DYNAMICS OF THE ACMAEID LIMPET COLLISELLA SUBRUGOSA
AND VERTICAL DISTRIBUTION OF SIZE AND ABUNDANCE
ALONG A WAVE EXPOSURE GRADIENT
MARCEL O. TANAKA 1 , TIAGO E. M. DUQUE-ESTRADA 2 &
CLÁUDIA A. MAGALHÃES 3
1
Depto de Biologia, Setor Ecologia, CCBS, CP 549, Universidade Federal de Mato Grosso do Sul, Campo Grande, MS, 79070-900, Brazil
2
Programa de Pós-Graduação em Ecologia, IB, CP 6109, Universidade Estadual de Campinas, Campinas, SP 13083-970, Brazil
3
Departamento de Zoologia, IB, CP 6109, Universidade Estadual de Campinas, Campinas, SP 13083-970, Brazil
(Received 9 October 2000; accepted 9 July 2001)
ABSTRACT
The vertical distribution of the acmaeid limpet Collisella subrugosa (Orbigny) was studied on subtropical Brazilian shores. In a semi-sheltered shore at Ubatuba, monthly monitoring indicated that
densities were higher in the mid-intertidal, and lower in the high- and low-intertidal. There was
evidence of continuous recruitment mainly to mid- and lower levels on the shore, with a peak in the
summer. Shell length increased with tidal height, and this pattern was maintained during the study
period. To verify whether these results were consistent over a larger spatial scale, the vertical distribution of size, abundance, and shell shape of C. subrugosa was studied along a wave exposure gradient.
Densities were not clearly related to wave action, and other sources of variation such as presence of
competitors or secondary substrata appear to influence C. subrugosa distribution. Shell length increased
towards the upper intertidal on more exposed shores, but no differences, or the reverse pattern was
recorded on sheltered shores. These results are consistent with other studies on limpet distribution,
and proposed causes include differential recruitment, migration, or microhabitat availability. Shell
height increased faster with shell length in lower intertidal levels, and on more exposed sites. Foot
surface area also increased faster with shell length on more exposed shores and indicate that wave
action is an important factor determining shell shape in C. subrugosa. Additional sampling of upper
and lower populations along a gradient of wave exposure in Florianópolis (southern Brazil) resulted
in similar patterns of shell size, but the relationships between shell height and length for these populations were similar and isometric. Thus, there is a geographic variation in the vertical distribution of
C. subrugosa, and possible causes include distinct physical conditions or differences in phenotypic
plasticity of this limpet.
INTRODUCTION
Vertical gradients in physical and biological factors strongly
influence the distribution of intertidal organisms, often resulting in interspecific zonation patterns characterized by dominant zones of sessile species (reviews in Connell, 1972; Sebens,
1991; Raffaelli & Hawkins, 1996). Similar pressures can influence the distribution and coexistence of mobile species, as
reflected in distinct vertical gradients of density and size distributions between or within species (Sutherland, 1970; Branch,
1976, 1981). Gastropods are thought to show two general intraspecific size distribution patterns, with an increase in size
towards the upper intertidal for species living higher in the
shore, and the opposite trend for species that live in the lower
intertidal (Vermeij, 1972). These patterns are generally related
to differential mortality of smaller gastropods, mainly through
desiccation in upper shore organisms and predation in lower
ones (Vermeij, 1972). The lower densities and competition
pressure found in the upper levels can also favour the occurrence of larger individuals, either through differential growth
rates (Sutherland, 1970; Creese, 1980) or active migration
(Marshall & Keough, 1994; Hobday, 1995).
Size gradients of limpets along other physical gradients have
rarely been investigated (Thompson, 1980; Hobday, 1995).
Stronger wave action can increase the vertical range of limpets
(Frank, 1965), and physical conditions between upper and
J. Moll. Stud. (2002), 68, 55–64
lower parts of the vertical range can be more accentuated
(Raffaelli & Hawkins, 1996). Hobday (1995) found vertical size
gradients for the upper shore limpet Lottia digitalis in sites with
more wave action, but no differences in a more sheltered site,
where only large individuals were found. Thompson (1980)
found increased sizes of Patella vulgata in upper levels of exposed
sites, and the opposite trend in sheltered shores. These patterns could be due to differences in recruitment or immigration by larger individuals (Creese, 1980; Hobday, 1995), and
sheltered sites less subject to ocean spray could be equivalent to
upper intertidal levels on rocky shores (Simpson, 1985). Also,
small-scale heterogeneity resulting from the distribution of
sessile organisms can influence density and size distributions
(Thompson, 1980). Vertical patterns are also likely to change
among seasons of the year, due to fluctuation of the factors that
influence distribution patterns, including temperature, emersion periods, and food availability (Breen, 1972; Branch, 1981;
Underwood, 1984; Liu, 1994). Differences in physical conditions or resource availability between tidal levels can be
stronger in some seasons, but less extreme in other periods
(Sutherland, 1970).
Thus, environmental gradients such as desiccation and wave
exposure can influence the distribution of limpets, and morphological differences of individuals occurring at the extremes
of these gradients are generally interpreted as phenotypic
(reviewed in Branch, 1981). Resistance to desiccation by larger
© The Malacological Society of London 2002
MARCEL O. TANAKA, TIAGO E. M. DUQUE-ESTRADA & CLÁUDIA A. MAGALHÃES
ure gradient to test whether size gradients depend on the
degree of wave action. We also test whether shell height/length
ratios of C. subrugosa are influenced by vertical position on the
shore or wave exposure, and compare the relative size of the
foot from individuals collected along a wave exposure gradient.
organisms can be a result of the smaller volume to evaporative
surface area ratio (Lowell, 1984), while smaller limpets are
generally subject to less drag than larger ones, and are less
likely to be detached by wave action (Warburton, 1976). Shell
shape can also influence these patterns (Branch, 1981). Limpets
with taller shells can hold more water than flatter ones, and are
generally found in upper intertidal zones, where desiccation
stress is higher (Vermeij, 1973; Branch, 1981; Fletcher, 1984;
Simpson, 1985), although other features such as a mucus layer
along the edge of the shell may sometimes be more effective
(Wollcott, 1973). Branch (1975) found that when shell height
increases faster than length, rate of water loss is reduced. For
species with isometric growth, water loss is proportional to shell
volume (Davies 1969; see discussion in Branch, 1981). Flatter
shells are less subject to hydrodynamic forces than taller ones
(Denny, 1988), but differences in height/length ratios are not
always related with water movement (Branch & Marsh, 1978),
and resistance to hydrodynamic forces may be more dependent on the limpets´ adhesive system (Denny, 2000; Denny &
Blanchette, 2000). Other adaptations that reduce the risk of
dislodgement such as a larger foot area, more rigid muscles, or
shell texture can also be important (Miller, 1974; Branch &
Marsh, 1978).
Collisella subrugosa (Orbigny, 1846) is the most abundant
archeogastropod of the Brazilian coast, occurring from northeastern tropical to subtropical southern shores (Rios, 1995).
This herbivore occurs throughout the whole intertidal region,
preferentially on bare rock patches within the sessile community, but also on mussels, oysters, and other sessile organisms
(Jaskow, 1990; Tanaka, 1997). Little information is, however,
available on the distribution and dynamics of this species. In
this study, we describe the distribution of C. subrugosa at different tidal levels of Brazilian subtropical shores. We analyse the
vertical size and density distributions along a year in a semisheltered shore to verify if the patterns are temporally stable.
Then, we compare the vertical distribution along a wave expos-
MATERIALS AND METHODS
Study areas
This work was carried out in shores located at two subtropical
major regions (Figure 1), Ubatuba district, northern coast of
São Paulo State, SE Brazil (approximate coordinates: 23°30S
and 45°04W), and Florianópolis district, Santa Catarina Island,
central coast of Santa Catarina State, southern Brazil (approximate coordinates: 27°30S and 48°25W). General physical
conditions and tidal regimes are similar, with semidiurnal
tides. Lowest mean water temperatures are recorded in July
(Ubatuba: 21.1°C, Florianópolis: 16.1°C), while highest water
temperatures are recorded in February (Ubatuba: 28.3°C,
Florianópolis: 25.3°C). Precipitation values range between
83–248mm in Ubatuba and 70–300mm in Florianópolis, with
highest values in the summer.
Temporal variation in the vertical distribution of C. subrugosa
The long-term vertical distribution of C. subrugosa was analysed
from June 1997 to April 1998 at Lamberto, a sheltered shore
dominated by boulders located in Flamengo Bay, Ubatuba
(Oliveira-Filho & Mayal, 1976). Sampling sites were located on
its northern side, halfway to Pereque-Mirim, where large boulders and bedrocks are subject to moderate wave action, as
reflected in community composition. Intertidal zonation at this
site differs from the sheltered side of the shore, and is similar to
other semi-exposed shores in Ubatuba region described by
Oliveira-Filho & Mayal (1976) and Johnscher-Fornasaro, Lopes
& Milanelli (1990) (see below). The sublittoral fringe is dominated by the brown alga Sargassum, while the lower intertidal is
Figure 1. Location of the studied sites in Brazil: (1) Grande, (2) Lamberto, (3) Lázaro, (4) Fortaleza, (5) Tabatinga, (6) Ponta das Canas, (7) Brava, (8)
Joaquina.
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ent in Florianópolis, between 05–16 August 2000: Joaquina
(exposed), Ponta das Canas (intermediate) and three sites in
Praia Brava, distant 50–200m from each other: a wave-beaten
site far from the sandy beach (Brava1—exposed), one site midway to the beach, parallel to wave direction (Brava2—intermediate), and the last site composed by boulders on the beach
(Brava3—sheltered). These shores were classified by community composition, as suggested by Oliveira-Filho & Mayal
(1976), Paula (1987) and Széchy & Paula (1998): presence of
the green alga Chaetomorpha and dwarf forms of the brown alga
Sargassum were indicative of exposed shores, while large Sargassum plants and dominance of the oyster Crassostrea rhizophorae
(Guilding, 1828) were characteristic of sheltered shores. Community composition at moderately exposed shores was intermediate between both types, with intermediate-sized Sargassum
and low numbers of Chaetomorpha and Crassostrea. General
zonation patterns of shores in Florianópolis are similar to
Ubatuba, with dominance of macroalgae—T. stalactifera—B.
solisianus—C. bisinuatus, from the lower to the upper intertidal.
Other mobile gastropods commonly found in the intertidal
zone of both Ubatuba and Florianópolis are the fissurelid
Fissurella clenchi Farfante and the thaidid Stramonita haemastoma
(Linné) in the lower intertidal and the littorinid Nodilittorina
lineolata (Orbigny) in the upper intertidal and supralittoral
zones (Rios, 1995; Magalhães, 1998).
To determine the vertical distribution of C. subrugosa, we
established a zone from the sublittoral fringe to the upper
distribution limit of this limpet, spanning the whole intertidal.
At Ubatuba shores, this zone was further divided into three
belts of equal height (high, mid and low), and within each belt
nine 20x20cm quadrats were randomly sampled. Each quadrat
had 100 equidistant points, which were used to estimate percent cover of bare rock. Densities of C. subrugosa and Fissurella
clenchi in the quadrat were also determined. The quadrat had
10 points randomly marked in the grid; the closest individual to
each mark was carefully collected for morphometric analyses.
When two or more individuals were at the same distance from
the marked point, they were all collected, giving a sample size
between 30 and 64 individuals. In the laboratory, shell height
and length were measured with dial calipers ( 0.05mm). To
evaluate the effect of hydrodynamism on foot size, all individuals from the upper zone were attached to a transparent plastic
plate, and the plate was immersed in seawater. After individuals
had stopped moving, the plate was carefully retrieved, dried,
and the foot of all individuals were traced on the plate. The
drawings were scanned and the foot surface area in pixels
determined with a graphics software and converted to millimeters. Additional sampling of C. subrugosa was carried out in
Florianópolis, where 20-31 individuals were randomly collected
from a strip 20cm in height in the lower and upper intertidal
zones. Individuals were taken to the laboratory, and shell
length and height were measured as described above.
Densities of C. subrugosa and F. clenchi, and percent cover of
bare rock on three vertical levels at four shores were analysed
with a two-way ANOVA with both factors fixed, as we were interested in differences of these specific treatments. As significant
interactions were found for C. subrugosa and bare rock, further
one-way ANOVAs comparing the vertical levels were made for
each shore (Sokal & Rohlf, 1995). The relationship between
morphometric variables was analysed with least-squares regression on log-transformed values, as we wanted to verify whether
shell form of the animals could be predicted by predefined
categories of vertical level and wave exposure (Sokal & Rohlf,
1995). Thus, we compared the regression lines using an ANCOVA model that included both categorical variables. Significant
interactions of continuous and categorical variables would indicate that the slopes of the regression lines differed, while significant effects of the categorical variables indicate that the
dominated by green algae such as Ulva and Chaetomorpha, and
some calcareous red algae. The intermediate and upper zones
are dominated by the barnacles Tetraclita stalactifera (Lamarck)
and Chthamalus bisinuatus Pilsbry, respectively. The mussel
Brachidontes solisianus (Orbigny) occurs above the T. stalactifera
belt, between both barnacle species. During the colder winter
months, the Chthamalus zone is colonized by the red alga
Porphyra atropurpurea Olivi (De Toni) (Oliveira-Filho & Mayal,
1976; Tanaka & Duarte, 1998).
Sampling was carried out monthly at Lamberto, on bedrock
of 8m length. This area was subdivided in five vertical levels,
each level with 0.3m height and 8.0m length, from the sublittoral fringe (level 1) to the supralittoral zone (level 5). To
estimate C. subrugosa density at each level, five 20 20cm
quadrats were randomly sampled each month and all individuals larger than 2mm were counted. The size distribution was
estimated by measuring six individuals randomly selected in
each quadrat with a dial caliper ( 0.05mm), totalling 30 individuals per level. When fewer than six individuals were present
in the quadrat, the nearest individuals at the same level were
measured.
Mean densities and shell lengths of C. subrugosa were analysed with a two-way ANOVA (time vs levels), with both factors
fixed. As previous work indicated that the main temporal differences in community structure in nearby shores were due
to increased desiccation and temperature stress in response
to low tides during daytime in the winter (Oliveira-Filho &
Mayal, 1976; Shenkman, 1989), we expected that the vertical
distribution of C. collisella would differ between the winter
(June–August) and summer (December–February). To verify
whether mean abundances and sizes on distinct vertical levels
differed between these contrasting periods, we used the months
mean values as replicates (n 3). Post-hoc comparisons were
made with Tukey’s HSD test (Day & Quinn, 1989). Data were
log-transformed to make variances homogeneous (Sokal &
Rohlf, 1995).
Patterns of abundance and size distribution along a wave exposure
gradient
To analyse the vertical distribution of C. subrugosa along a
gradient of wave exposure, four shores in Ubatuba district were
sampled between 24–26 July 1998: Praia Grande (exposed),
Lázaro (intermediate), Tabatinga (intermediate) and Fortaleza
(the sheltered side, as defined by Paula & Oliveira-Filho, 1982).
Physical characterization of sites and zonation of macroorganisms in relation to wave exposure were described in OliveiraFilho & Mayal (1976), Johnscher-Fornasaro, Lopes & Milanelli
(1990) and Paula & Oliveira-Filho (1982), and only a brief
description is given here. Praia Grande is characterized by
large boulders and bedrocks; a large area of bedrock was
selected, where three zones can be found found: a Corallinaceae belt above the sublittoral fringe, followed by the barnacles T. stalactifera in the mid-intertidal and C. bisinuatus in the
upper zone (Oliveira-Filho & Mayal, 1976). The rocky coast of
Lázaro is continuous, where the lower intertidal is dominated
by several species of algae and T. stalactifera, followed by a
mussel zone dominated by B. solisianus and B. darwinianus
(Orbigny), and C. bisinuatus in the upper zone. Tabatinga is
dominated by boulders, and sampling was conducted on a
large area of bedrock. Dominant belts were less clear, although
a general pattern from macroalgae—B. solisianus—C. bisinuatus
from the lower to the upper intertidal can be recognized.
Fortaleza has a large rocky coast, with one side exposed to
great wave action, while the other is more protected (Paula &
Oliveira-Filho, 1982). Sampling was conducted on the sheltered side, where zonation patterns are similar to Lamberto,
extending on a rocky wall with a slope of 60º.
Additional sampling was made along a wave exposure gradi57
MARCEL O. TANAKA, TIAGO E. M. DUQUE-ESTRADA & CLÁUDIA A. MAGALHÃES
the bimodal size distribution found in the other months
(Figures 3, 4). There was a peak in recruitment during the
summer, between December and February, mainly in the lower
tidal levels. Further, individuals in the lower tidal levels (1 and
2) were smaller than those in the upper levels (4 and 5), where
no change of the mode was visible through the year. There was
no interaction between season and vertical level (Table 1), and
larger individuals were found in the upper levels both in the
summer and winter (Figure 3). As no individuals were found
at level 5 in January and February, these observations were
excluded from the analysis, reducing the degrees of freedom in
the ANOVA (Table 1).
adjusted means for each category are different (Sokal & Rohlf,
1995).
RESULTS
Temporal variation in the vertical distribution of C. subrugosa
The abundance of C. subrugosa at Lamberto varied during the
year, with higher densities during the summer months (Figure
2). Abundance in the upper levels (4 and 5) was temporally less
variable, with consistently low densities. Individuals of C. subrugosa were only observed at level 5 from early winter to late
spring. Densities were higher in the mid- and lower intertidal
(levels 1–3), increasing in the summer. Differences in abundance of C. subrugosa among levels varied with sampling time
(Table 1). Levels 1, 4, and 5 had low densities during both
seasons, whilst higher densities were recorded at intermediate
levels, especially in the summer (Figure 2).
Collisella subrugosa recruits (shell length < 5mm) were found
during the whole year, except in April 1998, as represented by
Patterns of abundance and size distribution along a wave exposure
gradient
The abundance of C. subrugosa varied vertically on different
shores at Ubatuba, although patterns differed in each shore as
indicated by the significant interaction term (2-way ANOVA,
Shore: F3,96 2.90, p < 0.05; Level: F2,96 0.89, p > 0.40; Interaction: F6,96 6.95, p < 0.001) (Figure 5). Thus, one-way
ANOVAs were made to examine the vertical pattern found
within each shore. Density increased from the lower to the
upper midlittoral in Lázaro and Fortaleza, while no significant
differences were recorded in Praia Grande (Figure 5). Lower
densities of C. subrugosa were found in the mid-intertidal in
Tabatinga (Figure 5). Conversely, densities of F. clenchi
decreased significantly from the lower to the upper midlittoral
in all shores (2-way ANOVA, Shore: F3,96 8.75, p < 0.001;
Level: F2,96 8.49, p < 0.001; Interaction: F6,96 1.65, p > 0.15).
Further, abundance of F. clenchi in Tabatinga was lowest when
compared to the other shores (Figure 5). Cover of bare rock on
vertical levels depended on the shore considered (2-way
Figure 2. Mean densities ( SE) of C. subrugosa from the lower (Level 1) to
the upper intertidal (Level 5) at Lamberto during the study period.
Table 1. Results of ANOVA comparing mean density and shell length of
C. subrugosa in different seasons (summer or winter) and vertical levels
(1–5) on the shore at Lamberto, Ubatuba. ns p > 0.05, ** p < 0.01,
*** p < 0.001.
Density
Source
df
Shell length
MS
F
df
MS
F
Season
1
0.045
0.2 ns
1
0.015
11.0**
Vertical level
4
6.194
21.4***
4
0.062
46.7***
Interaction
4
1.591
5.5**
4
0.001
0.6 ns
20
0.289
18
0.001
Residual
Figure 3. Mean shell length ( SE) of C. subrugosa from the lower (Level 1)
to the upper intertidal (Level 5) at Lamberto during the study period.
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Figure 4. Size distribution of C. subrugosa at Lamberto in the lower (levels 1 and 2; solid bars) and upper (levels 4 and 5; open bars) intertidal zone along the
studied period. n 60 for each intertidal region, except in January and February where n 30 for the upper zone.
ANOVA, Shore: F3,96 50.3, p < 0.001; Level: F2,96 25.9, p <
0.001; Interaction: F6,96 9.6, p < 0.001). No differences among
levels were found in Praia Grande and Fortaleza, a significant
increase from the lower to the upper region was recorded in
Lázaro, and lower values were recorded in the mid-intertidal at
Tabatinga (Figure 5). Available bare rock weakly influenced
the mean density of C. subrugosa (p 0.067), due to the influence of an outlier (lower level at Fortaleza; see Figure 6A) (studentized residual –2.57; see Sokal & Rohlf, 1995). When the
analysis was re-run without the outlier, there was a significant
relationship between mean cover of bare rock and density of C.
subrugosa (y 4.78 0.12x, r2 0.51, n 11, p 0.013).
Individuals in the higher intertidal were larger than those at
lower levels at the two more exposed sites (Grande and Lázaro),
but no differences (Tabatinga) or the reverse pattern (Fortaleza) were found at the more protected sites in Ubatuba
(Table 2). These patterns were further complicated because
there was a significant relationship between mean cover of bare
rock and mean shell length in Ubatuba shores, with larger
individuals occuring more frequently on rocky substrate, and
smaller individuals on sessile organisms (Figure 6B). In Florianópolis, no vertical differences in shell length were found at
Joaquina (an exposed shore) and the sheltered site at Brava,
while larger individuals were found in the upper intertidal of
the other sites sampled (Table 2).
There was a significant relationship between shell height and
59
MARCEL O. TANAKA, TIAGO E. M. DUQUE-ESTRADA & CLÁUDIA A. MAGALHÃES
Figure 5. Mean density of limpets and available bare rock at three vertical levels (low, mid and high) on shores in Ubatuba. Bars represent standard errors
(n 5). P values indicate significance of one-way ANOVA tests. Similar letters connect means that do not differ (Tukey’s HSD test; p > 0.05).
Table 2. Mean shell length (mm SE) of Collisella subrugosa sampled from different levels on shores in Brazil, and
results from one-way ANOVAs. Similar letters connect means that are not significantly different according to
Tukey’s test. ns p > 0.05, ** p < 0.01, *** p < 0.001. exp exposed shore, int intermediate, she sheltered shore.
Exposure
Low
Mid
High
df
F
1) Ubatuba
exp
7.2 0.27 a
6.4 0.50 a
9.9 0.43 b
2,121
18.8 ***
Lázaro
int
5.3 0.20
6.6 0.39
a
10.0 0.46 b
2,116
34.1 ***
Tabatinga
int
8.6 0.58 a
5.4 0.38 b
8.3 0.19 a
2,133
23.3 ***
Fortaleza
she
13.1 0.78 a
11.3 0.73 a
8.7 0.53 b
2,116
7.9 **
9.9 0.49
Grande
a
2) Florianópolis
Joaquina
exp
10.5 0.35
Brava1
exp
10.5 0.16
10.7 0.37
2,67
1.4 ns
12.7 0.42
1,55
30.6 ***
Brava2
int
9.2 0.29
11.1 0.20
1,53
29.8 ***
Ponta das Canas
int
10.4 0.15
11.6 0.29
1,58
11.4 **
Brava3
she
10.7 0.23
10.4 0.74
1,50
1.4 ns
DISCUSSION
length for all sites and levels (Table 3, Figure 7), but this relationship varied among levels on the same shores at Ubatuba
(Table 4). The values for the regression slopes in Table 3 indicate that at the lowest level shell height increases faster than at
mid and high levels. Further, this increase in height is faster at
the more exposed shores (Grande and Lázaro) when compared to more protected ones (Table 3). In Florianópolis, the
relationship between shell height and length was isometric,
with no differences between upper and lower intertidal levels
(Tables 3, 4). Also, no differences among shores were found
(Table 4).
There was a positive relationship between foot surface area
and shell length of animals collected from Ubatuba shores.
However, this relationship was influenced by wave exposure, as
area of the foot increased faster with shell length at the more
exposed shores (Grande and Lázaro) relative to the sheltered
sites (Table 5). Thus, as individuals grow in more exposed
shores, a larger foot is developed when compared to individuals subject to less wave action.
Vertical distribution and population dynamics of C. subrugosa
The vertical distribution of Collisella subrugosa spanned the
whole intertidal region, from the lower intertidal to the upper
limit of the Chthamalus bisinuatus zone, sometimes even above
this limit. There was considerable variation in the distribution
along the intertidal, with higher densities in the middle zone at
Lamberto throughout the year. Density at lower levels was more
variable, with higher densities during summer months due to a
recruitment peak, but decreasing to pre-summer levels in the
autumn. Densities were much lower and more constant in
the upper intertidal, slightly decreasing during the summer,
which could be related to both higher mortality or increased
downward emigration during the warmer months (e.g., Lewis,
1954; Frank, 1965; Breen, 1972). The presence of the red alga
Porphyra atropurpurea in the upper intertidal during the winter
(Oliveira-Filho & Mayal, 1976; Tanaka & Duarte, 1998) could
also have allowed the presence of C. subrugosa in this region,
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8
Duque-Estrada, unpublished data). Another factor that could
influence the population dynamics of C. subrugosa is the presence of Fissurella clenchi in the lower intertidal, but no data is
available on this interaction.
Shell length of C. subrugosa generally increased in an upshore
direction and, at least in the semi-sheltered Lamberto site, the
size distribution is stable throughout the year. Maintenance of
the size gradient on this shore can be related to continuous
recruitment to the lower intertidal, with the presence of individuals < 5mm during the whole study period. The presence of
juvenile limpets could maintain a pressure on algal populations, forcing larger limpets to upper levels on the shore due to
exploitative competition (e.g., Marshall & Keough, 1994).
Another explanation could be differential growth at different
shore levels, with higher growth in the upper levels (e.g.,
Sutherland, 1970). Differences in growth rates are, however,
generally related to variation in population densities (Sutherland, 1970; Vermeij, 1972; Fletcher, 1984), and greater contrast
in densities between tidal levels were recorded only during
summer. We could not estimate the growth rates in upper and
lower levels because the recruitment period extended during
almost one year, and thus these estimates would be subject to
much error as continuous input of small individuals to the
population would increase the variance (Creese, 1981). More
experiments are needed to clarify the mechanism by which
vertical size gradients are maintained in C. subrugosa.
reducing the risk of desiccation. More constant limpet densities
in the upper intertidal have been recorded for other species
(Sutherland, 1970; Creese, 1980), as a consequence of episodic
recruitment during very favourable years, when wave action
allowed individuals to colonize this region. Other studies, however, suggest that limpet populations in upper tidal levels can be
maintained by migration of individuals to escape competition
pressure in the lower intertidal (Frank, 1965; Marshall &
Keough, 1994). The results obtained from other shores in Ubatuba indicate that densities can be higher in the upper intertidal
(Figure 4); thus, the occurrence of limpets in this region could
be related to factors other than intraspecific competition.
Our results suggest that the vertical distribution of C. collisella
can be complicated by the distribution of bare rock patches.
The availability of rock substrate may influence the distribution
of C. subrugosa, as limpets on primary rock substrate generally
grow better as compared with those on secondary substrata
formed by mussels and barnacles (Choat, 1977; Lohse, 1993).
The location of new patches of bare rock within the sessile community is unpredictable, and the distribution of patches along
the intertidal can differ in larger spatial and temporal scales
(Paine & Levin, 1981). Nevertheless, these patches are rapidly
colonized by limpets, indicating that it is a more favourable
microhabitat (Iwasaki, 1999; Tanaka, 1997), and previous
results indicate that C. subrugosa presents site fidelity, although
several factors could influence this behaviour (Magalhães &
Table 3. Relationship between C. subrugosa shell height and length from three tidal levels on shores in Brazil, and results of
tests for isometric growth, comparing the regression slopes to 1 (H0: b1). Symbols as in Table 2. * p < 0.05.
Shore
Exposure
Level
n
a
b
SE (b)
r2
p
H0: b1
1) Ubatuba
Grande
Lázaro
Tabatinga
Fortaleza
exp
int
int
she
Low
35
–1.52
1.32
0.13
0.77
***
*
Mid
35
–0.95
1.07
0.07
0.88
***
ns
High
54
–1.28
1.15
0.07
0.85
***
*
Low
30
–1.55
1.34
0.12
0.81
***
*
Mid
42
–1.39
1.28
0.09
0.85
***
**
High
47
–1.06
1.03
0.07
0.84
***
ns
Low
37
–1.34
1.13
0.09
0.84
***
ns
Mid
35
–0.45
0.75
0.09
0.66
***
*
High
64
–0.63
0.90
0.11
0.54
***
ns
Low
41
–1.85
1.21
0.07
0.89
***
**
Mid
37
–0.74
0.86
0.10
0.67
***
ns
High
41
–0.81
0.83
0.07
0.76
***
*
2) Florianópolis
Joaquina
Brava1
Brava2
Ponta das Canas
Brava3
exp
exp
int
int
she
Low
20
–0.54
1.06
0.22
0.57
***
ns
Mid
26
–0.31
0.93
0.09
0.82
***
ns
High
24
–0.54
1.19
0.13
0.80
***
ns
Low
30
–0.53
1.02
0.25
0.37
***
ns
High
27
–0.21
0.54
0.15
0.57
***
ns
Low
24
–0.26
0.76
0.15
0.55
***
ns
High
31
–0.83
1.39
0.27
0.47
***
ns
Low
30
–1.00
1.44
0.39
0.33
**
ns
High
30
–0.30
0.96
0.17
0.53
***
ns
Low
28
–0.40
0.87
0.26
0.30
**
ns
High
24
–0.16
0.79
0.10
0.72
***
ns
61
MARCEL O. TANAKA, TIAGO E. M. DUQUE-ESTRADA & CLÁUDIA A. MAGALHÃES
more contrasting physical conditions can be found between
the upper and lower levels. The patterns of size distribution
may also be related to greater recruitment densities in more
exposed sites (e.g., Hobday, 1995), but the small animals found
at Tabatinga indicate that recruitment does occur in more
sheltered sites, and other factors can influence C. subrugosa
shell size. The positive relationship between bare rock cover
and limpet shell length indicates that large gaps within intertidal communities can sustain larger limpets, and the food
resources found in these gaps can be limiting (Choat, 1977;
Iwasaki, 1999). Thus, the availability of suitable microhabitat
for limpet growth and survival may depend on both the population dynamics of the organisms that provide secondary substrata, and physical disturbance rates on these populations,
contributing to variation in limpet vertical size distributions
(Thompson, 1980).
Shell height and length were correlated with tidal levels and
wave exposure in Ubatuba, as C. subrugosa shells increase faster
in height in the lower zone on more exposed shores. Height/
length ratios have been correlated with tidal levels in a number
of studies, with taller shells in the upper intertidal generally
thought to be related to greater desiccation resistance
(Vermeij, 1973; Branch, 1981; Fletcher, 1984; Simpson, 1985).
Alternative explanations for taller shells, however, include
variation in growth rates (Vermeij, 1980) and greater muscle
development and insertion, which would be important for
living on more exposed shores (Branch & Marsh, 1978). The
results from Ubatuba shores suggest that C. subrugosa shell
height is more influenced by wave exposure than desiccation.
We expected that if desiccation influenced the distribution of
C. subrugosa, than height/length ratios would be always higher
in the upper tidal levels, but we found the opposite trend.
Lower intertidal levels are subject to wave action more frequently than the upper intertidal (Denny, 1988), and limpets
are likely to have to adhere firmly to the substrate to avoid
being washed away. The positive relationship between foot
surface area and shell length indicate that animals in more
exposed shores have a larger foot area, and this result is in
agreement with studies on other gastropods (Magalhães &
Coutinho, 1995; Chapman, 1997, and references therein).
These results suggest that wave action is an important factor
determining allometric variation in C. subrugosa (e.g., Miller,
1974), and desiccation is probably a weaker factor influencing
shell shape. In fact, general shell shape in limpets may be sufficient to support large hydrodynamic forces, when coupled
with a high tenacity provided by their adhesive system, and
behavioral responses to wave action (Denny, 2000; Denny &
Blanchette, 2000). On the other hand, the relationship between
shell height and length was isometric and much more variable
Size and morphometric relationships of C. subrugosa along a wave
exposure gradient
Wave exposure influenced vertical size gradients of C. subrugosa, with increased sizes in upper levels on exposed and
moderately exposed shores, and slight differences on semisheltered and sheltered shores. The exceptions to these patterns were at Joaquina, an exposed shore where no differences
between upper and lower levels were found; and Fortaleza,
where the size gradient was inverted, with smaller C. subrugosa
in the upper levels (Table 2). As noted by Thompson (1980)
and Hobday (1995), habitat gradients may strongly influence
size distributions, as water spray increases the vertical height of
the intertidal zone on more exposed shores, and therefore
Figure 6. Relationship between mean cover of bare rock and A. mean
density and B. mean shell length of C. subrugosa from three vertical levels,
low (L), mid (M), and high-intertidal (H) on Ubatuba shores: Praia Grande
(G), Lázaro (L), Tabatinga (T), and Fortaleza (F).
Table 5. Relationship between C. subrugosa foot surface area and shell
length, and results of the ANCOVA comparing the regression lines of
animals sampled in different shores of Ubatuba.
Table 4. Results of ANCOVA comparing the relationship between shell
height and length of C. subrugosa in upper vs. lower intertidal levels of shores
in Ubatuba and Florianópolis. ns p > 0.05, *** p < 0.001.
Ubatuba (r2 0.85)
Source
df
MS
a
Florianópolis (r2 0.81)
F
df
MS
F
Shore (S)
3
0.011
1.8 ns
4
0.004
1.0 ns
Level (L)
1
0.118
18.5 ***
1
0.003
1.0 ns
Length
1
5.814
912.9 ***
1
0.779
219.0 ***
SxL
3
0.010
1.6 ns
4
0.007
2.0 ns
b
r2
SE
p
Grande
–0.285
1.882
0.072
0.94
< 0.001
Lázaro
–0.621
2.185
0.131
0.88
< 0.001
Tabatinga
–0.179
1.810
0.096
0.85
< 0.001
Fortaleza
0.002
1.582
0.112
0.84
< 0.001
MS
F
p
ANCOVA (r2 0.89)
Source
df
S x Length
3
0.016
2.6 ns
4
0.004
1.1 ns
Length
1
10.874
1170.3
< 0.001
L x Length
1
0.089
13.9 ***
1
0.000
0.0 ns
Shore
3
0.070
7.5
< 0.001
S x L x Length
3
0.003
0.5 ns
4
0.005
1.5 ns
Interaction
3
0.056
6.1
0.001
333
0.006
248
0.004
181
0.009
Error
Residual
62
VERTICAL DISTRIBUTION OF COLLISELLA SUBRUGOSA
1
2
3
4
5
6
7
8
9
10
1
2
3
4
5
6
7
8
9
20
1
2
3
4
5
6
7
8
9
30
1
2
3
4
5
6
7
8
9
40
1
2
3
4
5
6
7
8
9
50
1
2
3
4
5
6
7
8
9
60
1
2
3
4
5
6
7
8
Figure 7. Relationship between shell length and height of C. subrugosa in four shores of Ubatuba, from three intertidal levels: low (L, solid lines), mid (M,
dashed lines) and high (H, dotted lines).
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