Download Changes in selection on gastropod shell size and thickness with

Journal of Experimental Marine Biology and Ecology,
232 (1999) 217–239
L
Changes in selection on gastropod shell size and thickness
with wave-exposure on Northeastern Pacific shores
Elizabeth G. Boulding*, Meike Holst 1 , Vicki Pilon 2
Department of Zoology, University of Guelph, Guelph, Ontario N1 G 2 W1, Canada
Received 23 September 1997; received in revised form 15 June 1998; accepted 18 June 1998
Abstract
Patterns of selection on gastropod shell morphology are generally believed to be different on
wave-exposed and wave-sheltered shores. The heavy surf on wave-exposed shores is thought to
select for small size whereas the high risk of shell-breaking predation on wave-sheltered shores is
thought to select for increased shell size and thickness. We compared the risk of shell-breaking
predation to littorinid gastropods of different sizes and shell-thicknesses by tethering them on
wave-exposed and wave-sheltered shores of the Northeastern Pacific. Over 2 years we found that
the predation rate on the direct-developing gastropod Littorina sitkana was consistently much
lower at two moderately wave-exposed sites (less than 0.01% d 21 ) than on the two wave-sheltered
sites (8% d 21 and 2% d 21 respectively). At least 30% of the shell-breaking predation resulted in
diagnostic ‘‘peeled’’ shell breakage patterns that could be directly attributed to predatory crabs.
Observations with SCUBA at high tide suggested that most of the remainder of the shell-breaking
predation was from the red rock crab, Cancer productus, and that only a small amount was from
pile perch, Rhacochilus vacca. In contrast to our expectations, the smallest size-class of L. sitkana
suffered significantly lower rates of predation than the largest size-class at one of the wavesheltered sites. The effect of shell thickness on predation mortality was as predicted from previous
laboratory experiments. The thin-shelled littorinid species, Littorina subrotundata, suffered
significantly higher rates of predation than two thicker-shelled species, L. sitkana and L. scutulata
s.l., at three of our four sites. We conclude that the higher rates of shell-breaking predation on
wave-sheltered shores of the Northeastern Pacific selects for L. sitkana with thicker but not
necessarily larger shells than those on wave-exposed shores.  1999 Elsevier Science B.V. All
rights reserved.
Keywords: Cancer productus; Hemigrapsus; Littorina sitkana; Predation; Rhacochilus vacca
*Corresponding author. Tel.: 11-519-8244120 (ext. 4961); fax: 11-519-7671656; e-mail:
[email protected]
1
Present address: Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9,
Canada.
2
Present address: Department of Physical Sciences, Virginia Institute of Marine Science, Gloucester Point, VA
23062, USA.
0022-0981 / 99 / $ – see front matter  1999 Elsevier Science B.V. All rights reserved.
PII: S0022-0981( 98 )00117-8
3164
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1. Introduction
A paradigm of intertidal ecology is that gastropods from wave-exposed shores tend to
be small with thin shells that have large apertures whereas conspecific gastropods from
wave-sheltered shores tend to be large with thick shells that have small apertures (e.g.,
Kitching and Lockwood, 1974; Elner and Raffaelli, 1980; Janson, 1982a; Crothers,
1983; Wellington and Kuris, 1983; Boulding, 1990; Trussell et al., 1993). This
convergence of shell features for each habitat type occurs in various species throughout
the world and is most parsimoniously explained by postulating agents of selection that
are characteristic of wave-exposed shores and different agents of selection that are
characteristic of wave-sheltered shores (reviewed by Boulding, 1990). However, the
identity of these agents of selection is in some dispute. The small size and large foot
and, thus, large shell aperture of wave-exposed shore gastropods are thought to be
adaptations to reduce the risk of dislodgment by waves (Kitching et al., 1966; Behrens,
1972; Underwood and McFadyen, 1983; Denny et al., 1985; Trussell et al., 1993). The
large size and thick shell with its small aperture of sheltered shore gastropods are
thought to be adaptations to the high abundance of highly motile predators, to crushing
by stones, and to desiccation and heat stress (e.g., Kitching et al., 1966; Heller, 1976;
Atkinson and Newbury, 1984; Johannesson, 1986). Unfortunately most of the evidence
for the adaptive nature of these shell features is circumstantial and few field studies have
investigated the mechanisms responsible for the differential survival of gastropods with
different shell morphologies on wave-exposed and wave-sheltered shores (Janson, 1983;
Seeley, 1986; Etter, 1989; Boulding and Van Alstyne, 1993).
Selective foraging by mobile predators such as crabs and fish on wave-sheltered
shores is thought to select for large body size, a thick shell, and a small shell aperture
but there is little direct evidence for this. Evidence for this view comes from laboratory
experiments where shell-breaking crabs have often shown a preference for smaller sizes
of shelled gastropods (reviewed by Juanes, 1992) and for gastropods with thin shells
(Palmer, 1985; Boulding and Van Alstyne, 1993). Relative consumption rates measured
in the laboratory do not, however, always give good estimates of those in the field (e.g.,
Boulding and Hay, 1984; Behrens Yamada and Boulding, 1996). This likely occurs
because field consumption rates of a predator will be a complex function of the
distribution and abundance of its different prey species, its size relative to its prey, and
the abundance of its predators. For this reason, one of the most powerful methods of
quantifying selective foraging at different sites is direct monitoring of the relative
predation rates on tethered prey (e.g., Aronson and Heck, 1995; Behrens Yamada and
Boulding, 1996). Another advantage of tethering experiments is that the observer does
not have to remain at the field site, thereby reducing the probability of observation
affecting the behaviour of the predators (Aronson and Heck, 1995). An additional
advantage of tethering experiments that use shelled gastropods is that the predator
responsible can often be identified by examining the shell fragments (Behrens Yamada
and Boulding, 1996).
The purpose of our study was to compare the risk of shell-breaking predation to the
direct-developing gastropod Littorina sitkana (Philippi, 1846) at the two extremes of its
distribution along a wave-exposure gradient and to determine whether such predation
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
219
was selective with respect to shell size and thickness. We set up a series of three
different tethering experiments at two moderately wave-exposed sites and two wavesheltered sites. We also set up an additional tethering experiment at the wave-sheltered
site where predation was size-selective and observed potential predators there with
SCUBA during seven high tide periods. Our results are interpreted in terms of the
selective pressures on shell size and thickness on wave-exposed and wave-sheltered
populations of littorinid gastropods.
2. Methods
2.1. Study areas and animals
Our experimental sites were located on rocky shores near Bamfield Marine Station
(488509, 1258089) within Barkley Sound, Vancouver Island, British Columbia, Canada
(Fig. 1). We chose four study sites that represent the extremes of Littorina sitkana’s
distribution along a wave-exposure gradient. We chose sites that had natural populations
of Littorina sitkana and were accessible by boat from Bamfield Marine Station in winter
Fig. 1. Map of Barkley Sound, B.C., Canada (after Gosselin and Chia, 1995). The wave-exposed study areas
were Nudibranch Point (exposed site 1) and Prasiola Point (exposed site 2) whereas the wave-sheltered study
areas were Grappler Inlet (sheltered site 3) and the shore behind Dixon Island (sheltered site 4). A collection
site for Littorina sitkana on Seppings Island (SP) and the location of the laboratories at Bamfield Marine
Station (BMS) are also shown.
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as well as summer. Two sites Nudibranch Point (hereafter exposed site 1), and Prasiola
Point (hereafter as exposed site 2) were moderately wave-exposed and two sites,
Grappler Inlet (hereafter sheltered site 3) and the shore across from Dixon Island
(hereafter sheltered site 4) were wave-sheltered. We classified these sites by considering
their flora and fauna and their degree of exposure to the waves of the open Pacific (Fig.
1). The alga Fucus distichus L. was present at all of our four sites, but was not present
in areas that were extremely wave-exposed next to exposed sites 1 and 2. The upper
limit of distribution of L. sitkana is about 3.5 m above 0.0 datum (average extreme low
water as defined by Canadian Hydrographic Services) at our two wave-exposed sites and
about 2.5 m above 0.0 datum at our two wave-sheltered sites.
We used three other species of snails in our experiments in addition to Littorina
sitkana: L. subrotundata (Carpenter, 1864), L. plena (Gould, 1849), and L. scutulata
(Gould, 1849). The focal species, L. sitkana is distributed from moderately waveexposed to wave-sheltered shores throughout the Northern Pacific (Behrens Yamada,
1977; Boulding et al., 1993; Reid, 1996). L. sitkana and L. subrotundata lay benthic egg
masses, which hatch directly into juvenile snails, whereas L. scutulata and L. plena have
planktonic egg capsules and a planktonic larval period of at least 3 weeks (reviewed by
Reid, 1996). Several papers have referred to the wave-exposed form of L. subrotundata
(Carpenter, 1864) as Littorina sp. (i.e., Boulding et al., 1993; Boulding and Van Alstyne,
1993; Boulding and Hay, 1993; Kim and DeWreede, 1996), but recent mitochondrial
DNA sequences obtained from different populations of this species (Kyle and Boulding,
1998) support Reid’s hypothesis that the wave-exposed form is L. subrotundata (Reid
and Golikov, 1991; Reid, 1996).
In our study Littorina sitkana, L. scutulata, and L. plena were collected from a large
tide pool on Seppings Island and L. subrotundata was collected from Prasiola Point near
our exposed site 2 (Fig. 1). L. scutulata and L. plena have very similar shell forms (see
Reid, 1996) and were not distinguished in our study, so are hereafter referred to as
Littorina scutulata sensu lato. The gastropods L. sitkana and L. scutulata s.l. were
present at all four of our study sites. However L. subrotundata was only abundant at
exposed site 1.
2.2. Shell morphometry
To determine if differences in the shell thickness of different littorinid species have at
least a partial genetic basis, we cultured snails in a common environment consisting of
tanks with a flow-through sea water system. The snails were collected from near exposed
site 1 as juveniles of shell length 1.5–2 mm on July 4–5, 1993. The snails were held in
modified petri dishes (Boulding and Hay, 1993) at a density of either 5 or 15 snails per
dish. At the higher density the snails have less surface area per snail to graze so grow
more slowly than at the lower density. Growth rate affects shell shape and thickness in
these littorinid snails (Boulding et al., 1993). Consequently, by growing the snails at a
range of densities we are ensuring we get a wide range of shell thickness. The snails
were held in an outdoor tank at Bamfield Marine Station until Oct. 14, 1993 when they
were moved to an illuminated indoor tank at the University of Guelph. In November
1993 we used an image analysis system to measure shell dimensions (Fig. 1 in Boulding
and Hay, 1993). At this point the final shell length of the snails was between 3.5–7.5
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
221
mm. We then froze the snails and removed the body tissue from the shell and weighed
the dried shells on an analytical balance.
To predict shell weight as a function of shell width we estimated linear regression
equations for each species using the log-transformed data. Shell width was used to define
size instead of shell length because it is more comparable among Littorina species with
different shapes. Littorina subrotundata of the same shell width as L. sitkana have about
the same amount of body tissue (E.G. Boulding, unpubl. data). In addition shell width
represents the minimum dimension of a Littorina shell so it is likely the measurement
most important to shell-breaking predators (see Boulding, 1984). To test whether the
differences in shell thickness among the three species were significant after we had
corrected for size we used ANCOVA on the log-transformed data with shell width as the
covariate. We then used the Fisher’s least significant difference (L.S.D.) test (Sokal and
Rohlf, 1981) to compute which pairs of species had significantly different shell
thicknesses.
2.3. Size-structure of Littorina sitkana populations
To determine whether the mean size of Littorina sitkana was larger at the wavesheltered sites than at the wave-exposed sites we sampled 100 individuals randomly
from each of the four study sites in May and June 1994. Random sampling within a site
was achieved by randomly selecting one of ten suitable positions for a metre stick. The
metre stick was then laid down at the selected position and ten points along the metre
stick were selected at random. The L. sitkana closest to each point was collected and the
shell length of the snail was measured to the nearest 0.5 mm and then placed back at the
collection point. This procedure was repeated until 100 snails of shell length $ 3.0 mm
were collected. We used the Kolmogorov-Smirnov two sample test to determine whether
the size distribution of L. sitkana was significantly different at our four study sites. We
did this by using the SYSTAT program to compare all possible pairs of sites. We chose
this method because it does not require that the size distribution of snails approximate a
normal distribution.
2.4. Tethering experiments
2.4.1. Setup and interpretation
At each of the four study sites, 15 holes were drilled into the rock just at the upper
end of the Fucus zone and a ‘‘tethering’’ screw was placed in each hole. The absolute
height of the upper end of the Fucus zone was higher at the two wave-exposed sites than
at the two sheltered sites. Consequently the mean height of our tethering screws was at
about 3.3 m above datum at the two wave-exposed sites and about 1.8 m at the two
sheltered sites. We chose to put the screws above the Fucus zone at all sites even though
that meant they were at different tidal heights because we wanted any artifact of
tethering, such as the number of refuges for the snails to hide from predators, to be as
constant as possible across sites (see Peterson and Black, 1994).
The locations of the tethering screws were chosen by placing a 20 m tape measure
parallel to the shore for the entire length of the ‘‘study site’’. A second tape measure was
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placed perpendicular to the shore line from the top of the Fucus zone to the upper limit
of distribution of L. sitkana. We then selected the x coordinate for the screw along the
first tape measure and the y coordinate for the screw along the second tape measure
using two random numbers. The area available at exposed site 1 was broken by a surge
channel so we curved the 20 m tape so that the same amount of length of shore could be
sampled. Note that we only tethered snails within one 20 m long ‘‘site’’ on each shore
therefore our conclusions only apply to that site and not to the rest of the very
heterogeneous shore.
Snails were individually tethered to a ‘‘tethering’’ screw using 500 mm of 1.8 kg test
fishing line. One end of the fishing line was fastened to the apex of the snail shell using
marine epoxy. The other end of the fishing line was then tied around the screw.
Each day we checked all the tethered snails at either the two wave-exposed sites or
the two wave-sheltered sites. We recorded the number of snails that were live, the
number that had been crushed or peeled by predators, the number that were dead but had
undamaged shells and the number that were missing. We replaced dead or missing snails
with similarly-sized snails of the same species but the live snails with undamaged shells
were not replaced.
Our interpretation of shell fragments was consistent among observers. We only
considered mortality to be from predation when a shell fragment was still attached to the
tether. The shell fragment either consisted of just the apex of the shell, in which case the
snail was listed as ‘‘crushed’’, or the entire shell with a spiral gouge along the body wall,
in which case the snail was listed as having been ‘‘peeled’’ by a crab. ‘‘Peeled’’ shell
fragments are diagnostic of predation by crabs of gastropod shells that are large relative
to their claw size (reviewed by Behrens Yamada and Boulding, 1996). In contrast
‘‘crushed’’ shell fragments are not diagnostic because they can result from either: (1)
predation by crabs with claws that are large relative to the snails, (2) from predation by
pile perch (Rhacochilus vacca) or (3) from crushing by stones dislodged during storms
(reviewed by Behrens Yamada and Boulding, 1996). A snail was listed as ‘‘dead and
undamaged’’ when only the empty, undamaged shell was found on the tether which most
likely occurred because of mortality from heat stress or desiccation. Purple starfish,
Pisaster ochraceus, would also leave an empty shell after consuming a littorinid snail,
but we rarely saw starfish as high as our tether screws even at the two sheltered sites. A
snail was recorded as ‘‘missing’’, when neither a snail nor a shell fragment was found on
the tether. Fewer than 10% of our tethered snails were recorded as missing. These snails
were excluded from our statistical analysis even though many of them are likely to have
been pulled off their tether by a predator.
We used logistic regression rather than ANOVA to analyze the results of our tethering
experiments because we could not assume the variances in predation rate were
homogeneous among sites that differed in wave-exposure. The heterogeneity of
variances occurred because we observed close to zero predation at our moderately
wave-exposed sites and high but variable predation rates at our wave-sheltered sites.
Logistic regression analysis is a type of generalized linear model based on the logit
transformation of a proportion and is especially appropriate for binary variables (Agresti,
1990). For example when a snail was tethered at a particular site over a particular time
period they either were preyed on or were not. For all logistic regression models the
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223
yield variable, p 5 (the number of shells crushed 1 number of shells peeled) /(the total
number of live, crushed, peeled, and dead-undamaged snails recovered). The logistic
regression analyses were done using the iterative ‘‘genmod’’ procedure which is part of
the SAS statistical package (SAS Institute Inc., 1993). We fitted interaction terms, such
as Date 3 Site, Site 3 Size, and Site 3 Species, in the initial version of the logistic
regression models but dropped them in the final version because these terms were not
significant.
We tried to do controls for our tethering experiments in summer 1995 to determine
whether tethering affected survival. We released two untethered snails that had been
marked with paint near each of our tethering screws and tried to recover them 2 days
later. We recovered a high proportion of snails at the wave-exposed sites but recovered
so few untethered snails at the two wave-sheltered sites that we had to give this up. We
could not tell whether the snails were being preyed on or were hiding as it was
impossible to effectively search the Fucus zone for them.
2.4.2. Size selection 1994
For our 1994 experiment, we collected L. sitkana of varying sizes (3.5 mm , shell
width , 10.4 mm as measured with calipers) and tethered them at the same site they
were collected from. Two snails of comparable size (within 2 mm) were tethered at each
screw, for a total of 30 snails at each site. Data were collected every 2 days for 30 days
for each site. We analyzed the predation data using the logistic regression model:
log( p / 1 2 p) 5 Date 1 Site
where Date is the dates on which we monitored the site.
2.4.3. Size selection 1995
For our 1995 experiment, we decided to improve our ability to detect size-selective
predation by using three distinct size-classes of Littorina sitkana. These were all
collected from Seppings Island in Barkley Sound, and one of each size-class was
tethered at each of the 15 screws, giving a total of 45 snails at each site. Shell width of
all but the largest size-class was determined by dry sieving the snails with a series of soil
test sieves. The size-classes used were small (2.0 mm,shell width,2.8 mm), medium
(4.7 mm,shell width,6.2 mm), and large (7.5 mm,shell width,8.2 mm). Shell
fragments, dead, and missing snails were replaced by snails of the same size-class.
Snails which were tangled were either untangled or replaced, since we thought
entanglement might increase desiccation rates. Data were collected every 2 days for 15
days for each site. We analyzed the predation data using the logistic regression model:
log( p / 1 2 p) 5 Date 1 Site 1 Size
where Date is the dates on which we monitored the site and Size is the size-class of
snails.
To determine if our size-classes of Littorina sitkana differed in their vulnerability to
heat stress / desiccation we ran a two-way ANOVA with site as a random effect and
size-class as a fixed effect. We used the proportion of intact, recovered snails that were
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dead with an undamaged shell as the dependent variable after transformation with an
angular transform. We then used Bonferroni pairwise comparisons to determine which
size-classes were significantly different from each other.
2.4.4. Predator identification 1997
In our size selection experiments in 1994 and 1995 we got higher predation rates on
larger size-classes of L. sitkana than on smaller size-classes at sheltered site 3. In our
1997 experiment we decided to improve our ability to identify the predators responsible
for the size selective predation at sheltered site 3 by using an extra-large size-class as
well as a small–medium size-class of Littorina sitkana. The advantage of using
extra-large L. sitkana is that only the very largest predatory crabs will be able to crush
extra-large snails outright. Any crabs that are smaller will have to peel the snails and
will leave the diagnostic ‘‘peeled’’ shell fragments that are produced by no other
predator (Behrens Yamada and Boulding, 1996).
The extra-large size-class of L. sitkana was only found just east of Nudibranch Point
but the small–medium L. sitkana were collected from the same site at Seppings Island as
was used in 1995. The L. sitkana from Nudibranch Point reach a larger size but show the
same rate of increase of shell thickness with shell length as that shown by L. sitkana
from Seppings Island (E.G. Boulding, pers. obs.). The size-classes used for this
experiment were small–medium (4.0 mm,shell width,4.7 mm) and extra-large (12
mm,shell width,15 mm). Two snails of each size-class were tethered at each of the 12
screws, giving a total of 48 snails at our sheltered site 3. Every 2 or 3 days over a period
of 19 days we visited the site at low tide and recorded each snail as being either live,
crushed, peeled, dead but undamaged, or missing. Shell fragments, dead, or missing
snails were replaced by live snails of the same size-class. Snails with tangled tethering
lines were either untangled or replaced, since we thought entanglement might increase
desiccation rates. As only one site was involved we analyzed our data using a two-way
x 2 contingency analysis using size-class and type of recovered shell as the two
categorical variables. We used the sum, over our seven monitoring dates, of the number
of snails recovered crushed calculated separately for each of the two size-classes, and the
sum of the number recovered peeled as our cell frequencies.
In addition, in July 1997 we did surveys of the sizes and abundance of shell-crushing
predators near our tethering site during daytime and nighttime high tides using SCUBA.
We chose to do all our SCUBA observations at our sheltered site 3 because ten day and
eight night dives at high tide had been previously done at our sheltered site 4 by Robles
et al. (1989) and because we thought it was too risky to dive at our exposed sites 1 and
2. To mark the transects for our surveys with SCUBA we used stones to fix two 50 m
pieces of 6.3 mm diameter white nylon rope on the pebble bottom parallel to shore. The
rope was positioned just below our tethering screws at a depth of 0.7–1.0 m above 0.0
datum. We also fixed another 30 m transect right along the rock at the level of our
tethering screws at a depth of 1.8–2.1 m above 0.0 datum. The visibility was fair to poor
(,2 m) so each of the two divers swimming along the transect line surveyed only a 1 m
strip on their side of the line. We counted the number of red rock crabs (Cancer
productus) of each sex and measured their carapace width using calipers. We also
counted the number of pile perch (Rhacochilus vacca) and striped perch (Embiotoca
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
225
lateralis) and estimated their total length. Rhacochilus vacca consume mussels by
ingesting the entire animal including the shell, then crushing the shell with their highly
modified pharyngeal teeth (Brett, 1979). The flesh of the crushed mussel is digested as
the mussel passes through the gut, then the shell fragments are defected (Brett, 1979).
Rhacochilus vacca has also be observed to ingest and crush littorinid snails (McCormack, 1982). In contrast, Embiotoca lateralis do not have pharyngeal teeth that are
highly modified for crushing and are known to mostly feed on caprellid and gammarid
amphipods rather than on hard-shelled prey (Holbrook and Schmitt, 1992).
2.4.5. Shell-thickness selection
To test the hypothesis that shell-breaking predators prefer thin-shelled species of
snails over thick-shelled ones, we tethered one individual of the small–medium sizeclass (3.35 mm,shell width,4.00 mm) of each of three different taxa: Littorina
subrotundata, L. scutulata s.l., and L. sitkana, at each of the 15 screws, at the same four
study sites as used for the previous experiment. The snails were tethered and checked
every second day for a total of 8 days for each site. To distinguish shell fragments of the
three different taxa in the field, one knot was tied in the fishing line marking the snail as
L. scutulata s.l., two knots were tied for L. subrotundata, and no knots were tied in the
line for L. sitkana.
We analyzed the predation data using the logistic regression model:
log( p / 1 2 p) 5 date 1 site 1 species
where date are the dates on which we monitored the site for predated snails and species
is the species of littorinid snails used.
3. Results
3.1. Shell morphometry
Shell width explained 72%, 91%, and 92% of the variance in dry shell weight for
Littorina subrotundata, L. sitkana, and L. scutulata s.l. respectively (Table 1). The
poorer fit of the regression for L. subrotundata likely occurred because there is a higher
measurement error associated with measuring the shell weight of their lighter shells.
The differences in shell thickness observed in the field persisted when the three
species of snails were cultured in a common environment in the outdoor tank (Table 1).
The adjusted shell weight of Littorina subrotundata (22.3 mg) was significantly less
than that of L. sitkana (27.7 mg) which was significantly less than that of L. scutulata
s.l. (44.6 mg) (L.S.D. test, P,0.001). The assumptions of the ANCOVA were upheld in
that the slopes of the regression of dry shell weight against the covariate, shell width,
were not significantly different for the three species (P.0.15).
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E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
Table 1
Regressions of dry shell weight (DW) on shell width (SW) and analysis of covariance (ANCOVA) on dry shell
weight with shell width as the covariate for three species of snails cultured in an outdoor tank
Species
Regression equation
N
Littorina subrotundata
Littorina sitkana
Littorina scutulata /plena
Log e (DW)5 27.4812.51 Log e (SW)
Log e (DW)5 28.1713.10 Log e (SW)
Log e (DW)5 26.9712.62 Log e (SW)
24
29
18
ANCOVA
Source
Species
Log e (SW)
Error
df
2
1
67
MS
2.27
12.8
0.031
r2
0.72
0.91
0.92
F
74.3
417.5
P
0.000
0.000
3.2. Size-structure of Littorina sitkana populations
The Littorina sitkana populations from the moderately wave-exposed site 2 had a
significantly different size distribution from the population at wave-sheltered site 3
Fig. 2. Size distribution of Littorina sitkana collected from the four study sites.
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
227
(Kolmogorov-Smirnov two sample test P,0.001) and from the population at wavesheltered site 4 (Kolmogorov-Smirnov two sample test P,0.021). There were few
individuals in either of the wave-sheltered populations that had a mean size of larger
than 8.0 mm (Fig. 2). In contrast a substantial proportion of the individuals in the
wave-exposed populations were larger than 8.0 mm (Fig. 2).
3.3. Tethering experiments
3.3.1. Size selection 1994
We consistently observed substantially lower rates of crab predation at our waveexposed sites than at our wave-sheltered sites in the June / July 1994 experiment (Fig. 3,
Table 2). Crab predation at the wave-sheltered site 3 (Grappler) and wave-sheltered site
4 (Dixon) was much higher than crab predation at moderately wave-exposed site 1
(Nudibranch) and moderately wave-exposed site 2 (Prasiola). At sheltered site 3, large
Littorina sitkana suffered a significantly higher rate of predation than smaller L. sitkana.
Of the first two sets of L. sitkana that were tethered on each screw, 38 were
‘‘medium–large’’ with a shell length of 6.0 and 7.9 mm and 14 were ‘‘large’’ with a
shell length of 8.0–9.9 mm. The mean survival time before predation of the large group
(3.3 days) was significantly less than the mean survival time of the medium–large group
(7.1 days) (t test, P,0.001) suggesting that the predators preferred larger snails.
3.3.2. Size selection 1995
We also consistently observed substantially lower rates of crab predation at our
wave-exposed sites than at our wave-sheltered sites in the June / July 1995 experiment
Fig. 3. Mean rate of shell-breaking predation of Littorina sitkana per 2 day period during the 1994 tethering
experiment. Bars on histograms represent one standard error.
228
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
Table 2
Logistic regression analysis of 1994 tethering experiment with 30 Littorina sitkana of shell length 3.5–13.0
mm at our four sites: Nudibranch – exposed site 1 (1) and Prasiola – exposed site 2 (2), Grappler – sheltered
site 3 (3), and Dixon – sheltered site 4 (4)
Source
df
x2
P
Date
Site
14
3
80.09
142.86
0.000
0.000
Contrast (Site)
1.vs. 2
3.vs.4
3 and 4. vs. 1 & 2
df
1
1
1
x2
4.818
30.56
88.4
P
0.041
0.000
0.000
Note: Model was initially fitted with interaction term Date3Site but it was non-significant so was dropped.
See Fig. 3 for means.
(Fig. 4, Table 3). Size selective predation occurred only at sheltered site 3, where
significantly fewer of the small size-class of snails were eaten than of the medium or
large size-class ( x 2 , P,0.01). At sheltered site 4, where predation rates were lower,
there were no significant differences in the number of snails eaten from a given
size-class (Fig. 4). At both wave-sheltered sites there was a trend for the larger-sized
snails to be peeled rather than crushed which allowed us to verify that crabs were
responsible. At sheltered site 3 none of the snails in the small size-class was peeled but
30% of those in the medium size-class and 43% of those in the large size-class was
peeled. At sheltered site 4 none of the small size-class was peeled but 33% of the
medium and 33% of the large size-class was peeled.
Fig. 4. Mean rate of shell-breaking predation of Littorina sitkana per 2 day period during the spring 1995
tethering experiment. Bars on histograms represent one standard error.
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
229
Table 3
Logistic regression analysis of Spring 1995 tethering experiment with 15 Littorina sitkana of each of three
size-classes at each of our four sites: Nudibranch – exposed site 1 (1) and Prasiola – exposed site 2 (2),
Grappler – sheltered site 3 (3), and Dixon – sheltered site 4 (4). The data for sites 1 and 2 were combined as
zero predation occurred at these sites
Source
x2
P
2
2
55.90
12.36
0.000
0.002
df
1
1
x2
42.71
20.15
P
0.000
0.000
df
Site
Size
Contrast (Site)
3,4. vs. 1,2
3. vs. 4
Note: Model was initially fitted with interaction term Site3Size but it was non-significant so was dropped. See
Fig. 4 for means.
Death from heat stress / desiccation was size-selective (Table 4). A significantly
¯
greater proportion of intact small snails (x50.051)
were recovered dead with a
¯
undamaged shell than were medium snails (x50.012
day, Bonferroni P,0.001). In
addition a significantly greater proportion of the intact small snails were recovered dead
¯
with an undamaged shell than were large snails (x50.007
per day, Bonferroni P,
0.001). There was no significant difference in the proportion of dead snails with
undamaged snails recovered among the four sites (Table 4).
3.3.3. Predator identification 1997
More than 52% of the extra-large Littorina sitkana that experienced shell-breaking
predation had been ‘‘peeled’’, clearly indicating the predation had been caused by crabs
(Table 5). The intensity of predation on the extra-large size-class (21% of recovered
individuals) was similar to that on the small–medium size-class (17% of recovered
individuals). However significantly fewer of the small–medium size-class were peeled
Table 4
Analysis of variance of proportion of intact Littorina sitkana recovered that were dead with undamaged shells
in our Spring 1995 tethering experiment with 15 Littorina sitkana of each of three size-classes at each of our
four sites: Nudibranch – exposed site 1 (1) and Prasiola – exposed site 2 (2), Grappler – sheltered site 3 (3),
and Dixon – sheltered site 4 (4)
Source
Site
Size
Site3size
Error
Size
Small
Medium
Large
df
MS
3
2
6
72
site 1
0.068
0.010
0.000
F
P
0.001
0.016
0.001
0.002
0.374
16
0.511
0.772
,0.005
0.798
site 2
0.059
0.019
0.010
site 3
0.040
0.010
0.000
site 4
0.039
0.011
0.020
Note: Mean proportions of intact Littorina sitkana recovered that were dead with undamaged shells are shown
in the lower part of the table.
230
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
Table 5
Percentage of total recovered tethered Littorina sitkana that were either crushed or peeled by predators in the
1997 predator identification experiment at sheltered site 3 (Grappler)
Size-class
Crushed
Peeled
Total recovered
% peeled
Small–medium
Extra-large
Total predation:
16.5%
9.8%
31
0.79%
10.8%
12
127
102
4.5%
52%
Note: Total recovered is the total number of live and dead snails summed over all seven monitoring periods.
Total predation means the total number of shell fragments attached to the tether that had been peeled or
crushed summed over all seven monitoring periods. % peeled refers to the mean percentage of snails that had
suffered mortality from predation that had been peeled by crabs. Two way x 2 test for independence of
size-class and method of predation (crushed or peeled) used with the expected values calculated from the
column and row sums: x 2 512.76, df52, P,0.002.
4.5% of recovered individuals) compared to the extra-large size-class (52% of recovered
individuals) x 2 test, P,0.01).
The types and sizes of shell-breaking predators seen at sheltered site 3 differed
considerably between SCUBA dives during the day and those during the night. More
Cancer productus were seen during the two nighttime dives than during all five daytime
dives. No juvenile C. productus were seen during the day but juveniles made up 46% of
the crabs that were seen during the night dives (Table 6). In contrast adult male C.
productus made up 83% of all crabs seen during the day but only 21% of all crabs seen
during the night. Cancer productus (total57) were seen foraging in the middle intertidal
(1.8 m datum) near where the tethering screws were during the two night dives but were
never observed there during the day dives. Only one individual of another crab species, a
7 cm female Cancer gracilis, was seen during any of the dives.
We observed few fish during our SCUBA transects. We observed a total of 20
Rhacochilus vacca and 8 Embiotoca lateralis in all dives. Only eight of the R. vacca and
none of the E. lateralis were larger than 20 cm in total length. A 21 cm R. vacca can
prey on extra-large L. sitkana even if they are tethered but is more efficient at preying on
smaller size-classes of these snails (E.G. Boulding, unpubl. data).
3.3.4. Shell-thickness selection
We also observed substantially lower predation rates at our wave-exposed sites than at
our wave-sheltered sites in the shell-thickness tethering experiment (Fig. 5, Table 7).
Table 6
Percentage of Cancer productus that were juveniles, females, or males on the five day and two night SCUBA
dives at sheltered site 3 during high tide
Type
Day dives
Night dives
Total number observed
Juveniles
Females
Males
Total N
0%
17%
83%
18
46%
32%
21%
28
13
12
21
Note: Test for independence of crab size and time of day: x 2 518.5 df52 P,0.0001. Juvenile crabs were
defined as those of either sex that were less than 90 mm in carapace width.
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
231
Fig. 5. Mean rate of shell-breaking predation of Littorina per 2 day period during the summer 1995 tethering
experiment. Bars on histograms represent one standard error.
This predation was selective in that two species with the greater shell thickness
experienced significantly lower rates of predation. Relatively more Littorina subrotundata were eaten at all four sites than of the other two taxa and at Nudibranch and
Prasiola only L. subrotundata were eaten (Fig. 5). At sheltered site 3, L. subrotundata
suffered a significantly higher predation rate than L. scutulata s.l. while L. sitkana
suffered a significantly higher predation rate than L. scutulata (Fig. 5, x 2 , P,0.001). At
sheltered site 4, L. subrotundata were eaten at a greater rate than the other two species
Table 7
Logistic regression analysis of Summer 1995 tethering experiment with 15 Littorina sitkana (Lsit) 15 Littorina
scutulata (Lc), and 15 Littorina subrotundata (Lsub) tethered at each of our four sites: Nudibranch – exposed
site 1 (1) and Prasiola – exposed site 2 (2), Grappler – sheltered site 3 (3), and Dixon – sheltered site 4 (4)
x2
P
7
3
2
33.5
102.8
43.0
0.000
0.000
0.000
Contrast (Site)
1,2.vs. 3,4
df
1
x2
48.9
P
0.000
Contrast (Species)
Lsub.vs. Lsit
Lsub.vs. Lc
Lsit.vs. Lc
df
1
1
1
x2
6.6
40.4
15.8
P
0.010
0.000
0.000
Source
df
Date
Site
Species
Note: Model was initially fitted with interaction term Site3Species but it was non-significant so was dropped.
See Fig. 5 for means.
232
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
(Fig. 5), but because of the small sample size, these differences in species selection were
not significant.
4. Discussion
4.1. Predation and wave-exposure
Our tethering experiments showed that the risk of shell-breaking predation to the
intertidal gastropod, Littorina sitkana, differed at the two extremes of its distribution
along a wave-exposure gradient and that predation could be selective with respect to
shell size and thickness. The predation rates by shell-breaking predators were much
higher on the two wave-sheltered shores than on the two moderately wave-exposed
shores. This is in agreement with the literature and likely occurs because most
shell-breaking predators are highly mobile and have difficulty foraging on wave-exposed
shores because of the heavy surf (e.g., Menge, 1978; Wellington and Kuris, 1983).
We saw no evidence for the paradigm that larger individual gastropods had a lower
risk of predation on wave-sheltered shores (reviewed by Boulding, 1990). Instead, in two
consecutive years in a row we observed higher predation rates on medium and large L.
sitkana than on small L. sitkana at our wave-sheltered site 3. The higher risk of
predation for larger L. sitkana seems to be a general finding for many Northeastern
Pacific shores. Behrens Yamada and Boulding (1996) tethered L. sitkana to four
moderately to very wave-sheltered sites 175 km to the southeast on San Juan Island and
found that extra-large L. sitkana consistently suffered rates of predation up to one and
one half times higher than large L. sitkana. The absence of a size-refuge from predation
for L. sitkana likely reflects the type of shell-breaking predators that are abundant on
wave-sheltered shores in the Northeastern Pacific. As we discuss below, the presence of
the shell-breaking crab, Cancer productus, appears to be the principal reason why no
size-refuge from predation exists on these shores. Indeed Boulding and Van Alstyne
(1993) did not find lower survival of large L. sitkana relative to medium–small L.
sitkana on moderately wave-sheltered shore in Northwestern Washington perhaps
because the predatory crab Cancer productus was very rare there (E.G. Boulding, pers.
obs.).
In contrast, our results support the paradigm that thin-shelled snails are more
vulnerable to shell-breaking predators than thick-shelled snails (reviewed by Vermeij,
1987). Significantly more of the thin-shelled species were eaten than of the two
thick-shelled species. Similar results were observed 60 km south by Boulding and Van
Alstyne (1993) who found that thin-shelled Littorina subrotundata survived less well on
wave-sheltered shores than L. sitkana and L. scutulata s.l. However they did not tether
the snails so were unable to recover the shell fragments and identify the predator(s).
4.2. Identity of predators
To understand why there was a lower risk of predation for our small size-class of L.
sitkana at wave-sheltered site 3 it is necessary to identify the predators. More than
33–43% of the predation on our tethered large L. sitkana and 52% of the predation on
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
233
our tethered extra-large L. sitkana at our sheltered site 3 could be attributed to
shell-breaking crabs because we recovered ‘‘peeled’’ shell fragments still attached to the
tether. Much of the remaining predation that left ‘‘crushed’’ shell fragments with only
the apex still attached to the tether was likely also to be the result of shell-breaking
crabs. The only shell-breaking crab abundant in our SCUBA transects during night high
tides was Cancer productus. In addition, more than 35% of the crabs we observed were
males larger than 140 mm in carapace width which can crush even our extra-large
size-class of L. sitkana outright (Behrens Yamada and Boulding, 1998) and would
therefore leave only the non-diagnostic ‘‘crushed’’ shell fragments. Cancer productus
seems to be generally abundant in subtidal areas below wave-sheltered shores in the
Northeastern Pacific. Previous SCUBA observations near our sheltered site 4 also found
a high abundance of C. productus foraging in intertidal areas especially during night
high tides (Robles et al., 1989). Cancer productus was also strongly implicated in the
high rates of predation of tethered L. sitkana on sheltered shores in Northern Washington
(Behrens Yamada and Boulding, 1996).
‘‘Crushed’’ shell fragments can also be produced by shell-breaking fish such as the
pile perch, Rhacochilus vacca. McCormack (1982) concluded that pile perch were the
major predator on Littorina sitkana at low tidal levels but we disagree because pile perch
large enough to eat extra-large L. sitkana were not abundant at sheltered site 3 and also
because so many of the recovered snails were ‘‘peeled’’ and could only have been
opened by crabs. McCormack (1982) may have overestimated the importance of pile
perch because she did not make observations during the night or with SCUBA.
However, the pile perch she observed did show size-selective predation and preferred
large L. sitkana (shell length 8–11 mm) over medium L. sitkana (shell length 6–7 mm)
when offered snails during daytime high tides on a wave-sheltered pebble beach near
Bamfield Marine Station (McCormack, 1982).
If C. productus is the major predator on L. sitkana then we can use the proportion of
snails of a particular size-class whose shell fragments were recovered ‘‘peeled’’ as an
index of the relative size of the crabs (Behrens Yamada and Boulding, 1998). In our
1995 tethering experiment at our sheltered site 3, 43% of the large size-class was
‘‘peeled’’. This suggests the crabs responsible are small. Laboratory feeding experiments
with L. sitkana the size of our large size-class have shown that ‘‘peeled’’ shell fragments
are produced by H. nudus smaller than a carapace width of 22–25 mm (5–7 g wet
weight) and by juvenile C. productus smaller than a carapace width of 41–48 mm (9–12
g wet weight) (Behrens Yamada and Boulding, 1998; Behrens Yamada, unpubl. data).
Our SCUBA observations at our sheltered site 3 also suggest that juvenile C. productus
were responsible for much of the predation on tethered shells as they made up 46% of
the crabs we observed. Small juvenile C. productus less than 50 mm in carapace width
made up 20% of the crabs observed during our night dives and likely were responsible
for many of the peeled shells we recovered.
We are unsure why juvenile C. productus would prefer the larger size-classes of
tethered L. sitkana when they often show a preference for smaller size-classes in
laboratory experiments (Behrens Yamada and Boulding, 1998) but it is possible that the
larger snails are more easily detected in the field. In a previous study Cancer productus
preferred the small size-classes of prey in the laboratory but large size-classes of prey
when preying on the bivalve, Protothaca staminea near our sheltered site 3 (Boulding
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E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
and Hay, 1984). In that case the crabs transported the large bivalves from the intertidal
to subtidal eelgrass beds before opening them. Even small crabs can open large
molluscan prey by repeatedly loading the shell over long periods of time (Boulding and
LaBarbera, 1986).
We are not sure why we observed higher predation rates on our large size-class of L.
sitkana than on our small size-class of L. sitkana at our sheltered site 3 but not at our
sheltered site 4 and believe we would need a much larger study with multiple sites on
the same shore and multiple shores to determine this. Interestingly, we observed a
similar size-distribution of Cancer productus at our sheltered site 3 (Grappler Inlet) to
that reported by Robles et al. (1989) at our sheltered site 4 (Dixon Island). They also
found no crabs less than 9 cm in carapace width during the day but about 33% of the
crabs they observed at night had a carapace width less than 9 cm (Fig. 1 in Robles et al.,
1989). In comparison we saw a slightly higher proportion of small crabs with up to 46%
of the crabs we observed at night having a carapace width of less than 9 cm. If our
sheltered site 3 consistently has proportionately more juvenile crabs than our sheltered
site 4 that might explain why we observed size-selective predation there but not at site 4.
We observed very little shell-breaking predation at our two wave-exposed sites. The
only predatory crab observed at the two wave-exposed sites was the shore crab,
Hemigrapsus nudus which is a known predator on Littorina spp. Robles et al. (1989) did
several day and night SCUBA transects at high tide in the intertidal zone near both of
our wave-exposed sites and observed no Cancer productus. In contrast with C.
productus, H. nudus is an inefficient predator (Behrens Yamada and Boulding, 1998)
and shows a very strong preference for the thin-shelled L. subrotundata over thickshelled species such as L. sitkana in laboratory experiments (Boulding and Van Alstyne,
1993; Boulding et al., in prep.). This likely explains the comparatively high predation
rates of L. subrotundata at our two wave-exposed sites relative to L. sitkana and L.
scutulata s.l.. Shore birds such as the black turnstone (Arenaria melanocephala) and the
surfbird (Aphrisa virgata) also occur seasonally at our wave-exposed sites and are
known to prefer Littorina spp. (2.1 mm,shell width,4.3 mm; Marsh, 1984). However,
we believe they would be unable to crush tethered snails in their crops without breaking
the tether line.
Other possible littorinid predators, such as ducks, starfish or predatory gastropods,
were not important at our sites. Diving ducks were rarely observed and again could not
crush tethered littorinid gastropods without breaking the tethering line. Such snails
would be recorded as missing so would not be included in our estimate of the rate of
shell-breaking predation. We observed one predatory starfish, Pisaster ochraceus
(Brandt, 1835), feeding on one tethered snail at sheltered site 3, but it did not break the
shell. We never observed dead, tethered littorinid snails with drill holes so believe
predation by gastropods is low.
4.3. Assumptions of tethering experiments
Tethering experiments are a powerful method of quantifying selective foraging but
tethered prey may be more vulnerable than untethered prey (Peterson and Black, 1994).
Barbeau and Scheibling (1994) concluded that tethering has differential effects on
predation intensities depending on the relative motility of the prey and the predator.
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
235
Their experiment with tethered scallops and crabs showed that when only encounter rate
is important (when the predator is quick enough to capture the prey even if it is
untethered), the effects of tethering of the prey on the predation intensity are minimal.
Indeed McGuinness (1997) found that tethering non mobile plant parts (mangrove tree
propogules and mangrove leaves) had no significant effect on their rate of loss relative to
those of untethered controls. The tethering technique used in our experiments is unlikely
to have greatly affected the risk of predation to crabs, since gastropods do not rely on
active escape from crabs. In addition, crabs are good at manipulating prey and tethering
had no significant effect on the vulnerability Littorina irrorata to blue crabs in the
laboratory (Warren, 1985). We have observed Hemigrapsus nudus preying on tethered
and untethered Littorina sitkana and the fine fishing line of the tether seems to have no
effect on the handling method or handling time (E.G. Boulding, pers. obs.) perhaps
because the tether is attached to a such small area of the shell. In contrast Rhacochilus
vacca in an aquarium has more difficulty preying on tethered L. sitkana than untethered
L. sitkana (E.G. Boulding, pers. obs.). Consequently tethered snails may experience
lower rates of mortality from this fish than untethered snails which would cause our total
estimates of predation mortality to be lower than they should be.
When comparing tethering experiments done at different sites it is important to realize
that the size of any tethering artifacts could be larger at some sites than others (Peterson
and Black, 1994). For example, tethered Littorina irrorata are significantly less able to
escape predatory crabs by climbing up grass stems than untethered snails (Vaughn and
Fisher, 1988) but this artifact will only be important at sites where grass stems are
present. We deliberately chose to work in the less topographically complex barnacle zone
above the Fucus zone where there was little opportunity for the snails to escape
predation by climbing vertically. In our experiments the tether restricts the snail into
choosing a hiding place within 0.5 m of the screw but we placed the screws in areas that
normally had L. sitkana present so had suitable hiding places between barnacles and in
rock crevices. Nevertheless we can not exclude the possibility that artifactual enhancement of predation rates by the tethers occurred and was not constant across all of our
sites.
In addition it is possible that tethered snails were disoriented and were more
vulnerable to predation for the few hours it took to find a suitable hiding place. This
would result in positive feedback so that screws that had the snails replaced more often
would suffer higher rates of predation because of the initial disorientation period. We do
not believe this effect was large because we also replaced snails whenever the tether
became badly tangled or when the snail died from heat or desiccation stress and that did
not result in an increased risk of predation before the next monitoring period. In
addition, our experiments in 1995 and 1997 used snails collected at a different shore
than the one they were tethered at and this could also result in increased predation if
these snails were slower to find a hiding place than snails on their home shore. However
Chapman (1986) found that disturbance, translocation, and transplantation had little
effect on the subsequent movement of Littorina unifasciata.
4.4. Selection on littorinid body size and shell thickness
The large differences in risk of predation experienced by Littorina sitkana at the two
236
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
extremes of its distribution along a wave-exposure gradient might be expected to lead to
genetic differences among wave-exposed and wave-sheltered populations. This is
especially likely because L. sitkana has the direct development and low vagility
(Boulding and Van Alstyne, 1993), which reduces the amount of gene flow among
populations and increases the potential for local adaptation. Indeed, genetic differences
between populations for traits such as shell form, behaviour, and life history traits have
been previously described for other direct-developing Littorina species (Janson, 1982b;
Johannesson and Johannesson, 1996).
Our study did not specifically investigate genetic differences among wave-exposed
and wave-sheltered populations of L. sitkana, but suggests which differences should be
looked for in future work. For example, we observed a larger mean size of L. sitkana at
our moderately wave-exposed sites than at our wave-sheltered sites. This difference
could be partially genetic and could occur because L. sitkana at our wave-sheltered sites
reduce their allocation to growth and increase their allocation to reproduction earlier
than those at our wave-sheltered sites. Alternatively, the larger mean size on waveexposed shores may not have a genetic basis and may simply reflect lower mortality
rates.
The benefit of larger mean body size on moderately wave-exposed shores would at
first seem questionable since large snails would have fewer refuges from wave shock
(e.g. Boulding and Harper, 1998). But our field experiments show that the risk of
mortality from thermal / desiccation stress is higher for small snails than for larger snails.
Smaller snails have a greater aperture surface area to body volume ratio than larger
snails, and will tend to lose water faster than larger snails. In summer the mean wave
height is low and desiccation stress is much more severe at our wave-exposed sites
which might select for larger mean body sizes. Snails at our wave-exposed sites rarely
got wet during neap tide periods because the upper limit of distribution of L. sitkana was
higher above 0.0 datum at our wave-exposed sites than at our wave-sheltered sites.
We might also expect genetic differences in shell thickness between Littorina sitkana
populations in wave-exposed areas and wave-sheltered areas because of the difference
this made to risk of predation. Indeed the vulnerability of L. subrotundata to shore crab
predation may explain why it was not found at our three most sheltered sites. The
differences in shell weight from our common environment experiment showed that a
difference in adjusted shell weight of 5.4 mg between L. subrotundata and L. sitkana
that is likely to be partially genetic. In our tethering experiments a similarly small
difference in the shell thickness between L. sitkana and L. subrotundata was sufficient to
affect their vulnerability of L. sitkana to the predatory shore crab, H. nudus. However
such a small difference in shell thickness may be difficult to detect statistically in
field-collected specimens. Raffaelli (1978) expected to see differences in shell thickness
of Littorina saxatilis between habitats varying in wave-exposure and crab predation
intensities but found no correlation.
Acknowledgements
We thank S. Behrens Yamada, R. Rochette, A.J. Underwood, and two anonymous
reviewers for their suggestions for improving the manuscript, O.B. Allen and X. Lu for
E.G. Boulding et al. / J. Exp. Mar. Biol. Ecol. 232 (1999) 217 – 239
237
assistance with the statistical analysis, T. K. Hay, T. Kehl, and J. Ferris for weighing and
digitizing shells, L. Kusumo for gluing tethers onto snails, S. Dudas for her SCUBA
observations, the Director and staff of Bamfield Marine Station for field support, and the
Huu-ay-aht First Nation for access to our study sites. Financial assistance was provided
by N.S.E.R.C. (Canada) research and equipment grants to E.G. Boulding.
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