Reproductive behavior of the dioecious tidal snail Cerithidea rhizophorarum (Gastropoda: Potamididae)*

2007·2.7 MB·English

by  Maya Takeuchi

Amer. Maine. Bull. 23: 81-87
Reproductive behavior of the dioecious tidal snail Cerithidea rhizophorarum
(Gastropoda: Potamididae)’^
Maya Takeuchi, Harumi Ohtaki, and Kiyonori Tomiyama
Department ofEarth and Environmental Sciences, Faculty ofScience, Kagoshima University, Korimoto, Kagoshima, 890-0065, lapan,
[email protected]
Abstract: The dioecious snail Cerithidea rhizophorarum (Adams, 1855) is distributed along the coasts of the western Pacific up to the
Tohoku district, northern Honshu, Japan. It inhabits reed grasslandsand mangrove forestswith Kaudelia candeland Hibiscus hauiaho trees
onamudflatlocatedatthemouth ofAtagogawaRiverin Kiire. Studiesofmatingand treeclimbingbehaviorsofthespecieswereconducted
atthissitefrom April 2000toMay2003. Matingbehaviorwasobservedin InlyandAugust 2002. Thetimeofcommencement, termination,
and duration were recorded foreach copulation. The peakofmatings duringdaytimewas seen at 1 to 2, and 5 hoursbeforethelowest tide
and during nighttime, between 1 hour before and after lowest tide. However, mating rarely occurred on cloudy days. Climbing behavior
was observed in an area of 100 square meters where only K. candel trees existed. The number ot snails on trees was counted, and daily
activityofthesnailson treeswas monitored in summerand winter, hourlythroughouttheday. Thesnailsweremainlyfound on mud from
spring to summer but frequently climbed up the tree at particular times during summer. Most individuals were on trees and motionless
during winter.
Key words: reproduction, dioecious snail, climbing behavior, gastropod
Molluscs have two types ofmating systems: dioecy and mating behavior of C. rhizophorarum were examined in the
hermaphroditism (simultaneous hermaphrodite, protandric field including duration of copulation both in daytime and
hermaphrodite, and protogynous hermaphrodite). These di- nighttime.
vergent patterns of mating systems are found even in the
same taxonomic classes. Bisexual reproduction is common MATERIALS AND METHODS
in molluscs, and the pattern offertilization in most classes is
internal, but external fertilization is found in some classes. Study site
Hermaphroditic species can be divided into ones that can The tidal flat is at the mouth ofAtagogawa River flow-
self-fertilize and ones that cannot. Hence molluscs have ing through Kiire-Cho, Kagoshima-city. This river is located
many divergences in the reproduction pattern and may be by the Nisseki oil camp, and it joins Yahata River in this
the phylum with the most variable reproductive patterns in point. A small mangrove forest consisting ofKaudelia candel
the animal kingdom. How could such various reproductive and Hibiscus hamabo, at the northern limit of mangrove
strategies evolve? distribution in the West Pacific, covers this tidal flat. Some
Thereare manyreports ofmatingbehavior in hermaph- speciesofgastropod, such as Cerithideopsilla djadjariensis (K.
rodites such as Pulmonata and Opisthobranchia, but it is Martin, 1899), Cerithideopsilla cingulata (Gmelin, 1791), Ba-
rarely reported in dioecious Prosobranchia. A clearer under- tillaria multiformis (Lischke, 1869), Batillaria cumiugi
standing ofthe mating behavior ofthis group would be one (Crosse, 1862), Clypeomorus coraliuui (Kiener, 1834), Reti-
of the keys to solve the evolution of various reproductive cimassa festiva (Powy, 1833), Clithou oualauieusis (Lesson,
strategies in molluscs. 1831), and Clithou faba (Sowerby, 1836) inhabit the tidal
The dioecious prosobranch snail Cerithidea rhizophora- flat. We established three studysites (A, B, C) 60 m from the
rum (Adams, 1855) commonly inhabits tidal flats in eastern shore of Atagogawa River.
Asia. In the tidal flat of the Atagogawa River, Kiire-Cho,
Kagoshima, matingbyshell mountingwas observed (Ohtaki Size distribution
et al. 2001). Ohtaki et al. (2001) also reported mating be- We collected 100 Cerithidea rhizophorarum with a net
mm
havior, but itwas incomplete. In thisstudy, several aspectsof (1 mesh) at random at the three stations (A, B, C) and
* From the symposium “Gastropod Mating Systems” presented at the joint meeting ofthe American Malacological Society and Western
Society ofMalacologists, held 26-30 June 2005 at Asilomar, Pacific Grove, California.
81
AMERICAN MALACOLOGICAL BULLETIN 23 • 1/2 • 2007
18000 ^ Figure 1. Seasonal change at each
60 N=95 N=57 -]N=149 station in the width-frequency distri-
40 JTL k
20 ^-iTL bution in Cerithidea rhizophomrum.
0 . .
fOO
80 N=ni N=55 N=108
60
40
20 —rTh-.- r-ffh
0 .
100 N=105
80 N=125 N=107
60
40
20 jiTu_ x4i ru rfK
0
100
80 N=100 N=111 N=113
60
40 JTTL n
20 ^^-TTh-i
0
100
80 N=102 N=100 =170
60 ^
40
20 rfTL .n
0 f~'l I I
100
80 N=103 N=104 N=136
60
40
20 -rm-1 Ek_
0
100
80 N=103 N=103 N=118
60
40
20 -rfh-
0 r"'i * ^ '
too N=108
80 N=105 N=108
60
40
jiTu
20
0
100
so N=101 N=109 N= 149
GO
2400 -tITl JILl =
0
100
80 N=103 N= 121 N= 102
60
40
20 -rfh.
0
100
80 N=106 N=103 N=118
60
40
20 .jilL — tTIb
0 ^ I 1 1
100
3 BO N=99 N=99 N^IOS
2 60
3 40
' 200 —twMcH l*r~l.
;0 5 7 9 II 13 15 S3 6 7 9 II 13 15 S3 5 7 9 II 13 15
Shellwidtli(mm)
StationA StationB StationC
—
REPRODUCTIVE BEHAVIOR OF CERITHIDEA 83
2001 18000 p• N=126 Figure 1. (continued)
60 • N= 100 N=101
Apr. 40 •
20 • jfTU
0
100
60 N=114 N= 115
May 60
40
N=109
Jun.
-.-.-rrrhi-.
N=100 N=100 N=127
Jul.
rru^
-T~i 1 I I' I I 1—
N=100 N=100 N=100
Aug.
jiTI
.
N=100 N=103 N= 145
Sep.
rfh.^
i-rTh-h^
100 P
80 • N=163 N=109
60
Oct. 40 •
20 • -x-TU,
0 I
100 -
80 1* N=101 N=115
60
Nov. 40
20 TT-l —
0 1__ .
N=91 N=124
“1
N=98 N=89
j — _ ^
. . Tl—1 . ~l-._ I—TT—
N=110 N=58
cCt.
N=99 N=109 N=81
Mar. "SG 40 -
.
£3 5 7 9 11 13 15 S3 6 7 9 II 13 15 S3 6 7 9 II 13 15
Shellwidtli(mm)
StationA StationB StationC
1I
84 AMERICAN MALACOLOGICAL BULLETIN 23 • 1/2 • 2007
Figure 1. (continued)
2002 N=99
N=80
Apr.
-r-TTh-^ JJJ
N=106 N=110 N=100
May
-H~rh- -n-ri-._ -rfln
100 r
80 N=100 N=84
60
Jun. 40
20
100
80 N=123 N=104
J1ul.1 4200 n_rm-. rnTi-
100
80 N=116 N=100 N=94
A 60
20 1—h-tTI 1—1—1 -TTT -rfTh-.
100
80 N=101 N=94
60
S©p. 40
20 n-i III.
,..
100
80 N=114 N-87
Oct. 40
20 rTTii— —
*
100
80 N=121 N=105 N=97
Nov. 40
20 i-rlTl-n-^
100
80 N=100 N=87
Dec.
40
20 r-TTn—
I—
100
2003 “ N=99 N=50
Jan. 40
20 r-rfTTl_ n-.
100
80 N=100 N=85
Feb. 40 -
20 m~r-T-i
100 p
N=104 N=85
^ 60 -
Mar. -S 40 .
^§ 20
n
go 5 1 9 II 13 15 S3 5 7 9 II 13 16 S3 5 7 9 11 13 15
ShSetlaltwiiodnthA(mm) StationB StationC
REPRODUCTIVE BEHAVIOR OF CERITHIDEA 85
100 Figure 1. (continued)
80 N=157 N=102 N=91
60
2003
40
Ap^r. 0 — r~i 1 1 1 . ,-_r-rh-i
S3 80 N=110 N=107 N=^109
§
May ^ rhi-rTl-i— . . . . . _rin-4H~l—1—• . . . . .
$3 5 7 9 n 13 15 S3 6 7 9 II 13 16
^3 ) 7 9 It 13 15
StationA StationB StationC
mm
measured their shell width in situ every month from April cruited juveniles (3-6 in shell width) of C. rhizophora-
2000 through May 2003. ruin were found in higher tidal zones than the other pot-
amidid and batillariid species. The distribution of juveniles
1. Copulation frequency of C. rhizophorarurn was limited to lower tidal zones.
Snail mating can be categorized as face-to-face mating
or shell-mounting mating (Asami 1998). Cerithidea rliizo- Copulation frequency
phorarum mates by shell mounting (Ohtaki et al. 2001). The largest number of copulations was observed be-
Ohtaki et al. (2001) reported that copulatory behavior was tween one and two hours before the lowest tide in the af-
observed from the middle of June to the middle ofAugust ternoon and two hours before and after the lowest tide at
aInndthpiesakstoufdyi,nitwiael tciomuentoefdcotphuelantuiomnbewrasobfefionrdeivliodwueasltstaidned. n1i0g.h9t6(±Fig2..326).mThme m(emaeannsh±ellSwDi,dtNh-of1u0p0p,errainngdeiv=idu8a.l6s-1w3a.s0
copulating couples along the route every 15 minutes on 4 mm) and 11.72 ± 29 mm (mean ± SD, N = 100, range =
July and 21 July 2001, 12 and 25 June, 12 and 13 July, and 8.8-13.9 mm) for lower individuals (Fig. 3). There was no
10August 2002 in daytime, and 12 and 13 July2002 at night. significant correlation between the shell width ofupper and
While sampling the transect eveiy 15 minutes, we placed lower individuals {R^ = 0.082), but upper individuals were
little flags marked with an identification number near each significantly smaller than lower ones (Student’s f-test,
pair of C. rhizophomruni in the act of coupling. When the P < 0.05). From the reproductive organs of the 100 pairs,
pair of C. rhizophorarurn separated, it was assumed that the 65% were male (upper) - female (lower) pairs, 31% were
copulation was terminated. The length between the begin- male - male pairs, 1% female - female pair, and 3% female
ning and the end ofthe copulation was checked and noted. (upper) - male (lower) pairswere observed. The mean width
We used aheadlamp for night searches. On thesameday, we of individuals with male reproductive organs was 11.49 ±
picked 100 copulation pairs at random and marked upper 2.69 mm (mean ± SD; N- 69, range = 8.8-13.9 mm). There
snails with a permanent marker. We brought copulating was no relation in shell width between the females and the
pairs back to laboratory and measured them (both weight males (f-test; P > 0.05).
and shell height). Their shells were broken, and we deter-
Climbing behavior
mined their sex by examining the reproductive gland.
There were clear seasonal changes in total number of
individuals of Cerithidea rhizophorarum on the trunk ofthe
2. Climbing behavior
Cerithidea rhizophorarurn is known as an intertidal snail mangrove tree Kandelia candel (Fig. 4). In 2000, 1071 snails
were observed on trees in May, 1355 in June, 601 in July, 46
species, but it does climb trees. This behavior was observed snails in August, and in September the number of snails
in a small mangrove forest of the Atagogawa River (Waka-
matu and Tomiyama 2000, Ohtaki etal. 2002). In this study, increased to 1041. The following year, from September to
we observed snails on the trees from May 2000 to May 2003, December, the number of snails climbing up the trunk of
2 hours after the lowest tide ofspring tides every month. mangrove trees was at its peak, with the number decreasing
from Februarythrough March. This tendencywasseen every
year at the same period.
RESULTS
DISCUSSION
Size distribution
During this period no large change in the number of Wakamatsu and Tomiyama (2000) reported that re-
Cerithidea rhizophorarurn was noticed (Fig. 1). Newly re- cruitment of Cerithidea rhizophorarum at this site was so
86 AMERICAN MALACOLOGICAL BULLETIN 23 • 111 - 2007
Jul.4th2001 Jul21st2001 Figure 2. Daily changes in percent-
12 T age ofcopulating individuals in the
10 population. Arrows indicate the
8
6 lowest tides.
4
2
0
9:45 17:30
Jun.25th2002
Jun.12th2002
12T
0-i 1 1 1 1 1-
10:00 12:00 14:00 16:00 10:00 12:00 14:00 1600
JuL12fh2002 Ju1.13th2002
16 A R^=00033 Figure 3. A, Relationship between
=0.0048
shellwidth ofupper individuals and
lower individuals. R~ = 0.0033, P >
0.05, N- 100. B, Frequency ofshell
width of upper individuals and
0.5-- lower individuals. Solid bar, upper
2-
0-- 0A i 1 1 1 1 individuals; open bar, lower indi-
0 2 4 uppers6hellwidth(m8m] 10 12 14 0 0.5 uppIerwetweight11.5^ 2 2-6 viduals; N = 100. C, Relationship
between shell width of upper indi-
viduals and lower individuals. =
0.0048, P > 0.05, N = 100. D, Fre-
quency of shell width of male and
female. Solid bar, male; open bar,
female; N = 100.
shellwidth|mm|
Figure 4. Seasonal changes in total
number ofindividuals ofCerithidea
rhizophorarum on the trunk of the
mangrovetreeKaiidelia cmidel(May
2000 - May 2003).
REPRODUCTIVE BEHAVIOR OE CERITHIDEA 87
small that it could not be detected. But in this study, newly
recruitedjuveniles (3-6 mm) appeared from November 2001
mm
to March 2002, and they grew to 10 in length from
March to Inly 2002. However, new recruitment was not
observed everyyear. Wakamatsu and Tomiyama (2000) and
Ohtaki et al. (2001) suggested that C. rhizophomnu}i had
deceased in numbers at this site. We conclude that the de-
crease in population is due to imposex caused byTBT. Erom
the results of proportions of copulation pairs, it appears
males mount females.
More male-to-male (31%) than female-to-female
couples were observed (1%), supporting the hypothesis of
Wakamatsu and Tomiyama (2000) and Ohtaki etal (2001).
The peak frequency of copulation was generally before
the lowest tide in daytime. Copulation was most frequently
observed during the 3-6 hours around the time ofthe lowest
tide and mostly during 1-2 hours around the time of the
lowest tide at night. As we did not observe copulation when
it had begun to rain, rain may block the copulation ofCeri-
thidea rhizophorarum.
The population of Cerithidea rhizophorarum on trees
increased at the highest tide and decreased at the lowest tide.
This might be the daily rhythm to avoid the water. Snails
were observed on trees from the beginning ofspring to lune
and descended from trees in luly to August. These rhythms
synchronize with the copulation period. The population on
the trees increased in September, and decreased in winter.
Climbingtrees at the beginning ofwinter could be in prepa-
ration for hibernation.
ACKNOWLEDGEMENTS
We thank Janet Leonard for her help and the invitation
to present this study at the symposium, and all participants
at the symposium.
LITERATURE CITED
Asami, T., R. H. Cowie, and K. Ohbayashi. 1998. Evolution of
mirrorimagesbysexuallyasymmetric matingbehaviorin her-
maphroditic snails. TheAmerican Naturalist 152: 225-236.
Ohtaki, H., E. Maki, and K. Tomiyama. 2001. Seasonal changes in
distribution and reproduction behavior of Cerithidea rhizo-
phorarum. Venus 60 199-21.
:
Ohtaki,H., E. Maki, andK. Tomiyama. 2002. Climbingbehaviorof
Cerithidea rhizophorarum. Venus 61 215-223.
:
Wakamatsu, A. and K. Tomiyama. 2007. Seasonal changes in size
distribution ofPotamididae (Gastropoda) on Mangrove tidal
flat. Venus 59: 225-243.
Accepted; 9 May 2007