Quantification of radular marks as a method for estimating grazing of intertidal gastropods on rocky shores

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<ul><li><p>Journal of Experimental Marine Biology and Ecology .258 2001 155171</p><p>www.elsevier.nlrlocaterjembe</p><p>Quantification of radular marks as a method forestimating grazing of intertidal gastropods on</p><p>rocky shoresR.E. Forrest, M.G. Chapman), A.J. Underwood</p><p>Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories, A11,Uniersity of Sydney, Sydney, NSW 2006, Australia</p><p>Received 25 May 2000; received in revised form 8 December 2000; accepted 5 January 2001</p><p>Abstract</p><p>Wax discs have been used previously on intertidal rocky shores to record the grazing activityof gastropods. This study has evaluated this methodology for recording grazing of four commonintertidal microalgal grazers on intertidal shores in New South Wales, Australia. In the laboratory,</p><p> .the four species examinedthe patellid limpet, Cellana tramoserica Sowerby , the trochid, .Austrocochlea porcata A. Adams , the neritid, Nerita atramentosa Reeve and the littorinid,</p><p> .Bembicium nanum Lamarck made distinctive marks in the wax. These allowed identificationof each species or combinations of species grazing over the different discs. Field experimentsshowed that the intensity of grazing, as indicated by the mean number of scratches per disc, waspositively related to the number of gastropods in the surrounding area during low tide for C.tramoserica. The number of scratches per disc in any area was correlated with the percentage of</p><p>discs scratched. The relationship for C. tramoserica was found at two scalesin sites approxi-. .mately 3=3 m and also in plots 50=50 cm within sites. Therefore, densities that were</p><p>measured when these limpets were inactive during low tide provided good estimates of grazingactivity during high tide. This is largely because these limpets do not move far between wherethey rest and where they feed. The amount of microalgal food in the vicinity was not correlatedwith density, nor with grazing intensity. No relationship between density and grazing intensity was</p><p>found for N. atramentosa, although experiments were only done in the field at one spatial scale in.sites, 3=3 m . Results obtained in the laboratory and in the field show that wax discs are useful</p><p>to distinguish grazing by different species of gastropods on Australian rocky shores and allowtests of hypotheses about grazing activity at different spatial scales. q 2001 Elsevier Science B.V.All rights reserved.</p><p>Keywords: Gastropods; Grazing; Microalgae; Quantification; Rocky shores</p><p>) Corresponding author. Tel.: q61-2-9351-4778; fax: q61-2-9351-6713. .E-mail address: gee@bio.usyd.edu.au M.G. Chapman .</p><p>0022-0981r01r$ - see front matter q2001 Elsevier Science B.V. All rights reserved. .PII: S0022-0981 01 00212-X</p></li><li><p>( )R.E. Forrest et al.rJ. Exp. Mar. Biol. Ecol. 258 2001 155171156</p><p>1. Introduction</p><p>Grazing by large herbivorous gastropods on intertidal shores has important effects onthe distribution and abundance of algae Castenholz, 1961; Nicotri, 1977; Lubchenco,</p><p>1980, 1983; Underwood, 1980, 1984a; Lubchenco and Gaines, 1981; Underwood and.Jernakoff, 1981, 1984; Hawkins and Hartnoll, 1983; Jernakoff, 1985a,b . The cover of</p><p>algae, in turn, influences many other components of intertidal assemblages, for example,by providing shelter from desiccation during low tide Hruby and Norton, 1979;</p><p>. Brawley and Johnson, 1991 , overgrowing and killing other sessile organisms Connell,.1961; Dayton, 1971; Denley and Underwood, 1979; Jernakoff, 1985c , modifying</p><p> . ecological processes, such as competition Kastendiek, 1982 or predation Underwood,. .1999 , or pre-empting space and thereby preventing recruitment Hawkins, 1983 .</p><p>Because of such strong direct and indirect effects of grazing, there is much interest inspatial and temporal patterns of distribution and activity of intertidal gastropods. Grazingbehaviour is not, however, easy to measure directly with many levels of spatial andtemporal replication. Most procedures that have been used to measure grazing directly</p><p> .are time-consuming e.g. Boyden and Zeldis, 1979; Kitting, 1979; Petraitis, 1992 andonly allow relatively few animals to be measured during any single period of foraging.Therefore, the intensity of grazing in an area has usually been estimated indirectly, bymeasuring the movement of animals, assuming that there are straightforward relation-</p><p> .ships between movement and grazing. It is usually assumed e.g. Branch, 1971 thatwhen snails and limpets move, they are feeding.</p><p>A common, but even more indirect measure of grazing is the local density of grazersMackay and Underwood, 1977; Underwood, 1977; Chelazzi et al., 1983; Levings and</p><p>.Garrity, 1983; Chapman, 1995 . For logistic reasons, it is usual to record densitiesduring low tide when the animals are relatively inactive and the habitat is easily</p><p>accessible e.g. Underwood, 1976a, 1978, 1984b; Creese, 1980; Creese and Underwood,.1982; Marshall and Keough, 1994 , even though many animals feed at other states of the</p><p> .tide reviewed by Underwood, 1979; Hawkins and Hartnoll, 1983 . The density ofgrazers is not always a reliable measure of grazing in an area, especially for species that</p><p>feed far from their positions during low tide Cook and Cook, 1981; Levings and.Garrity, 1983; Chelazzi et al., 1990; reviewed by Chapman and Underwood, 1992 .</p><p>Intertidal gastropods are often patchily distributed at very small spatial scales cmm;.Chapman, 1994; Underwood and Chapman, 1996, 1998 and this may result in</p><p>concentrated patterns of grazing, especially if the animals do not move far when .foraging Chapman, 1995 . Limited extent of movement while foraging may concentrate</p><p>grazing within very small patches of habitat Mackay and Underwood, 1977; Under-.wood, 1977; Chapman, 2000a , either because of the distribution of particular microhab-</p><p> .itats Creese, 1982; Chapman, 1995, 2000b or because of patchiness in the microalgal .food supply Nicotri, 1977; Underwood, 1984a,b; MacLulich, 1987 . Therefore, if</p><p>density of animals is to be used to infer intensity of grazing, care must be taken tomeasure densities at appropriate spatial scales. Such scales are, however, not alwayseasy to identify.</p><p>Recently, a new method for recording grazing by gastropods in the field wasdeveloped, which can address directly the links between local densities, extent of</p></li><li><p>( )R.E. Forrest et al.rJ. Exp. Mar. Biol. Ecol. 258 2001 155171 157</p><p> .movement and intensity of grazing Thompson et al., 1997 . This method used waxdiscs, inserted into the rocky intertidal substratum, to record the radular scratches ofgrazing gastropods, thus providing a quantitative measure of grazing intensity. Becauseradular morphology varies among species, different species of gastropod can leaveidentifiable scratches in the surface of the wax. Discs can be placed in many sitessimultaneously and left for varying periods of time, thereby providing direct quantitativemeasures of grazing of a variety of species in different places and at different times, to</p><p> .test directly various hypotheses about intensity of grazing Thompson et al., 1997 .This study examines the applicability of this technique for measuring grazing of</p><p>gastropods on Australian rocky shores. First, laboratory experiments were done to test .the hypothesis that the patellid limpet, Cellana tramoserica Sowerby , the trochid,</p><p> .Austrocochlea porcata A. Adams , the neritid, Nerita atramentosa Reeve and the .littorinid, Bembicium nanum Lamarck , which have different types of radulae, would</p><p>leave distinctive and identifiable scratches when feeding. These species are among thelargest and most common intertidal herbivorous gastropods in New South Wales andhave been the subject of many previous investigations into their feeding behaviour,</p><p> .movements and distribution e.g. Underwood, 1975, 1976a,b, 1977, 1978 . They feed inthe same areas on the same microalgal food, for which they often compete Underwood,</p><p>.1984b .Wax discs were also used in field experiments to test hypotheses about the relation-</p><p>ship between density of gastropods and intensity of grazing. The first field experimentexamined the model that densities of N. atramentosa and C. tramoserica, measuredduring low tide in sites approximately 3=3 m, would be reliable indirect estimates ofthe relative amount of grazing activity in these sites during high tides.</p><p> . .Microalgal food Underwood, 1984a,b , feeding Mackay and Underwood, 1977 and .density of limpets Underwood and Chapman, 1996, 1998 are all patchy at small spatial</p><p> .scales. The model was therefore proposed that density in very small plots 50=50 cm .within various sites 3=3 m sites, as used before would correlate better with intensity</p><p>of grazing than was the case at the larger scale of sites. A second field experiment was .therefore done using C. tramoserica, to examine the models that: 1 local density</p><p>during low tide is a better estimate of grazing activity at small scales than at larger .scales, 2 densities of inactive animals during low tide are a reliable measure of</p><p> .densities of active feeding animals in the same area during high tide and 3 grazingintensity is related to the amount of microalgae in the immediate vicinity.</p><p>2. Materials and methods</p><p>2.1. Preparation of the wax discs</p><p> .Plastic holders 14- mm diameter were placed upside-down on glass and filled with . . hot 958C dental wax Boral Investo via the hole in the base of the holder after</p><p>.Thompson et al., 1997 . To avoid uneven cooling of the wax, the glass was kept hot by</p></li><li><p>( )R.E. Forrest et al.rJ. Exp. Mar. Biol. Ecol. 258 2001 155171158</p><p>resting it over a bath of hot water. After the holders had been filled, the glass andholders were refrigerated for 1 h. They were then allowed to return to room temperature,after which, holders were removed from the glass, resulting in wax discs with a smooth,shiny surface. The wax-filled holders could then be inserted into holes drilled into therock-surface. The discs fitted snugly into the holes, with the surface of the wax flushwith the rock surface.</p><p>2.2. Laboratory experiments</p><p>The first laboratory experiment tested the hypothesis that different species of grazerswould leave distinctive and identifiable marks in the wax discs. Twelve wax discs were</p><p> .embedded into the top surfaces of each of four sandstone plates 25=25 cm . One platewas placed into each of four aquaria, each containing 12 individuals of either C.tramoserica, N. atramentosa, B. nanum or A. porcata. Discs were removed from theaquaria after 7 days, and the experiment was repeated. The discs were examined for</p><p> .scratches under a light microscope and also using scanning electron microscopy SEM .To test the hypothesis that marks from different species could be identified when discswere scratched by more than one species, a similar experiment was done usingcombinations of two of the four species in each aquarium. All six possible combinationsof two species were tested. Again, discs were removed after 7 days and examined undera light microscope. Finally, to test the hypothesis that the marks could be used reliablyto identify the species making the marks, blind tests were conducted with six volunteers.Volunteers were given a set of SEM images of the marks made by different species and20 discs that had been scraped by one or two species. They were asked to identify whichspecies had scraped each of the discs.</p><p>2.3. Field experiments</p><p>The experiments were done on intertidal shores in the Cape Banks Scientific MarineResearch Area, New South Wales, Australia described in detail in Underwood et al.,</p><p>.1983 . The first experiment tested the hypothesis that the number of scratches on discswould be significantly larger in places with large densities of gastropods, becausedensity was considered an indirect measure of the intensity of grazing in a given area.</p><p>For each of the two species, C. tramoserica and N. atramentosa, two sites each.approximately 3=3 m with large densities of animals and two sites with small</p><p>densities were chosen. Density was estimated from counts in 10 AlargeB randomly .placed quadrats 50=50 cm in each site. Densities of N. atramentosa were measured</p><p>on Days 1, 3 and 8 of the experiment; densities of C. tramoserica were measured onDays 1 and 6. Sites were at similar heights on the shore and did not noticeably differ interms of topographical complexity or cover of macroalgae. Sites varied in their distancesfrom one another, but the average distance between sites was approximately 10 m.</p><p>In each site, four arrays of nine regularly spaced discs were inserted into the rock.Each array was a grid with approximately 5-cm spacing between adjacent discs. Arrays</p></li><li><p>( )R.E. Forrest et al.rJ. Exp. Mar. Biol. Ecol. 258 2001 155171 159</p><p>were approximately 13-m apart and were haphazardly placed on relatively flat patchesof substratum, which were free of foliose algae. In sites with N. atramentosa, discs wereplaced in each site on the same day and were left for 8 days. In sites with C.tramoserica, due to poor weather, discs could only be placed in one site with largedensity and one site with small density on the first day. These discs were collected after6 days, when the experiment was repeated in two new sites. This period of time waschosen because previous experiments with other species indicated that a period of 714</p><p>days was optimal i.e. discs should be scratched but not yet saturated with scratches;.Thompson et al., 1997 . All discs were returned to the laboratory, examined under the</p><p>light microscope and the scratches made on each disc by the species of interest werecounted.</p><p>The second experiment, designed to test the hypothesis that there would be a closerpositive relationship between number of scratches per disc and density of gastropods atsmaller spatial scales within sites than at the scale of sites, was done using only C.</p><p> .tramoserica. Six sites approximately 3=3 m were chosen, three with large and threewith small densities of limpets, measured as described previously. Density measured</p><p> .using AlargeB quadrats 50=50 cm over the whole site was referred to as density at thelarger scale. Density was measured on four occasions for over 5 weeks to ensure that thedensities were maintained prior to and during the experiment. Density was also</p><p> .measured in three plots 50=50 cm within each site, which were haphazardly chosenand approximately 0.51m apart. In each plot, limpets were counted in four replicate</p><p> .AsmallB quadrats 13=13 cm . Density measured using AsmallB quadrats, in plots, wasreferred to as density at the smaller scale. The experiment started after ensuring that thedensities in sites had remained consistent for 3 weeks. Two replicate arrays of nine wax</p><p> .discs each array approximately 13=13 cm were placed into each plot and left in thefield for 1 week. They were then returned to the laboratory, where the scratches made byC. tramoserica on each disc were counted as previously. The mean number of scratchesper disc and mean density at the larger and at the smaller spatial scale were recorded. Inboth cases, the mean density was the a...</p></li></ul>


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