J. Moll. Stud. (1998), 64, 329-343
© The Malacological Society of London 1998
CONTRIBUTION OF GENETIC AND ENVIRONMENTAL
FACTORS TO SHELL SHAPE VARIATION IN THE LOTIC
SNAIL SEMISULCOSPIRA REINIANA (PROSOBRANCHIA:
PLEUROCERIDAE)
MISAKO URABE
Department of Biosciences, Faculty of Science, Nara Womens' University Kitauoyanishi-machi, Nara, Japan
(Received 8 March 1996; accepted 3 November 1997)
genetical and morphological divergence among
populations of Goniobasis proximo.
The genetic and environmental factors affecting shell
It has long been known that a great deal of
shape in the freshwater snail Semisulcospira reiniana morphological variation can be found even in a
at Takahashi in Kyoto, central Japan, were studied
single population of Pleuroceridae (Adam,
by means of a rearing experiment and field obser1915; Goodrich, 1945). In such cases, the shell
vations. Shell shape was characterized by three
variation
is not explained by genetic isolation
parameters; W (whorl expansion rate), T (whorl
or the chemical components of the water.
translation rate), and S (roundness of generating
Urabe (1992) showed that the adult shell
curve). Estimated heritabilities were low in all three
variation of Semisulcospira reiniana (Brot) was
parameters and the largest component of the great
shell variation in the Takahashi population was
greater in the population from the middle
environmental variance, suggesting that the main
reaches than in the population from the lower
source of shell variation was phenotypic modulation,
reaches of the Kamo River in Kyoto, central
in response to the external environment. In the field, Japan. In the middle reaches, shells of S. reinisnails that were active in fast currents had larger W
and smaller T, that is, a larger body whorl and a ana vary from the slender ribbed type typical
for this species, to a globular smooth type. The
lower spire, than snails in slow currents. Substratum
latter type cannot be distinguished on shell
conditions related to T in resting periods although its
characteristics from the congeneric species
cause was unclear. Mechanisms are suggested which
S. libertina (Gould) which also occurs in the
in the absence of selection of genetic variation could
cause and maintain shell variation in S. reiniana in middle reaches of the river. That is to say, the
different microhabitats.
range of shell variation within a single population of 5. reiniana can sometimes overlap that
of another species.
The purpose of this study is to discover how
INTRODUCTION
such a large amount of variation in shell
The freshwater viviparous snails Semisul- morphology, especially shell shape, originates
cospira Bftettger (Family Pleurocendae) show within a population. Many field experiments
inter- and intra-population variation in shell have suggested that variation in shell shape is
characteristics, such as size, shape, sculpture an adaptation to different environmental conand colour of both the adult shell and the pro- ditions (e.g. Kitching, Muntz & Ebling, 1966;
toconch (Kuroda, 1929; Davis, 1968, 1969, Janson, 1983). Few studies, however, have
1972;' Urabe, 1992). This has often caused investigated the mechanism whereby variation
difficulties in species identification. For the in shell shape (rather than in shell ornament or
subfamily Pleurocerinae in North America, thickness) emerges (Appleton & Palmer, 1988;
Palmer, 1985, 1990). The main source of shell
several authors have analysed shell variation
among populations in relation to either phy- variation may be either genetic diversity or
logeny (Dillon & Davis, 1980; Chambers, phenotypic modulation without genetic differ1982), or environmental factors (Dazo, 1965, a ence (Smith-Gill, 1983; Gibbs, 1993), or a
review), or both (Dillon, 1984). Dillon (1984) combination of the two (Boulding & Hay,
listed geographic distance and chemical com- 1993). A study of the genetic and environponents of water as important factors affecting mental factors influencing shell morphology is
ABSTRACT
MISAKO URABE
330
necessary to know the relative importance of
natural selection and phenotypic modulation
on shell morphology. Since shell morphology
can be adaptive in either case, the relative
importance of these factors cannot be evaluated by experiments merely revealing selection
pressure acting on adult snails. Additionally, to
know the environmental factors affecting shell
variation within a population, the environmental conditions must be measured in each
microhabitat.
In this paper, I estimate from a rearing
experiment the heritability of shell shape of
5. reiniana in order to clarify the contribution
of genetic factors to shell shape. I also analyse
the relationships between shell shape and
micTohabitat conditions at the different times
of the day when snails are active or inactive.
Finally, I discuss the possible causes of morphological variation and a mechanism whereby
the variation is maintained in a population.
MATERIALS AND METHODS
Snail rearing
Semisulcospira reiniana was reared in aquaria over
two generations to estimate the heritability of shell
shape and to examine the variation in shell shape
under uniform environmental conditions. Founder
individuals were collected from the Kamo River at
Takahashi (135°45' E; 35°5' N.) in Kyoto (Fig. 1), in
November 1989. At Takahashi, the river is not
embanked and ariffle-poolsystem is well developed.
The shell variation of S. reiniana at Takahashi is the
largest among all populations of Semisulcospira in
the Kamo River (Urabe, 1992). All of the snails
collected were of immature size (shell width
< 6.4 mm).
The snails were reared with small goldfish in an
aquarium (45 x 30 x 30 cm) paved with pieces of
coral (grain diameter > 4 mm) to provide a supply of
calcium. The aquarium was maintained in the laboratory at 23°C under a regime of 12 h light and 12 h
darkness. TetraMin flakes were fed every 3 days.
TetraMin, faeces from the goldfish, and periphyton
on the glass walls were available as food for snails.
The water was changed once a month.
When the snails grew to 7 to 8 mm in shell length,
they were individually marked with small pieces of
waterproof paper. Sex and maturity cannot be determined from exterior appearance in Semisulcospira.
Accordingly, after the snails had copulated in the
aquarium, each snail was placed in a plastic cup with
a mesh bottom which was hung in an aquarium,
thereby isolating each mother-offspring lineage. I
obtained 20 families of mothers and their offspring.
The shells of the mother snails were measured with
calipers every month, except that aperture length and
aperture width (see below) were measured only once
after reproduction stopped, during February and
November in 1993.
The number of newborn snails was counted every
3 days. Each brood was kept separately in a 50 ml
plastic cup. When their shell length reached 6.8 mm,
H
cliff
::: dry riverbed
1990(daytime sampling) j
Takahashi
i
Kamo R.
•35"N
I992&1993(nighttime)
< ^ 1 9 9 1 (nighttime)
100km
135°E
Figure 1. Map of the observation sites.
100m
SHELL SHAPE VARIATION IN SEMISULCOSPIRA REINIANA
they were individually marked and transplanted into
aquaria paved with pieces of coral (> 4 mm). Thenshells were measured at the age of one year.
Estimation of heritability of shell shape
The measured dimensions of shells are shown in Fig.
2, as follows: shell width (SW), penultimate whorl
width (PWW), third whorl width (TWW), penultimate whorl length (PWL), third whorl length (TWL),
aperture length (AL) and aperture width (AW).
Using these measurements, approximate values for
parameters describing shell shape of gastropods
(Raup, 1966) were calculated. The rate of whorl
expansion (W) was calculated as PWW/TWW
(Newkirk & Doyle, 1975), and the rate of whorl
translation (T) was calculated from the following
formula;
T = 1 + VW>V|PWL2-(PWW-TWW)2/
(1 + VW))2/(PWW-TWW)
B
w=pwwmvw
1
T=
PWL2-(PWW-TWW)2/(1+VW)2
(PWW-TWW)
=A/B
S=AL/AW
Figure 2. Measurements of the shell and formulae of
the three parameters describing shell shape. SW,
shell width; PWW, penultimate whorl width; TWW,
third whorl width; PWL, penultimate whorl length;
TWL, third whorl length; AL, aperture length; AW,
aperture width.
331
which indicates the ratio of A to B (Fig. 2). When W
and T are regressed on SW, the partial correlation
coefficient between them is highly significant both in
the reared and the wild snails (p < 0.001). The correlation of W and T seems inevitable when whorls are
coiling without forming an umbilicus. However,
some researchers make the point that the correlation
also results from a natural selection process, not only
from the mechanistic constraints of shell development (Boulding & Hay, 1993).
The roundness of the generating curve (S) was
described by AL/AW. I did not calculate the position
of the generating curve relative to the axis (D) and
assumed that the inner margin of the whorls always
contacted the coiling axis. For statistical analysis, all
the parameters were log transformed to reduce the
skewness of the data.
To estimate the heritability of each shell-shape
parameter, the regression coefficient of the means of
offspring against their mothers was calculated. Snails
having more than two additional whorls in the aquarium were selected so that only the part of the shell
formed in the aquarium was measured.
The mean SW of offspring was significantly different among families of siblings (ANOVA, p < 0.001)
and each of the three parameters was correlated with
SW. Hence, to exclude size effects, I adjusted the
mean parameter of each family to correspond with
the mean SW of all offspring (7.28 mm) using relevant regression equations. The parameters W and T
of the mothers were estimated from the shell
measurements when SW was close to 7.28 mm. The
parameter S of the mothers was calculated from the
measurement when they were 10.0 to 12.8 mm in SW.
However, the size effect for S was small because the
correlation between SW and S is nearly zero when
SW is more than 7 mm.
Then regression coefficients of the adjusted mean
parameters against the mother's parameters were
calculated. The adjusted mean parameter of each
family is weighted according to family size (Falconer,
1989). The heritability (additive genetic variance/
phenotypic variance) of each parameter is estimated
as twice the mother-offspring regression coefficient,
since Semisulcospira is dioecious and never selfs
(Falconer, 1989). I assumed that they had copulated
randomly since the mating pairs were uncertain.
Daytime sampling
Daytime sampling to examine the relationship
between shell shape and the environmental factors of
resting sites was carried out at Takahashi on 7th and
15th August, 1990. At Takahashi, adult S. reiniana
show nocturnal activity (Urabe, 1998).
The sampling area was a 50 m length of the river
including a riffle and two pools (Fig. 3). In an area
where the snail density was high (the lower right area
of the left map in Fig. 3) 17 quadrats (50 cm X 50 cm)
were set on intersections of a 2 m X 2 m grid and all
the snails in the quadrats were collected. In the other
area, all snails that I could find were collected. I
could not collect snails at the centre of pools deeper
1991
(Left bank)
f
1992&1993
(Right bank)
1990(daytime sampling)
Figure 3. Maps of the sampling and the observation sites with depth contour lines. Arrows show the current directions. Left: Daytime sampling site in 1990. Dots
show the sampling points of S. reiniana uninfected by trematodes. The smallest dot indicates one snail and the largest seven. Shaded areas show muddy bottom and
the other area pebble, boulder and rock. The lower right corner is the quadrat sampling area. Centre: Night-time observation site in 1991. Right: Night-time observation site in 1992-1993. In shaded areas the current velocity was less than 10 cm/s.
10m
\
m
i
o
SHELL SHAPE VARIATION IN SEMISULCOSPIRA REINIANA
than 70 cm, but the sampling bias seemed to be negligible because of the scarcity of snails in the pools.
The sampling started at KfcOO and finished by 18:00,
before sunset. Only snails with a SW larger than
6 mm were collected because of the difficulty of
identifying smaller snails.
At sampling, the current velocity and substratum
type at the capture site of each snail were recorded.
The current velocity was ranked into three classes;
0-1 cm/s, 1-10 cm/s and > 10 cm/s (maximum
30 cm/s). The substratum was categorized into 'hardbottom' and 'soft-bottom'. The latter category
includes substrata into which snails can bury themselves, i.e., mud, sand and granules smaller than the
snails.
The shells of the collected snails were measured
and their shell-shape parameters compared between
environmental categories. When the parameters had
a significant correlation with SW, the slope and intercept of the regression lines were compared (Sokal &
Rohlf, 1981). In the other cases, the means of the
parameters were compared.
The soft bodies of the collected snails were dissected to examine for infection by trematodes.
Infected snails were excluded from the data since
trematodes could modify distribution, activity or
shell morphology of the hosts (Goodrich, 1945; Shinagawa, 1995).
Night-time observation of microhabitat utilization
I observed the microhabitat utilization by snails at
night to examine the relationship between shell
shape and environmental factors during their active
period. The night observations were made fifteen
times from May to September in 1991-1993.
The central and right maps in Fig. 3 show topographical features of the observation sites. In 1991,
observations were carried out on the left bank at
Takahashi (part of the daytime sampling area in
1990) where the current velocity was less than 1 cm/s
and the substratum was mud and boulders.
Observations in 1992 and 1993 were carried out on
the right bank approximately 50 m downstream from
the 1991 site. The area was divided into two subareas
according to the current velocity on the river bed, i.e.
5-10 cm/s and > 10 cm/s. (maximum 80 cm/s). The
subareas of 5-10 cm/s were restricted to small indentations in the bank, as shown in Fig. 3. Although the
behavioural observations were only carried out on
days with normal water level, the current velocity
might vary within a certain range among the observation days. However, because water levels change the
maximum current velocity more than the velocity in
the indentations or in the lee of rocks, I believe that
this classification is justifiable. The substratum was
rock, boulder and sand in both subareas.
The snails were individually marked more than 3 h
before sunset or on the previous day, in order to
diminish the handling effects on their activity
pattern. They were released at the capture points
within 30 min. The trails of each snail were recorded
on maps every 5-15 min with notes on the
333
substratum on which the snail crawled. The observations started more than 2 hours before sunset and
ended more than 3 hours after sunrise the next morning. I used a torch for observations at night. Following the observations, the snails were brought to the
laboratory for shell measurement and examination
for trematode infection. Infected snails were
excluded from the data.
The size of a panmictic unit of Semisulcospira is
uncertain. If snails are collected from a larger area
than a panmictic unit, the sample includes some
genetically uneven subpopulations. Such samples
might cause misinterpretation of the influences of
inheritance and environment on shell morphology
(Clarke, Arthur, Horsley & Parkin, 1978). The only
data that I can use are the movement of adult 5.
reiniana in usual water levels. On average snails
crawled 1.8 m per day in the area on the left bank,
and 1.1 m in the area on the right bank (Urabe,
1998). The maximum upstream migration distance
traced was 12 m in two days (Urabe, unpublished
data). These data indicate the minimum ability of
migration of S. reiniana, because juvenile snails can
migrate by floating, and adult snails may also be
carried away by flood. Thus, I believe that the
samples are not divided into genetically uneven subpopulations.
The parameters of shell shape were compared first
between the two observation sites and then among
the three areas with different current velocities.
Snails that moved in both 5-10 cm/s and > 10 cm/s
areas were classified into the > 10 cm/s area group.
When the parameters had a significant correlation
with SW, the slope and intercept of the regression
lines were compared. In the other cases the means of
the parameters were compared.
Then the relationships between the parameters
and the condition of substratum used in the active
period were examined. To represent the substratum
condition used by each active snail, the percentage of
hard-bottom utilization was calculated. Snails that
were motionless all night were excluded from the
data. Snails that stayed still for more than 30 minutes
was regarded as resting, and the resting period were
excluded from the analysis. The hard-bottom utilization percentages were ranked into 0-30%, 30-70%
and 70-100%. The three hard-bottom utilization
classes included snails from the left and right banks
at different ratios. The ratios of snails from the left
bank in each of the three classes were 1.00 (28/28),
0.84 (26/31) and 0.36 (15/42), respectively.
RESULTS
Heritability of shall shape
Data were obtained in 20 mother snails and
their offspring. The range of brood size was
8 to 73 (mean = 29.4). Table 1 shows the
regression coefficient of each parameter. All
of the regression coefficients are negative and
334
MISAKO URABE
Table 1. Heritabilities of the shell parameters in S. reiniana calculated from mother-offspring
regression lines.
Parameter
regression coefficient
W
T
S
-0.021
-0.052
-0.203
the heritability was estimated at 0%. If one
considers the upper limits of the 95% confidence intervals, the heritability of each parameter is estimated as less than 8.4%, 11.4%
and 4.6%, respectively.
When the parameters were plotted against
SW, the residua] variance of the reared
snails was not different from that of the wild
snails for log10W (jackknifing for the statistics
of absolute variance (Van Valen, 1978): t =
1.24, DF = 724, p > 0.05). For log10T and
log10S, the residual variance was smaller than
that of wild snails (jackknifing for the statistics
of absolute variance: log10T, t = 5.15, DF =
724, p < 0.001; log1(>S, t = 3.10, DF = 724,
p < 0.01). Thus, variance of shell shape was
smaller under homogeneous environment
conditions in the laboratory, compared with
the field.
Comparison of shell shape among microhabitats in the resting period
Figure 3 shows the distribution of S. reiniana in
a riffle-pool system during the day. Most of the
snails were distributed in the indentations on
both banks. Forty-four snails were collected
from the hard-bottom and 49 from the softbottom. Some snails were in completely
sheltered situations; 17 snails (18.3%) were
under stones, and 19 (20.4%) snails had buried
themselves in sand or mud.
Figures 4 and 5 compare the parameters W
and T on a log scale among classes of current
velocity and categories of substratum, respectively. The regression lines of logi0W and log10T
plotted against SW were not significantly
different among velocity classes (logi0W; slope,
F(2, 87) = 2.22, p > 0.05; intercept, F(2, 89) =
3.05, p > 0.05: log10T; F(2, 87) = 2.82, p > 0.05;
intercept, F(2,89) = 2.44, p > 0.05). The slopes
of the regression lines of both parameters
were significantly different between substrata
(log10W; F(l, 89) = 5.39, p < 0.05: log,0T; F(l,
89) = 5.59, p < 0.05). The differences of slope
seem to be due partly to outliers of SW less
than 10 mm. For logioW, the significance was
standard error
0.030
0.052
0.108
confidence limits
lower 95%
upper 95%
-0.084
-0.161
-0.430
0.042
0.057
0.023
removed by omitting them (after the outliers
have been excluded: F(l, 86) = 2.70, p > 0.05).
However, the difference was still significant for
log,0T (F(l, 86) = 4.90, p < 0.05). Since the
parameter logioS was not correlated with
SW, the means of logioS for each class were
compared. The results were non-significant
(substratum category; t = 0.481, DF = 91,
p > 0.05: velocity classes; F(2, 90) = 2.03,
p > 0.05).
Comparison of shell shape among
microhabitats in active period
Figure 6 shows the regression line of the
parameters W and T on a log scale plotted
against SW for each observation site. The
slopes of the regression lines were not significantly different between the sites (log10W;
F(l, 125) = 0.00, p > 0.05: log10T; F(l, 125) =
0.04, p > 0.05) while the intercepts were significantly different (log,0W; F(l, 126) = 11.86, p
< 0.001: log,0T; F(l, 126) = 11.43, p < 0.001).
The means of log10S were also significantly
different (left bank; mean = 0.293: right bank;
mean = 0.303: t = 2.44, DF = 127, p < 0.05).
Snails on the left bank had smaller W, S, and
larger T than those on the right bank.
Figure 7 shows the regression lines of the
parameters W and T on a log scale plotted
against SW for each class of the current velocity. For logioW and logioT, the slopes of the
regression lines were not different among the
classes (log,0W; F(2, 95) = 0.43, p > 0.05:
log,0T; F(2, 95) = 1.31, p > 0.05) while the
intercepts of the lines were significantly different (log10W; F(2, 97) = 5.06, p < 0.01: log,0T;
F(2, 97) = 7.44, p < 0.001). For log,0W, the
intercept of the 0-1 cm/s class was smaller than
that of the > 10 cm/s class (analysis using
Tukey's method of multiple comparisons, p <
0.01), while the reverse was true of logioT
(ditto, p < 0.01). In both cases, the regression
lines of the 5-10 cm/s class, based on the data
on the right bank, were closer to those of the
0-1 cm/s class from the left bank rather than
the > 10 cm/s class.
SHELL SHAPE VARIATION IN SEMISULCOSPIRA REINIANA
1.7
335
0-1cm/s y=1.58»10-°0063x r=-0.450*"
1-10cm/sy=1.72»10-°0089x r=-0.873"
>10cm/s y=2>04»1CH)C)14x r=-0.836"
1.6
1.5
1.4
1.3
.CD
CO
O
C/)
O)
O
1.2
1.1
CD
•4—»
14
12
CD
E
0-1cm/sy=2.18»100031xr=0.568***
1-10cm/sy=6.34»10OO31xr=0.802*"
10
9
8
7
CO
CO
\-
>10cm/sy=1614«100052x r=0.820*
6
5
10
12
14
16
18
20
Shell width (mm)
Figure 4. Scatter plots and regression lines of the parameters W and T plotted against SW for each current
velocity class for snails in the resting period. Symbols are explained in the figure. *p x, 0.05, **p < 0.01, ***p <
0.001
336
MISAKO URABE
1.7
1.6
•
soft bottom y=1.83*1 CH3 o06* r=-0.513**
o
hard bottom y=1.56»10-°011* r=-0.788*
1.5
1.4
1.3
CO
1.2
o
1.1
o •
o
CD
CD
•*—>
14
12
E
10
9
8
7
CO
Q_
H
6
0024x
r =0.561***
soft bottom y=1.52«10
- ^ —
o
hard bottom y=2 79«10 0 0 4 1 x r=0.78r**
-
•
o
•
t
I
o
o
f
•
o
-
5
^ ^ ^ ^
#
..--'"
o
.-••'"
o
o
o
I
1
1
1
I
1
10
1
1
1 1
12
i
i
i
14
i
i
16
i
i
•
1
18
1
1
!
20
Shell width (mm)
Figure 5. Scatter plots and regression lines of the parameters W and T plotted against SW for each substratum
category for snails in the resting period.
SHELL SHAPE VARIATION IN SEMISULCOSPIRA REINIANA
337
1.7
— • — '91(left bank) y= i.53«10-° 0057x r=0.485"*
1.6
—-O-— '92-3(right bank) y=1.59*10.-00058" r=-0.421"
1.5
1.4
1.3
_CD
CO
O
(/)
D)
O
CD
-»—>
CD
CO
CO
1.2
oo
1.1
14
12
— • —
'91 (left bank) y=2.16«100032x r=0.572***
— - o — • '92-3(right bank) y=2.01»10°°31x r=0.545*"
10
9
8
7
6
5
j
10
12
14
16
i_
18
Shell width (mm)
Figure 6. Scatter plots and regression lines of the parameters plotted against SW for each observation site for
snails in the active period.
MISAKOURABE
338
1.7
1.6
left bank(0-1cm/s) y=1.59»10-°0069x r=-0.457*"
right bank(5-1 Ocm/s) y=1.68«10-°0082x r=-0.719"
right bank(>1 Ocm/s) y=1.54»10-°0046x r=-0.295
4-
1.5
1.4
1.3
_CD
CO
o
1.2
o
1.1
CO
CD
CD
14
E
12
CO
CO
CL
10
9
i
i
i
left bank(0-1cm/s) y=1.81«100037x r=0.530***
right bank(5-1 Ocm/s) y=1.5CM00042x r=0.791
right bank(>1 Ocm/s) y=2.14«10°-28x r=0.470*
8
7
_i
I
10
I
12
I
i
14
16
18
Shell width (mm)
Figure 7. Scatter plots and regression lines of the parameters W and T plotted against SW for each current
velocity class for snails in the active period.
339
SHELL SHAPE VARIATION IN SEMISULCOSPIRA REINIANA
The difference in logioS among the velocity tability (Falconer, 1989), the real heritability is
classes was non-significant (F(2,98) = 2.81, p > never much higher than this result. Therefore,
0.05).
the largest contributor of the morphological
Before comparing among the hard-bottom variance in the Takahashi population is enviutilization classes,' the regression lines of the ronmental influences. This view is supported by
parameters plotted against SW from the left the small residuals of T and S of the snails
and right banks were compared to test for reared in the laboratory in which the environdifferences between the observation sites. mental conditions were more consistent than
Within the same hard-bottom utilization class, the field.
no regression line was significantly different
Urabe (1992) reported that there was greater
between the two banks. Accordingly, the data variation in the shell morphology of 5. reiniana
from the two banks were combined and the at Takahashi than at Hiragino-Dam in lower
regression lines were obtained for each of the reaches of the Kamo River. The environmental
hard-bottom utilization classes as a whole. conditions of a natural river bed are obviously
Figure 8 shows the relationship of the para- more complicated than a simple sandy bottom
meters W and T to hard-bottom utilization. in a dam. The large variation in the wild popuThe difference among hard-bottom utilization lation might result from the large variance in
classes was not significant for either parameter environmental conditions.
(log,0W; slope F(2, 95) = 1.52, p > 0.05: intercept, F(2, 97) = 1.10, p > 0.05: log,0T; slope,
Relationship between shell shape and
F(2, 95) = 0.81, p >. 0.05: intercept, F(2, 97) =
0.11, p > 0.05). The difference in log10S among microhabitat during the day and at night
the hard-bottom utilization classes was also The relationship between the parameters of
non-significant (F(2, 98) = 2.20, p > 0.05).
shell shapes and microhabitat environmental
factors varied between day and night.
The shell shape was clearly related to current
velocity at night. Snails that were active in fast
DISCUSSION
currents had larger W and smaller T, that is, a
relatively larger body whorl and aperture and a
Heritability of shell shape
lower spire than snails in slow currents. The
Before the discussion, I call attention to the result is concordant with studies on intrarisk that some statistical significances in the specific shell-shape variation in other freshpresent results may come out by chance, water gastropods (Hutchinson, 1993; a review).
because of the number of tests conducted For marine gastropods, snails exposed to heavy
(heritability, 3 comparisons; daytime, 10 com- wave-action have larger apertures and lower
spires than those from sheltered habitats (e.g.
parisons; night-time, 17 comparisons).
Some authors have reported the heritability Newkirk & Doyle, 1975; Naylor & Begon,
of molluscan shell traits such as size or growth 1982; Crothers, 1992; Gibbs, 1993). Crossrate (Asami, 1994: a review). However, only a transplantation experiments to measure a
few papers have reported the heritability of selectional process on shell shape have proved
shell shape in spite of its great ecological and that these features are adaptive against heavy
evolutionary interest. Boulding & Hay (1993) wave action (e.g. Kitching, Muntz & Ebling,
1966; Janson, 1983). Large body whorls and/or
calculated the heritability of shell shape in
Littorina sp. by half-sibling analysis. According apertures certainly enlarge the area adhering
to them, the heritabilities of the ratios that are to the substratum and low spires reduce resisequivalent for W (whorl expansion rate), T tance of water movement. The process in which
(spire height ratio), and S (aperture shape) are the match between shell shape and current
22 to 32%. The present study estimated that velocity emerges will be discussed later.
the heritability of the parameters of shell shape
During the day, the slopes of log10W and
in S. reiniana was 0%. If one considers the log10T were different between the substratum
95% upper confidence limits, the heritabilities categories, while no regression lines differed
of the parameters are less than 4.6% to 11.4%. among the current velocity classes. The differAlthough the experiment was not repeated and ence of log,0W between substratum categories
the standard errors were large, the heritability may be due to the outliers, but that of log10T
of shell shape seems to be very low. Since the was still significant after their exclusion. These
heritability values resulted from the mother- results may suggest that the difference of shell
offspring regression which overestimates heri- shape between substratum category exists
MISAKO URABE
340
1.7
0-30% y=1.64«10^0071)< r=-0.461"
"°
1.6
30-70% y=1.46*10"° o039* r=-0.334*
70-100% y=1.70»10-°0082* r=-0.544*
1.5
1.4
1.3
CD
CO
1.2
O
if)
D)
O
1.1
1
1
1
1
1
1
s_
CD
CD
E
CO
CO
14
12
0-30% y=1.70»100040x r=0.491"
30-70%y=1.99«100033x r=0.543*"
70-100%y=0.56«100040* r=0.645"*
10
9
8
7
6
+
5
o o
I
8
10
12
I
I
14
16
18
Shell width (mm)
Figure 8. Scatter plots and regression lines of the parameters W and T plotted against SW for each hardbottom utilization ratio for snails in the active period.
SHELL SHAPE VARIATION IN SEMISULCOSPIRA REINIANA
only in young snails; however, it is difficult to
interpret the biological significance from Fig. 5.
As yet, the relationship between shell shape
and environmental condition during the day is
not clear.
The possibility that shell morphology is not
correlated to habitat during the day but to
habitat at night was pointed out by Cain (1977)
in a study of nocturnal land snails. He argued
that land snails with different shell shape
may prefer different modes of locomotion or
surface types (horizontal or vertical) on which
to move. Cain's discussion could be applied to
a lotic environment. Since the environments of
a river bed in small streams change dramatically in a small scale, it is quite probable that
lotic macrobenthos show a diel shift of habitat
depending on their activity (Ohgushi, 1956;
Kovalak, 1976). At the daytime sampling in
1990 at Takahashi, 39% of snails were hiding in
completely sheltered sites such as under stones
or in sediment, and most of the remainder
stayed in the lee of rocks or stones or in
crevices where they could keep out of the fast
current. Thus, at least for current velocity, the
environmental variance of their microhabitats
is smaller in the daytime than at night.
It is important also to consider the nighttime activity of S. reiniana in relation to the
timing of shell growth, because the shell variation is caused mainly by environmental conditions. Since shell material is secreted by glands
in the mantle edge (Stasek & McWilliams,
1973), a shell does not grow when the soft body
of the snail is retracted in the shell. Thus, the
environment can affect shell formation only
when the head-foot of a snail is at least flush
with the aperture so that the mantle edge can
contact the aperture. Consequently, it is only
the environment that a snail experiences when
it is active at night-time that affects shell
formation.
Emergence and maintenance of shell variation
within a population ofS. reiniana
As mentioned above, the difference in shell
shape of S. reiniana between fast and slow
currents in the active period may be adaptive.
However, there are two reasons to think that
the process that makes shell shape correspond
to each microhabitat is not local genetic selection. First, the main source of shell variation in
S. reiniana is not genetic and the shell shape
can be modified by environment. Secondly,
the water current may sort the snails into
corresponding microhabitats rather than cull
341
non-adapted individuals. A transplantation
experiment showed that a fast current did not
lower the survival rate of snails transplanted
from a slow current habitat, but only made
them disperse downstream (Urabe, 1998).
Undisturbed snails on both banks did not have
a tendency to disperse either upstream or
downstream and seemed to stay in their original habitat (Urabe, 1998). This suggests that
snails rarely settle in currents faster than in
their original habitat. For riffle-pool systems
repeating in a natural river bed (Kani, 1944),
snails moving downstream would reach a
similar environment to their original habitat.
Even if snails are dislodged and washed downstream, it may be not fatal for Semisulcospira.
The ability to cling to the substratum as a
defense against predators is not important for
them, because of the scarcity of predators that
attack snails detached from the substratum in
this fluvial habitat, in contrast to a marine
habitat. Although larvae of the firefly Luciola
cruciata are well-known predators of Semisulcospira in Japan, they can attack snails whether
clinging to the substratum or not, by biting
their soft bodies and anaesthetizing them. Also
a freshwater crab Potamon dehani is reported
as a predator of juvenile Semisulcospira (2 mm
in diameter) in streams (Mishima, 1973). Some
species of benthos-feeding cyprinid fish are
reported as predators of young snails in Lake
Biwa (Fishery Institute of Shiga Prefecture,
1941), that may also be potential predators in
streams. However, they occur mainly in lakes,
ponds and large rivers, and are rarely found in
streams. In fact, the tenacity of Semisulcospira
is so weak that they often detach from the
substratum and float downstream even in usual
water levels. One snail detached from the
substratum, on average, 0.75 (n = 69), 0.29
(n = 11) and 0.78 (n = 21) times per observation period in the 0-1 cm/s, 5-10 cm/s and
> 10 cm/s classes of water current, respectively.
Thus, the downstream floating of Semisulcospira could be interpreted rather as a
normal way of dispersal than as a forced move
detrimental to their survival. This process may
tend to allocate each snail to an appropriate
microhabitat and thus promote the shell variation observed between microhabitats.
Phenotypic modulation by the environment
may cause a large amount of shell variation
in many gastropod species, taking account
of both a high plasticity in shell formation
(Gibbs, 1993) and environmental heterogeneity. In addition, the shell variation among
microhabitats would be maintained even
342
MISAKO URABE
& J. Peake, eds), 2A: 219-270. Academic Press,
within a population through restricted disperNew York.
sal without local genetic selection. In further
studies, more stress should be placed on the CROTHERS, J.H. 1992. A re-evaluation of shell variation in Shetland dog-whelks, Nucella lapillus (L.)
process suggested here as a mechanism which
and their use as biological exposure indicates.
maintains the variation between shells from
Journal of Molluscan Studies, 58: 315-328.
different microhabitats without the selection of DAVIS, G.M. 1968. Biosystematic analysis of Semigenetic variation.
sulcospira trachea (Gastropoda: Pleuroceridae).
ACKNOWLEDGMENTS
I am very grateful to all members of the Laboratory
of Animal Ecology, Kyoto University, especially to
Ms. J.C.W. Chang, Drs. T. Inoue, K. Iwasaki and K.
Nakata, Mr. T. Wada, Dr. T. Yamamoto and Ms. K.
Yoshida for their help which made my field work
possible. I thank Professors T. Abe and M. Hori and
Dr. M. Yuma, Kyoto University, Professor N.C.
Watanabe, Kagawa University, Dr. T. Kondo, Osaka
University of Education, and Dr. J.M.C. Hutchinson,
Bristol University, for their valuable advice and
comments on the earlier draft. Professor T. Shotake,
Drs. Y. Kawamoto and H. Hirai, Primate Research
Institute, Kyoto University, kindly supported my
electrophoretic study to identify the species. I thank
also the staff of the Laboratory of Animal Physiology
and Ecology, Nara Womens' University, for daily
help and support.
Proceedings of the Symposium on Mollusca, 1:
16-35. Marine Biological Association of India,
Bangalore Press.
DAVIS, G.M. 1969. A taxonomic study of some
species of Semisulcospira in Japan (Mesogastropoda: Pleuroceridae). Malacologia, 7: 211-294.
DAVIS, G.M. 1972. Geographic variation in Semisulcospira libertina (Mesogastropoda: Pleuroceridae).
Proceedings of the Malacological Society of
London, 40: 5-32.
DAZO, B.C. 1965. The morphology and natural
history of Pleurocera acuta and Goniobasis
livescens (Gastropoda: Cerithiacea: Pleuroceridae). Malacologia, 3:1-80.
DILLON, R.T. 1984. Geographic distance, environmental difference, and divergence between
isolated populations. Systematic Zoology, 33:
69-82.
DILLON, R.T. & DAVIS, G.M. 1980. The Goniobasis
of southern Virginia and northwestern North
Carolina: Genetic and shell morphometric relationships. Malacologia, 20: 83-98.
FALCONER, D.S. 1989. Introduction to quantitative
genetics. 3rd ed. Longman, New York.
FISHERY INSTITUTE OF SHIGA PREFECTURE, 1941.
Report of natural food offishesin Lake Biwa. 80
pp. (In Japanese)
GOODRICH, C. 1945. Goniobasis livescens of MichiADAM, C.C. 1915. The variations and ecological disgan. Miscellaneous Publications Museum of
tribution of the snails of the genus lo. National
Zoology, 64:1-36. University of Michigan.
Academy of the Sciences of Washington, 2nd
Memoir, 12: 1-185.
GIBBS, P.E. 1993. Phenotypic changes in the progeny
of Nucella lapillus (Gastropoda) transplanted from
APPLETON, R.D. & PALMER, A.R. 1988. Water-borne
an exposed shore to sheltered inlets. Journal of
stimuli released by predatory crabs and damaged
Molluscan Studies, 59:187-194.
prey induce more predator-resistant shells in a
marine gastropod. Proceedings of the National
HUTCHINSON, G.E. 1993. Gastropod molluscs. In: A
Academy of Sciences of the United States of Amertreatise on limnology FV. The zoobenthos, Ml-215.
ica, 85:4387-4391.
John Wiley & Sons, New York.
JANSON, K. 1983. Selection and migration in two
ASAMI, T. 1994. Genetics of Mollusca. In: Handbook
distinct phenotypes of Littorina saxatilis in
of malacology (T. Habe, T. Okutani & S. NishiSweden. Oecologia, 59: 58-61.
waki, eds), 1: 177-215. Scientist Inc., Tokyo. (In
Japanese)
KANI, T. 1944. Keiryu-sei konchu no seitai (Ecology
of aquatic insects). In: Nihon-seibutsushi, The
BOULDING, E.G. & HAY, T.K. 1993. Quantitative
insects (H. Hurukawa, ed.), 1:171-317. Kenkyusya,
genetics of shell form of an intertidal snail:
Tokyo. (In Japanese)
constraints on short-term response to selection.
Evolution, 47:576-592.
KITCHING, J.A., MUNTZ, L. & EBLING, FJ. 1966. the
ecology of Lough Ine. XV. The ecological signifiCAIN, A. 1977. Variation in the spire index of some
cance of shell and body forms in Nucella. Journal
coiled gastropod shells, and its evolutionary signifiof Animal Ecology, 35: 113-126.
cance. Philosophical Transactions of the Royal
Society of London. B 277: 377-428.
KOVALAK, W.P. 1976. Seasonal and diel changes
in the positioning of Glossosoma nigrior Banks
CHAMBERS, S.M. 1982. Chromosomal evidence for
(Trichoptera: Glossosomidae) on artificial subparallel evolution of shell sculpture pattern in
strates. Canadian Journal of Zoology, 54: 1585Goniobasis. Evolution, 36:113-120.
1594.
CLARKE, B., ARTHUR, W., HORSLEY, D.T. & PARKIN,
D.T. 1978. Genetic variation and natural selection
KURODA, T. 1929. On Japanese Melanians. Venus, 1:
in pulmonate molluscs. In: Pulmonates (V. Fretter
179-193. (In Japanese)
REFERENCES
SHELL SHAPE VARIATION IN SEMISULCOSPIRA REINIANA
MISHIMA, Y. 1973. Production estimation of a freshwater snail, Semtsulcospira bensoni (Phillipi)
(Mollusca: Gastropoda) in a rapid stream. Report
from the Ebino Biological Laboratory, Kyushu
University, 1: 49-63.
343
SHINAGAWA, K. 1995. Effects of trematodes infection
on distribution of Semisulcospira libertina. Unpublished graduation thesis, Nara Womens' University, Nara. (In Japanese)
SMITH-GILL, SJ. 1983. Developmental plasticity:
NAYLOR, R. & BEGON, M. 1982. Variation within and
Developmental Conversion versus phenotypic
between populations of Littorina nigrolineata Gray
modulation. American Zoologist, 23: 47-55.
on Holy Island, Anglesey. Journal de Conchyliolo- SOKAL, R.R. & ROHLF, FJ. 1981. Biometry. 2nd ed.
gie, 31:17-30.
W.H. Freeman and Company, San Francisco and
NEWKIRK, G.F. & DOYLE, R.W. 1975. Genetic analyLondon.
sis of shell-shape variation in Littorina saxatilis STASEK, C.R. & MCWILLIAMS, W.R. 1973. The
on an environmental cline. Marine Biology, 30:
comparative morphology and evolution of the
227-237.
molluscan mantle edge. Veliger, 16:1-19.
OHGUSHI, R. 1956. Daily rhythmic activities of
URABE, M. 1992. A discrimination and morphoaquatic insects in a mountain stream. The Insect
logical comparison of two snail species of the
Ecology, 5:12-17. (In Japanese)
genus Semisulcospira in a single river. Venus, 50:
270-286. (In Japanese, with English abstract)
PALMER, A.R. 1985. Quantum changes in gastropod
shell morphology need not reflect speciation.
URABE, M. 1998. Diel change of activity and moveEvolution, 39: 699-705.
ment on natural nver beds in Semisulcospira reiniana. Venus, 57: 17-27.
PALMER, A.R. 1990. Effect of crab effluent and scent
of damaged conspecifics on feeding, growth, and
VAN VALEN, L. 1978. The statistics of variation.
shell morphology of the Atlantic dog whelk
Evolutionary Theory, 4: 33-43.
Nucella lapUlus (L.). Hydrobiologia, 193:155-182. WATANABE, C.N. 1981. A comparative study of the
RAUP, D.M. 1966. Geometric analysis of shell coiling:
life history characteristics of two Melanian snails,
general problems. Journal of Paleontology, 40:
Semisulcospira dectpiens and 5. reticulata in Lake
1178-1190.
Biwa. Physiological Ecology Japan, 18: 7-38.