BULLETIN OF MARINE SCIENCE, 68(1): 27–36, 2001
GROWTH OF THE INTERTIDAL SNAIL, MONODONTA LABIO
(GASTROPODA, PROSOBRANCHIA) ON THE PACIFIC COAST
OF CENTRAL JAPAN
Akiko Iijima
ABSTRACT
Growth of the trochid snail Monodonta labio was investigated by individual marking
on a Pacific coast rocky shore of Honshu, central Japan. Growth rates of small sized M.
labio were greater during summer to fall than during winter. However, the growth of large
sized M. labio did not fluctuate all year round. Estimated growth curves were gained
from growth data of monthly recaptured M. labio. From the estimated growth curves it
was showed that newly recruited M. labio (1.6 mm in shell height) grew 10.3 mm at 1 yr
after recruitment, 16.7 mm after 2 yrs, 20.2 mm after 3 yrs, 22.6 mm after 4 yrs, 24.4 mm
after 5 yrs and reached the maximum size at the study shore of 25.0 mm after 5 yrs 2 mo.
Monodonta labio is a common trochid snail which inhabits rocky-boulder or boulder
shores of Japan, Korea and the southern part of China. Growth of M. labio have been
studied in Hakata (Sumikawa, 1955) and in Shima Peninsula (Nakano and Nagoshi, 1981,
1984) in Japan (Fig. 1) by using cohort analysis. Although cohort analysis is a convenient
method to study about growth, overlap of different cohorts in frequency histograms make
it difficult to monitor the growth of each cohort especially in the older age classes (Nakaoka,
1992). Furthermore, growth of each individual can not be followed by this method. The
mark-recapture method is reliable to estimate molluscan growth (Hughes and Roberts,
1980; Phillips, 1981; Wada et al., 1983; Fletcher, 1984; Chow, 1987; Katoh, 1989; Bowling, 1994). Takada (1995) shows the growth pattern of M. labio by mark-recapture at a
boulder shore in Amakusa (Fig. 1), but variation of the growth rate among individuals
was not clear in this study because the recapture rates were low (highest is 4.3% during 2
mo). In contrast, recapture rates of M. labio in Kominato (Fig. 1) were high (12.0–67.4 %
during 1 mo)(Iijima and Furota, 1996). In the present study, I analyzed the growth rate of
individuals of M. labio by the mark-recapture method in Kominato and (1) growth curve
of this species is proposed and compared with previous results, and (2) the variation of
individual growth is analyzed.
METHODS
The monitoring of M. labio growth was conducted on a rocky-boulder shore at Uchiura Cove,
Kominato, Boso Peninsula, central Honshu (35o7'N, 140o10'E) from April 1990 to April 1991. The
study area was protected from human disturbances such as fishing and harvesting of shellfish. The
shore is comprised of a mosaic distribution of bed-rock and boulder areas (Fig. 1).
MARKING METHOD.—Individuals for marking were collected using four quadrats (50 cm × 50 cm)
in the boulder area and the bed-rock (7 m2): All individuals with shell height (SH) larger than 4.0
mm were captured monthly during the spring low tide, marked with three or four colored dots on
the outer lip of the shell using paint-markers (Mitsubishi Pencil Co.) to identify individual specimens. The colored dots were then coated with instant glue to preserve the marking (Takada, 1995).
Then, their SH were measured to nearest 0.1 mm with hand calipers and they were released at the
site of collection.
27
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Figure 1. Location of study sites used for determining growth of Monodonta labio and the present
study shore. Straight lines indicate a concrete dike. Arrows show the first release areas.
IIJIMA: GROWTH OF MONODONTA LABIO
29
Table 1. Parameters of regression (µ = a × mx) and coefficient of determination (r), calculated
from the shell height at recapture (see text for the formula). Maximum and minimum shell height
at recapture are listed.
No. of snails
1990 Apr.−May
May−June
June−July
July−Aug.
Aug.−Sep.
Sep.−Oct.
Oct.−Nov.
Nov.−Dec.
Dec.−Jan.
1991 Jan.−Feb.
Feb.−Mar.
Mar.−Apr.
Released Recaptured
181
54
1,020
377
1,186
232
780
141
733
88
594
159
805
313
368
248
832
173
205
83
675
337
845
397
Recapture
rate (%)
r
a (SE)
m (SE)
29.8
37.0
19.6
18.1
12.0
26.8
38.9
67.4
20.8
40.5
49.9
47.0
0.725
0.640
0.705
0.752
0.640
0.662
0.339
0.620
0.534
0.090
0.380
0.326
0.433 (0.086)
0.597 (0.058)
1.036 (0.089)
1.839 (0.135)
0.827 (0.185)
1.034 (0.136)
0.558 (0.162)
0.720 (0.109)
0.434 (0.103)
0.281 (0.441)
0.241 (0.099)
0.213 (0.107)
0.862 (0.013)
0.833 (0.007)
0.784 (0.010)
0.734 (0.015)
0.799 (0.018)
0.779 (0.014)
0.810 (0.017)
0.819 (0.010)
0.845 (0.012)
0.873 (0.048)
0.863 (0.010)
0.849 (0.012)
Size range
(mm)
Min. Max.
4.8 17.2
5.0 21.9
5.0 20.7
5.6 18.9
6.8 20.5
5.4 15.9
5.1 18.5
6.0 21.6
4.6 16.8
7.1 15.8
4.2 20.0
4.2 18.2
Recapture and Growth Measurements.—The area depicted in Figure 1 was surveyed thoroughly
twice a month during April to October, 1990 and once a month during November, 1990 to April,
1991, in spring low tide and marked individuals were recovered. The SHs were measured as above
and then individuals were released at the site where they were recaptured.
Individual growth rates (µ) of the recaptured snails were estimated using the equation
µ = ∆X X ⋅ (30 T ) ,
where T is the time (d) from the last release to recapture, X the SH at the last release, ∆X the
increment in SH during the period T.
RESULTS AND DISCUSSION
The number of recaptured snails after 1 mo at liberty ranged from 54 to 397 and the
recapture/release ratio ranged 12.0 to 67.4% (Table 1). Individual growth rates are plotted
against SH at release for May–June, July–August, September–October and December–
January samples (Fig. 2). Trends are apparent that smaller snails showed higher growth
rates than larger individuals. In order to assess seasonal change in growth rates, the snails
were grouped into six size groups and mean growth rates for each category were plotted
against time (Fig. 3). Growth rates for smaller individuals less than 9.9 mm in SH showed
seasonal changes with higher values in the summer. However, seasonal trends for large
snails more than 10.0 mm in SH were not apparent. M. labio more than 10.0 mm matured
and reproduced during early summer to autumn in Kominato (Iijima, in prep.). Matured
M. labio may allocate energy to reproduction during summer, breeding season, instead of
shell growth (Wright and Hartnoll, 1981; Stoeckmann and Garton, 1997).
Individual growth rates varied greatly even in a fixed size category and period (Fig. 2,
Table 2). SD values of the growth rate showed tendencies that high values were observed
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BULLETIN OF MARINE SCIENCE, VOL. 68, NO. 1, 2001
Figure 2. Relationships between the released size and the growth rate of marked Monodonta labio.
Figure 3. Seasonal change of mean growth rates of marked Monodonta labio classified into 6 size
groups: ● 4.0–5.9 mm; 앪 6.0–7.9 mm; ▲ 8.0–9.9 mm; 왕 10.0–11.9 mm; ■ 12.0–13.9 mm; 14.0–
15.9 mm. Individuals more than 16.0 mm were omitted because of small numbers sampled (n < 10).
IIJIMA: GROWTH OF MONODONTA LABIO
31
Table 2. Variation of growth rates of marked Monodonta labio which were divided into size
classes by size in release.
Size at release
(mm)
May−June
July−Aug
Sep−Oct
Dec−Jan
Mean
SD
SD/Mean
Min.
Max.
n
126
4.0−5.9
0.254
0.088
0.347
0.067
0.675
6.0−7.9
0.184
0.056
0.304
0.059
0.378
14
8.0−9.9
0.124
0.041
0.330
0.000
0.198
32
10.0−11.9
0.092
0.024
0.257
0.041
0.123
24
12.0−13.9
0.067
0.025
0.369
0.022
0.101
20
14.0−15.9
0.042
0.023
0.538
0.007
0.081
13
16.0−17.9
0.031
0.012
0.370
0.018
0.060
11
4.0−5.9
0.311
0.066
0.212
0.172
0.456
16
6.0−7.9
0.222
0.061
0.274
0.109
0.373
53
8.0−9.9
0.140
0.040
0.283
0.064
0.214
37
10.0−11.9
0.060
0.027
0.451
0.011
0.113
21
29
4.0−5.9
0.331
0.073
0.219
0.190
0.452
6.0−7.9
0.194
0.032
0.165
0.121
0.233
16
8.0−9.9
0.114
0.036
0.316
0.029
0.211
52
10.0−11.9
0.074
0.039
0.529
0.000
0.225
43
12.0−13.9
0.047
0.020
0.421
0.016
0.083
13
4.0−5.9
0.172
0.055
0.318
0.118
0.327
13
6.0−7.9
0.131
0.030
0.226
0.053
0.201
80
8.0−9.9
0.107
0.019
0.179
0.067
0.154
53
10.0−11.9
0.077
0.010
0.123
0.065
0.097
11
12.0−13.9
0.063
0.011
0.170
0.046
0.084
12
in the small size class, 4.0–5.9 mm, and in warm seasons. However, trends for SD/average were not apparent.
In order to clarify whether the variation of growth rate was due to inheritance, correlation between growth rate of each individual in one period and that of the same individual
in the following period was examined. For calculation, growth rates of individuals recaptured on three consecutive sampling times were used. Figure 4 shows typical trends. All
results are shown in Table 3 and the correlation was not significant (α = 0.05) except for
6.0–7.9 mm and 8.0–9.9 mm individuals during 18 October to 1 December. This indicates that individuals that showed a high growth rate in one period did not always grow
rapidly during the following period. This tendency suggests that the factor that controlled
individual growth rate was not a genetic character, though there are no explanation why
two exceptions were there.
Since small individuals with SH of 4.0–5.0 mm were abundant at the start of the experiment (April, 1990), growth of these individuals was simulated as follows: First, growth
rate at period i (µi) as a function of SH (x) was approximated by :
µ i = a ⋅ miX ,
Eq. 1
BULLETIN OF MARINE SCIENCE, VOL. 68, NO. 1, 2001
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Figure 4. Comparison of growth rates between the first recapture (X axis) and the next recapture (Y
axis) of Monodonta labio. Release date was 9 May, the first recapture date was 23 May and the next
recapture was 10 June.
where a and m are fitting parameters and are summarized in Table 1. Second, SH at period
i+1 (xi+1) was calculated from µi and xi:
x i +1 = x i ⋅ (1 + µ i ).
Eq. 2
Using the initial condition of SH = 4.5 mm in April and calculating the SH in the next
month stepwise, growth curve was calculated (Fig. 5) until x reached to 25.0 mm, the
maximum size collected in the study site.
The size class including 4.5 mm in April 1990 originated from the newly recruited
cohort (mean SH is 1.6 mm, SD is 0.79 mm) in September, 1989 (Iijima and Furota,
1996). The estimated growth curve (Fig. 5) shows rapid growth in the first year. SH was
10.3 mm at after 1 yr, 16.7 mm after 2 yrs, 20.2 mm after 3 yrs, 22.6 mm after 4 yrs, 24.4
mm after 5 yrs and reached the maximum size at the study shore of 25.0 mm after 5 yrs 2
mo from recruitment in the study site.
IIJIMA: GROWTH OF MONODONTA LABIO
33
Table 3. Correlation between growth rate of each individual in one period and that of the same individual
in the following period. Size groups which have large number of individuals (n > 10) were used for
calculation. The first date shows date of release, the second and third show dates of recapture.
Date
Size at
release (mm)
4.0−5.9
1990 Apr. 12, Apr. 25, May 9
6.0−7.9
May 9, May 23, June 10
June 21, July 8, July 22
July 22, Aug. 5, Aug. 17
Sep. 17, Oct. 5, Oct. 18
Oct. 18, Nov. 2, Dec. 1
Dec. 1, 1991 Jan. 13, Feb. 19
Jan. 13, Feb. 19, Mar. 13
Feb. 19, Mar. 13, Apr. 2
r
n
tcal
−0.2301
36
−1.3787
n.s.
−0.3704
26
−1.9536
n.s.
4.0−5.9
0.0768
54
0.5551
n.s.
6.0−7.9
0.0085
62
0.0662
n.s.
4.0−5.9
0.3684
17
1.5348
n.s.
6.0−7.9
−0.2715
28
−1.4383
n.s.
8.0−9.9
−0.3146
14
−1.1481
n.s.
6.0−7.9
−0.3325
11
−1.0575
n.s.
8.0−9.9
−0.0209
16
−0.0780
n.s.
10.0−11.9
0.1347
11
0.4077
n.s.
4.0−5.9
−0.0669
18
−0.2681
6.0−7.9
0.4044
48
8.0−9.9
0.5579
14
10.0−11.9
−0.3410
24
−1.7014
n.s.
6.0−7.9
−0.0853
43
0.5479
n.s.
8.0−9.9
0.2338
20
1.0202
n.s.
6.0−7.9
−0.0582
15
−0.2103
n.s.
8.0−9.9
−0.3299
25
−1.6759
n.s.
4.0−5.9
−0.1065
45
−0.7025
n.s.
6.0−7.9
−0.1080
28
−0.5541
n.s.
8.0−9.9
−0.0102
57
−0.0759
n.s.
10.0−11.9
−0.1761
32
−0.9799
n.s.
12.0−13.9
0.3047
10
0.9048
n.s.
n.s.
2.9985 t46(0.005)<tcal<t46(0.002)
2.3285 t12(0.05)<tcal<t12(0.02)
In Hakata Bay (Fig. 1), M. labio grew to 9 to 11.9 mm at after 1 yr from newly recruitment (Sumikawa, 1955). In Shima Peninsula, newly recruited snails grew to 7.9 to 10.0
mm in the first year and 15.0 to 17.3 mm in the second year (Nakano and Nagoshi, 1984).
These growth rates are similar to the present results for Kominato, in spite of the difference in methodology, cohort analysis and mark-recapture. On the other hand, at Amakusa,
the growth rate in the first year was similar to the other studies (10 mm in shell width),
but in the second year the growth rate seemed to be lower than in other studies (reaching
13.0 to about 14.5 mm in shell width) (Takada, 1995). Shell width is almost equivalent to
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BULLETIN OF MARINE SCIENCE, VOL. 68, NO. 1, 2001
Fig. 5. Estimated growth curve of Monodonta labio.
shell height in M. labio (Nakano and Nagoshi, 1984). Furthermore, the maximum size of
M. labio is smaller (17 mm) in Amakusa than in the other study sites (more than 20 mm in
Shima Peninsula and 25 mm in SH in Kominato). Takada (1995) suggested the possibility
that growth rates of M. labio varied between localities due to environmental factors, such
as food resources. However, the abundance of epilithic micoroalgae, food of M. labio in
Amakusa (1–40 mg Chla m−2), was comparable with that in Kominato (3.5–15.6 mg Chla
m−2, Iijima, in prep.). Since population density of M. labio in Amakusa (37–175 m−2) was
comparable to that in Kominato (17.3–522 m−2, Iijima and Furota, 1996), overpopulation is
considered not to be responsible for the lower growth rates in Amakusa in contrast to many
other growth rate variations recorded in intertidal gastropods (Haven, 1973; Black, 1977;
Underwood, 1978; Williamson and Kendall, 1981). The cause of the difference in the growth
rate is still uncertain. One explanation about the small size of M. labio in Amakusa is the
harvesting pressure by humans. M. labio is an edible snail, and people collect the snail to
eat and to sell in Amakusa (Takada, pers. comm.), although they are not eaten it in Shima
Peninsula (Nakano, pers. comm.) and Kominato due to differences in customs. In Amakusa,
growth rate might possibly be slow on the surface because the selective collection of large
M. labio by human.
Longevity of M. labio was assumed to be 2.5–3.0 yrs in Hakata Bay (Sumikawa, 1955)
and 3 yrs in Shima Peninsula (Nakano and Nagoshi, 1981, 1984). Based on the estimated
growth curve (Fig. 5), over 5 yrs is required for M. labio to reach the maximum size in
Kominato. The technique used in other studies to estimate longevity of M. labio was
cohort analysis. Since this method is prone to underestimate the longevity due to the
overlapping of older cohorts (Nakaoka, 1992), the difference observed was probably due
to the difference in the method used.
IIJIMA: GROWTH OF MONODONTA LABIO
35
ACKNOWLEDGEMENTS
I would like to express my appreciation to the staff of the Marine Biosystems Research Center of
Chiba University for granting permission to conduct this study. The valuable comments of M.
Okada and T. Furota are greatly appreciated. I thank Y. Takada for technical assistance in the marking experiments, and H. Kato for his assistance with the computer programming for this study. T.
Sunobe, Y. Nakamura and G. Ohi kindly revised the manuscript. I also thank students of Toho
University who helped with the field sampling.
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DATE SUBMITTED: September 9, 1999.
DATE ACCEPTED: May 12, 2000.
ADDRESS: Marine Biology Laboratory, Department of Biology, Faculty of Science, Toho University,
Miyama 2-2-1, Funabashi, Chiba, 274-8510 Japan. E-mail: <[email protected]>.