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Population dynamics of the soldier crab Mictyris guinotae (Brachyura: Mictyridae) in Amparu Tidal Lagoon on Ishigaki Island, Japan
Accepted Manuscript Population dynamics of the soldier crab Mictyris guinotae (Brachyura: Mictyridae) in Amparu Tidal Lagoon on Ishigaki Island, Japan A. Kawachi, T. Ishikawa, M. Irie PII: DOI: Reference:
S2352-4855(16)30317-6 http://dx.doi.org/10.1016/j.rsma.2017.05.006 RSMA 249
To appear in:
Regional Studies in Marine Science
Received date: 1 November 2016 Revised date: 8 May 2017 Accepted date: 8 May 2017 Please cite this article as: Kawachi, A., Ishikawa, T., Irie, M., Population dynamics of the soldier crab Mictyris guinotae (Brachyura: Mictyridae) in Amparu Tidal Lagoon on Ishigaki Island, Japan. Regional Studies in Marine Science (2017), http://dx.doi.org/10.1016/j.rsma.2017.05.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1 2
Population dynamics of the Soldier Crab Mictyris guinotae (Brachyura: Mictyridae) in Amparu Tidal Lagoon on Ishigaki Island, Japan
3
A. Kawachi1, T. Ishikawa2, and M. Irie3
4 5 6 7 8 9 10 11 12
1
Token C.E.E. Consultants Co., Ltd, 1-15-6, Kitaohtsuka, Toshima-ku, Tokyo, 170-0004, Japan Tokyo Institute of Technology, 2-12-1 Ookayama, Meguro-ku, Tokyo, 152-8550, Japan 3 Department of Civil and Environmental Engineering, University of Miyazaki, 1-1, Gakuen Kibanadai-nishi, Miyazaki-shi, Miyazaki, 889-2192, Japan 2
Corresponding author: Atsushi Kawachi ([email protected]) Submitted to: Regional Studies in Marine Science on 8th January 2017 Re-submitted to: Regional Studies in Marine Science on 8th May 2017
13 14
ABSTRACT
15
The life history of the soldier crab Mictyris guinotae in Amparu Tidal Lagoon on Ishigaki Island, Japan was
16
investigated through population measurements with detailed size classifications. Surveys and measurements
17
were carried out at 15 sampling points every 2 weeks during the 4-month incubation season starting in
18
December 2005, and twice in April and in June 2006 when juveniles started and finished settlement,
19
respectively, in the lagoon. Supplementary measurements were conducted every month from December 2006
20
to May 2007 to corroborate the results of the first experiment and to examine the growth rate of the juvenile
21
population.
22 23
The results showed that (a) the peak of incubation was from mid-January to mid-February, and the season of
24
juvenile settlement was April to early June, which means that the duration of larval life in the ocean was about 2
25
months; (b) juveniles were distributed widely in the lagoon, and adults clustered to the west and south of the
26
lagoon where the bed sediment was relatively fine with high ignition loss; (c) the survival rates of adults and
1
27
juveniles in 1 year were 0.73 and 0.17, respectively, and the mean longevity of adults was about 3.7 years; (d)
28
reproduction efficiency from eggs to juveniles was about 0.0040, which is much smaller than the survival rate
29
of juveniles as well as adults, which means that the propagation of M. guinotae is mainly controlled by the
30
condition that the larvae experience in the ocean.
31 32 33
KEYWORDS: intertidal crab, life history, breeding season, population sampling, Ryukyu Islands
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1 INTRODUCTION
36
In the intertidal zone ecosystems and material cycles, small crabs are one of the major components, taking in
37
organic detritus from bed sediment (Meziane et al., 2002; Quinn, 1986; Robertson and Newell, 1982; Takagi et
38
al., 2010; Webb and Eyre, 2004), being eaten by higher order organisms like birds (Zharikov and Skilleter, 2004,
39
2003) and aerating bed sediment by burrowing to enhance organic compound decomposition (Otani et al.,
40
2010). Therefore, studying their biology is important to understand the structure of tidal lagoon ecosystems.
41 42
Intertidal crabs have two life stages: larval and benthic. Larvae just after hatching, called zoea, flow out from the
43
tideland to the ocean at ebb tide, return to the tideland as megalopa, the final larval form after moltings, several
44
weeks later on spring tide days (Epifanio and Cohen, 2016) and start benthic life as juvenile crabs. They mature
45
to reproduction after 1 to 2 years of benthic life (Nakasone and Akamine, 1981; Shih, 1995; Yamaguchi, 1976).
46
Beyond this general understanding, the details of their biology in tidelands are species-specific and also depend
47
on the meteorological and hydraulic conditions of each site (Henmi, 1993; Jones and Simons, 1983; Wada,
48
1991; Yamasaki et al., 2010). Thus, there is still much to learn about their biology from field measurements.
2
49 50
Recent DNA analysis has clarified the classification of crab species into several subspecies based on
51
divergences in the evolutionary lineage under different conditions (i.e., Aoki et al., 2012; Naderloo et al., 2016).
52
There are several closely related crabs having common as well as divergent biological characteristics in the
53
Ryukyu Islands, which are located between Kyushu Island of Japan and Taiwan and are isolated from each
54
other by submarine trenches and swift ocean currents (Jan et al., 2002; Lan et al., 2008; Qi et al., 2016).
55 56
Ecological diversity of intertidal crabs, which is induced by isolation and is influenced by the differing
57
conditions of each site’s habitat, can provide hints to understanding the evolutionary process of life on Earth.
58
The basis for research of ecological diversity will be a steady effort to investigate lifecycles and population
59
dynamics of each species in its habitat condition (Costa and Soares-Gomes, 2009; Frith and Brunenmeister,
60
1980; Hines et al., 1987; Hsueh et al., 1993; Litulo, 2005; Mokhtari et al., 2008; Tina et al., 2015).
61 62
In the present study, the life history of Mictyris guinotae, which is an endemic crab species in the Ryukyu
63
Islands, was investigated by sampling populations in the Amparu Tidal Lagoon on Ishigaki Island located near
64
Taiwan. M. guinotae is a subspecies of Mictyris (soldier crab), which is distinguished from the related species,
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M. brevidactylus, which inhabits Taiwan, Hong Kong, Singapore, and Indonesia (Davie et al., 2010).
66 67
Several field studies in the Ryukyu Islands have clarified that some differences in the characteristics of M.
68
guinotae depend on location. Yamaguchi (1976) reported that the mean size of M. guinotae was significantly
69
larger on Ishigaki Island than on Amami-oshima Island. Nakasone and Akamine (1981) found that the
70
incubation season was from November to February at the mouth of the Okukubi River on Okinawa Island,
3
71
while Kosuge and Kohno, (2010) reported that the incubation season of the same species was from December
72
to February at the mouth of the Urauchi River on Iriomote Island. On the other hand, Shih (1995) reported that
73
the incubation season of M. brevidactylus, a closely related species of M. guinotae, was from January to April
74
based on field experiments in Taiwan. These findings suggest that the biology of intertidal crabs depends not
75
only on species but also on habitat conditions.
76 77
In this study, population structure measurements based on detailed size classifications were carried out every 2
78
weeks during the 4-month incubation season starting in December 2005, and twice in April and in June 2006
79
when juveniles started and finished settlement in the lagoon. Supplementary measurements were conducted
80
monthly from December 2006 to May 2007 to corroborate the incubation season observed in the previous year
81
and to examine the growth rate of the juvenile population. Based on experimental data, seasonal variation of the
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size distribution, growth probability of eggs to juvenile crabs, growth rate of adult crabs, and generation change
83
rate were analyzed.
84 85
2 STUDY SITE
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The Ryukyu Islands comprise 34 islands of various sizes extending from Kyushu Island, Japan to Taiwan. The
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population density of M. guinotae has been previously reported for four islands in this region: Amami-Oshima,
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Okinawa, Ishigaki, and Iriomote.
89 90
This study was conducted on the west coast of Ishigaki Island in the Amparu Tidal Lagoon in Nagura Bay (Fig.
91
1), which is famous for having a great variety of intertidal crabs; the words of a folk song for community work
92
on the Ishigaki Island includes the names of fifteen kinds of crabs (Ohyama, 1994; Takeda and Ohyama, 1994).
4
95
The laagoon was dessignated as an internationally i y important sitee of the Ramsaar Convention in 2005 owing g to its
96
wl, for which th he intertidal cra rabs are one off major food sou urces. diverssity of waterfow
96 98 99
A Location off the Ryukyu Islands, B: Lo ocation of the Amparu Tidaal Lagoon, C: Aerial Fig. 11. Study site. A: photoggraph image of o the Amparu Tidal T Lagoon.
99 105
8 ha, extendin ng north-southh with the easst side Ampaaru Tidal Laggoon is sand-ccovered with aan area of 18
106
om the ocean by a long san nd spit surrouunded by shalllow mangrovee swamps andd the west sidee separated fro
107
h of the lagoonn is located at the t north end with w a channell 100 m wide and a 50 covereed with oak treees. The mouth
108
hat is about 1 kkm wide. A streeam named thee Nagura River er flows from th he east m lonng extending too a coral reef th
109
w a watersh hed of 15 km2. Two small drainage d chann nels flow out ffrom farmland d and a to the tidal lagoon with
110
ve swamps at thhe east side to the tidal lagoon n. sugar factory througgh the mangrov
106 109
elevation of thee tidal lagoon obtained by an automatic leeveling The ccontour map inn Fig. 2 showss the ground el
110
op sensor. Three T creeks in the lagoon are a formed by the inflows m mentioned prev viously. apparaatus with an optical
111
i the figure inndicate the loccations of statiions for popullation sampling g. The The oopen and closeed rectangles in 5
113
elevattion difference in the lagoon is about 0.5 m m, except at the channel of thee Nagura Riverr. The tide amp plitude
114
pring tide and 00.5 m at a neap p tide. Almost the entire sandd bed area of th he tidal in Naggura Bay is aboout 1.5 m at sp
115
b ocean waterr at high waterr of the even ebb e tide and drried out at low w tide, except for f the lagoonn is covered by
116
three ccreeks.
114
115 116
u Tidal Lagoonn. Fig. 2. Contour mapp of the Amparu
117 121
w and close-uup views of thee surface of thee lagoon at low w tide showing g many The phhotographs in Fig. 3 show wide
122
b intertidal craabs after remooving the nutriients from the sediments: Thhe crabs come to the sand bballs spit out by
123
a low tide and d burrow underrground beforee high tide, leav ving sand ballss behind. The square, s surfacce for feeding at
124
i the 50 cm × 50 cm quadratt for population n sampling. woodeen frame in thee right picture is
122
6
123 125 126
Fig. 3. Ground surfaace condition of o the Amparu Tidal Lagoon.. A: Wide view w. B: Close-up view with a 50 0 cm x 50 cm m quadrate fram me for sampling g.
126 136
und surface seediments are sh hown for six po oints (E3, E4, W W2, W5, S5, and a S7 Grain size and ignitiion loss of grou
137
C sand off a narrow band nd of grain sizee and lower ign nition loss weree observed at E3 E and in Figg. 2) in Fig. 4. Coarse
138
which are locateed at the north heast part of thhe lagoon. At W2 W and W5 lo ocated on the nnorthwest part of the E4, w
139
p of sediment s was coarse sand, but b a small am mount of fine silt was preseent and lagoonn, the major proportion
140
he lagoon, in contrast, c the m major componen nt was ignitioon loss was higgh. At S5 and S7 at the soutthern part of th
141
meter with a w wide range of silt, which had high ignitionn loss. Wada (1982) fine saand around 2000 μm in diam
142
ment in sand ba balls made by two kinds off small intertiddal crabs, Scop pimera analyzzed the grain size of sedim
143
globosse and Ilyoplaxx pusilla, and reported r that thhey preferred fine f sand of 63 3 to 125 μm inn diameter for taking
144
he southern parrt of Amparu Tidal Lagoon is more suitab ble for nourisshment. Thereffore, it is conssidered that the
145
wth of small inteertidal crabs thhan the northern n part. suppoorting the grow
137
7
138 139
Fig. 4. Grain size annd ignition loss of ground surfface sediment
140 145
position based on a survey carried c by Irie et al. (2005). M M. guinotae was w the Fig. 5 shows the poopulation comp
146
b Scopimera ryukyuensis, th he remaining species s being ppresent only in minor most ddominant speccies, followed by
147
ortions. S. ryukyyuensis is an in ntertidal crab thhat is classified d in genus Scop pimera in the ffamily Dotillid dae and propor
148
he most domin nant crab specie ies in total volu ume as is mucch smaller thann M. guinotae.. Therefore, M. guinotae is th
149
well aas in populationn on the Amparru Tidal Lagooon.
146
8
147 148
c in the Am mparu Tidal Laagoon (Irie et all., 2005). Fig. 5. Major speciess of intertidal crabs
149 150
3 ME ETHOD
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3.1 Sampling
161
Popullation samplingg was conducted over two peeriods from December D 2005 to July 2006 and December 2006
162
wn in Fig. 6, which w nearly coovers the seaso ons from incub bation to juvennile settlement.. In the to Maay 2007 as show
163
mpling was caarried out at loow tide just before b each sprring tide from m December 20 005 to first eexperiment, sam
164
cause spawning g tends Marchh 2006 in ordeer to investigatee the incubatioon of females; this timing waas selected beca
165
fter approximat ately 1 month of incubation (Nakasone annd Akamine, 1981). to occcur on a sprinng tide day aft
166
w conducted d to determine the settlementt and growth of o juvenile crabbs in April and d June Anothher sampling was
167
s was cconducted eveery month from m December 22006 to June 2007 2 in 2006. In the secondd experiment, sampling
168
riment regardin ng incubation timing t and to cclarify the settllement order to corroboratee the results of the first experi
169
niles. Samplinng points weree in common to t the two expperiments with h three duratioon and growthh rate of juven
170
ment to balancee the sampling distribution, d ass shown in Fig. 2. additioonal sampling points in the seecond experim
162
9
163 164
s and thee times of meassurements. Fig. 6. Tide level reccord (Ishigaki station)
165 173
w an averagee spatial densitty distribution of sand ball ppiles was samp pled by At eacch sampling pooint, an area with
174
5 cm quadratee frame on thee ground and collecting bed sediment s to a ddepth of 30 cm m from placinng a 50 cm × 50
175
g fine sedimennt by sieving through t a 2 mm mesh, crabss were picked up by insidee the frame. Affter eliminating
176
on in reference to illustrationss in the hand oor with tweezeers and identified to the speciies level by vissual observatio
177
1 The len ngth and widthh of carapace (hereafter, CL L and CW) weere measured for M. literatuure (Takeda, 1978).
178
guinottae using a Veernier scale. Th he sex of each crab was recorded for each adult a based onn visual inspecttion of
179
men, while juve venile crabs weere too small to o distinguish thhe generative organs. o the geenerative organns at the abdom
180
her they carried d eggs. Ovaryy condition wass inspected forr females to dettermine wheth
174 175
3.2 D Data Processiing
176
3.2.1 Seasonal channges in populaation density
180
First, tthe correlationn between CL and a CW was exxamined, and only o CL was adopted a as a sizze indicator baased on
181
L and CW (corrrelation coeffi ficient, r = 0.96 6). Then, valuees of CL were sorted high llinear correlatioon between CL
182
opulation denssity at each sam mpling with 00.5 mm intervaals to constructt a size histogrram of populattion density. Po
183
ment time point are written as follows: point aand measurem 10
180
Population density: Pi , j ,k 4 Ni , j ,k
(1)
181
where N is the number of crabs collected in the quadrat, P is the population density (individuals/m2), i is the size
182
band number, j is the sampling point number, and k is the measurement time number.
183 184
However, because the histogram for each set of (i, j, k) was unstable due to the limited number of samples in
185
each band width, tendencies of the space distribution and time variation were investigated separately as follows:
186
First, the population density of each size band, i, was averaged over the entire area of the lagoon to find the
187
tendency of seasonal population dynamics.
188
Pm (i, k )
1 M
M Pi , j , k j 1
(2)
189
where M is the number of sampling points, and Pm (i, k) is the size distribution histogram averaged over the
190
entire area of the lagoon at time k.
191 192 193
Further, the normalized population density at each measurement time point was defined as follows: I
(3)
Qm (i, k ) Pm (i, k ) / Pm (i, k ) i 1
194
where I is the number of size bands and Qm (i, k) is the normalized size distribution histogram at time k, the
195
integral of which over all size bands is unity.
196
3.2.2 Spatial population distribution in the tidal lagoon
197
As will be shown later, the normalized histograms had a clear nodal point in the season of juvenile settlement,
198
and juvenile crabs (age; Ta < 1 year)” were separated from “adults (Ta ≥ 1 year)” using the position of the
199
nodal point as a threshold. Then, the population density of adults was averaged over the measurements before
200
the season of juvenile settlement to examine the spatial distribution of crabs, which settled earlier than in the
201
previous years. On the other hand, the spatial distribution of juveniles was represented by the results of the last
11
202 203
measurement when the juvenile settlement was nearly ended, PAd ( j )
I KS 1 1 Pi , j , k for adults KS 1 i 1 k 1 I
PJu ( j ) Pi , j , k KT
(4)
for juveniles
i 1
204
where KS indicates the time at which juvenile settlement started, and KT indicates the time of the last
205
measurement. PAd (j) and PJu (j) show the spatial distributions of populations for the adult and juvenile groups,
206
respectively.
207 208
3.2.3 Generation change rate
209
A nodal point was also observed in Pm (i, k) obtained before the season of juvenile settlement (k < KS), and the
210
population of adult group was further divided into the younger group (Ta = 1 year) with Pm (1) and the older
211
group (Ta > 1 year) with Pm (>1), using the nodal point as the threshold,
212
Pm (1)
KS 1 k 1
Pm ( 1)
213
In
P (i, k ) i 1
KS 1
(5)
m
I
P (i, k ) k 1
i In 1
m
where In is the value of CL at the nodal point.
214 215
Assuming a constant death rate over the year for crabs of all ages except juveniles, the following relationship
216
would be observed:
217
(6)
Pm (n 1) rPm ( n)
218
where Pm (n) is the population with age of n, and r is the rate of survival in a year. By summing the series at each
219
side from n=1 to infinity, we obtain the following relationship:
220 221
(1 r ) Pm ( 1) rPm (1)
(7)
Using the above equation, the survival rate in 1 year, r, and the average longevity of M. guinotae were estimated
12
222
from observation results as follows:
Pm ( 1) Pm (1) Pm ( 1)
223
r
224
Lm m r m 1 / r m 1
225
m 1
m 1
(8) 1 1 Pm ( 1) / Pm (1) 1 r
(9)
where Lm is the average longevity.
226 227
On the other hand, the survival rate of juvenile was obtained from the observed result: M M M M Pm (1) r (0) PAd ( j ) / PJu ( j ) (1 r ) PAd ( j ) / PJu ( j ) j 1 j 1 j 1 Pm (1) Pm ( 1) j 1
228
(10)
229
where r(0) is the survival rate of juvenile; the numerator is the population of the younger adults (Ta = 1 year)
230
observed before the season of juvenile settlement, and the denominator indicates the population of juveniles at
231
the end of the season of settlement.
232 233
3.2.4 Reproduction efficiency
234
Only a small proportion of eggs in the female ovary reach the stage of juvenile crabs due to losses of larvae at
235
stages before flowing out to the ocean, during metamorphosis at ocean, on the return trip to the lagoon, and
236
during the process of landing. The reproduction efficiency of M. guinotae was calculated from the data as
237
follows:
238
Erep
1 M
M
P j 1
Ju
( j)
(11)
TN egg
239
where Erep is the reproduction efficiency, the numerator is the average population density of juveniles calculated
240
by Eq. 4, and TNeeg in the denominator is the spatially average number of eggs produced per unit area in a
241
breeding season.
242
13
243
Nakasone and Akamine (1981) reported the following relationship between the number of eggs and the
244
carapace length, CL, for ovigerous females from field observations on Okinawa Island:
245 246
N egg 1.389 CL3.2746
(12)
where Negg is the number of eggs carried in the ovary of a female.
247 248
Writing the spatially averaged population density of ovigerous females whose CL is in the ith size band as
249
PFOm,(i, k) in the same way as for Eq. 2, and assuming that the observed female spawns eggs at the spring tide
250
day after a 1-month incubation, TNegg can be calculated by the following equation because the measurement
251
was carried out every spring tide during the incubation season:
252
KS 1 I TN egg 1.389 CL3i .2746 PFO m (i , k ) / 2 k 1 i 1
(13)
253
where CLi is the CL value of the ith band size, and KS is the measurement time point at the end of incubation
254
season. The factor 1/2 was multiplied because the measurement frequency was twice in a month, while the
255
spawning was assumed as being after 1-month incubation.
256 257
4 RESULTS AND DISCUSSION
258
4.1 Seasonal Change in Population Density
259
The total corrected number of M. guinotae was 1,257 for the 10 measurements at 15 stations and 1,056 for 6
260
measurements at 18 stations in the first and second experiments, respectively. Average population density for the
261
duration of each of the two experiments was 34.0 and 39.1 individuals/m2, respectively. The male:female ratio
262
was 1:0.88 at a minimum and 1:1.41 at a maximum, and the average was 1:1.20.
263 264
Fig. 7 shows the normalized size distribution for each measurement, Qm (i, k) expressed by Eq. 2, and
14
265
incubation progress over time is plotted in Fig. 8. Incubation already started just before the first measurement in
266
mid-December, peaked from mid-January to mid-February, and finished at the end of March. The size of
267
ovigerous females among all females was larger in the early stage of the incubation, and gradually, participation
268
of smaller females increased. From mid-January to mid-February, almost 100% of the largest group was
269
ovigerous, and some of the large group had a second clutch in mid-March. This tendency was more distinctly
270
observed in the second experiment, suggesting that fully matured females had eggs twice, as was observed by
271
Henmi and Kaneto (1989) for another intertidal species: Scopimera globose, Ilyoplax pusillus and
272
Macrophthalmus japonicus on Hakata Bay in the north of Kyushu Island.
273 274
Juveniles appeared from mid-March, and had a size of around 3 mm. The red vertical arrows in each figure
275
after March in Fig. 7 indicate the node of size distribution, which was considered to separate the juvenile group
276
from the adult group. The number of juvenile members increased with time, and in April, the juvenile
277
population exceeded that of adults which had settled in the lagoon in previous years. In June, juveniles grew to
278
exceed 4.5 mm in size, at which point sex could be distinguished.
279
15
281 2 285 2 286 2 287 2 288 2
Fig. 77. Seasonal variation v in siize distributioon of normaliized populatio on density. Fiigures are arrranged chronoologically from m top to bottom m for each expperiment. Malle and female sizes are plotteed above and below, respecctively, the horrizontal axis off each graph; oovigerous fem males are repressented by filledd bars; and juv veniles that w were too small to t distinguish th he sex are marrked in gray an nd divided even nly above and bbelow the axiss.
16
286 2 289 2 290 2 291 2
Fig. 88. Seasonal varriation in the proportion p of oovigerous fem males. Dotted red lines indicaate the proporttion of ovigerrous female too the total female, and the hoorizontal bar graphs g indicatee the size distriribution of ovig gerous (blackk) and non-oviggerous female (white) in CL.
290 2 292 2
p den nsity at each m measurement time t point, Pm (i, k), in Eq.. 2 was divideed into Spatiaally averaged population
293 2
ws: juveniile and adult grroups as follow
293 2
Id Pm j (k ) Pm (i, k ) Juvenile grouup i 1 I Pm a ( k ) Pm (i, k ) Adult group i Id 1
(14)
296 2
wheree Id is the thresshold to separaate the two grouups indicated by b the red arrow ws on the grapphs (after mid-M March
297 2
y of these two groups shown n in Fig. 9 ind dicates that thee juvenile popu ulation in Figg. 7). The popuulation density
298 2
a became alm most steady inn June, while th he population of adults decre reased graduallly. The increaased in April and 17
299 2
time oof juvenile settllement was about 2.5 monthhs after the peak k of incubation n shown in Figg. 8, meaning th hat the
300 2
larval life of M. guinnotae in the ocean has a duraation of about 2 months with a lag of about 0.5 months beetween
301 2
spawnning and incubbation.
300 2 304 3
k nodal points of Qm (i, k) caan also be seen n before April, as indicated by b blue In Figg. 7, on the othher hand, weak
305 3
ws, when juveni nile settlement did d not yet star art. In the size distribution d av veraged for all m measurement results arrow
306 3
December to February F beforre juvenile settttlement (Fig. 10), 1 a clear no ode can be seenn, and the left group from D
307 3
y populaation, Pm (1), annd the right corrresponds to th he older populaation, Pm (>1). corressponds to the younger
305 3
306 3 307 3
Fig. 9. Seasonal variiation in juveniile and adult poopulation densities.
18
308 3 309 3
Fig. 100. Size distribuution of populaation density beefore juvenile settlement. s
310 3
316 3
h group at arou und 7.0 and 111.0 mm, respecctively, Smooothed curves foor Pm (1) and Pm (>1) place thhe peak of each
317 3
5.5 mm, respecctively. Taking g the peaks and d the largest of C CL of juvenilee group with thhe largest arouund 10.0 and 15
318 3
ment in Fig. 7, we w obtain a meeasure of growtth rate based on n CL (Fig. 11),, for which thee origin for evvery measurem
319 3
me on the horizoontal axis of th he logarithmic sscale was assum med to start at the end of Febbruary, and the age of of tim
320 3
w assumed to t be in a rangge from 2 to 4 years becausee they could no not be separated. The the Pm (>1) group was
321 3
n inverse propo ortion to time. lineariity of the carappace size indicaates that the groowth shows an
317 3
Growthh rate
d (CL ) a dtt t
(15)
19
318 3 320 3 321 3
Fig. 11. Increase in carapace c length h, CL. Black m means juvenilees; blue means young adults ((Ta =1 year); and a red meanss older adults (T ( a >1 year).
321 3
322 3
4.2 Sppatial Populaation Distribu ution
328 3
The hhistograms of teemporally averraged populatiion density of juveniles j and adults a at each ssampling pointt using
329 3
r expressed by E Eq. 4 and plottted on a map of the lagoonn (Fig. 12) sho ow that PJu (j)) and PAd (j), respectively,
330 3
ntrated around d 24°23'50''N w where shallow terrace t juveniiles settled in a wide range off the lagoon, buut were concen
331 3
de flow. On thee other hand, th he adult population was low w at the northeaast part widenning might staggnate flood tid
332 3
l (Fig. 4), annd spread to thee west and the south from thee area where ju uvenile wheree sediment igniition loss was low
333 3
ment was conccentrated. settlem
329 3 332 3
w controlled d by the hydrauulic characterisstics at Thesee data suggesteed that the spattial distributionn of juveniles was
333 3
me of settlemeent, while the adults migrateed to areas wh here the ground d was coveredd with nutritiou us fine the tim
334 3
ment. sedim
20
333 3 334 3
Fig. 122. Spatial distrribution of (A) juvenile j groupp and (B) adult groups.
335 3 336 3
4.3 G Generation Chhange Rate
342 3
As shhown in Fig. 10, 1 there was a nodal point around 8.5 mm m in CL for samples colleected before ju uvenile
343 3
ment, and the CL C value was used u as the thre reshold to sepaarate the adults into the youngger group that settled settlem
344 3
a the older grroup (Ta > 1 yeear), the populaations of whichh are described d as Pm in the previous year (Ta = 1 year) and
345 3
o of Pm (1) and d Pm (>1) was eestimated to bee about (1) to Pm (>1), respeectively, in Eq. 5. From the Fiig. 10, the ratio
346 3
was calculated as a 0.73 from Eq. E 8, and the mean longevitty was 1:2.7. Therefore, thee survival rate over a year w
347 3
calcullated as 3.7 yeaars from Eq. 9.
343 3 346 3
w assumed in this study, there t was a po ossibility of theeoretical immo ortality, Becauuse a constant survival ratio was
347 3
here must be a limit to the lifeespan of the inntertidal crabs. Nakasone and d Akamine (19981) reported th hat the but the
348 3
o in thee mouth of the Okukubi Riveer on Okinawaa Island lived loonger than 3 yeears. If oldestt M. guinotae observed
21
346
we assume that all of the 3-year-old population would die in the following year, Eq. 7 and Eq. 9 can be modified
347
as follows:
348
Pm ( 1) (r r 2 r 3 ) Pm (1)
(16)
349
Lm (1 2r 3r 2 4r 3 ) /(1 r r 2 r 3 )
(17)
350
From these equations, survival rate r and mean longevity Lm become 0.96 and 2.44 years, respectively.
351 352
This discussion applies to the adult group population. The survival rate of juveniles must be smaller due to less
353
physical strength and mobility. Using the values of juvenile population observed in June 2006 and the
354
population of the young adult group (Ta = 1 year) averaged over the term from December to February, the
355
juvenile survival rate r (0) was estimated as 0.17 form Eq. 10.
356 357
4.4 Reproduction Efficiency
358
Using Eq. 13, the average density of eggs produced in a unit area of the lagoon during the incubation period,
359
TNegg, was 10,270 individuals/m2. Substituting this value into Eq. 11, a reproduction efficiency of 0.0040 was
360
obtained, which was much smaller than the survival rate of juveniles. Therefore, it can be said that the
361
propagation of M. guinotae is mainly controlled by conditions that larvae experience in the ocean.
362 363
4.5 Range of Incubation Season in the Ryukyu Islands
364
In Fig. 13, the incubation season for M. guinotae on Ishigaki Island is compared with previous reports of those
365
observed at various locations, including M. guinotae on Okinawa Island and Iriomote Island, and M.
366
brevidactylus, which is a closely related species of M. guinotae, in Taiwan. The site locations line up along the
367
Ryukyu Islands from Kyushu Island to Taiwan (Fig. 1), and the incubation seems to occur earlier at sites closer
22
373 3
to Kyuushyu Island and a later at the sites closer too Taiwan, but th here is no marrked differencee between incu ubation
374 3
w are locaated in very cllose proximity y to each otherr (see Fig. 1-A A). The on Ishhigaki and Irioomote islands which
375 3
mperature of thhe Kuroshio Current, C reasonn for the spatiaal variation of incubation seaason might bee the water tem
376 3
h along the Ryyukyu Islands, but this is no ot definite due to the lack off water whichh loses heat as it flows north
377 3
t locations of the habitats oof crabs. tempeerature data in the
374 3
375 3 376 3
n season amongg islands. Fig. 133. Comparisonn of incubation
377 3 378 3
5 CO ONCLUSION NS
381 3
In thiss study, the life fe history of M. M guinotae in Amparu Tidall Lagoon on Isshigaki Island was investigaated by
382 3
u 50 cm × 50 cm quadraats over a 6-mo onth period off the breeding season in two years. field oobservations using
383 3
major conclusioons are as follows: The m
383 3
Population dennsity was high at the southernn part of the laagoon where th he bed sedimeent was compo osed of (1) P
384 3
fi fine sand and silt s with high ignition i loss. T The male:femaale ratio ranged d from 1:0.88 to 1:1.41, aveeraging
23
383
1:1.20, but the difference in this sex ratio was not significant statistically in each measurement according to
384
the Pearson's chi-squared test. The survival rate of adults (Ta ≥ 1 year) in a year and the mean longevity
385
were estimated as 0.73 and 3.7 years, respectively.
386
(2) Incubation had already started before the first measurement in mid-December, peaked from mid-January to
387
mid-February, and finished in late-March. The size of ovigerous females among total females was larger in
388
the early stage and became smaller with time. Fully matured female had eggs twice: in the early stage as
389
well as at the last stage of the incubation season.
390
(3) Juveniles appeared from March, and their population exceeded that of adults at the peak of settlement in
391
April. In June, juveniles exceeded 6.0 mm in size, at which point sex could be thoroughly distinguished.
392
The time difference between the juvenile settlement and the peak of spawning means that larval life in the
393
ocean was about 2 months. Juvenile population was high on the wide shallow terrace where the flood tide
394
flow stagnates. On the other hand, the adult population spreads to the west and the south, suggesting that M.
395
guinotae migrates after gaining mobility with growth.
396
(4) The ratio of the observed number of juveniles to the number of eggs observed in the female ovary
397
(reproduction efficiency) was 0.0040. On the other hand, juvenile survival rate in a year was estimated
398
from the results of population measurements as 0.17. The reproduction rate became much smaller than the
399
survival rate of juveniles, meaning that the propagation of M. guinotae is mainly controlled by the
400
conditions to which the larvae are exposed in the ocean.
401
(5) The incubation period seems to occur earlier at sites closer to Kyushyu Island and later at the sites closer to
402
Taiwan. The reason for this tendency might be that the Kuroshio Current loses heat as it flows north along
403
the Ryukyu Islands, but it should be proved in field study on habitat conditions.
24
404
ACKNOWLEDGEMENTS
405
We would like to thank Dr. Tohru Naruse, Dr. Takashi Nagai, and Dr. Misuzu Aoki of University of the
406
Ryukyus for their professional advice. We also thank the Yaeyama Office of Okinawa Prefecture for providing
407
us facilities for field measurements. This study was supported by a grant from the RIVER FOUNDATION
408
(grant number, 171241005).
409 410
APPENDIX
411
Table A.1 Breakdown of population sampling data Experiment 1 Measurement
Total
Number of samples Female Male (ovigerous)
Sex indistinctive
Male:female
1-1 1-2 1-3 1-4 1-5 1-6 1-7 1-8 1-9 1-10
72 113 150 81 119 48 105 140 207 222
31 60 63 42 53 21 46 56 49 90
41 (7) 53 (18) 87 (49) 39 (25) 66 (35) 27 (10) 59 (10) 73 (11) 55 (0) 117 (0)
0 0 0 0 0 0 0 11 103 15
1:1.32 1:0.88 1:1.38 1:0.93 1:1.25 1:1.29 1:1.28 1:1.30 1:1.15 1:1.30
Total
1257
510
617 (165)
130
1:1.21
0 0 0 12 150 22 184
1:1.06 1:1.28 1:0.97 1:1.34 1:1.15 1:1.41 1:1.20
Experiment 2 2-1 2-2 2-3 2-4 2-5 2-6 Total
132 169 156 136 253 210 1056
64 74 79 53 48 78 396
68 (12) 95 (56) 77 (44) 71 (23) 55 (0) 110 (0) 476 (135)
412
25
413
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414
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S2352-4855(16)30317-6 http://dx.doi.org/10.1016/j.rsma.2017.05.006 RSMA 249
To appear in:
Regional Studies in Marine Science
Received date: 1 November 2016 Revised date: 8 May 2017 Accepted date: 8 May 2017 Please cite this article as: Kawachi, A., Ishikawa, T., Irie, M., Population dynamics of the soldier crab Mictyris guinotae (Brachyura: Mictyridae) in Amparu Tidal Lagoon on Ishigaki Island, Japan. Regional Studies in Marine Science (2017), http://dx.doi.org/10.1016/j.rsma.2017.05.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1 2
Population dynamics of the Soldier Crab Mictyris guinotae (Brachyura: Mictyridae) in Amparu Tidal Lagoon on Ishigaki Island, Japan
3
A. Kawachi1, T. Ishikawa2, and M. Irie3
4 5 6 7 8 9 10 11 12
1
Token C.E.E. Consultants Co., Ltd, 1-15-6, Kitaohtsuka, Toshima-ku, Tokyo, 170-0004, Japan Tokyo Institute of Technology, 2-12-1 Ookayama, Meguro-ku, Tokyo, 152-8550, Japan 3 Department of Civil and Environmental Engineering, University of Miyazaki, 1-1, Gakuen Kibanadai-nishi, Miyazaki-shi, Miyazaki, 889-2192, Japan 2
Corresponding author: Atsushi Kawachi ([email protected]) Submitted to: Regional Studies in Marine Science on 8th January 2017 Re-submitted to: Regional Studies in Marine Science on 8th May 2017
13 14
ABSTRACT
15
The life history of the soldier crab Mictyris guinotae in Amparu Tidal Lagoon on Ishigaki Island, Japan was
16
investigated through population measurements with detailed size classifications. Surveys and measurements
17
were carried out at 15 sampling points every 2 weeks during the 4-month incubation season starting in
18
December 2005, and twice in April and in June 2006 when juveniles started and finished settlement,
19
respectively, in the lagoon. Supplementary measurements were conducted every month from December 2006
20
to May 2007 to corroborate the results of the first experiment and to examine the growth rate of the juvenile
21
population.
22 23
The results showed that (a) the peak of incubation was from mid-January to mid-February, and the season of
24
juvenile settlement was April to early June, which means that the duration of larval life in the ocean was about 2
25
months; (b) juveniles were distributed widely in the lagoon, and adults clustered to the west and south of the
26
lagoon where the bed sediment was relatively fine with high ignition loss; (c) the survival rates of adults and
1
27
juveniles in 1 year were 0.73 and 0.17, respectively, and the mean longevity of adults was about 3.7 years; (d)
28
reproduction efficiency from eggs to juveniles was about 0.0040, which is much smaller than the survival rate
29
of juveniles as well as adults, which means that the propagation of M. guinotae is mainly controlled by the
30
condition that the larvae experience in the ocean.
31 32 33
KEYWORDS: intertidal crab, life history, breeding season, population sampling, Ryukyu Islands
34 35
1 INTRODUCTION
36
In the intertidal zone ecosystems and material cycles, small crabs are one of the major components, taking in
37
organic detritus from bed sediment (Meziane et al., 2002; Quinn, 1986; Robertson and Newell, 1982; Takagi et
38
al., 2010; Webb and Eyre, 2004), being eaten by higher order organisms like birds (Zharikov and Skilleter, 2004,
39
2003) and aerating bed sediment by burrowing to enhance organic compound decomposition (Otani et al.,
40
2010). Therefore, studying their biology is important to understand the structure of tidal lagoon ecosystems.
41 42
Intertidal crabs have two life stages: larval and benthic. Larvae just after hatching, called zoea, flow out from the
43
tideland to the ocean at ebb tide, return to the tideland as megalopa, the final larval form after moltings, several
44
weeks later on spring tide days (Epifanio and Cohen, 2016) and start benthic life as juvenile crabs. They mature
45
to reproduction after 1 to 2 years of benthic life (Nakasone and Akamine, 1981; Shih, 1995; Yamaguchi, 1976).
46
Beyond this general understanding, the details of their biology in tidelands are species-specific and also depend
47
on the meteorological and hydraulic conditions of each site (Henmi, 1993; Jones and Simons, 1983; Wada,
48
1991; Yamasaki et al., 2010). Thus, there is still much to learn about their biology from field measurements.
2
49 50
Recent DNA analysis has clarified the classification of crab species into several subspecies based on
51
divergences in the evolutionary lineage under different conditions (i.e., Aoki et al., 2012; Naderloo et al., 2016).
52
There are several closely related crabs having common as well as divergent biological characteristics in the
53
Ryukyu Islands, which are located between Kyushu Island of Japan and Taiwan and are isolated from each
54
other by submarine trenches and swift ocean currents (Jan et al., 2002; Lan et al., 2008; Qi et al., 2016).
55 56
Ecological diversity of intertidal crabs, which is induced by isolation and is influenced by the differing
57
conditions of each site’s habitat, can provide hints to understanding the evolutionary process of life on Earth.
58
The basis for research of ecological diversity will be a steady effort to investigate lifecycles and population
59
dynamics of each species in its habitat condition (Costa and Soares-Gomes, 2009; Frith and Brunenmeister,
60
1980; Hines et al., 1987; Hsueh et al., 1993; Litulo, 2005; Mokhtari et al., 2008; Tina et al., 2015).
61 62
In the present study, the life history of Mictyris guinotae, which is an endemic crab species in the Ryukyu
63
Islands, was investigated by sampling populations in the Amparu Tidal Lagoon on Ishigaki Island located near
64
Taiwan. M. guinotae is a subspecies of Mictyris (soldier crab), which is distinguished from the related species,
65
M. brevidactylus, which inhabits Taiwan, Hong Kong, Singapore, and Indonesia (Davie et al., 2010).
66 67
Several field studies in the Ryukyu Islands have clarified that some differences in the characteristics of M.
68
guinotae depend on location. Yamaguchi (1976) reported that the mean size of M. guinotae was significantly
69
larger on Ishigaki Island than on Amami-oshima Island. Nakasone and Akamine (1981) found that the
70
incubation season was from November to February at the mouth of the Okukubi River on Okinawa Island,
3
71
while Kosuge and Kohno, (2010) reported that the incubation season of the same species was from December
72
to February at the mouth of the Urauchi River on Iriomote Island. On the other hand, Shih (1995) reported that
73
the incubation season of M. brevidactylus, a closely related species of M. guinotae, was from January to April
74
based on field experiments in Taiwan. These findings suggest that the biology of intertidal crabs depends not
75
only on species but also on habitat conditions.
76 77
In this study, population structure measurements based on detailed size classifications were carried out every 2
78
weeks during the 4-month incubation season starting in December 2005, and twice in April and in June 2006
79
when juveniles started and finished settlement in the lagoon. Supplementary measurements were conducted
80
monthly from December 2006 to May 2007 to corroborate the incubation season observed in the previous year
81
and to examine the growth rate of the juvenile population. Based on experimental data, seasonal variation of the
82
size distribution, growth probability of eggs to juvenile crabs, growth rate of adult crabs, and generation change
83
rate were analyzed.
84 85
2 STUDY SITE
86
The Ryukyu Islands comprise 34 islands of various sizes extending from Kyushu Island, Japan to Taiwan. The
87
population density of M. guinotae has been previously reported for four islands in this region: Amami-Oshima,
88
Okinawa, Ishigaki, and Iriomote.
89 90
This study was conducted on the west coast of Ishigaki Island in the Amparu Tidal Lagoon in Nagura Bay (Fig.
91
1), which is famous for having a great variety of intertidal crabs; the words of a folk song for community work
92
on the Ishigaki Island includes the names of fifteen kinds of crabs (Ohyama, 1994; Takeda and Ohyama, 1994).
4
95
The laagoon was dessignated as an internationally i y important sitee of the Ramsaar Convention in 2005 owing g to its
96
wl, for which th he intertidal cra rabs are one off major food sou urces. diverssity of waterfow
96 98 99
A Location off the Ryukyu Islands, B: Lo ocation of the Amparu Tidaal Lagoon, C: Aerial Fig. 11. Study site. A: photoggraph image of o the Amparu Tidal T Lagoon.
99 105
8 ha, extendin ng north-southh with the easst side Ampaaru Tidal Laggoon is sand-ccovered with aan area of 18
106
om the ocean by a long san nd spit surrouunded by shalllow mangrovee swamps andd the west sidee separated fro
107
h of the lagoonn is located at the t north end with w a channell 100 m wide and a 50 covereed with oak treees. The mouth
108
hat is about 1 kkm wide. A streeam named thee Nagura River er flows from th he east m lonng extending too a coral reef th
109
w a watersh hed of 15 km2. Two small drainage d chann nels flow out ffrom farmland d and a to the tidal lagoon with
110
ve swamps at thhe east side to the tidal lagoon n. sugar factory througgh the mangrov
106 109
elevation of thee tidal lagoon obtained by an automatic leeveling The ccontour map inn Fig. 2 showss the ground el
110
op sensor. Three T creeks in the lagoon are a formed by the inflows m mentioned prev viously. apparaatus with an optical
111
i the figure inndicate the loccations of statiions for popullation sampling g. The The oopen and closeed rectangles in 5
113
elevattion difference in the lagoon is about 0.5 m m, except at the channel of thee Nagura Riverr. The tide amp plitude
114
pring tide and 00.5 m at a neap p tide. Almost the entire sandd bed area of th he tidal in Naggura Bay is aboout 1.5 m at sp
115
b ocean waterr at high waterr of the even ebb e tide and drried out at low w tide, except for f the lagoonn is covered by
116
three ccreeks.
114
115 116
u Tidal Lagoonn. Fig. 2. Contour mapp of the Amparu
117 121
w and close-uup views of thee surface of thee lagoon at low w tide showing g many The phhotographs in Fig. 3 show wide
122
b intertidal craabs after remooving the nutriients from the sediments: Thhe crabs come to the sand bballs spit out by
123
a low tide and d burrow underrground beforee high tide, leav ving sand ballss behind. The square, s surfacce for feeding at
124
i the 50 cm × 50 cm quadratt for population n sampling. woodeen frame in thee right picture is
122
6
123 125 126
Fig. 3. Ground surfaace condition of o the Amparu Tidal Lagoon.. A: Wide view w. B: Close-up view with a 50 0 cm x 50 cm m quadrate fram me for sampling g.
126 136
und surface seediments are sh hown for six po oints (E3, E4, W W2, W5, S5, and a S7 Grain size and ignitiion loss of grou
137
C sand off a narrow band nd of grain sizee and lower ign nition loss weree observed at E3 E and in Figg. 2) in Fig. 4. Coarse
138
which are locateed at the north heast part of thhe lagoon. At W2 W and W5 lo ocated on the nnorthwest part of the E4, w
139
p of sediment s was coarse sand, but b a small am mount of fine silt was preseent and lagoonn, the major proportion
140
he lagoon, in contrast, c the m major componen nt was ignitioon loss was higgh. At S5 and S7 at the soutthern part of th
141
meter with a w wide range of silt, which had high ignitionn loss. Wada (1982) fine saand around 2000 μm in diam
142
ment in sand ba balls made by two kinds off small intertiddal crabs, Scop pimera analyzzed the grain size of sedim
143
globosse and Ilyoplaxx pusilla, and reported r that thhey preferred fine f sand of 63 3 to 125 μm inn diameter for taking
144
he southern parrt of Amparu Tidal Lagoon is more suitab ble for nourisshment. Thereffore, it is conssidered that the
145
wth of small inteertidal crabs thhan the northern n part. suppoorting the grow
137
7
138 139
Fig. 4. Grain size annd ignition loss of ground surfface sediment
140 145
position based on a survey carried c by Irie et al. (2005). M M. guinotae was w the Fig. 5 shows the poopulation comp
146
b Scopimera ryukyuensis, th he remaining species s being ppresent only in minor most ddominant speccies, followed by
147
ortions. S. ryukyyuensis is an in ntertidal crab thhat is classified d in genus Scop pimera in the ffamily Dotillid dae and propor
148
he most domin nant crab specie ies in total volu ume as is mucch smaller thann M. guinotae.. Therefore, M. guinotae is th
149
well aas in populationn on the Amparru Tidal Lagooon.
146
8
147 148
c in the Am mparu Tidal Laagoon (Irie et all., 2005). Fig. 5. Major speciess of intertidal crabs
149 150
3 ME ETHOD
151
3.1 Sampling
161
Popullation samplingg was conducted over two peeriods from December D 2005 to July 2006 and December 2006
162
wn in Fig. 6, which w nearly coovers the seaso ons from incub bation to juvennile settlement.. In the to Maay 2007 as show
163
mpling was caarried out at loow tide just before b each sprring tide from m December 20 005 to first eexperiment, sam
164
cause spawning g tends Marchh 2006 in ordeer to investigatee the incubatioon of females; this timing waas selected beca
165
fter approximat ately 1 month of incubation (Nakasone annd Akamine, 1981). to occcur on a sprinng tide day aft
166
w conducted d to determine the settlementt and growth of o juvenile crabbs in April and d June Anothher sampling was
167
s was cconducted eveery month from m December 22006 to June 2007 2 in 2006. In the secondd experiment, sampling
168
riment regardin ng incubation timing t and to cclarify the settllement order to corroboratee the results of the first experi
169
niles. Samplinng points weree in common to t the two expperiments with h three duratioon and growthh rate of juven
170
ment to balancee the sampling distribution, d ass shown in Fig. 2. additioonal sampling points in the seecond experim
162
9
163 164
s and thee times of meassurements. Fig. 6. Tide level reccord (Ishigaki station)
165 173
w an averagee spatial densitty distribution of sand ball ppiles was samp pled by At eacch sampling pooint, an area with
174
5 cm quadratee frame on thee ground and collecting bed sediment s to a ddepth of 30 cm m from placinng a 50 cm × 50
175
g fine sedimennt by sieving through t a 2 mm mesh, crabss were picked up by insidee the frame. Affter eliminating
176
on in reference to illustrationss in the hand oor with tweezeers and identified to the speciies level by vissual observatio
177
1 The len ngth and widthh of carapace (hereafter, CL L and CW) weere measured for M. literatuure (Takeda, 1978).
178
guinottae using a Veernier scale. Th he sex of each crab was recorded for each adult a based onn visual inspecttion of
179
men, while juve venile crabs weere too small to o distinguish thhe generative organs. o the geenerative organns at the abdom
180
her they carried d eggs. Ovaryy condition wass inspected forr females to dettermine wheth
174 175
3.2 D Data Processiing
176
3.2.1 Seasonal channges in populaation density
180
First, tthe correlationn between CL and a CW was exxamined, and only o CL was adopted a as a sizze indicator baased on
181
L and CW (corrrelation coeffi ficient, r = 0.96 6). Then, valuees of CL were sorted high llinear correlatioon between CL
182
opulation denssity at each sam mpling with 00.5 mm intervaals to constructt a size histogrram of populattion density. Po
183
ment time point are written as follows: point aand measurem 10
180
Population density: Pi , j ,k 4 Ni , j ,k
(1)
181
where N is the number of crabs collected in the quadrat, P is the population density (individuals/m2), i is the size
182
band number, j is the sampling point number, and k is the measurement time number.
183 184
However, because the histogram for each set of (i, j, k) was unstable due to the limited number of samples in
185
each band width, tendencies of the space distribution and time variation were investigated separately as follows:
186
First, the population density of each size band, i, was averaged over the entire area of the lagoon to find the
187
tendency of seasonal population dynamics.
188
Pm (i, k )
1 M
M Pi , j , k j 1
(2)
189
where M is the number of sampling points, and Pm (i, k) is the size distribution histogram averaged over the
190
entire area of the lagoon at time k.
191 192 193
Further, the normalized population density at each measurement time point was defined as follows: I
(3)
Qm (i, k ) Pm (i, k ) / Pm (i, k ) i 1
194
where I is the number of size bands and Qm (i, k) is the normalized size distribution histogram at time k, the
195
integral of which over all size bands is unity.
196
3.2.2 Spatial population distribution in the tidal lagoon
197
As will be shown later, the normalized histograms had a clear nodal point in the season of juvenile settlement,
198
and juvenile crabs (age; Ta < 1 year)” were separated from “adults (Ta ≥ 1 year)” using the position of the
199
nodal point as a threshold. Then, the population density of adults was averaged over the measurements before
200
the season of juvenile settlement to examine the spatial distribution of crabs, which settled earlier than in the
201
previous years. On the other hand, the spatial distribution of juveniles was represented by the results of the last
11
202 203
measurement when the juvenile settlement was nearly ended, PAd ( j )
I KS 1 1 Pi , j , k for adults KS 1 i 1 k 1 I
PJu ( j ) Pi , j , k KT
(4)
for juveniles
i 1
204
where KS indicates the time at which juvenile settlement started, and KT indicates the time of the last
205
measurement. PAd (j) and PJu (j) show the spatial distributions of populations for the adult and juvenile groups,
206
respectively.
207 208
3.2.3 Generation change rate
209
A nodal point was also observed in Pm (i, k) obtained before the season of juvenile settlement (k < KS), and the
210
population of adult group was further divided into the younger group (Ta = 1 year) with Pm (1) and the older
211
group (Ta > 1 year) with Pm (>1), using the nodal point as the threshold,
212
Pm (1)
KS 1 k 1
Pm ( 1)
213
In
P (i, k ) i 1
KS 1
(5)
m
I
P (i, k ) k 1
i In 1
m
where In is the value of CL at the nodal point.
214 215
Assuming a constant death rate over the year for crabs of all ages except juveniles, the following relationship
216
would be observed:
217
(6)
Pm (n 1) rPm ( n)
218
where Pm (n) is the population with age of n, and r is the rate of survival in a year. By summing the series at each
219
side from n=1 to infinity, we obtain the following relationship:
220 221
(1 r ) Pm ( 1) rPm (1)
(7)
Using the above equation, the survival rate in 1 year, r, and the average longevity of M. guinotae were estimated
12
222
from observation results as follows:
Pm ( 1) Pm (1) Pm ( 1)
223
r
224
Lm m r m 1 / r m 1
225
m 1
m 1
(8) 1 1 Pm ( 1) / Pm (1) 1 r
(9)
where Lm is the average longevity.
226 227
On the other hand, the survival rate of juvenile was obtained from the observed result: M M M M Pm (1) r (0) PAd ( j ) / PJu ( j ) (1 r ) PAd ( j ) / PJu ( j ) j 1 j 1 j 1 Pm (1) Pm ( 1) j 1
228
(10)
229
where r(0) is the survival rate of juvenile; the numerator is the population of the younger adults (Ta = 1 year)
230
observed before the season of juvenile settlement, and the denominator indicates the population of juveniles at
231
the end of the season of settlement.
232 233
3.2.4 Reproduction efficiency
234
Only a small proportion of eggs in the female ovary reach the stage of juvenile crabs due to losses of larvae at
235
stages before flowing out to the ocean, during metamorphosis at ocean, on the return trip to the lagoon, and
236
during the process of landing. The reproduction efficiency of M. guinotae was calculated from the data as
237
follows:
238
Erep
1 M
M
P j 1
Ju
( j)
(11)
TN egg
239
where Erep is the reproduction efficiency, the numerator is the average population density of juveniles calculated
240
by Eq. 4, and TNeeg in the denominator is the spatially average number of eggs produced per unit area in a
241
breeding season.
242
13
243
Nakasone and Akamine (1981) reported the following relationship between the number of eggs and the
244
carapace length, CL, for ovigerous females from field observations on Okinawa Island:
245 246
N egg 1.389 CL3.2746
(12)
where Negg is the number of eggs carried in the ovary of a female.
247 248
Writing the spatially averaged population density of ovigerous females whose CL is in the ith size band as
249
PFOm,(i, k) in the same way as for Eq. 2, and assuming that the observed female spawns eggs at the spring tide
250
day after a 1-month incubation, TNegg can be calculated by the following equation because the measurement
251
was carried out every spring tide during the incubation season:
252
KS 1 I TN egg 1.389 CL3i .2746 PFO m (i , k ) / 2 k 1 i 1
(13)
253
where CLi is the CL value of the ith band size, and KS is the measurement time point at the end of incubation
254
season. The factor 1/2 was multiplied because the measurement frequency was twice in a month, while the
255
spawning was assumed as being after 1-month incubation.
256 257
4 RESULTS AND DISCUSSION
258
4.1 Seasonal Change in Population Density
259
The total corrected number of M. guinotae was 1,257 for the 10 measurements at 15 stations and 1,056 for 6
260
measurements at 18 stations in the first and second experiments, respectively. Average population density for the
261
duration of each of the two experiments was 34.0 and 39.1 individuals/m2, respectively. The male:female ratio
262
was 1:0.88 at a minimum and 1:1.41 at a maximum, and the average was 1:1.20.
263 264
Fig. 7 shows the normalized size distribution for each measurement, Qm (i, k) expressed by Eq. 2, and
14
265
incubation progress over time is plotted in Fig. 8. Incubation already started just before the first measurement in
266
mid-December, peaked from mid-January to mid-February, and finished at the end of March. The size of
267
ovigerous females among all females was larger in the early stage of the incubation, and gradually, participation
268
of smaller females increased. From mid-January to mid-February, almost 100% of the largest group was
269
ovigerous, and some of the large group had a second clutch in mid-March. This tendency was more distinctly
270
observed in the second experiment, suggesting that fully matured females had eggs twice, as was observed by
271
Henmi and Kaneto (1989) for another intertidal species: Scopimera globose, Ilyoplax pusillus and
272
Macrophthalmus japonicus on Hakata Bay in the north of Kyushu Island.
273 274
Juveniles appeared from mid-March, and had a size of around 3 mm. The red vertical arrows in each figure
275
after March in Fig. 7 indicate the node of size distribution, which was considered to separate the juvenile group
276
from the adult group. The number of juvenile members increased with time, and in April, the juvenile
277
population exceeded that of adults which had settled in the lagoon in previous years. In June, juveniles grew to
278
exceed 4.5 mm in size, at which point sex could be distinguished.
279
15
281 2 285 2 286 2 287 2 288 2
Fig. 77. Seasonal variation v in siize distributioon of normaliized populatio on density. Fiigures are arrranged chronoologically from m top to bottom m for each expperiment. Malle and female sizes are plotteed above and below, respecctively, the horrizontal axis off each graph; oovigerous fem males are repressented by filledd bars; and juv veniles that w were too small to t distinguish th he sex are marrked in gray an nd divided even nly above and bbelow the axiss.
16
286 2 289 2 290 2 291 2
Fig. 88. Seasonal varriation in the proportion p of oovigerous fem males. Dotted red lines indicaate the proporttion of ovigerrous female too the total female, and the hoorizontal bar graphs g indicatee the size distriribution of ovig gerous (blackk) and non-oviggerous female (white) in CL.
290 2 292 2
p den nsity at each m measurement time t point, Pm (i, k), in Eq.. 2 was divideed into Spatiaally averaged population
293 2
ws: juveniile and adult grroups as follow
293 2
Id Pm j (k ) Pm (i, k ) Juvenile grouup i 1 I Pm a ( k ) Pm (i, k ) Adult group i Id 1
(14)
296 2
wheree Id is the thresshold to separaate the two grouups indicated by b the red arrow ws on the grapphs (after mid-M March
297 2
y of these two groups shown n in Fig. 9 ind dicates that thee juvenile popu ulation in Figg. 7). The popuulation density
298 2
a became alm most steady inn June, while th he population of adults decre reased graduallly. The increaased in April and 17
299 2
time oof juvenile settllement was about 2.5 monthhs after the peak k of incubation n shown in Figg. 8, meaning th hat the
300 2
larval life of M. guinnotae in the ocean has a duraation of about 2 months with a lag of about 0.5 months beetween
301 2
spawnning and incubbation.
300 2 304 3
k nodal points of Qm (i, k) caan also be seen n before April, as indicated by b blue In Figg. 7, on the othher hand, weak
305 3
ws, when juveni nile settlement did d not yet star art. In the size distribution d av veraged for all m measurement results arrow
306 3
December to February F beforre juvenile settttlement (Fig. 10), 1 a clear no ode can be seenn, and the left group from D
307 3
y populaation, Pm (1), annd the right corrresponds to th he older populaation, Pm (>1). corressponds to the younger
305 3
306 3 307 3
Fig. 9. Seasonal variiation in juveniile and adult poopulation densities.
18
308 3 309 3
Fig. 100. Size distribuution of populaation density beefore juvenile settlement. s
310 3
316 3
h group at arou und 7.0 and 111.0 mm, respecctively, Smooothed curves foor Pm (1) and Pm (>1) place thhe peak of each
317 3
5.5 mm, respecctively. Taking g the peaks and d the largest of C CL of juvenilee group with thhe largest arouund 10.0 and 15
318 3
ment in Fig. 7, we w obtain a meeasure of growtth rate based on n CL (Fig. 11),, for which thee origin for evvery measurem
319 3
me on the horizoontal axis of th he logarithmic sscale was assum med to start at the end of Febbruary, and the age of of tim
320 3
w assumed to t be in a rangge from 2 to 4 years becausee they could no not be separated. The the Pm (>1) group was
321 3
n inverse propo ortion to time. lineariity of the carappace size indicaates that the groowth shows an
317 3
Growthh rate
d (CL ) a dtt t
(15)
19
318 3 320 3 321 3
Fig. 11. Increase in carapace c length h, CL. Black m means juvenilees; blue means young adults ((Ta =1 year); and a red meanss older adults (T ( a >1 year).
321 3
322 3
4.2 Sppatial Populaation Distribu ution
328 3
The hhistograms of teemporally averraged populatiion density of juveniles j and adults a at each ssampling pointt using
329 3
r expressed by E Eq. 4 and plottted on a map of the lagoonn (Fig. 12) sho ow that PJu (j)) and PAd (j), respectively,
330 3
ntrated around d 24°23'50''N w where shallow terrace t juveniiles settled in a wide range off the lagoon, buut were concen
331 3
de flow. On thee other hand, th he adult population was low w at the northeaast part widenning might staggnate flood tid
332 3
l (Fig. 4), annd spread to thee west and the south from thee area where ju uvenile wheree sediment igniition loss was low
333 3
ment was conccentrated. settlem
329 3 332 3
w controlled d by the hydrauulic characterisstics at Thesee data suggesteed that the spattial distributionn of juveniles was
333 3
me of settlemeent, while the adults migrateed to areas wh here the ground d was coveredd with nutritiou us fine the tim
334 3
ment. sedim
20
333 3 334 3
Fig. 122. Spatial distrribution of (A) juvenile j groupp and (B) adult groups.
335 3 336 3
4.3 G Generation Chhange Rate
342 3
As shhown in Fig. 10, 1 there was a nodal point around 8.5 mm m in CL for samples colleected before ju uvenile
343 3
ment, and the CL C value was used u as the thre reshold to sepaarate the adults into the youngger group that settled settlem
344 3
a the older grroup (Ta > 1 yeear), the populaations of whichh are described d as Pm in the previous year (Ta = 1 year) and
345 3
o of Pm (1) and d Pm (>1) was eestimated to bee about (1) to Pm (>1), respeectively, in Eq. 5. From the Fiig. 10, the ratio
346 3
was calculated as a 0.73 from Eq. E 8, and the mean longevitty was 1:2.7. Therefore, thee survival rate over a year w
347 3
calcullated as 3.7 yeaars from Eq. 9.
343 3 346 3
w assumed in this study, there t was a po ossibility of theeoretical immo ortality, Becauuse a constant survival ratio was
347 3
here must be a limit to the lifeespan of the inntertidal crabs. Nakasone and d Akamine (19981) reported th hat the but the
348 3
o in thee mouth of the Okukubi Riveer on Okinawaa Island lived loonger than 3 yeears. If oldestt M. guinotae observed
21
346
we assume that all of the 3-year-old population would die in the following year, Eq. 7 and Eq. 9 can be modified
347
as follows:
348
Pm ( 1) (r r 2 r 3 ) Pm (1)
(16)
349
Lm (1 2r 3r 2 4r 3 ) /(1 r r 2 r 3 )
(17)
350
From these equations, survival rate r and mean longevity Lm become 0.96 and 2.44 years, respectively.
351 352
This discussion applies to the adult group population. The survival rate of juveniles must be smaller due to less
353
physical strength and mobility. Using the values of juvenile population observed in June 2006 and the
354
population of the young adult group (Ta = 1 year) averaged over the term from December to February, the
355
juvenile survival rate r (0) was estimated as 0.17 form Eq. 10.
356 357
4.4 Reproduction Efficiency
358
Using Eq. 13, the average density of eggs produced in a unit area of the lagoon during the incubation period,
359
TNegg, was 10,270 individuals/m2. Substituting this value into Eq. 11, a reproduction efficiency of 0.0040 was
360
obtained, which was much smaller than the survival rate of juveniles. Therefore, it can be said that the
361
propagation of M. guinotae is mainly controlled by conditions that larvae experience in the ocean.
362 363
4.5 Range of Incubation Season in the Ryukyu Islands
364
In Fig. 13, the incubation season for M. guinotae on Ishigaki Island is compared with previous reports of those
365
observed at various locations, including M. guinotae on Okinawa Island and Iriomote Island, and M.
366
brevidactylus, which is a closely related species of M. guinotae, in Taiwan. The site locations line up along the
367
Ryukyu Islands from Kyushu Island to Taiwan (Fig. 1), and the incubation seems to occur earlier at sites closer
22
373 3
to Kyuushyu Island and a later at the sites closer too Taiwan, but th here is no marrked differencee between incu ubation
374 3
w are locaated in very cllose proximity y to each otherr (see Fig. 1-A A). The on Ishhigaki and Irioomote islands which
375 3
mperature of thhe Kuroshio Current, C reasonn for the spatiaal variation of incubation seaason might bee the water tem
376 3
h along the Ryyukyu Islands, but this is no ot definite due to the lack off water whichh loses heat as it flows north
377 3
t locations of the habitats oof crabs. tempeerature data in the
374 3
375 3 376 3
n season amongg islands. Fig. 133. Comparisonn of incubation
377 3 378 3
5 CO ONCLUSION NS
381 3
In thiss study, the life fe history of M. M guinotae in Amparu Tidall Lagoon on Isshigaki Island was investigaated by
382 3
u 50 cm × 50 cm quadraats over a 6-mo onth period off the breeding season in two years. field oobservations using
383 3
major conclusioons are as follows: The m
383 3
Population dennsity was high at the southernn part of the laagoon where th he bed sedimeent was compo osed of (1) P
384 3
fi fine sand and silt s with high ignition i loss. T The male:femaale ratio ranged d from 1:0.88 to 1:1.41, aveeraging
23
383
1:1.20, but the difference in this sex ratio was not significant statistically in each measurement according to
384
the Pearson's chi-squared test. The survival rate of adults (Ta ≥ 1 year) in a year and the mean longevity
385
were estimated as 0.73 and 3.7 years, respectively.
386
(2) Incubation had already started before the first measurement in mid-December, peaked from mid-January to
387
mid-February, and finished in late-March. The size of ovigerous females among total females was larger in
388
the early stage and became smaller with time. Fully matured female had eggs twice: in the early stage as
389
well as at the last stage of the incubation season.
390
(3) Juveniles appeared from March, and their population exceeded that of adults at the peak of settlement in
391
April. In June, juveniles exceeded 6.0 mm in size, at which point sex could be thoroughly distinguished.
392
The time difference between the juvenile settlement and the peak of spawning means that larval life in the
393
ocean was about 2 months. Juvenile population was high on the wide shallow terrace where the flood tide
394
flow stagnates. On the other hand, the adult population spreads to the west and the south, suggesting that M.
395
guinotae migrates after gaining mobility with growth.
396
(4) The ratio of the observed number of juveniles to the number of eggs observed in the female ovary
397
(reproduction efficiency) was 0.0040. On the other hand, juvenile survival rate in a year was estimated
398
from the results of population measurements as 0.17. The reproduction rate became much smaller than the
399
survival rate of juveniles, meaning that the propagation of M. guinotae is mainly controlled by the
400
conditions to which the larvae are exposed in the ocean.
401
(5) The incubation period seems to occur earlier at sites closer to Kyushyu Island and later at the sites closer to
402
Taiwan. The reason for this tendency might be that the Kuroshio Current loses heat as it flows north along
403
the Ryukyu Islands, but it should be proved in field study on habitat conditions.
24
404
ACKNOWLEDGEMENTS
405
We would like to thank Dr. Tohru Naruse, Dr. Takashi Nagai, and Dr. Misuzu Aoki of University of the
406
Ryukyus for their professional advice. We also thank the Yaeyama Office of Okinawa Prefecture for providing
407
us facilities for field measurements. This study was supported by a grant from the RIVER FOUNDATION
408
(grant number, 171241005).
409 410
APPENDIX
411
Table A.1 Breakdown of population sampling data Experiment 1 Measurement
Total
Number of samples Female Male (ovigerous)
Sex indistinctive
Male:female
1-1 1-2 1-3 1-4 1-5 1-6 1-7 1-8 1-9 1-10
72 113 150 81 119 48 105 140 207 222
31 60 63 42 53 21 46 56 49 90
41 (7) 53 (18) 87 (49) 39 (25) 66 (35) 27 (10) 59 (10) 73 (11) 55 (0) 117 (0)
0 0 0 0 0 0 0 11 103 15
1:1.32 1:0.88 1:1.38 1:0.93 1:1.25 1:1.29 1:1.28 1:1.30 1:1.15 1:1.30
Total
1257
510
617 (165)
130
1:1.21
0 0 0 12 150 22 184
1:1.06 1:1.28 1:0.97 1:1.34 1:1.15 1:1.41 1:1.20
Experiment 2 2-1 2-2 2-3 2-4 2-5 2-6 Total
132 169 156 136 253 210 1056
64 74 79 53 48 78 396
68 (12) 95 (56) 77 (44) 71 (23) 55 (0) 110 (0) 476 (135)
412
25
413
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