255 (2000) 1–19
www.elsevier.nl / locate / jembe
Grazing by two species of limpets on artificial reefs in the
northwest Mediterranean
*
Fabio Bulleri , Massimo Menconi, Francesco Cinelli, Lisandro Benedetti-Cecchi
Dipartimento di Scienze dell’Uomo e dell’Ambiente, via A. Volta 6, 56126 Pisa, Italy Received 14 January 2000; received in revised form 7 July 2000; accepted 1 August 2000
Abstract
The extensive presence of artificial reefs in marine coastal habitats demands a better understanding of the extent to which these structures can be considered surrogates of natural rocky shores for populations of plants and animals. The primary aim of this study was to test the hypothesis that removing limpets from the midlittoral of artificial breakwaters in the northwest Mediterranean led to changes in assemblages similar to those observed on rocky shores in the same area. Orthogonal combinations of the presence / absence of two species of limpets, P. aspera and P rustica, were produced using manual removals from June 1997 to February 1998. To test the hypothesis that the effects of limpets were variable at spatial scales comparable to those investigated on rocky shores, we repeated the experiment at two locations tens of kilometres apart, and on two reefs within each location a few kilometres apart. The results revealed strong and relatively consistent negative effects of limpets on filamentous algae, whereas interactions with other members of assemblages were complex and variable. Several taxa (Cyanophyta, encrusting and articulated coralline algae, Ralfsia and Rissoella) were abundant at one location but nearly absent at the other. This large-scale variability in patterns of distribution generated inconsistencies in the effects of limpets between locations. Within locations, several effects of P. aspera and P. rustica were observed, ranging from independent effects on some organisms, to additive or interactive effects on others. Apparently, the removal of filamentous algae by limpets resulted in positive indirect effects on Ralfsia and Rissoella. Collectively, these effects were comparable to those described for rocky shores in the northwest Mediterranean. The processes accounting for large-scale variation in grazing, however, appeared different between the natural and the artificial habitat. 2000 Elsevier Science B.V. All rights reserved.
*Corresponding author. Present address: Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories A 11, University of Sydney, Sydney NSW 2006, Australia. Tel.: 161-2-9351-2039; fax: 161-2-9351-6713.
E-mail address: [email protected] (F. Bulleri).
Keywords: Artificial reefs; Intertidal; Limpets; Patella aspera; Patella rustica; Grazing; Indirect effects; Spatial heterogeneity
1. Introduction
Artificial reefs and breakwaters are common structures in marine coastal habitats. Breakwaters are used to build marinas and harbours and to protect sandy shores from erosion. Subtidal reefs are thought to attract species previously absent in the area, and are often used to restore over-fished populations by increasing the complexity of the habitat and the availability of shelter (Seaman et al., 1989; Carr and Hixon, 1997). Since these structures act as surrogates of rocky shores, it is important to understand whether they support assemblages that are comparable to those found on natural substrata and if the ecological processes operating in the two environments are also similar.
Most of the ecological studies on artificial reefs and breakwaters have been confined to subtidal habitats. There have been studies assessing the effectiveness of artificial reefs in mitigating losses of commercial species due to human disturbance (Ambrose, 1994; Carr and Hixon, 1997), some experimental investigations on the effects of dispersal, recruitment, physical processes and biological interactions in influencing the structure of epibiota on artificial structures (Grosberg, 1982; Keough and Butler, 1983; Keough, 1984; Breitburg, 1985; Anderson and Underwood, 1997), and comparisons of assem-blages on these structures with those of rocky shores (Connell and Glasby, 1999; Glasby, 1999). More generally, studies on artificial substrata have contributed to the development and refinement of ecological models to explain patterns in natural habitats (e.g., Sutherland, 1974; Sutherland and Karlson, 1977; Anderson, 1998). In contrast, much less is known about patterns and processes of intertidal assemblages on artificial substrata.
The present study is part of a research programme on the ecology of epibenthic assemblages on hard substrata, including both rocky shores and artificial reefs, in the northwest Mediterranean. Here we focus on the effects of limpets in midshore habitats provided by artificial reefs. Understanding grazing on artificial substrata is important for comparative purposes, since this is one of the most intensively studied and better understood processes on rocky shores. Many studies from different geographical areas have shown that molluscan herbivores can have profound effects on the structure of assemblages in natural habitats (Underwood, 1980; Lubchenco and Gaines, 1981; Hawkins and Hartnoll, 1983). In addition to the direct effects documented by these studies, intertidal gastropods can also exert a variety of indirect effects. For example, they can prevent the monopolization of the substratum by ephemeral algae thereby enhancing the establishment of other algae and invertebrates (reviewed in Sousa and Connell, 1992).
overlap at heights on the shore between 0.1 and 0.2 m above the mean-low-water-level (Menconi et al., 1999). Previous experiments (Benedetti-Cecchi and Cinelli, 1993, 1997; Benedetti-Cecchi et al., 1996; Benedetti-Cecchi, 2000) revealed the important role of these grazers in regulating patterns of colonization in disturbed patches. The removal of limpets resulted in the monopolization of the substratum by filamentous algae, whereas in the presence of grazers succession proceeded with the establishment of the fleshy red alga Rissoella verruculosa (Bertolini) J. Agardh, barnacles and the Cyanophyta Rivularia spp. More recently, large-scale studies (employing scales similar to those of the present work) have shown considerable spatial variability in the effects of limpets among shores tens to hundreds of kilometres apart (Benedetti-Cecchi et al., in press). These experiments were carried out on rocky shores adjacent to the artificial structures studied in the present paper and the two species of limpets, which were found at densities similar to those here reported (see Section 3), were considered as a guild and excluded by means of cages (Benedetti-Cecchi et al., in press).
The focus of this paper is on the effects of P. aspera and P. rustica on assemblages of algae and barnacles developing on artificial reefs in the northwest Mediterranean. The primary aim of this study was to test the hypothesis that removing limpets from these manufactures led to changes in the structure of assemblages similar to those observed on rocky shores. Furthermore, we examined whether there were inconsistencies in the effects of limpets at spatial scales comparable to those investigated on rocky shores. These hypotheses were tested with a multifactorial experiment involving the orthogonal manipulation of the presence / absence of the two species of limpets. The experiment was repeated at different locations (tens of kilometres apart), on different reefs within each location (a few kilometres apart), and using replicate boulders within reefs (tens to hundreds of metres apart) as the experimental units. This experiment also allowed us to test the null hypotheses that P. rustica and P. aspera had similar effects on assemblages, and that one species had no influence on the distribution of the other on the artificial reefs (these hypotheses have not been tested yet on rocky shores).
2. Materials and methods
2.1. Study site
This study was done at two exposed locations (Carrara, 448029N, 108019E and Livorno, 438279N, 108219E), on the northwest coast of Italy, between June 1997 and February 1998. The two locations were about 70 km apart and were characterised by the presence of industrial developments and marinas. Two artificial reefs, about 4 km apart, were used at each location (referred to as Reef 1 and Reef 2 from north to south at each location, respectively). These reefs were 150–300 m long and run parallel to the coastline experiencing intense wave action due to western winds (from southwest to northwest). The reefs were made of transplanted carbonatic boulders, with their longer axis ranging from 1 to 3 m.
Cinelli, 1993, 1997; Cecchi et al., 1996; Menconi et al., 1999; Benedetti-Cecchi, 2000). The most common algae were encrusting corallines, the brown crust Ralfsia verrucosa (Areschoug) J. Agardh, Cyanophyta of the genus Rivularia, and erect algae such as Rissoella verruculosa (Bertolini) J. Agardh, Nemalion helmintoides (Velley) Batters, Porphyra leucosticta Thuret, the articulated corallines Corallina elongata Ellis and Solander and Haliptilon virgatum (Zanardini) Garbary and Johansen, the coarsely branched Laurencia obtusa (Hudson) Lamouroux and Chondria spp. (De Notaris) De Toni, and the filamentous Polysiphonia spp. and Ceramium spp. The most abundant sessile invertebrates were the barnacles Chthamalus montagui Southward and Chthmalus stellatus (Poli), while the main herbivores were the limpets Patella aspera, Patella rustica and the snail Osilinus turbinatus (Von Born); these herbivores were distributed at heights on the shore ranging from 20.2 to 0.4 m with respect to mean-low-water-level.
2.2. Experimental designs and analysis of data
Twelve boulders with the longer axis no less than 2 m in length were selected randomly on the seaward side of each reef. These boulders were numbered with marine epoxy for identification and randomly allocated to four treatments with three replicates each. Treatments were: (1) control, where all limpets had been left in place (1Pa1Pr), (2) removal of P. aspera (2Pa1Pr), (3) removal of P. rustica (1Pa2Pr), and (4) removal of both species (2Pa2Pr). Limpets were removed by hand with the aid of a screw driver; boulders were searched thoroughly at the beginning of the experiment and every 3–4 weeks thereafter to maintain the experimental conditions.
The percentage cover of sessile organisms and the density of mobile grazers were assessed after 4 and 8 months using quadrats of 10310 cm in size. Estimates of percentage cover were obtained visually by subdividing the quadrat in 25 232cm sub-quadrats (Dethier et al., 1993; Benedetti-Cecchi et al., 1998). Densities of grazers were expressed as the number of animals present in each quadrat. Sampling was restricted to the seaward side of the boulders, because only this side provided a habitat comparable to that of rocky shores (authors’ personal observation). Three quadrats were placed randomly on each boulder at each sampling occasion. To avoid re-sampling the same quadrats and to maintain temporal independence in the data, the first set of replicates was marked with epoxy putty so that they were avoided when boulders were sampled the second time.
2.3. Analysis of data
Data from the two locations were analysed separately, since the densities of the two species of limpets and the assemblages were markedly different.
(2) Cyanophyta, (3) articulated coralline algae, (4) filamentous algae, (5) Ralfsia verrucosa, (6) Rissoella verruculosa, and (7) Chthamalus spp. The same model of analysis was used to determine the efficacy of the manipulation and to test for the effects of one species of limpet on the density of the other. In these tests, the factor corresponding to the species of limpet which was also the response variable in the analysis, was termed Removal and tested for the efficacy of the experimental manipula-tion. Cochran’s C-test (Winer, 1971; Underwood, 1997) was used to check the assumption of homogeneity of variances. In some cases it was necessary to transform the data (square root or logarithmic scale) to meet this assumption. Pooling procedures were also used when appropriate, according to Winer (1971). Student–Newman–Keuls tests (SNK) were used for a posteriori comparisons of the means.
3. Results
3.1. Density and size of limpets
Manual removal was effective in reducing the density of P. aspera in the appropriate treatments at Carrara, although it was impossible to maintain boulders completely free of these herbivores (Fig. 1A,C); the analysis detected a significant main effect of Removal (F1,1567.11, P,0.05, MSReef3Removal50.250), indicating that the manipulation was consistent across treatments.
At Livorno, no significant effect of the manipulation of P. aspera was disclosed by the analysis, but a sensible decrease in its density, in particular on Reef 2, can be noticed by inspection of the graphs (Fig. 1B,D).
The efficacy of removing P. rustica changed significantly from time to time and from reef to reef at Carrara (analysis on ln(x11) transformed data, C50.119, P.0.05; Reef3Removal3Time: F1,1655.97, P,0.05, MSBoulder3Time50.278 and Fig. 1E,G). SNK tests within this interaction, however, indicated that manual removal of P. rustica significantly reduced the density of this species compared to unmanipulated boulders on all reefs at both sampling occasions, but on Reef 1 at Time 1.
In contrast, the effectiveness of the manipulation of P. rustica at Livorno was consistent in time and between reefs (Fig. 1F,H), resulting in a significant main effect of the Removal (analysis on ln(x11) transformed data, C50.120, P.0.05; F1,16567.11, P,0.01, MSBoulder50.641).
At both locations the analysis disclosed a large heterogeneity among boulders in the density of P. aspera (Carrara: F16,9653.66, P,0.001, MSResidual59.139; Livorno: F16,9653.12, P,0.001, MSResidual53.611) and P. rustica (Carrara: F16,9652.23, P,0.001, MSResidual50.407; Livorno: F16,9654.51, P,0.001, MSResidual50.142).
The size of P. aspera was not affected by the manual removal and was variable among boulders at both locations (Carrara: F16,9651.85, P,0.05, MSResidual522.023; Livorno: F16,9653.07, P,0.001, MSResidual529.218). Furthermore the analysis indi-cated as significant the effect of main term Time at Carrara (F1,15781.53, P,0.05, MSReef3Time50.005).
at Carrara, but the effects of the manipulation were not consistent through time and between reefs (Reef3Removal3Time: F1,9653.78, P,0.05, MSResidual536.580); SNK tests revealed that larger specimens always dwelled on boulders where this species was left at natural densities, except for Reef 1 after 4 months from the initiation of the experiment, where the size did not differ between treatments.
At Livorno the analysis detected a significant effect of the interaction Removal3P. aspera3Time (F1,15271.50, P,0.05, MSTime3Reef3Removal3P. aspera50.052), suggest-ing that the size of P. rustica was affected by the manipulation, which effects varied through time and with the removal of the other species. Anyway, the SNK test indicated that larger individuals were on the boulders where this species was left untouched, irrespectively for the presence or absence of P. aspera, at both times of sampling.
3.2. Effects on algae and barnacles
Limpets had no effect on the percentage cover of Cyanophyta (Fig. 2A–D), which were abundant at Livorno and nearly absent at Carrara. At the former location the abundance of Cyanophyta also varied among boulders and between reefs (Table 1); variability was not consistent through time at the smaller spatial scale.
P. aspera had significant effects on the percentage cover of encrusting coralline algae at Livorno, but they were variable between reefs (Fig. 2F,H and Table 1). The removal of P. aspera resulted in a significant reduction in the percentage cover of encrusting coralline algae on Reef 1, while the opposite occurred on Reef 2 (Fig. 2F,H and Table 1). The pattern observed on Reef 1 probably reflected initial differences in the abundance of these algae among boulders assigned to different treatments (Fig. 2F). Finally, the analysis detected a large variability among boulders (Table 1).
Encrusting coralline algae were nearly absent at Carrara and their percentage cover varied through time (F1,15270.18, P,0.05, MS Reef3Time50.065).
In contrast to the patterns described above, Ralfsia verrucosa was abundant on reefs at Carrara while it was poorly represented at Livorno (Fig. 2I,N). At the former location, both the limpets affected the abundance of this species, but their effects were variable between reefs, resulting in a significant Reef3P. rustica3P. aspera interaction (Table 1). SNK tests within this interactions did not indicate any effect of limpets (Table 1). Also the interaction P. aspera3Time was significant (Table 1) and SNK tests showed that the removal of this species negatively affected the percentage cover of R. verrucosa at Time 1, while it had no effect at Time 2.
At Livorno, the abundance of R. verrucosa was higher on boulders where P. aspera was removed (especially on Reef 2), but the analysis did not disclose any significant effect of the manipulation of this species. The percentage cover of R. verrucosa was variable among boulders (F16,965P,0.01, MS Residual50.910).
Table 1
ANOVAs on the effects of the removal of limpets, Reef, Boulder and Time on the percent cover of encrusting algae
Source of d.f. Cyanophyta Encrusting corallines Ralfsia verrucosa
variation
Livorno Livorno Carrara
MS F MS F MS F
Reef 5Re 1 32.911 10.72** 1.799 1899.507
ns ns
P. rustica 5Pr 1 4.341 2.85 0.360 0.05 2491.674
ns
P. aspera 5Pa 1 5.337 0.69 0.043 122.840
ns ns
Time 5Ti 1 3.809 0.838 0.81 1302.007 72.08
ns ns
Re3Pr 1 1.526 0.50 7.022 1.71 955.840
ns
Re3Pa 1 7.704 2.51 34.095 8.32* 2409.174
ns ns ns
Pa3Ti 1 1.373 102.55 0.214 1.84 3277.562 8.47*
ns ns
Boulder (Re3Pr3Pa) 16 3.071 4.097 7.92*** 1352.514 2.75
ns ns
Re3Pa3Ti has been eliminated as no significant at P50.25.
*P,0.05; **P,0.01; ***P,0.001. ns, not significant. Analysis relating to locations where the percentage cover of these algae was very low
are not reported in this table, but relevant results are reported in the text (see Section 3).
reefs or times. For these reasons, this interaction was not considered likely to invalidate comparisons of other sources of variation. The other significant interaction was that between Reef and P. rustica (Table 2). The removal of P. rustica resulted in a significant increase in cover of articulate coralline algae on Reef 1, but not on Reef 2 (Fig. 3A,C and Table 2); this effect was more evident at Time 2.
F
ANOVAs on the effects of the removal of limpets, Reef, Boulder and Time on the percent cover of erect algae
Source of d.f. Articulated corallines Filamentous algae Rissoella verruculosa
variation Carrara Carrara Livorno Livorno
MS F MS F MS F MS F
ns
Reef 5Re 1 1.342 0.442 0.22 0.010 0.813 0.27
ns
P. rustica 5Pr 1 1.450 2.497 0.92 5.646 0.080
P. aspera 5Pa 1 0.288 24.813 329.78** 3.334 0.001
ns
Time 5Ti 1 41.247 77.005 22.57 5.509 44.821
a ns ns
Pr3Pa 1 0.294 0.153 0.04 2.520 229.71* 1.019
ns ns
Boulder (Re3Pr3Pa) 16 1.472 2.04* 2.016 1.587 1.83* 48.272 2.62**
ns ns
Boulder (Re3Pr3Pa)3Ti 16 0.715 0.99 3.412 2.59* 0.664 0.76 23.616 1.28
Residual 143 0.722 1.316 0.868 1.153
Cochran’s test C50.131, P.0.05 C50.093, P.0.05 C50.080, P.0.05 C50.081, P.0.05
Transformation ln (x11) ln (x11) None ln (x11)
SNK tests Articulated corallines Filamentous algae (Livorno) Rissoella verruculosa
Re3Pr Pr3Pa Pr3Pa3Ti
Re3Ti has been eliminated from the analysis, as no significant at P50.25.
*P,0.05; **P,0.01; ***P,0.001. ns, not significant. Analysis relating to locations where the percentage cover of these categories of algae was very low are not displayed in this table, but relevant results are reported
Table 3
ANOVAs on the effects of the removal of limpets, Reef, Boulder and Time on the percent cover of Chthamalus spp.
Re3Pr3Pa has been eliminated from the analysis as no significant at P50.25.
b
See text for details.
*P,0.05; **P,0.01; ***P,0.001. ns, not significant.
P. aspera significantly reduced the percentage cover of filamentous algae at Carrara (Fig. 3E,G and Table 2). This effect was not evident at Time 2 because there were few filamentous algae in all plots on that sampling occasion (Fig. 3E,G); anyway, the analysis indicated as significant the effect of the main terms P. aspera and Time, but not that of their interaction (Table 2). There were significant differences among boulders in the percentage cover of filamentous algae that changed from time to time (Table 2).
could not identify a clear pattern for this interaction, but suggested that in absence of P. rustica the percentage cover of these algae was higher when also was P. aspera removed.
Furthermore, there were large differences in the abundance of filamentous algae from reef to reef and from boulder to boulder, which were not consistent through time in the former case.
Rissoella verruculosa was absent at Carrara, while it occurred on the reefs at Livorno (Fig. 3I–N). The effects of the two species of limpets at Livorno were complex and interactive, also changing from time to time and resulting in a significant P. rustica3P. aspera3Time interaction (Table 2). No effects of limpets were revealed at Time 1, while at Time 2 the removal of one species of limpets resulted in a significant increase in the percentage cover of Rissoella, but only if the other species was present. In contrast, removing both species produced a decline in cover of the alga (Fig. 3L,N and Table 2). The percentage cover of Rissoella changed significantly among boulders (Table 2).
Barnacles were more abundant at Livorno than at Carrara (Fig. 4). At the latter location, P. rustica and P. aspera affected the percentage cover of Chthamalus spp. but these effects were not consistent across reefs and times of sampling, according to the significant Reef3P. rustica3P. aspera3Time interaction (Fig. 4A,C and Table 3). As just a few significant differences, not consistent across reefs and times, were pointed out
by SNK tests, lower order significant interactions were further considered. This was the case of the interaction Reef3P. rustica3Time, which indicated that the removal of P. rustica increased the percentage cover of barnacles on Reef 1 at Time 1, and on Reef 2 at Time 2 (Fig. 4 and Table 3). At Livorno also, the analysis suggested an interactive effect of both the species of limpets on the percentage cover of Chthamalus spp. (Fig. 4B,D and Table 3). The removal of P. rustica and P. aspera had a positive effect on the abundance of these barnacles, but only when the other species was left untouched; there were no further effects of removal of a species in absence of the other (SNK test, Table 3). Furthermore, the interaction Reef3P. rustica was significant and the SNK test indicated that the removal of this limpet increased the abundance of barnacles on Reef 1, while the opposite occurred on Reef 2. The percentage cover of barnacles varied among boulders at both locations (Table 3).
4. Discussion
The results of this study indicate that limpets can have strong and relatively consistent effects on filamentous algae on artificial reefs, whereas interactions with other members of assemblages were complex and variable. This complexity was revealed by inconsis-tencies in the effects of the limpets at different spatial scales and through time. Our data cannot test for the effects of grazing at the largest spatial scale, between locations, since they are totally confounded with differences between assemblages: Cyanophyta, encrusting coralline algae and Rissoella were abundant at Livorno but nearly absent at Carrara, whereas the opposite was true for articulate coralline algae and Ralfsia; only filamentous algae showed a similar abundance at the two study locations. Also the density of limpets was different at the scale of tens of kilometers, being the two species more abundant at Carrara.
Within locations, effects due to one or the other species of limpets, additive or multiplicative effects of these grazers and interactions between limpets and time, were common.
Previous studies in the northwest Mediterranean have shown that limpets can have strong effects on filamentous algae both in mid-shore and low-shore habitats on rocky coasts (Cecchi and Cinelli, 1993; Cecchi et al., 1996; Benedetti-Cecchi, 2000). Similar effects have been documented in the present study on artificial reefs, where filamentous algae rapidly colonised boulders maintained at reduced densities of grazers, and in particular when P. aspera was removed.
(a location very close to Livorno) (Cecchi and Cinelli, 1993; Benedetti-Cecchi, 2000; Benedetti-Cecchi et al., in press), the largest effects of limpets on artificial reefs occurred at Carrara. The opposite direction of these patterns strongly suggest that the processes driving large-scale variation in the effects of limpets on rocky shores are different from those operating on artificial reefs. Differences in the methodology used to manipulate limpets (fences were used to exclude limpets on rocky shores while manual removal was used in the present study), might also account for some of these inconsistencies.
Collectively, the results above suggest that filamentous algae are largely affected by limpets both on rocky shores and artificial reefs. Grazing on artificial reefs, however, appeared more consistent than grazing on rocky shores, provided that the filamentous algae were able to colonize. Further experiments are needed to determine whether or not these patterns reflect real differences between natural and artificial habitats in the processes accounting for large-scale variation in grazing.
Our results show that of the two species of limpets manipulated, P. aspera had major effects on filamentous algae. Although less abundant than P. aspera, P. rustica was 22
common on control boulders at densities in the range of 1.5–3 ind. 100 cm . Differences between removal and control boulders were maintained throughout the experiment by manual removals, despite spatial and temporal variability in the efficacy of the manipulation. The proportional reduction of P. rustica by manual removal was, however, larger than that achieved with P. aspera (Fig. 1). These patterns suggest that the lack of any effect of P. rustica at Carrara on filamentous algae is not an artifact of the experimental procedure. A tentative explanation for the observed patterns is that P. rustica did not graze for long enough in the experimental plots to keep fast-growing organisms, such as the filamentous algae, under control (although this species did affect other members of the assemblage, as discussed below). Possibly, individuals of P. rustica tended to move up-shore during their foraging excursions to graze on different assemblages of microalgae. Unfortunately, studies on rocky shores do not assist in the interpretation of these results, since no attempt has been done to separate the effects of the two species of limpets in the natural habitat.
was no way for Rissoella to benefit from the presence of limpets and negative effects predominated. In contrast, when both species of limpets were removed and colonization by filamentous algae was, to some extent, successful (at Time 2), the cover of Rissoella declined compared to boulders where only one species of limpets was present (Fig. 3H,N). These outcomes suggest that under moderate grazing, and in the presence of filamentous algae, limpets can generate patterns like those expected in the presence of indirect effects. Differences among treatments were, however, negligible and probably biologically irrelevant.
Limpets are known to affect the abundance of barnacles on rocky shores in different ways. For example, they can enhance the cover of barnacles indirectly, by preventing the monopolization of the substratum by algae (see above). These patterns have been described for rocky shores at Calafuria (Benedetti-Cecchi, 2000) and in other regions around the world (Hawkins, 1983; Underwood et al., 1983; Dungan, 1986; Van Tamelen, 1987). Other studies, however, have shown that limpets can reduce the cover of barnacles by grazing newly settled cyprids or by bulldozing juveniles from the substratum (Dayton, 1971; Branch, 1975; Denley and Underwood, 1979). Barnacles were mostly affected by P. rustica in the present study and effects were largely negative. On Reef 2 at Livorno, however, the removal of P. rustica resulted in a decline in cover of barnacles indicating a positive effect. As already discussed for Rissoella (see above), this might reflect an indirect effect mediated by filamentous algae. This interpretation is, however, only tentative, because filamentous algae never monopolized the substratum on Reef 2. At present, we lack a better explanation for the observed patterns.
Studies on rocky shores have shown that grazing by limpets may be important for the persistence of encrusting algae that otherwise would be replaced by erect species (Paine, 1980; Steneck, 1982). Interactions between limpets and encrusting algae were not so clear on artificial reefs. Removal of P. aspera resulted in an increase in percentage cover of encrusting coralline algae on Reef 2 at Livorno, revealing negative rather than positive effects of grazing. Anyway, the effect of P. aspera on these algae must be interpreted with caution, since the differences between presence / absence of this limpet were present from the beginning of the experiment. The opposite was observed on Reef 1 at Livorno, but this probably reflected the fact that, by chance, boulders with extensive cover of encrusting corallines were assigned to the control treatment at the beginning of the experiment, while boulders supporting few encrusting coralline algae were assigned to the removal treatment (see Fig. 2F). Thus, there was no evidence of positive effects of grazing on encrusting corallines from these data.
Ralfsia can shift from a positive indirect interaction in the presence of filamentous algae, to a direct negative effect that occurs only in the absence of filamentous algae.
The effects of limpets on Ralfsia could not be interpreted in light of the significant Reef3P. aspera3P. rustica interaction, which reflected the average effects of grazing over the two sampling occasions, since no clear pattern could be identified. Although the magnitude and generality of these interactions is far from clear from our results, they do indicate that on artificial reefs the positive effect of limpets on encrusting algae cannot be simply typified as a chain of interactions involving grazers, encrusting algae and their competitors. Rather, patterns are likely to involve complex and yet unexplained interactions among consumers and between consumers and a range of potential resources.
In conclusion, this study has shown that grazing by limpets is an important process on artificial reefs, and a wide range of effects of P. aspera and P. rustica have been documented. The collective effects of the two species are, in large part, comparable to those described for rocky shores in the same area. The processes accounting for large-scale variation in grazing seem, however, different between the natural and the artificial habitat. Understanding this variability is important to assess whether artificial reefs can reproduce the same scales of variation, both in terms of patterns and processes, observed on rocky shores. Future studies should be directed to understand whether P. aspera and P. rustica display the same range of interactions on rocky shores as those described here (from independent to additive and multiplicative effects). Filling this gap would provide an additional basis to assess the extent to which artificial reefs can be considered substitutive of natural habitats in terms of relevant ecological processes.
Acknowledgements
We sincerely thank A. Del Nista and P. Nugnes for their help on field, R.A. Coleman, L. Airoldi and G. Ceccherelli and two anonymous referees for their criticism on the early draft of the manuscript. This work was partially supported by the EC under MAST programme contract MAS3-CT95-0012 (EUROROCK). [AU]
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