quantification of radular marks as a method for estimating grazing of intertidal gastropods on rocky...
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Journal of Experimental Marine Biology and Ecology .258 2001 155171
Quantification of radular marks as a method forestimating grazing of intertidal gastropods on
rocky shoresR.E. Forrest, M.G. Chapman), A.J. Underwood
Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories, A11,Uniersity of Sydney, Sydney, NSW 2006, Australia
Received 25 May 2000; received in revised form 8 December 2000; accepted 5 January 2001
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,
.the four species examinedthe patellid limpet, Cellana tramoserica Sowerby , the trochid, .Austrocochlea porcata A. Adams , the neritid, Nerita atramentosa Reeve and the littorinid,
.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
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
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
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
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.
Keywords: Gastropods; Grazing; Microalgae; Quantification; Rocky shores
) Corresponding author. Tel.: q61-2-9351-4778; fax: q61-2-9351-6713. .E-mail address: firstname.lastname@example.org M.G. Chapman .
0022-0981r01r$ - see front matter q2001 Elsevier Science B.V. All rights reserved. .PII: S0022-0981 01 00212-X
( )R.E. Forrest et al.rJ. Exp. Mar. Biol. Ecol. 258 2001 155171156
Grazing by large herbivorous gastropods on intertidal shores has important effects onthe distribution and abundance of algae Castenholz, 1961; Nicotri, 1977; Lubchenco,
1980, 1983; Underwood, 1980, 1984a; Lubchenco and Gaines, 1981; Underwood and.Jernakoff, 1981, 1984; Hawkins and Hartnoll, 1983; Jernakoff, 1985a,b . The cover of
algae, in turn, influences many other components of intertidal assemblages, for example,by providing shelter from desiccation during low tide Hruby and Norton, 1979;
. Brawley and Johnson, 1991 , overgrowing and killing other sessile organisms Connell,.1961; Dayton, 1971; Denley and Underwood, 1979; Jernakoff, 1985c , modifying
. ecological processes, such as competition Kastendiek, 1982 or predation Underwood,. .1999 , or pre-empting space and thereby preventing recruitment Hawkins, 1983 .
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
.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-
.ships between movement and grazing. It is usually assumed e.g. Branch, 1971 thatwhen snails and limpets move, they are feeding.
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
.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
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
.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
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 .
Intertidal gastropods are often patchily distributed at very small spatial scales cmm;.Chapman, 1994; Underwood and Chapman, 1996, 1998 and this may result in
concentrated patterns of grazing, especially if the animals do not move far when .foraging Chapman, 1995 . Limited extent of movement while foraging may concentrate
grazing within very small patches of habitat Mackay and Underwood, 1977; Under-.wood, 1977; Chapman, 2000a , either because of the distribution of particular microhab-
.itats Creese, 1982; Chapman, 1995, 2000b or because of patchiness in the microalgal .food supply Nicotri, 1977; Underwood, 1984a,b; MacLulich, 1987 . Therefore, if
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.
Recently, a new method for recording grazing by gastropods in the field wasdeveloped, which can address directly the links between local densities, extent of
( )R.E. Forrest et al.rJ. Exp. Mar. Biol. Ecol. 258 2001 155171 157
.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
.test directly various hypotheses about intensity of grazing Thompson et al., 1997 .This study examines the applicability of this technique for measuring grazing of
gastropods on Australian rocky shores. First, laboratory experiments were done to test .the hypothesis that the patellid limpet, Cellana tramoserica Sowerby , the trochid,
.Austrocochlea porcata A. Adams , the neritid, Nerita atramentosa Reeve and the .littorinid, Bembicium nanum Lamarck , which have different types of radulae, would
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,
.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,
.1984b .Wax discs were also used in field experiments to test hypotheses about the relation-
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.
. .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
.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
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
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
.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.
2. Materials and methods
2.1. Preparation of the wax discs
.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
.Thompson et al., 1997 . To avoid uneven cooling of the wax, the glass was kept hot by
( )R.E. Forrest et al.rJ. Exp. Mar. Biol. Ecol. 258 2001 155171158
resting it over a bath of hot water. After the holders had been filled, the glass andholders were refrigerated fo