BULLETIN OF MARINE SCIENCE, 68(1): 27–36, 2001

GROWTH OF THE INTERTIDAL SNAIL, LABIO (, PROSOBRANCHIA) ON THE PACIFIC COAST OF CENTRAL JAPAN

Akiko Iijima

ABSTRACT Growth of the trochid snail 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; Bowl- ing, 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 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 speci- mens. 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 28 BULLETIN OF MARINE SCIENCE, VOL. 68, NO. 1, 2001

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.

Neo. of snails Recaptur r)a)(SE me(SE Size rang rate (%) (mm) Rdeleased R.ecapture M.in Max 1.990 Apr −M1ay 148 58259. 0).72 0).433 (0.086 08.862 (0.013 42. 17. May−J1,0une 072 307 307. 0).64 0).597 (0.058 00.833 (0.007 59. 21. June−J1,6uly 128 263 159. 0).70 1).036 (0.089 00.784 (0.010 57. 20. July−A0ug. 718 114 128. 0).75 1).839 (0.135 06.734 (0.015 59. 18. Aug.−S3ep. 783 80102. 0).64 0).827 (0.185 08.799 (0.018 65. 20. Sep.−O4ct. 599 185 226. 0).66 1).034 (0.136 04.779 (0.014 59. 15. Oct.−N5ov. 830 391 398. 0).33 0).558 (0.162 01.810 (0.017 55. 18. Nov.−D8ec. 386 244 607. 0).62 0).720 (0.109 00.819 (0.010 66. 21. Dec.−J2an. 833 187 240. 0).53 0).434 (0.103 06.845 (0.012 48. 16. 1.991 Jan −F5eb. 230 85400. 0).09 0).281 (0.441 01.873 (0.048 78. 15. Feb.−M5ar. 677 393 409. 0).38 0).241 (0.099 02.863 (0.010 40. 20. Mar.−A5pr. 874 309 467. 0).32 0).213 (0.107 02.849 (0.012 42. 18.

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=∆XX⋅()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 30 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; Ț 6.0–7.9 mm; ▲ 8.0–9.9 mm; ̅ 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 MDean SnS.D/Mea M.in Mnax (mm) May−June 44.0−5.9 08.25 07.08 07.34 05.06 06.67 12 64.0−7.9 06.18 04.05 09.30 08.05 04.37 1 84.0−9.9 01.12 00.04 00.33 08.00 02.19 3 120.0−11.9 04.09 07.02 01.25 03.04 04.12 2 172.0−13.9 05.06 09.02 02.36 01.02 00.10 2 124.0−15.9 03.04 08.02 07.53 01.00 03.08 1 116.0−17.9 02.03 00.01 08.37 00.01 01.06 1 July−Aug 41.0−5.9 06.31 02.06 02.21 06.17 06.45 1 62.0−7.9 01.22 04.06 09.27 03.10 03.37 5 80.0−9.9 00.14 03.04 04.28 04.06 07.21 3 100.0−11.9 07.06 01.02 01.45 03.01 01.11 2 Sep−Oct 41.0−5.9 03.33 09.07 00.21 02.19 09.45 2 64.0−7.9 02.19 05.03 01.16 03.12 06.23 1 84.0−9.9 06.11 06.03 09.31 01.02 02.21 5 140.0−11.9 09.07 09.03 00.52 05.00 03.22 4 172.0−13.9 00.04 01.02 06.42 03.01 03.08 1 Dec−Jan 42.0−5.9 05.17 08.05 08.31 07.11 03.32 1 61.0−7.9 00.13 06.03 03.22 01.05 00.20 8 87.0−9.9 09.10 09.01 07.17 04.06 03.15 5 170.0−11.9 00.07 03.01 05.12 07.06 01.09 1 132.0−13.9 01.06 00.01 06.17 04.04 02.08 1

in the small size class, 4.0–5.9 mm, and in warm seasons. However, trends for SD/aver- age were not apparent. In order to clarify whether the variation of growth rate was due to inheritance, correla- tion 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 recap- tured 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 indi- cates 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 experi- ment (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 :

am , µi = ⋅ iX Eq. 1 32 BULLETIN OF MARINE SCIENCE, VOL. 68, NO. 1, 2001

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:

xxii+1 = ⋅()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.

Dtate Size a rntcal release (mm) 1990 Apr. 12, Apr. 25, May 9 41.0−5.9 −0.230 376 −1.378 n.s. 64.0−7.9 −0.370 266 −1.953 n.s.

May 9, May 23, June 10 48.0−5.9 04.076 510.555 n.s. 65.0−7.9 02.008 620.066 n.s.

June 21, July 8, July 22 44.0−5.9 07.368 181.534 n.s. 65.0−7.9 −0.271 238 −1.438 n.s. 86.0−9.9 −0.314 114 −1.148 n.s.

July 22, Aug. 5, Aug. 17 65.0−7.9 −0.332 151 −1.057 n.s.

Sep. 17, Oct. 5, Oct. 18 89.0−9.9 −0.020 106 −0.078 n.s. 170.0−11.9 01.134 170.407 n.s.

Oct. 18, Nov. 2, Dec. 1 49.0−5.9 −0.066 118 −0.268 n.s. 64.0−7.9 08.404 452.998 t46(0.005)

Dec. 1, 1991 Jan. 13, Feb. 19 6..0−7.9 −0 03853 490.547 n.s. 88.0−9.9 00.233 221.020 n.s.

Jan. 13, Feb. 19, Mar. 13 62.0−7.9 −0.058 15 −0.2103 n.s. 89.0−9.9 −0.329 295 −1.675 n.s.

Feb. 19, Mar. 13, Apr. 2 4..0−5.9 −0 15065 4.−0 7025 n.s. 6.0−7.9 −00.128108 −0.554 n.s. 82.0−9.9 −0.010 597 −0.075 n.s. 1.0.0−11.9 −0 12761 3 −0.9799 n.s. 172.0−13.9 00.304 180.904 n.s.

In Hakata Bay (Fig. 1), M. labio grew to 9 to 11.9 mm at after 1 yr from newly recruit- ment (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 differ- ence 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 34 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 mark- ing 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: .