F . Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19
5
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 F
5 67.11, P , 0.05, MS 5 0.250, indicating that the manipulation was
1,1 Reef
3Removal
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 lnx
1 1 transformed data, C 5 0.119, P . 0.05; Reef
3 Removal 3 Time: F 5 5.97, P , 0.05, MS
5 0.278 and Fig. 1E,G.
1,16 Boulder
3Time
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 lnx
1 1 transformed data, C 5 0.120, P . 0.05; F 5 67.11,
1,16
P , 0.01, MS
5 0.641.
Boulder
At both locations the analysis disclosed a large heterogeneity among boulders in the density of P
. aspera Carrara: F 5 3.66, P , 0.001, MS
5 9.139; Livorno:
16,96 Residual
F 5 3.12, P , 0.001, MS
5 3.611 and P. rustica Carrara: F 5 2.23,
16,96 Residual
16,96
P , 0.001, MS
5 0.407; Livorno: F 5 4.51, P , 0.001, MS
5 0.142.
Residual 16,96
Residual
The size of P . aspera was not affected by the manual removal and was variable
among boulders at both locations Carrara: F 5 1.85, P , 0.05, MS
5 22.023;
16,96 Residual
Livorno: F 5 3.07, P , 0.001, MS
5 29.218. Furthermore the analysis indi-
16,96 Residual
cated as significant the effect of main term Time at Carrara F 5 781.53, P , 0.05,
1,1
MS 5 0.005.
Reef 3Time
Conversely the size of P . rustica was different between removal and control boulders
6 F
. Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19
Fig. 1. Mean density 1 S.E., n 5 9 of Patella aspera and Patella rustica in the different treatments before
the initiation of the experiment, and after 4 and 8 months. Data are values from three replicate quadrats pooled across three replicate boulders at each time.
F . Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19
7
at Carrara, but the effects of the manipulation were not consistent through time and between reefs Reef
3 Removal 3 Time: F 5 3.78, P , 0.05, MS
5 36.580;
1,96 Residual
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 Removal
3 P. aspera
3 Time F 5 271.50, P , 0.05, MS
5 0.052, suggest-
1,1 Time
3Reef3Removal3P. aspera
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 F
5 270.18, P , 0.05, MS 5 0.065.
1,1 Reef
3Time
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 Reef
3 P. rustica 3 P. aspera interaction Table 1. SNK tests within this interactions did not indicate any effect of limpets Table 1.
Also the interaction P . aspera
3 Time 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 F
5 P , 0.01, MS 5 0.910.
16,96 Residual
P . aspera and P. rustica interactively affected the percentage cover of articulated
coralline algae at Carrara, but patterns changed from reef to reef and from time to time Fig. 3A,C and Table 2. This was shown by the significant Reef
3 P. rustica 3 P. aspera
3 Time interaction Table 3. SNK tests within this interaction, however, showed few significant differences and those that were significant were not consistent across
8 F
. Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19
Fig. 2. Effect of different combination of absence presence of Patella aspera and Patella rustica on mean percentage cover of encrusting algae
1 S.E., n 5 9 as a function of time. Data are values from three replicate quadrats pooled across three replicate boulders at each time.
F . Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19
9 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
5 Re 1
32.911 10.72
1.799 1899.507
ns ns
P . rustica
5 Pr 1
4.341 2.85
0.360 0.05
2491.674
ns
P . aspera
5 Pa 1
5.337 0.69
0.043 122.840
ns ns
Time 5 Ti
1 3.809
0.838 0.81
1302.007 72.08
ns ns
Re 3 Pr
1 1.526
0.50 7.022
1.71 955.840
ns
Re 3 Pa
1 7.704
2.51 34.095
8.32 2409.174
ns ns
ns
Re 3 Ti
1 1.057
0.63 1.032
1.19 18.062
0.05
ns ns
ns
Pr 3 Pa
1 1.627
0.30 1.065
0.91 130.340
0.02
ns ns
ns
Pr 3 Ti
1 0.058
0.04 0.155
11.48 7.562
0.01
ns ns
Pa 3 Ti
1 1.373
102.55 0.214
1.84 3277.562
8.47
ns ns
Re 3 Pr 3 Pa
1 5.444
1.77 1.165
0.28 6765.062
5.00
ns ns
ns
Re 3 Pr 3 Ti
1 1.627
0.30 0.013
0.02 637.562
1.65
ns ns
a ns
Re 3 Pa 3 Ti
1 0.013
0.01 0.116
0.13 473.062
1.22
ns ns
ns
Pr 3 Pa 3 Ti
1 0.406
0.43 0.478
103.07 76.562
0.27
ns ns
ns
Re 3 Pr 3 Pa 3 Ti
1 0.935
0.55 0.005
0.01 280.562
0.72
ns
Boulder Re 3 Pr 3 Pa
16 3.071
4.097 7.92
1352.514 2.75
ns ns
Boulder Re 3 Pr 3 Pa 3 Ti
16 1.688
2.86 0.869
1.68 387.097
0.79 Residual
143 0.591
0.157 491.750
Cochran’s test C
5 0.131, P . 0.05 C
5 0.093, P . 0.05 C
5 0.080, P . 0.05 Transformation
ln x 1 1
ln x 1 1
None SNK tests
Encrusting corallines Ralfsia verrucosa
Re 3 Pa
Re 3 Pr 3 Pa
d.f. 5 1,16; S.E. 5 0.337
d.f 5 1,16; S.E. 5 8.668
Reef 1: 1 Pa . 2 Pa
Reef 1 1 Pa: 1 Pa 5 2 Pr
2 Pa: 2 Pr 5 1 Pr Reef 2:
2 Pa . 1 Pa Reef 1
1 Pr: 1 Pa 5 2 Pa 2 Pr: 2 Pa 5 1 Pa
Reef 2 1 Pa: 1 Pr 5 2 Pr
2 Pa: 2 Pr 5 1 Pr Reef 2
1 Pr: 2 Pa 5 1 Pa 2 Pr: 2 Pa 5 2 Pa
Pa 3 Ti
d.f. 5 1,16; S.E. 5 5.680
Time 1 Time 2
1 Pa . 2 Pa 2 Pa 5 1 Pa
a
Re 3 Pa 3 Ti has been eliminated as no significant at P 5 0.25.
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.
The data about articulated corallines algae from Livorno were not analysed, since they were in practice absent at this location.
10 F
. Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19
Fig. 3. Effect of different combination of absence presence of Patella aspera and Patella rustica on mean percentage cover of erect algae
1 S.E., n 5 9 as a function of time. Data are values from three replicate quadrats pooled across three replicate boulders at each time.
F .
Bulleri et
al .
J .
Exp .
Mar .
Biol .
Ecol .
255 2000
1 –
19
11 Table 2
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 5 Re
1 1.342
0.442 0.22
0.010 0.813
0.27
ns
P . rustica
5 Pr 1
1.450 2.497
0.92 5.646
0.080 P
. aspera 5 Pa
1 0.288
24.813 329.78
3.334 0.001
ns
Time 5 Ti
1 41.247
77.005 22.57
5.509 44.821
a ns
ns
Re 3 Pr
1 9.078
6.17 0.005
0.00 0.131
0.08 1.208
ns ns
Re 3 Pa
1 0.804
2.727 1.35
0.188 0.12
0.334
b ns
Re 3 Ti
1 1.605
0.821 0.24
4.249 6.40
1.869
ns
Pr 3 Pa
1 0.294
0.153 0.04
2.520 229.71
1.019
ns ns
Pr 3 Ti
1 0.002
0.851 0.17
0.001 0.00
0.302
ns ns
Pa 3 Ti
1 0.176
9.292 46.99
0.215 2.12
0.225
ns ns
Re 3 Pr 3 Pa
1 1.167
4.259 2.11
0.011 0.01
0.665 0.22
ns ns
Re 3 Pr 3 Ti
1 0.095
4.881 1.43
1.525 2.30
3.204 2.20
ns ns
Re 3 Pa 3 Ti
1 2.075
0.198 0.06
0.102 0.15
0.245 0.17
ns ns
Pr 3 Pa 3 Ti
1 0.048
0.353 0.14
1.721 1.01
0.558 240.91
ns ns
Re 3 Pr 3 Pa 3 Ti
1 9.675
13.54 2.441
0.72 1.705
2.57 0.002
0.00 Boulder Re
3 Pr 3 Pa 16
1.472 2.04
2.016 1.587
1.83 48.272
2.62
ns ns
Boulder Re 3 Pr 3 Pa 3 Ti
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
C 5 0.131, P . 0.05
C 5 0.093, P . 0.05
C 5 0.080, P . 0.05
C 5 0.081, P . 0.05
Transformation ln x
1 1 ln x
1 1 None
ln x 1 1
SNK tests Articulated corallines
Filamentous algae Livorno Rissoella verruculosa
Re 3 Pr
Pr 3 Pa
Pr 3 Pa 3 Ti
d.f. 5 1,16; S.E. 5 0.202
d.f. 5 1,16; S.E. 5 0.030
d.f. 5 1,16; S.E. 5 0.011
Reef 1: 2 Pr . 1 Pr
1 Pa: 2 Pr 5 1 Pr Time 1
Time 2 Reef 2:
1 Pr 5 2 Pr 2 Pa: 2 Pr 5 1 Pr
1 Pa: 2 Pr 5 1 Pr 1 Pa: 2 Pr 5 1 Pr
1 Pr: 2 Pa 5 1 Pa 2 Pa: 2 Pr 5 1 Pr
2 Pa: 1 Pr . 2 Pr 2 Pr: 2 Pa . 1 Pa
1 Pr: 2 Pa 5 1 Pa 1 Pr: 2 Pa . 1 Pa
2 Pr: 2 Pa 5 1 pa 2 Pr: 1 Pa . 2 Pa
a
See Section 3 for details.
b
Re 3 Ti has been eliminated from the analysis, as no significant at P 5 0.25.
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
in the text.
12 F
. Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19 Table 3
ANOVAs on the effects of the removal of limpets, Reef, Boulder and Time on the percent cover of Chthamalus spp.
Source of d.f.
Carrara Livorno
variation MS
F MS
F Reef
5 Re 1
0.000 4.778
P . rustica
5 Pr 1
4.551 1.082
P . aspera
5 Pa 1
0.088 6.440
Time 5 Ti
1 0.646
0.026 Re
3 Pr 1
1.096 27.779
18.20
ns
Re 3 Pa
1 0.983
0.771 0.51
Re 3 Ti
1 0.065
2.519 0.75
Pr 3 Pa
1 0.206
7.574 4.96
ns
Pr 3 Ti
1 0.020
0.317 4.92
ns
Pa 3 Ti
1 0.001
0.053 0.71
a ns
Re 3 Pr 3 Pa
1 0.000
1.094 0.72
b ns
Re 3 Pr 3 Ti
1 2.126
9.94 0.064
0.19
ns
Re 3 Pa 3 Ti
1 0.230
0.074 0.22
ns
Pr 3 Pa 3 Ti
1 0.007
0.391 0.59
ns
Re 3 Pr 3 Pa 3 Ti
1 1.207
5.64 0.661
1.97 Boulder Re
3 Pr 3 Pa 16
1.855 8.87
1.526 5.62
ns ns
Boulder Re 3 Pr 3 Pa 3 Ti
16 0.214
1.02 0.336
1.24 Residual
143 0.722
0.272 Cochran’s test
C 5 0.132, P . 0.05
C 5 0.099, P . 0.05
Transformation ln x
1 1 ln x
1 1 SNK tests
Carrara Re
3 Pr 3 Ti d.f.
5 1,16; S.E. 5 0.109 Time 1
Time 2 Reef 1:
2 Pr . 1 Pr Reef 1:
1 Pr 5 2 Pr Reef 2:
2 Pr 5 1 Pr Reef 2:
2 Pr . 1 Pr Livorno
Pr 3 Pa
Re 3 Pr
d.f. 5 1,16; S.E. 5 0.206
d.f. 5 1,16; S.E. 5 0.206
1 Pa: 2 Pr . 1 Pr 2 Pa: 1 Pr 5 2 Pr Reef 1:
2 Pr . 1 Pr 1 Pr: 2 Pa . 1 Pa 2 Pr: 1 Pa 5 2 Pa
Reef 2: 1 Pr . 2 Pr
a
Re 3 Pr 3 Pa has been eliminated from the analysis as no significant at P 5 0.25.
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.
At the other location, both the species of limpets affected the cover of filamentous algae Fig. 3F,H, resulting in a significant P
. rustica 3 P. aspera interaction. SNK test
F . Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19
13
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 . rustica
3 P. aspera
3 Time 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 Reef 3 P. rustica 3 P. aspera 3 Time interaction Fig. 4A,C and Table 3. As
just a few significant differences, not consistent across reefs and times, were pointed out
Fig. 4. Effect of different combination of absence presence of Patella aspera and Patella rustica on mean density of Chthamalus spp.
1 S.E., n 5 9 as a function of time. Data are values from three replicate quadrats pooled across three replicate boulders at each time.
14 F
. Bulleri et al. J. Exp. Mar. Biol. Ecol. 255 2000 1 –19
by SNK tests, lower order significant interactions were further considered. This was the case of the interaction Reef
3 P. rustica 3 Time, 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 Reef 3 P. 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
