process of growth,migration,and reproduction of middle-and

Benthos Research Vol.58,No.2:87-104(2003)

BENTHOS

RESEARCHThe Japanese Association of

Benthology

Process of Growth,Migration,and Reproduction of Middle-and Large-sized

Japanese Mitten Crab Eriocheir japonica(de Haan)in a Small River

and its Adjacent Sea Coast

Satoshi Kobayashi

Abstract:I investigated the process of growth, migration, and reproduction of the Japanese mitten crab Eriocheir japonica in the Saigo River,Fukuoka Prefecture,Japan.Samples were collected by hand-held nets in the lower freshwater,tidal river,and sea coast areas.Above the upper tidal river area,males and juvenile females appeared nearly all year round,but adult females only from August to February.Exuviae and postmolt crabs were collected only in this area,from March to November.Below the middle tidal river area,adult females of>38mm CW and males of>28mm CW appeared from September to June.Duration of occurrence was longer in the lower tidal river and sea coast areas than in the middle tidal river area.In the lower tidal river and sea coast areas, postcopulatory guarding pairs were collected in December,January,and March,and ovigerous females appeared from October to the following June.Carcasses(>38mm CW and>34mm CW for females and males,respectively)were collected mostly in the tidal area.Therefore,growth molts of juvenile crabs appeared continuously except in the winter season,and the puberty molt to the adult stage from August to November,mainly in the freshwater area.Adult crabs migrated downstream from September to February,and reproduction took place mainly in the lower tidal river and sea coast areas.

Key words:Japanese mitten crab,Eriocheir japonica(de Haan),molting growth,catadromous migration,reproduction,death of crab,life history process.

INTRODUCTION

The Japanese mitten crab Eriocheir japonica(de Haan)is a grapsid crab distributed in Sakhalin, eastern Korea,the entire Japanese archipelago, and Taiwan(Miyake1983).This crab is a common large,benthic species

(large ones are usually over70mm in carapace width),widely distributed from the upper reaches of rivers to tidal river estuaries and sea coast areas.It is a catadromous species,migrating from the freshwater area of rivers to the sea for copulation and oviposition

(Kobayashi&Matsuura1991;1995a;1995b;Kobayashi1999).Additionally,this crab is an important fishery tar

get in many Japanese rivers and its population has been exposed to strong fishing pressure.Many fishermen in these rivers are worried about the decrease in E.japonica

populations owing to the effects of the fishing,and several experimental stations and fishery associations carry out restocking management programs including seed

production and the release of young crabs(Kobayashi et al.1997).Research on the life history process(e.g.,

growth,reproduction,and migration)of E.japonica is urgently necessary for their effective management in many Japanese rivers.

Various freshwater species of brachyuran crab have

been recorded throughout the world.Aside from

potamonids and some gecarcinids and grapsids,they spend their larval stages in the marine environment.Con

sequently,they migrate between the sea and freshwater

or terrestrial habitats over short or long distances [e.g.,

Received December24,2002:Accepted August4,2003

87

Kobayashi

Gecarcoidea natalis(Pocock):Adamczewska&Morris(2001);for a review,Anger(1995);see also Kobayashi

(2000)].The migration process of diadromous species similar to E.japonica has been poorly reported.The Chinese mitten crab Eriocheir sinensis H.Milne Edwards is also catadromous and was originally distributed in China and western Korea.This species is an important and traditional fishery target in China and has been widely cultured and stocked in ponds or lakes(Jin et al.2001).It has also invaded many countries in Europe and North America;actively moving along the rivers and sea coast,E.sinensis has spread widely in these areas since the be

ginning of the20th century(Peters&Panning1933;Nepszy&Leach1973;Cohen&Carlton1997;Clark et

al.1998).After the1990's,this species resumed its active population growth and dispersal,and investigations into the dispersion process within its life cycle and im

pacts on native ecosystems have been undertaken again in the invaded countries(Anger1991;Cohen&Carlton1997;Clark et al.1998).Two congeneric species of E.sinensis,E.japonica and E.hepuensis Dai are distributed only in East Asia(Guo et al.1997),and ecological information on these mitten crabs(e.g.,concerning migration or the dispersion process)is in demand for the control and extermination of E.sinensis population in these countries.

Kobayashi&Matsuura(1991)have already re

ported the outline of the distribution and migration process of E.japonica along a river,based on trap data.However,the crabs collected by traps were limited to larger sizes(ca.>25mm carapace width,CW)within the total size range of the population(ca.2-85mm CW:Kobayashi&Matsuura1991;Kobayashi1998).The larger size range was suitable for investigating the process of maturation and reproduction(Kobayashi&Matsuura1991,1995b,1995c),but not for elucidating the whole ecology of the postlarval stages and the population structure of this species within the riverine environment.Combining other sampling data using different methods was necessary to solve the problem.Collecting by hand or by using hand-held nets is not as efficient as methods that rely on traps for gathering large numbers of large crabs distributed at low densities with cryptic habits,hiding under large rocks,but they are effective for

younger crabs in shallow rivers,and the result possibly reflects the natural distribution pattern(Kobayashi&Matsuura1991).

Within the habitat of mitten crabs,the tidal river area(estuary)is a transitional area from the freshwater

phase to the marine phase during the catadromous migration process.Diadromous animals,including mitten

crabs,are exposed to drastic changes of salinity and

other environmental factors in this area.I have studied

the reproductive ecology of E.japonica(process of mat

ing,oviposition,embryonic development and hatching,

and death after reproduction)along the open coast

(Kobayashi&Matsuura1994a,1995a;Kobayashi

1999).It is now evident that the tidal river area(estu

ary),as well as the sea,is an important reproductive area

for mitten crabs(Morita1974,Kobayashi&Matsuura

1991),but it has remained unclear how adult mitten

crabs behave in this area after their downstream migra

tion and where the main reproductive area is within the

wide tidal area.The behavior of crabs in the tidal area

also may explain the relationship between the freshwater

and marine phases in their life history,and the degree of

interchange between populations in different rivers.It

was necessary to investigate the occurrence pattern of

adult crabs within a wide tidal area(upper to lower tidal

reaches of a river and the adjacent sea coast).

Thus I carried out sampling by hand and hand-net in

the lower freshwater area and tidal area of a small river

and along the adjacent sea coast.Using the data ob

tained,I have already reported the occurrence of

megalopa larvae and unsexed small juveniles of carapace

width(CW)<10mm(Kobayashi1998);megalopa lar

vae settled in the upper reaches of the tidal river area and

metamorphosed to the crab stage in this region.First

instar crabs were of nearly2mm CW,and after growing

to at least3.6mm CW,the crabs began to migrate up

stream and reached the freshwater area.In the present

paper,I report the growth and migration pattern of sexed

medium-size and large crabs(CW ca.8mm or more)

and infer the whole life process of E.japonica.

MATERIALS AND METHODS

Study area

The study area was the lower-most2km of the Saigo

River and the adjacent sea coast,in Fukuma Town,

Munakata County,Fukuoka Prefecture,Japan(33•K46'

N, 180•K30' E,Fig.1).The main stream of the Saigo

River is nearly6km long,running through paddy fields

and the residential area of Fukuma Town,into the open

coast of the Genkai-nada.Preliminary surveys in this

river suggested that E.japonica was not as abundant in

the upper region as in the lower region,so collections

were made only in the lower region in the present sur

vey.Seven sampling stations were established as follows

(Fig.1):Stn1,intertidal and shallow subtidal zones of

the sea coast near the river mouth on both the north and

88

Life shistory of the Japanese mitten crab

south sides;Stn2,the lower tidal river area near the river

mouth;Stn3,middle tidal river area;Stn4,upper tidal

river area between the extreme high water of spring tide

and the extreme high water of neap tide in this river.

Thus Stn1-4are in the tidal area,whereas Stn5-7are

further upstream in a freshwater area.The channel width

of the river within the study site was3-20m.At the

upper limit of Stn4,there is a weir,which is nearly50

cm high with a fishway made of concrete(about3m

wide and6m long).At the upper limit of Stn6,a con

crete weir nearly 1m high is present.This weir has nofishway,and it was covered with green algae Spirogyra

sp.The substrate type was sand and pebbles at Stn1,

sand and mud at Stn2,3,and5,sand,mud,and concrete

at Stn4,and sand,mud,and clay at Stn6and7.

Kobayashi(1998)gives further description of the sta

tions.

The salinity(psu)of the interstitial water during

ebb tide(within the uppermost5cm of the bottom sedi

ments,measured using a specific gravity meter)was O

(Stn5,6,and7),0-4(Stn4),6-12(Stn3),14-18

(S-2),and26-30(Stn1).The salinity of the river

and sea water during the low water of ebb tide(in the

uppermost5cm of the water column)was O(Stn3,4,

5,6,and7),＜5(Stn2),and26-29(Stn1)

(Kobayashi1998).During the high water of spring tide,

high salinity(＞18)was observed from Stn2to Stn4in

the deep layer of the water　 column(within10cm above

the substratum).Thus the tidal river area of the　 Saigo

River is considered to be of the weakly mixed type

(Okuda1996),and a salt wedge invades the tidal river

area,reaching Stn4during high water of the spdng tide.

The water temperature at Stn4varied from

(January)to30.0℃(August)during the sampling Pe

riod.It was lower than10.0℃from December to Febru

ary(Kobayashi1998).

Within the study site,organically polluted water al

ways flows into the Saigo River from its tributaries and

the surrounding residences and paddy fields;mud in re

duced condition was widely distributed and Sphaerotilusspp.grew and covered a large part of substratum in the

freshwater area and the upper tidal river area(Stn4-7),

particularly in winter(December-February).Traps are set by amateur fishermen in several parts of the river to

catch large mitten crabs,especially in autumn,and I

oten encountered fishermen catching mitten crabs with

hand-held nets within the study site.

Sampling

Sampling of Eriocheir japonica was conducted at all

1300巳

340N

～

≠

3km-一

漁誹轟踊、叢

StnIwel「weirStn2Stn3

… 慧瓢蘭 ≠

500m

口F・e・hw・t・・111111

Fig.1.Map showing the collection sites.

sampling stations mainly during the daytime of spring

tide twice a month(once a month only in August1996)

from June,1996,to September,1997(sampling1).

From October,1997,to May,1998,E.japonica was col

lected only from the seacoast to the middle tidal river

area(Stnl-3)one to three times a month(sampling

2).At the tidal river stations,sampling was conducted

during the ebb tide.During sampling2,sampling was

done only on sunny and windless days when the sea was

calm,because mitten crabs are comparatively active and

easy to catch in the sea on such days.The sampler wear

ing waders searches each site for about half an hour.Mit

ten crabs hiding under rocks were captured using a hand

held net(mesh size1.0mm)by kicking and tuming over rocks,both under water(in all area)and above the

water line(only in the intertidal area).Crabs buried in

the substratum and those wandering about were also col

lected.When crabs engaged in mating behavior(copula

tion or guarding behavior)were collected,this fact was

recorded.The water depth of the sampled areas ranged

from 0cm(exposed,intertidal zone at tidal stations)to

60cm regardless of the amount of flowing water.

Carcasses and exuviae were also collected during

sampling 1except in June and July,1996.Carcasses and

exuviae decay rapidly under water;the exoskeleton be

comes brittle and within7-10days it becomes impossible to measure its size,even in the laboratory;further

more,birds(e.g.,crows and gulls)often peck and break

carcasses into pieces along the sea coast(Kobayashi

89

Kobayashi

unpublished).Dead crabs can thus be assumed to have

been alive no later than several days prior to observation.

The maximum carapace width(CW)of crabs,both

living and dead,was measured using a vernier caliper.

They were sexed in the field according to the shape of

the abdomen.Crabs of<8mm CW were difficult to sex

accurately by naked eye and were scored as unsexed ju

venile crabs.Only the data for sexed crabs were used for

analysis in the present paper;the results for unsexed ju

veniles were reported by Kobayashi(1998).Female

crabs were categorized into juveniles and adults,based

on the morphological difference of the abdominal seg

ments;the abdomens are nearly triangular and the edges

of the thoracic sterna are exposed in juveniles whereas

the abdomen is nearly oval and all parts of the thoracic

sterna are covered by the abdomen in adults(Kobayashi

&Matsuura1992).Occurrences of soft-shell crabs just

after molting(Stages A and B)(Sather1966;O’

Halloran&O’Dor1988)were also noted during sam

pling l.Live crabs were released at each collection site

after measurement,and carcasses and exuviae were bur

ied in the ground at each site after breaking the cara

paces.

RESULTS

Sampling1

At Stn1-3,live crabs including47females and75males and dead crabs including166females and 149

males were collected only from September,1996,to

June,1997.No exuviae or soft-shell crabs were collected at these stations.The female crabs were all adults of37.5

-69.5mm CW,including both non-ovigerous(22live

and138dead)and ovigerous ones(35live and28dead)

(Fig.2).Ovigerous adults of38.5-63.2mm CW were

collected from October,1996,to June,1997,Only at Stn

Table1.Comparisons of carapace width in Eriocheir japonica

collected in the tidal river area of the Saigo River,among three

intervals in1996-1997,using the Mann-Whitney U-test.

Months Sex Nl,N2 U p

Sep.-Oct.vsFemale6,84105<0.05

Nov.-Feb.Malel3,102148<0.01

Sep.-Oct.vsFemale6,132137<0.01

Mar.-Jun.Male13,112113<0.Ol

Nov.-Feb.vsFemale84,1324,737>0.05

Mar.-Jun.Male102,1125,304>0.05

1 and2.At Stn3crabs were collected only from Novem

ber to December,1996,but from September,1996,to

June,1997,at Stn1and2.Male crabs,including75live

and149dead ones,were of28.5-78.9mm CW(Fig.3).

At Stn3,crabs including dead ones were collected only

from September,1996,to February,1997,but they were

collected from September,1996,to June,1997,at Stn1

and2.For both sexes,crabs collected from September10

to October25,1996,were larger than those collected

later;mean±SD of CW(mm)was58.1±8.5and

60.2±9.8(female and male,respectively)from Sep

tember to October,but decreased to49.7±5.5and46.6

±7.6from November to February and48.4±5.5and

45.9±7.0from March to June.CW of crabs collected

from September to October was significantly larger than

those in the other two seasons,but there were no signifi

cant differences between the latter two seasons in either

sex(Mann-Whitney U-test,Table1).Two pairs of crabs

in postcopulatory guarding were collected in March,

1996,and December,1997,at Stn2(Table2).They

were found on a sandy bottom underwater.The females

were halfway dug into the sand and the males were

grasping the legs of the females from their backside.

At Stn4-7,live crabs including489females and

589males,dead crabs including8females and10males,

exuviae including15females,and20males,and post

molt crabs including53females and65males were col

lected from June,1996,to September,1997.Live female

juveniles of8.5-52.6mm CW appeared nearly all year

round,but adults of37.5-61.8mm CW were collected

only from August,1996,to February,1997,and from

August,1997,to September,1997(Fig.4).Mean±SD

of adult CW(mm)was47.6±4.9in the former period

and52.3±2.8in the latter.Exuviae and soft-shell crabs

(post-molt crabs)were collected from August to No

vember,1996,and from March to September,1997.The

post-molt crabs included36juveniles(10.4-47.8mm

CW)and17adults(38.5-57.2mm CW),but the

exuviae were all of juveniles of12.4-41.6mm CW.

Adult soft-shell crabs occurred from August to October,

1996,and from August to September,1997.Male crabs

Table2.Pairs of Eriocheir japonica in postcopulatory guard

ing.For the locations of the stations,see Fig.1.

Date Sampling stationC器饗cewidt糠

Mar.22,1996Stn243.945.9

Dec.18,1997Stn255.549.4

Jan.17,1998Stnl45.951.9

90

Life history of the Japanese mitten crab

Stn1 Stn2 Stn3

1996

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__一闘_竺J　 3'0203　 6070

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Carapace width(mm)

Fig.2.Carapace width composition of female Eriocheir japonica,including dead ones,collected at Stn1-3from September ,1996,

to June,1997.

91

Kobayashi

StnlStn2Stn3

1畿1・2L ____■L二」2L____」以二

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1鑑.・・2n=82L一叫ご一2L_4-一_ユ

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n=16nニ7

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May192L __」L_里1020304050607080

」肌32L -_」L己1020304050607080

Carapace width(mm)

Fig.3.Carapace width composition of male Eriocheir japonica,including dead ones,collected at Stn1-3from September,1996,

to June,1997.

92


Juvemile Adult Juvenile Adult

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Carapace width(mm)

Fig.4.Carapace width composition of live female Eriocheir japonica collected at Stn4-7from June,1996,to September,1997.

93

Kobayashi

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Fig.5.Carapace width composition of live male Eriocheir japonica collected at Stn4-7from June,1996,to September,1997 .

94


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舅Fe-2÷ 漏8。2L欝淵4

Mar.92L-_」ぐ2n=9'02030如50607080

6102030菊鉛607080L皿鼠

一222L謡 ∴2。3。_;∴ 幅謙糟

Apr・72L___』一ご一2n=9

4102030⑳m607080102030⑳50607080

Apr.2・2n=m2L__皿L三.

610203040506070801020304050607080

44

May42n=202n=6

」u臨32L望802L鯉8010203040506070801020304050607080

Camp紐cewidth(mm)

Fig.6.Carapace width composition of dead female Eriocheir japonica collected from July ,1996,to June,1997.

95

Kobayashi

StnlStn2Stn3Stn4-7

1996

Amg252L____」=L三

Seレ27「-2L望亘020304050607080瞳020304050607080

・cL1・2L _____己2L __」L__旦10203040506070801020304050607080

・ct252L __』」三2L__」皿__三10203040506070801020304050607080

N・▼.62L ___』一__三1020304050607080

N。v.222L__』』_三2L __圧L』己2L_」 ∬。L二2L__↓ 一三1020304050607080102030405060708010203040506070801020304050607080

D㏄.82L___一_三2L___皿__旦10203040506070801020304050607080

De。2・2L _」h_竺2L__⊥__三1997且02030⑳m6070801・2・3・恥m6・708・

」an・lo2L____」L己一2-102030405060708010203040506070801020304050607080

。」an・232L____皿_三2L_._阻一_旦rΩ 置0203040506070801020304050607080尉

4』

碁Fe臨92L_』__三2n=11』畳02030⑳50607080102030⑳50607080

誉Feh202÷ 緊8。:÷ 論詣一論ZM　 92L一L

_三2・=9且0203040506070801020304050607080

4

M　 222n=162L_⊥ 皿三

102030405060708010203040506070804

n=10

Ap「・722L_一一」一Lこ

10203040506070801020304050607080

4

Ap「●212n=102L

__皿__三2L__」一一一一三

4102030⑳506070801・2・3・ ⑳m6・708・1・2・3・ ⑳m6・7・8・

May42n=112L

_」一L_里10203040506070801020304050607080

May192L-1020304050607080

」un.32L___-1020304050607080

」uL292L___⊥_三量020304050607080

Aug.102L ____ユ__巴1020304050607080

Aug.222L ___』一_」=1020304050607080

Carapace width(mm)

Fig.7.Carapace width composition of dead male Eriocheir japonica collected from August,1996,to August,1997.

96


Number of crabs三ε

三目

5z

StnlStn2Stn3

5n=25n=55n=5

1997

0ct.8100304050607010203405670100300560

5n=15n=15nニ3

5n=55n=105n=6

No▼.51020304050607010203040506070102030405070

5n=35n=55n=1

5n珂5n=105n=7

Dec・3102030405060701020304000100305000

5n=85n=35

n=55nニ24

Dec.1812307010203040506070

5nニ25n=13

5n=25n=12

1998

Jan.171020304050607010203040506070

5n=25n=16

5nニ45n=3

1Feb.14003050607010203040506070

5nニ3

5n=4

Mar.210203040506070

55n=18n=7

Apr.1蓋020304050607010203040506070

5n=125n=4

5n=95n=2

Apr.1710230⑳506001237

Male

5n=205n=1

5nニ1

FemaleApr.27藍0203040506070

5nニ210vigerous5

n=2Non-ovigcrousadult

adult

May610203040506070

n=95

Carapace width(mm)

Fig.8.Carapace width composition of live Eriocheir japonica,including both sexes,collected at Stn1-3from October,1997,to

May,1998.

97

Kobayashi

of8.0-58.8mm CW were collected nearly all year round at Stn4-7(Fig.5).Exuviae of16.0-45.2mm CW and soft-shell crabs of8.6-58.8mm CW were also collected from August to November,1996,and from March to September,1997.Large crabs(>ca.38mm CW)occurred mainly from July,1996,to January,1997,and from May to September,1997,but were not collected from February to March,1997.Crabs of8-14mm CW of both sexes,were abundantly collected at Stn4-7from March to May,1997,and from August to September,1997.

Carcasses were collected in both the freshwater and tidal areas,but95.4%(166/174)of female carcasses and91.4%(149/163)of those of males were found at Stn1-3(Figs.6,7).For both sexes,the duration of occurrence of carcasses at Stn1and2was longer than at Stn3and Stn4-7.Dead females were collected only from July to November,1996,at Stn4-7and from November to December,1996,at Stn3,but from September,1996,to June,1997,at Stn2and from November,1996,to June,1997,at Stn1.Dead males occurred from August to November,1996,April of1997,and at July to August,1997,at Stn4-7and from November,1996,to February,1997,at Stn3,but from September,1996,to May,1997,at Stn2and from October,1996,to June,1997,at Stn1.Female carcasses comprised99.4%(173/174)adults of38.7-65.5mm CW;the sole juvenile,having a CW of45.0mm,was collected in the freshwater area(Stn7).As for males,only large carcasses of35.8-79.8mm CW were collected both in the freshwater area and the tidal area.Within the tidal area,dead

ovigerous females were found at Stn1(14.5%of total dead females from Stn1)and Stn2(21.8%).These carcasses mostly lay on the substratum under the water,but some had dried up during the ebb tide.There was no marked injury on the hard exoskeleton for new carcasses found under the water,only decay of internal organs and

joints.

Sampling2

From October,1997,to May,1998,42non-ovigerous

and86ovigerous adult females and147males were collected at Stn1-3(Fig.8).At Stn3,crabs occurred only from October to December,1997,but from October,1997,to May,1998,at Stn1and from October,1997,to April,1998,at Stn2.Male crabs were of33.2-69.8mm CW and female crabs were of38.5-63.5mm CW at these three stations,and ovigerous ones were collected

from November,1997,to May,1998,only at Stn1and2.After April17,1998,the ratio of male crabs

decreased;from October8,1997,to April1,1998,male:female=133:77(males63.3%and significantly

male-biased by the binomial test,p<0.001),but after April17,1998,14:51(males21.5%and significantly

female-biased by the binomial test,p<0.01).One pair of crabs engaged in postcopulatory guarding was collected in January,1998,at Stn1(Table2).

DISCUSSION

In the present study,juvenile crabs underwent growth

molts from March to November,and reached adulthood

by the puberty molt from August to October,only in the

freshwater and upper tidal river areas(Stn4-7).These

crabs all migrated downstream to the tidal area in hard

shell condition from September to February.Kobayashi

&Matsuura(1991)had concluded earlier that the pu

berty molt of E.japonica in the Kaminokawa River,

Kagoshima Prefecture,was concentrated in August,and

that crabs migrated downstream to the tidal area from

September to the following January.The present data

nearly agree with this estimation,but the duration of this

process in the Saigo River was a little longer and shifted

to later months.Molting growth paused during the winter

season(from December to February)when the water

temperature was lower than10.0•Ž.In rivers in winter,

crab activity decreases with low water temperature,and

catch per unit effort using traps also drastically decreases

(Kobayashi&Matsuura1991).

In the early reproductive season,the crabs collected at Stn1-3were larger than those taken later from the middle tidal river to the sea coast(Fig.2&3).A similar tendency has been reported elsewhere(Kobayashi&Matsuura1991,1995a).There are two reasons.Downstream migration starts in early autumn from the upper region of the river,where larger crabs are distributed,and large crabs tend to reach the tidal area earlier in the season(Kobayashi&Matsuura1991).The sampling stations for the present study were located in lower reaches of the Saigo River,and the average size of adult

females collected at Stn4-7(mean=48.2mm CW for the whole season)was much smaller than at Stn1-3in

the early reproductive season(58.1mm CW).In addition,there are two groups differing in their reproductive season,an early-reproducing group composed of large adults and a late-reproducing group composed of small to large ones.In the early reproductive season,the former mainly occurs in the tidal area(Kobayashi&Matsuura1995b).

Kobayashi(1998)reported that megalopa larvae

98


settled and metamorphosed to the crab stage(ca.2mm

CW)at Stn4mainly in autumn(October-November,

1996)and late spring to early summer(May-June,

1997)in the Saigo River population.After growing to at

least3.6mm CW,the crabs began to migrate upstream

and reached the freshwater area(Stn5-7).The earlier

group grew to10mm CW from May to June,1997,and the later one from August to September,1997

(Kobayashi1998).The appearance of young crabs of8-14mm CW at Stn4-7from March to May and from

August to September,1997,in the present data agree

with this growth pattern.However,crabs in this size

class were not abundant in the latter period.The decrease

in the number of captured juveniles of<10mm CW sug

gests the upstream migration and dispersion along the river of this size class and high predatory pressure by

fishes(Suzuki et al.1998;Takeshita and Kimura 1995).

In the tidal area between the middle tidal river area

and the sea coast(Stn 1-3),only mature crabs(adult

females of37.5-69.5mm CW and males of28.5-78.9

mm CW)which had migrated downstream from the

upper region for mating and oviposition occurred from

September to the following June.Eriocheir japonica re

produces mainly in the lower part of the tidal area,where the salinity is comparatively high(Stn1&2).Although

live crabs were not abundantly collected in the tidal area

in the present data,Kobayashi and Matsuura(1995a)re

corded that E.japonica was abundantly distributed on the sea coast for about ten months from September to the

following June(at Tsuyazaki Beach,nearly2.5km from

the mouth of the Saigo River,which is the only freshwa

ter source providing E.japonica,Fig.1).

Mating behavior,including copulation and

postcopulatory guarding,and ovigerous females were observed during the whole period of occurrence in the

sea area(Kobayashi and Matsuura1994a,1995a).Mat

ing behavior can be observed in the laboratory using

crabs caught in the sea area from September to the fol

lowing June(Kobayashi&Matsuura1994b;Kobayashi

1999).Mating is initiated without any regular

precopulatory behavior,while in the hard-shell(intermolt)condition.Copulation continues for14to50minutes.After release from the copulatory posture,the

males begin to grasp the females from their back side and

cradle them.This postcopulatory guarding lasts for at

least several hours and the females lay eggs within a day

(Kobayashi&Matsuura1994b;Kobayashi1999).Thus,it can be assumed that the process of copulation,

postcopulatory guarding,and oviposition is completed within a day and in the same area.Morita(1974)re

ported copulation of E.japonica within a wide portion of

the tidal river area.However,observed results in the

open sea area(Kobayashi&Matsuura1994a,1995a)

and the present data(Figs.2,3,8)show that the repro

ductive area where paired or ovigerous E.japonica oc

curred was not restricted to the tidal river area,but

mainly comprised the lower tidal river area and the wide

sea coast area(Stnl&2),where comparatively high sa

linity(18-33)occurs constantly or predominantly.

At the end of the reproductive season,male crabs

decreased and the proportion of females increased(Fig.

8).A similar tendency has been recognized at Tsuyazaki

Beach(Kobayashi&Matsuura1995a).Adult crabs re

producing in the sea area are male-biased in total and males are easier to catch than females because males

move more actively on the substrate than females

(Kobayashi&Matsuura1994b,1995a).However,males tend to die earlier at the end of the reproductive

season(Kobayashi&Matsuura1995a),and the

locomotory activity of females may be raised with the in

crease of water temperature in the early summer.As a re

sult,the samples changed to female-biased at the end of

the season.

In the Kaminokawa River,large males and adult fe

males were absent in spring and early summer in the

freshwater area,most of them evidently having migrated

downstream to the tidal area(Kobayashi&Matsuura

1991).Additionally,beach collections and rearing ex

periments at Tsuyazaki revealed that adult E.japonica did not molt,copulated in the hard-shell condition,and

died after one reproductive season(three ovipositions

for females)while in the marine phase(Kobayashi&

Matsuura1995a,1997).The present data agree with

these results.In the tidal river and sea coast areas,only hard-shell crabs and a large quantity of carcasses of

adults occurred from autumn to spring,and there were no

crabs in summer.In contrast,in the freshwater area,large

males and adult females were absent in spring and early

summer,and large males and adult females just after

molting began to appear in summer.These results sug

gest that crabs do not molt and grow after their seaward migration;rather,all crabs die within one reproductive

season and do not return to the freshwater area.Most dead crabs were adult and large-sized(mostly

>35mm CW).For juveniles and middle-sized crabs

(ca.10-35mm CW),exuviae were often observed,but carcasses were not found.Adults may die more easily

than juveniles,or the main cause of death may be differ

ent in juveniles and adults;small crabs are abundantly

eaten by predators in the freshwater area[freshwater

fishes such as Odontobutis obscura(Temminck et

Schlegel),Rhinogobius sp.,Phoxinus oxycephalus

99

Kobayashi

(Sauvage et Darby),Zacco temmincki(Temminck et Schlegel),Pseudogobio esocinus esocinus(Temminck

et Schlegel),Hemibarbus barbus(Temminck et

Schlegel):after Suzuki et al.1998;Takeshita&Kimura

1995],but few predators of large crabs with hard exo

skeleton are found in the freshwater and tidal areas.Car

casses without marked injury indicate the lack of preda

tors in these habitats.

Ovigerous females bearing developing embryos

were included in carcasses in a high percentage,and fe

males were often dead,leaving reproduction unfinished.

At Stn3(middle tidal river area),dead crabs considered

to have just migrated downstream but not yet started to

reproduce were collected only in the earlier part of the

reproductive season(autumn-early winter).Erioc

heir japonica possesses hyper-and hyposmoregulatory ability and adaptability to a wide range of salinity(Watanabe&

Yamada 1980);however,repeated drastic changes of sa

linity(0-18),especially in a weakly-mixed type of tidal

river such as the Saigo River,may have a large impact

on this crab.They may have failed to acclimate to high

salinity or to drastic changes of salinity after reaching the

tidal area.In the open sea area(Tsuyazaki Beach),col

lections of exhausted crabs and dead crabs including fe

males with worn pleopods were concentrated at the end

of the reproductive season.Rearing experiments also re

vealed that all crabs died by July after reproduction.

Therefore,the main cause of death there may be assumed

to be exhaustion through reproduction(Kobayashi and

Matsuura1995a).In the tidal river,however,death may

be also caused by drastic and rapid changes of environmental factors regardless of the conditions of the crabs.

In the freshwater area,dead crabs were found only from

July to November.These crabs died before starting the

downstream migration.After attaining maturity,crabs

may not necessarily die only as a consequence of ex-

haustion through reproduction.There are few predators

aside from high fishing pressure by humans for large E

.japonica.Rapid environmental changes involving water

quality,dissolved oxygen,and salinity within their habitat may cause large crabs to die suddenly under natural

conditions.

StageMonth

JanFebMarAprMayJunJulAugSepOctNovDec

Embry・1陥i囲

lHatching

ZoeaBarva(1st・5th)■ ■ ■■

■晩gT脇u↓ 團1國ll

J・ ▼enilecrabu↓

IPube質ym・ultAdu膿

_D↓ll日

Freshwater口

T常1蝿璽U職nU寺

bwe・ZヨD鎚艦mD ↓

Seac・ast■

Fig.9.Time table of the occurrence pattern of Eriocheir japonica during each stage of its life history in the Saigo River and ad

jacent sea area.

100


The occurrence patterns of Eriocheir japonica in the Saigo River and adjacent sea area are schematically

depicted in Fig.9.Eggs(embryos)are laid in the lower tidal river area and adjacent sea area from September to

the following June(Kobayashi and Matsuura1995a).Hatched zoea larvae spend their pelagic life in the sea

area during the same interval.Megalopa larvae then mi

grate upstream from the sea to the tidal river area and settle only in the upper tidal river area where the tip of

salt wedge(salinity>18)reaches(Stn4).Settlement is concentrated from September to January and from April

to May(Kobayashi1998).Juvenile crabs migrate upstream from the upper tidal river area to the freshwater

area and disperse along the river there(Kobayashi1998).They are distributed in the freshwater area all

year round.After the puberty molt between August and October,adult crabs migrate downstream to the tidal area

(middle to lower tidal river area and sea coast area)from September to the following January.Crabs exhibit

reproductive behavior in the lower tidal river area and sea coast area from September to the following June

(Kobayashi&Matsuura1995a).In the Saigo River,small juvenile crabs(ca.<20mm CW)have not been

collected in the middle-lower tidal river and sea coast areas(Kobayashi1998).Additionally,only large crabs

(mostly adults of CW>36mm for females and>34mm for males)occurred on the sea coast (Kobayashi&

Matsuura1995a).Therefore,no crabs,at least in the Saigo River population,were found to spend their whole

life within the tidal river and sea coast areas without mi

grating upstream to the freshwater area.However,this is a matter of a small,weakly-mixed type of tidal river,an

d different patterns may be present in other rivers.Life style may be inferred to be rather different be

tween the freshwater and marine phases of E.japonica.During the freshwater phase,they continue to grow from

the juvenile stage just after settlement(ca.2mm CW)until the adult stage(ca.35-80mm CW)and disperse

widely along the river from the upper tidal area(mostly freshwater flow)to the upper freshwater area

(Kobayashi&Matsuura1991;Kobayashi1998).While in the marine phase,adult crabs reproduce without

growth and wander around the tidal river and sea coast;they can move along the beach for at least2km.Additionally,hatched zoea larvae spend their planktonic life

in the open sea(Kobayashi&Matsuura1994a,1995a).Thus,E.japonica migrates over a wide range of environments between the two phases in its life cycle.

Active interchanges between populations in different rivers may be expected through the dispersion of

adult crabs and pelagic larvae during the marine phase.

In some brachyuran species reproducing in tidal rivers,zoea larvae undergo vertical migration following the

tidal rhythm,and this facilitates active dispersion into the sea or,conversely,retention within the tidal river[e.g.,

Rhithropanopeus harrisii(Gould)(Cronin&Forward1983,1986);Carcinus maenas(Leach)(Henrique et al.1997)].As for Eriocheir japonica,adult crabs are actively motile in the tidal area(Kobayashi&Matsuura1994a),and this facilitates the wide dispersion of

hatched planktonic larvae.Studies on genetic variation in nine alleles of E.japonica using horizontal starch gel

electrophoresis have shown that genetic variation is very small among the populations of22locations from Hok

kaido to Okinawa(Gao&Watanabe1998).In E.japonica,therefore,individual river populations are not com

pletely isolated within each river, and there is significant genetic flow between them through the marine phase of

the crabs'life.

Acknowledgments.I wish to thank the members of the Marine Biological Laboratory,Kyushu University,and

the Laboratory of Marine Biological Function,Kyoto University,for their kind assistance.I also thank Dr.Y.

Takemon,Kyoto University,and Dr.C.P.Norman,University of Tsukuba,for comments that improved this

paper.

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