,exclusion area; C, control; O, open area) and site (1, 2, 3)

Sequence 1 Sequence 2 Sequence 3

Factor df F P F P F P

Exclusion vs. Control

Treatment (Tr) 1 27.39 0.002 25.86 0.002 48.88 , 0.001Site (S) 2 10.48 0.011 9.50 0.014 5.88 0.039S 3 Tr 2 1.30 0.34 1.08 0.396 2.65 0.150Error 6Exclusion vs. Open

Treatment 1 40.19 0.001 53.34 , 0.001 104.3 , 0.001Site 2 6.43 0.032 7.64 0.022 8.10 0.02S 3 Tr 2 4.75 0.058 6.12 0.036 9.35 0.014Error 6Open vs. Control (No significant differences were recorded)

SNK testsExclusion vs. Control

All sequences:Treatment Ex . CSite 3 1 2

]]Exclusion vs. Open

Sequence 1:Treatment Ex . OSite 3 1 2

]]Sequence 2:S 3 Tr 3Ex 1Ex . 2Ex . 3O . 2O . 1O

]]Sequence 3:S 3 Tr 3Ex .1Ex 2Ex . 1O . 3O . 2O

]]

To ensure independence of replicates pairwise comparisons of treatments (randomly chosen three times) werecarried out (see text for further details). Data were ln (x 1 1) transformed. SNK results are shown whenP , 0.05; underlined means are not significantly different.

highest chlorophyll levels, especially in exclusion areas, followed by Site 1 and finallySite 2. This order was consistent for the exclusion areas but did vary for the open areas(Table 2).

4. Discussion

The pest barrier (Tree tangle gum) used to exclude littorinids, proved to be aneffective and efficient method and was quick and relatively easy to deploy. Pest barrieronly excluded grazing gastropods, the isopod, Ligia, could freely enter the area.Exclusion barriers can, however, produce unintended artifacts, e.g., reduce light intensityand water flow; increase fouling and moisture in the immediate environment ofexperimental areas (Paine, 1977; Hawkins and Hartnoll, 1983). One method to control


these effects is to employ partial fences to mimic the physical barrier but which stillallow grazers access to the plot. A potential problem with partial barriers, however, isthe tendency for herbivores to either accumulate in them (Menge, 1976; Underwood,1980; Foster, 1982) or their presence to inhibit grazer access. In the present study, halfbarriers attempted to control for possible procedural effects and chlorophyll a con-centrations in these were not significantly different from the open areas of the shore.

Although the physical conditions (e.g. rock types) and biota (e.g. chlorophyll a levelsand littorinid density) present varied between the three sites, all the sites showed anincrease in biofilm growth after 36 days when littorinids were excluded. In exclusionareas, considerable growth of cyanobacteria, Dermocarpa and Gloeocapsa species (Fig.5, S. Nagarkar, pers. comm.), was observed on Day 24 and a significant increase inchlorophyll a was recorded by Day 42. SEM micrographs from Site 3 on Days 0 and 36showed a considerable increase in thickness and cover of cyanobacteria on the rocksurface (Fig. 5). A cryo-stage preparation of the gut contents of foraging littorinidscontained the same cyanobacteria, confirming that the littorinids ingest these species(Fig. 5).

There was a high abundance of small littorinids at Site 2 which may account for thelow standing crop as compared to the other sites. Differences in chlorophyll aconcentration between sites may also be due to site specific variation in physicalproperties, such as rock type (Sites 1 and 3 were granodiorite, Site 2 was coarselycrystalline tuff) or physical conditions. The tuff rock at Site 2 was more soft and easierto chip than the granodiorite sites and also had more cracks and crevices and smalldepressions which could serve as refuges for the littorinids. Such enhancement inroughness may increase the density of resident littorinids (Emson and Faller-Fritsch,1976; Raffaelli and Hughes, 1978) and may account for the difference in littorinidpopulation structure and individual size between the sites (Underwood, 1979). Site 3 hadhigher chlorophyll levels than the other sites (especially in exclusions), although thisdoes not seem to be related to rock type (Sites 1 and 3 were both granodiorite). Thehigher chlorophyll levels at Site 3 may reflect site specific production rates, suggestingthat the density of littorinids supported could vary between sites according to localbiofilm production rates (see Underwood, 1985).

There was a considerable temporal change in microalgal abundance during the courseof the experiment which reflected variation in physical conditions (e.g. high solarradiation, desiccation) during the experiment. High temperatures and dry conditionsappear to depress chlorophyll levels at the three sites. Overall, the effects of physicalfactors may, therefore, act in synergy with biological interactions in structuring the highshore assemblages. In summer, daily growth periods for epilithic microalgae are knownto be reduced by desiccating conditions (Castenholz, 1961).

In a similar experiment (Williams, 1994), performed at nearly the same time of year(April–June), there was a distinct increase in colour in exclusion areas although nosignificant change in chlorophyll levels. Differences between these two studies may be aresult of the slightly different experimental tidal heights used. The present experimentwas conducted at a lower tidal level ( 1 2.00–2.25 m C.D.) than that of Williams( 1 2.5–2.75 m C.D.). The growth of microalgae may be reduced at higher shore levelsdue to prolonged emersion periods and resultant increase in physical stress. Nodilittorina


Fig. 5. Selected representative SEM micrographs of the epilithic biofilm, principally cyanobacteria, Der-mocarpa and Gloeocapsa spp.: (a) rock surface on day 0 (exclusion area), note patchy distribution ofcyanobacteria; (b) Day 36 (exclusion area), total cover of unicellular cyanobacteria, from Site 3, Caped’Aguilar; (c) cryo-stage preparation of the littorinid gut contents.


species forage when awash, following the ebb and flow of the tide (Norton et al., 1990;Britton and McMahon, 1992; Williams, 1994). At slightly higher tidal levels, therefore,the grazing effect of the littorinids will be reduced due to decreased foraging times. Theexclusion of littorinids at . 2.5 m above C.D. is, therefore, unlikely to have such astrong effect as foraging at these levels only takes place during spring tides or stormydays when wave action is high. The relative importance of littorinid grazing, is thereforelikely to decrease with increasing tidal height in the high shore, and even a 25–50 cmvertical height difference may cause a considerable difference in community dynamics(see discussion in Underwood, 1985), especially given the narrow vertical tidal range inHong Kong. In the extreme high shore, physical conditions limit littorinid foraging time,and as a result these grazers have little impact on the biofilm. Only slightly lower on thehigh shore, however, littorinids do control biofilm assemblages, despite the relativelyharsh physical conditions (long emersion times; thermal and desiccation stress ontropical shores) at this tidal height. There is, clearly, a variable boundary where physicalcontrol replaces the impact of biological factors, e.g. grazer impact. On seasonal tropicalshores, like Hong Kong, this boundary is likely to vary temporally with environmentalconditions such as monsoons, which bring strong seasonal changes in physicalconditions, and as a result distribution of intertidal herbivores.

Acknowledgements

Thanks to Dr. Robin Kennish for help in setting up all the sticky barriers on amiserable afternoon; Dr Sanjay Nagarkar for identifying the cyanobacteria; the SEM unitfor assistance with the SEM preparations (all The University of Hong Kong) and Prof.A.J. Underwood (University of Sydney) for improving the analysis. This studyrepresents part of a dissertation submitted in partial fulfilment of requirements for aPh.D. to MYM at HKU. Preparation of the manuscript was supported by a CroucherFoundation Fellowship to MYM.

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