J OURNAL OF C RUSTACEAN B IOLOGY, 32(5), 753-761, 2012
MOLTING GROWTH PATTERNS OF THE JAPANESE MITTEN CRAB ERIOCHEIR
JAPONICA (DE HAAN) UNDER LABORATORY-REARED CONDITIONS
Satoshi Kobayashi ∗
3-36-36-401, Hakozaki, Higashi-ku, Fukuoka 812-0053, Japan
ABSTRACT
The molting growth pattern of the Japanese mitten crab Eriocheir japonica (de Haan, 1835) was investigated under laboratoryreared conditions. Crabs were individually reared in freshwater for 5 years in a constant temperature room at 23-25°C. The age after
metamorphosis and instar number were recorded for each molt, and the intermolt period was calculated for each crab. Carapace width
(CW) was measured and the percentage molt increment was calculated. Eleven crabs reached a CW > 10 mm. Each growth curve (ageCW relationship) had two phases in the juvenile stage. Growth rate gradually decreased in the younger phase before changing to nearly
constant in the older phase. During the younger phase, the percentage molt increment decreased from 25.0%-38.1% to 6.0%-26.2% (ca.
2-10 mm CW, 1st to 11th instars), and the intermolt period increased from 4-9 days to 40-300 days (ca. 2-20 mm CW, first to thirteenth
instars). During the older phase, both parameters became broadly flat but showed marked fluctuations. Crabs reached minimum adult size
(ca. 35 mm CW) or the adult stage at 2-4 years after metamorphosis. The instar numbers required by E. japonica to reaching maturity was
more than that required by other brachyuran species. The adult stage appeared after the twentieth instar in females, and crabs reached their
minimum adult size during the sixteenth to twenty-first instars. After puberty, one female continued molting growth. This suggests that
adults could live longer and grow larger in size if they remain in a freshwater environment.
K EY W ORDS: Eriocheir japonica, instar number reaching maturity, intermolt period, molt increment,
molting growth
DOI: 10.1163/193724012X649796
I NTRODUCTION
The Japanese mitten crab Eriocheir japonica (de Haan,
1835) is a commercially important varunid crab distributed
in eastern Asia including the entire Japanese archipelago
except Ogasawara Islands (Guo et al., 1997; Komai et al.,
2006). The congener E. sinensis H. Milne-Edwards, 1853
(the Chinese mitten crab) is a well-known invasive alien
species that is widely dispersed in Europe and North America, and both species are catadromous, i.e., migrating for
long distances through various environments (Kobayashi,
1999a). Recent ecological studies have characterized its life
cycle in Japan. The reproductive area for E. japonica is lower
tidal rivers and adjacent seacoasts (Kobayashi and Matsuura,
1994, 1995a; Kobayashi, 2003). After a period of drifting as
planktonic larva in the sea, settlement and metamorphosis
occurs in upper tidal river areas (Kobayashi, 1998). Young
crabs migrate upstream to freshwater areas and disperse
widely along rivers. In the fall, crabs migrate downstream to
the sea after reaching the adult stage through a puberty molt
in freshwater areas. Adult crabs die at the river mouth or
seacoast after one reproductive season (Kobayashi, 1999a).
Thus, mitten crabs spend a considerable amount of their
life in freshwater rivers, where the growth phase determines
their survival rate, longevity and future reproductive success.
I previously investigated a natural population of E. japonica inhabiting a small river in Fukuoka Prefecture, a temperate region in Japan and characterized the general growth
∗ E-mail:
pattern and age of maturity using a cohort analysis method
(Kobayashi, 2011). As a second method to elucidate growth
patterns, I also conducted rearing experiment in freshwater environment. Enlargement of crustacean body mass intermittently occurs by ecdysis; therefore, individual growth
rates should be analyzed as indicated by intermolt duration
and molt increment (Hartnoll, 1982). However, marked individuals of E. japonica are difficult to track in their natural habitat, because of their active locomotion and dispersion along rivers. Thus, direct observation under laboratoryreared conditions is the best method for observing molting
growth, although the effect of artificial conditions on natural crab growth patterns should be taken into consideration
(Hartnoll, 1982). The data from the rearing experiment was
particularly helpful for evaluating the potential for specific
growth patterns. For example, the range of instar numbers
that attain maturity and the total instar number during its
lifetime can be evaluated only by direct observation of individuals during long-term rearing experiment.
Rearing mitten crabs in freshwater is comparatively easy,
if researchers solved the problems of dietary conditions and
the escape of crabs from aquariums. Before the present
study, I reared several ovigerous crabs collected from the
sea and hatched larvae from their eggs in the laboratory
(Kobayashi and Matsuura, 1995a; Kobayashi, 2005). The
young crabs that metamorphosed from these larvae were
used for the present experiment. After acclimation to fresh-
[email protected]
© The Crustacean Society, 2012. Published by Brill NV, Leiden
DOI:10.1163/193724012X649796
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 32, NO. 5, 2012
water, molting growth was recorded for each crab. I succeeded in raising several crabs to adult (mature) size. The
present paper deals with the growth pattern of E. japonica
recorded during long-term rearing in an artificial environment. In addition, the specific growth pattern of E. japonica,
a unique brachyuran crab, is discussed.
M ATERIALS AND M ETHODS
Breeding and Culture of Larvae in Sea Water
Adult E. japonica were collected from Tsuyazaki Beach,
Fukutsu City, Fukuoka Prefecture, Japan (34°46 N,
130°28 E) between January 1990 and July 1992. Crabs were
transferred to the Fishery Research Laboratory, located less
than 500 m from the collection site. Crabs were individually reared in baskets (33 cm × 55 cm × 33 cm) immersed
in 500 l tanks with an open seawater system till June 1992.
The development of eggs was observed, and just before egg
hatching, the ovigerous crabs were transferred from the baskets to smaller aquaria (15 cm × 25 cm × 15 cm) with an
open seawater system. A bag net was placed at the outlet of
the aquaria and larvae were collected with the net.
Samples of newly-hatched larvae that were collected
with the net were placed to small beakers. Each brood
was continuously reared in the natural seawater (ca. 33h
salinity, without filtration) until the 1st instar crab stage.
Each beaker was mildly aerated during the earlier zoea
stages and the aeration was gradually increased in the
later stages. Beakers containing larvae in 500 ml seawater
were immersed in trays with flowing natural seawater
supplied to the laboratory. Sand was laid at the bottom and
nylon strings were floated after megalopa larvae emerged.
Photoperiod was left in ambient condition. Larvae were
continuously reared in each beaker until the survivors
reached the 1st instar crab stage (Kobayashi, 2005). Under
natural conditions, megalopa larvae and 1st instar crabs
appear in the upper tidal river area, where mostly freshwater,
before they move to the freshwater phase (Kobayashi, 1998).
However, the megalopa larvae were reared in seawater in
the present experiment, similar to zoea larvae to avoid
death owing to the shock of acclimation to freshwater. The
1st instar crabs were acclimated to freshwater soon after
emergence and used for the continuous rearing experiment.
Rearing Crabs in Freshwater
First instar crabs within two days following metamorphosis were transferred from the Fishery Research Laboratory
in Fukutsu City to a constant temperature room in Kyushu
University in Fukuoka City. The transfer took almost 1 hour.
Crabs were individually reared in plastic cases in a constant temperature room, and rearing was continued as long
as crabs survived from September 1990 to February 1996.
The temperature of the room was constantly maintained at
23-25°C, which corresponded to the water temperature of
September to October and May to June in rivers flowing
through Fukutsu City (Kobayashi, 1998). Light was maintained for 24 hour (24 L) in the room, but areas were set
aside as shaded areas, except during periods of water changing. Crabs were always maintained in underwater conditions
in plastic cubic cases completely filled with water. They
were mildly aerated and an opaque vinyl chloride pipe was
laid as a shelter at the sand bottom in each case so that the
crabs could hide their whole body. The cases were replaced
with larger ones as the crabs grew larger as to ensure sufficient space for free movement (from 200 cm3 to 400 cm3 ,
800 cm3 , and 2000 cm3 ). The tops of the cases were covered
with porous polyvinyl films that were tied with a rubber band
to prevent the crabs from escaping.
Food was carefully selected to improve the survival
rate. This crab is an omnivore biased toward herbivory
and a deposit feeder that mainly feeds on detritus derived
from plant fiber or filamentous algae during its river phase
(Kobayashi, 2009). Preliminary rearing revealed that food
selectivity of this species is low, and they eat various
materials, but plant materials are essential for longevity. The
food items provided to crabs were as follows.
1. Plant materials including living freshwater filamentous
algae (Cladophora etc.), wheat, boiled Chinese cabbage and spinach.
2. Animal materials including isopods (Ligia exotica
Roux, 1828), clams (Venerupis philippinarum
[A. Adams et Reeve, 1850] etc.), freshwater snails
(Semisulcospira libertina Gould, 1859), polycheate
worms (Hediste), crabs (Geothelphusa dehaani [White,
1847]) and various fish species (Spratelloides gracilis
[Temminck and Schlegel, 1846] etc.).
3. Several kind of pellet diets for prawns and gold fishes.
Crabs were fed daily with a mixture of these items. The
diet was changed daily when possible. Plant materials were
provided everyday.
All residues, except live freshwater algae, were removed
each day when possible to prevent water contamination.
Freshwater algae were allowed to remain in the case until
they were completely consumed. Water was provided from
a tank filled with dechlorinated tap water that was aerated
for more than 24 h. The water in the cases was exchanged
every 2-3 days.
Crabs were observed daily when possible and the date of
molting was recorded. Intermolt period (days) was calculated from the dates of continuous molting, and maximum
carapace width (CW) of exuviae was measured. When crabs
were dead, the date and CW of carcasses were recorded.
When CW 10 mm, it was measured with vernier calipers
to the nearest 0.1 mm. Small crabs with a CW < 10 mm
were measured with a ruler referring to the magnified image
on a profile projector to the nearest 0.01 mm.
Data Analysis
Data was analyzed only for the crabs that grew to CW >
10 mm without loss of legs, because regeneration substantially affects the growth pattern of crabs. When analyzing
data, the environmental conditions of water temperature,
light, and food were kept nearly constant, and data from
each crab was collected by the method used for the single
growth pattern from in the first instar stage. It was difficult
to sex young crabs without harming them; therefore, sexes
were determined after they reached 10 mm CW. The growth
increment (%) was calculated as follows: 100 × (post-molt
CW − pre-molt CW)/pre-molt CW. Mean values and standard deviation were calculated for CW, growth increments,
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KOBAYASHI: GROWTH PATTERNS OF ERIOCHEIR JAPONICA (DE HAAN)
Table 1. Carapace width of female parent and date of spawning and hatch of Eriocheir japonica used
for the rearing experiment.
No.
Carapace width of
female parent (mm)
1
2
3
4
5
6
7
8
9
10
11
48.5
50.0
65.6
48.0
55.0
47.2
50.9
50.9
45.8
51.8
48.5
and intermolt periods in each instar. Female crabs were categorized as juveniles and adults, based on morphological
difference in the pleomeres. In female crabs, the pleon is almost triangular; the edges of the thoracic sterna are exposed
in juveniles. The crab is nearly oval and all parts of the thoracic sterna are covered by the pleon in adults. Differences
in the growth patterns of sexes and stages were not detected
because the sample size in the current study was excessively
small for precise analysis.
R ESULTS
Crab-Rearing Data
Seven male and four female crabs reached CW > 10 mm
without the loss of legs. Five crabs (Nos. 1, 2, 6, 8, and 9)
were hatched from ovigerous females collected from the sea,
but the period of spawning was unknown. Two crabs (Nos. 3
and 4) were derived from the same brood spawned from the
same parent (Tables 1 and 2). These crabs continued molting
growth, with 11.0-44.0 mm CW and 9-22 instars for males,
and 11.0-56.0 mm CW and 10-22 instars for females. Death
of crabs was mostly caused by human errors that occurred
during the long rearing period. Loss and desiccation after
escape from cases occurred in five crabs, water pollution
Date
Spawning
Hatching
–
–
May 16 1990
May 16 1990
March 13 1991
–
March 30 1991
–
–
October 29 1991
May 22 1922
May 26 1990
June 2 1990
June 6 1990
June 6 1990
May 2 1991
May 14 1991
May 10 1991
May 26 1991
June 21 1991
November 23 1991
June 11 1992
from food residues killed three crabs, while failure to molt
due to unknown causes killed three crabs. The longest
rearing period was 1730 days (4 years and 10 months after
metamorphosis) for a female crab (No. 4), although this crab
later died after escaping from the case.
Although similar diets were supplied, the daily rate of
food intake considerably varied for each crab, and the
amount of food intake directly affected growth rate. In
general, crabs with high growth rate (Nos. 2, 3, and 5)
actively consumed food everyday, whereas those with a low
growth rate (Nos. 1, 4, and 7) exhibited a lower appetite.
Relationships between Age after Metamorphosis: Carapace
Width and Instar Number
Carapace width was 1.95-2.21 mm (mean ± standard
deviation = 2.03 ± 0.09) for the 1st instar crabs. This
increased to 11.0-22.4 mm (14.6 ± 3.4) after 1 year
(365 days), 16.6-33.1 mm (23.3 ± 6.0) after 2 years
(730 days), and 24.8-51.3 mm (36.5 ± 12.0) after 3 years
(Fig. 1). Growth rate varied considerably, and the CW of
crabs with a high growth rate was nearly twice that of
crabs with a low growth rate after 1 year. Three of four
female crabs remained in the juvenile stage until their death,
Table 2. Record of rearing of Eriocheir japonica in the laboratory: sex, date of metamorphosis to 1st instar crab and death or escape, rearing period after
metamorphosis, carapace width and instar attained during rearing period. As for death or escape, D: death, E: escape and missing.
No.
1
2
3
4
5
6
7
8
9
10
11
Sex
male
male
male
female
female
male
female
male
male
female
male
Date
Metamorphosis to
1st instar crab
Death/
escape
June 24 1990
June 25 1990
July 2 1990
July 2 1990
June 14 1991
June 15 1991
June 16 1991
June 28 1991
July 17 1990
February 22 1992
July 15 1992
August 3 1994 E
May 22 1994 D
August 3 1994 D
March 27 1995 D
December 19 1995 D
March 5 1992 E
February 4 1996 D
May14 1993 E
December 28 1992 E
April 19 1993 E
March 28 1995 D
Rearing period after
metamorphosis
(days)
Carapace width
attained during
rearing period (mm)
Instar attained
during rearing
period
907
1428
1494
1730
1650
264
1895
687
531
423
956
18.0
43.0
44.0
39.5
56.0
11.0
37.1
15.7
16.3
11.0
31.0
14
18
17
22
21
10
21
22
12
9
17
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 32, NO. 5, 2012
Fig. 2. Eriocheir japonica instar number plotted against days after
metamorphosis.
Fig. 1. Eriocheir japonica carapace width plotted against the number of
days after metamorphosis. The figure shows each stepwise growth line and
the No. of crab, while the horizontal dotted line indicates a carapace width
of 35 mm.
while one attained maturity after a puberty molt at 1059
days (2 years and 10 months) following metamorphosis and
she became an adult with a 51.3 mm CW. This adult crab
molted again after 300 days (post-puberty molt), reached to
56.0 mm CW, and survived for an additional 291 days after
that molt (No. 5).
Irrespective of the exact sexual maturity of the exoskeleton and gonads, the age at which these crabs reached 35 mm
CW was determined. This size was equivalent to the approximate minimum size among adult cohorts of E. japonica (Kobayashi, 2011). Among the females, No. 5 reached
35.2 mm CW at 866 days after metamorphosis (2 years and
5 months), No. 4 reached 36.5 mm at 1574 days (4 years
and 4 months), and No. 7 reached 37.1 mm at 1653 days
(4 years and 7 months). Among the males, No. 3 reached
40.0 mm CW at 760 days after metamorphosis (2 years and
1 month) and No. 2 reached 38.6 mm at 967 days (2 years
and 8 months).
Crabs Nos. 3 and 4 were spawned from the same parent
and they exhibited considerably different growth rates. They
reached 22.4 mm and 12.9 mm CW after one year (365
days), 33.8 mm and 19.9 mm after 2 years (730 days),
and 44.0 mm and 24.0 mm after 3 years (1095 days),
respectively.
Although the sample size was considerably small, growth
rate tended to be independent of the CW of their parent crab
(Table 1). Among the crabs that exhibited rapid growth, the
CW of their female parents were 48.0 mm, 50.0 mm, and
65.6 mm for Nos. 5, 2, and 3, respectively. Among the crabs
that exhibited slow growth, the female parents measured
65.6 mm and 47.2 mm for Nos. 4 and 7.
Metamorphosis occurred during June-July, except in one
case (February for No. 2). The two types of high and low
growth rate were mixed.
Each growth curve (age-CW relationship) during the
juvenile stage showed two similar phases. The growth rate
gradually decreased in the younger phase (0-1 year) and
then changed to nearly constant in the older phase (after
1-2 years). The division into two phases affected the total
growth pattern. The total growth rate was determined by the
decreasing rate during the first phase and the nearly constant
rate during the second phase.
Relationships between age after metamorphosis and instar
number is shown in Fig. 2. Crabs were 9-12th instars at
1 year (365 days) of age, 13-16th instars at 2 years (730
days), and 17-20th instars at 3 years (1095 days). Among
the females, No. 5 with a high growth rate reached adult
stage at 20th instar by the puberty molt. However, No. 4
and No. 7 with a low growth rate remained in the juvenile
stage even at 21st or 22nd instar. In general, crabs molted
frequently (ca. 10 times) during the first year (<365 days
after metamorphosis), but thereafter the frequency decreased
to ca. 4-5 times per year during the second year (365-729
days) and the third year (730-1094 days). From the fourth
year (1095 days), frequency became ca. 1-3 times per year.
Relationships between instar number and carapace width
showed that the CW continued growth with every molting
(Fig. 3). Carapace width of 1.95-2.21 mm at the 1st instar
increased to 4.5-6.3 mm (mean ± standard deviation =
5.28 ± 0.66 mm) at 5th instar, 11.6-15.8 mm (12.1 ±
1.73 mm) at 10th instar, 19.9-33.8 mm (23.8 ± 5.73 mm)
at 15th instar, and 30.5-51.3 mm (38.9 ± 12.4 mm) at 20th
instar. The instar number at which crabs exceeded 35 mm
CW (minimum CW size of adult cohort) was 16-21. Among
the female, No. 5 with a high growth rate reached 35.2 mm
at 17th instar, and No. 4 and No. 7 with a low growth rate
reached 36.5 mm at 21st instar and 37.1 mm at 21st instar,
respectively. Among the male, No. 3 and No. 2 with a high
growth rate reached 40.0 mm at 16th instar and 38.9 mm
at 18th instar, respectively. Crabs with a high growth rate
tended to reach adult size at earlier instars.
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KOBAYASHI: GROWTH PATTERNS OF ERIOCHEIR JAPONICA (DE HAAN)
Fig. 4. Percentage molt increment of Eriocheir japonica carapace width
plotted against the log of the pre-molt carapace width.
Intermolt Period
Fig. 3. Log of Eriocheir japonica carapace width plotted against instar
number. A, continuous change in each crab; B, mean and standard deviation
for each instar. Horizontal dotted line indicates a carapace width of 35 mm.
Growth Increment per Molt
Changes in the percentage growth increment relative to the
pre-molt CW (Fig. 4) and the pre-molt instar number (Fig. 5)
indicated the general tendency of the growth increment.
Initially, it gradually decreased as the crabs grew larger and
the mean increment became nearly flat thereafter despite
fluctuations. Crabs in the 1st instar and with ca. 2 mm
CW showed the highest growth increment of 25.0%-38.1%
(mean ± S.D. = 30.9 ± 4.28), but the increment decreased
to low values of 6.0-26.6% (mean ± S.D. = 15.1 ± 5.04)
among older crabs after eleventh instar and CW > 10 mm.
Considerable fluctuations were always observed, but the
mean increment generally remained almost steady within the
range of 11-14% thereafter.
Individual changes in the tendency for growth molts did
not follow a simple general pattern. Values did not change
monotonically, and they fluctuated substantially. Among
the older crabs, high values of >20% were occasionally
observed (No. 11: 24.5%; and No. 5: 26.2%), but this did
not continue and low values of ca. 10%-16% were recorded
before and after the high values.
The growth increment of the post-puberty molt (No. 5,
9.7%) showed low value compared with the mean values of
the pre-puberty molt by older juveniles.
Changes in the intermolt period relative to the pre-molt CW
(Fig. 6) and the pre-molt instar number (Fig. 7) showed the
same general tendency as the intermolt period. Initially, the
intermolt period gradually increased as the crabs grew larger,
before becoming nearly flat. From 2 mm to ca. 20 mm CW
and from 1st to 13th instar, the intermolt period changed
from 4-9 days (mean ± S.D. = 6.5 ± 1.5 days) to 65-310
days (128.9 ± 86.7 days).
Individual changes in the tendency of the intermolt period
did not follow a simple general pattern. In particular, older
crabs of >20 mm CW and 14th instar exhibited a mean value
of ca. 120-180 days, but the values fluctuated substantially.
The maximum difference between the minimum and maximum values during this period was 5.5 times, even in the
same crab (No. 5: 55-300 days, and No. 2: 40-218 days).
The intermolt period after reaching the adult stage (No. 5)
was 300 days and much longer than that during its prepuberty molt (less than 100 days).
D ISCUSSION
In laboratory-reared conditions, E. japonica reached their
mature size or the adult stage at 2-4 years after metamorphosis. Analysis of natural growth pattern in Fukuoka Prefecture (Kobayashi, 2011) revealed that crabs attained maturity at the earliest 2 years after settlement (metamorphosis).
An adult cohort with the smallest CW (mean CW: 39.7 mm)
found in the reproductive area during November was 2 years
old (ca. 24 months), while the second small-sized cohort
(47.8 mm CW) was ca. 29 months old. These crabs exhibited a cessation of growth during winter when the water temperature dropped below 10°C with the high growth rate at
nearly 30°C during summer. The present experiment was
conducted under artificial conditions with almost constant
moderate temperature (23-25°C) and 24 L light conditions,
and the age of attaining maturity was nearly 2 years after
metamorphosis in crabs with high growth rate (Nos. 2, 3,
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 32, NO. 5, 2012
Fig. 6. Log of Eriocheir japonica intermolt duration plotted against the
Log of carapace width.
Fig. 5. Percentage molt increment of Eriocheir japonica carapace width
plotted against pre-molt instar number. A, continuous change in each crab;
B, mean and standard deviation for each instar.
and 5), which was almost similar to the results obtained under natural conditions.
The growth curves of E. japonica indicated that juvenile
stage could be divided into two phases. Growth rate gradually decreased during the younger phase, where the growth
increment decreased by ca. 10 mm CW or the eleventh instar, while the intermolt period increased by ca. 20 mm CW
or thirteenth instar. Following this, growth rate was almost
constant in the older phase. Growth rate fluctuated substantially, but the growth increment and the intermolt period became almost flat.
According to the life history of E. japonica, young crabs
of less than 1.5-2 years of age and CW < 20 mm actively
disperse and migrate upstream along rivers (Kobayashi,
1998). They have relatively long walking legs (Kobayashi,
2002). Older crabs with CW > 20 mm are believed to
settle in specific regions of rivers until they reach maturity.
Therefore, the mature size was approximately the same in
each region, with clinal variations along the rivers, i.e., adult
Fig. 7. Log of Eriocheir japonica intermolt duration plotted against instar
number. A, continuous change in each crab; B, mean and standard deviation
for each instar.
KOBAYASHI: GROWTH PATTERNS OF ERIOCHEIR JAPONICA (DE HAAN)
size increased toward upstream regions (Kobayashi, 1999a).
Differences in the mode of life between the two stages may
be related to the observed differences in growth patterns.
Two general types of growth patterns have been reported
among decapod crustaceans. In some species, the growth
rate decreases with increase in CW, and the extent of growth
determines the maximum size. Several species of brachyuran crabs belong to this category including the cancrid
crab Cancer pagurus Linnaeus, 1758 (Bennett, 1974); xanthid crab Rhithropanopeus harrisii (Gould, 1841) (Hartnoll,
1978); and grapsid crab Pachygrapsus crassipes Randall,
1840 (Hiatt, 1948). In contrast, the growth rate of other
species mostly remains unchanged with the increase in CW,
and boundless growth is theoretically possible (Hartnoll,
1982). This is observed in the portunid crabs Carcinus maenas (Linnaeus, 1758) (Needham, 1950; Hogarth, 1975) and
Callinectes sapidus (Rathbun, 1896) (Haefner and Shuster,
1964). Furthermore, other types change their growth pattern
in the middle of growth process. Growth rate substantially
decrease in the females of some species after attaining maturity (Hiatt, 1948; Hartnoll, 1982). These data were mostly
obtained from grown-up stages, but in some studies also
investigated growth rate changed during juvenile stage. In
the snow crab Chionoecetes opilio (O. Fabricius, 1780), the
growth rate is substantially decreased initially before weakly
increasing. Consequently, its growth rate shows a minimum
value at the middle size (Miller and Watson, 1976).
The growth rate of E. japonica also decreased gradually at first, before changing to a nearly constant rate at
a much smaller size compared with the onset of maturity
(ca. 35 mm). Crabs larger than middle size exhibited nearly
constant growth patterns until reaching maturity. This suggested that a growth limit did not exist at least until maturity. Most adult E. japonica in natural conditions correspond
to instars just after the puberty molt and adult CW sizes varied substantially in the range of ca. 30-90 mm (Kobayashi
and Matsuura, 1995b; Kobayashi, 2003). This indicates that
the adult size is basically determined by a maturity process
that is different from the growth process. Despite reaching
the size where maturity is possible, the timing of maturity
onset varies depending on certain environmental conditions.
Thus, small adults will emerge if the maturity process starts
at a young age (2 years old) in the lower regions of rivers,
whereas maturity is delayed in the upper regions where juvenile crabs continue to grow larger and consequently become
larger old adults (3-4 years old) (Kobayashi, 1999a, 2011).
Some reports suggested that the instar number required
before reaching maturity is fixed to some extent in several
brachyuran species including: the cancrid crab Romaleon
antennarium (Stimpson, 1856), which reaches maturity
at the 11-12th instar (Carroll, 1982); the portunid crab
Carcinus maenas (Linnaeus, 1758), at the twelfth and
thirteenth instar (Mohamedeen and Hartnoll, 1990); the
majid crab Chionoecetes opilio (O. Fabricius, 1780) at
the eleventh instar (Kon, 1980) and Pyromaia tuberculata
(Lockington, 1877) at the seventh instar in females and the
sixth to eighth instars in males (Furota, 1996). The grapsoid
crab, Pachygrapsus crassipes Randall, 1840, attains maturity
at approximately the tenth to twelfth instar and reaches its
maximum size at 19th instar in males and the 22nd instar
759
in females (Hiatt, 1948). The wide variations in the adult
size of E. japonica in the reproductive area suggest that
a fixed instar number is not required to attain maturity. In
addition, the instar numbers after which E. japonica reached
maturity in the present study were large compared with
that required by other related marine species. The instar
number at which adults first appeared exceeded the twentieth
instar in females, and crabs reached their minimum adult
size at the seventeenth and twenty-first instar in females,
and the sixteenth and eighteenth instar in males. Probably,
crabs reach their adult size after the twentieth instar in
larger adults, because larger adults spend 1-2 years longer
in the freshwater phase (Kobayashi, 2011). This may be a
specific (possibly genus-specific) strategy of E. japonica.
The body size of E. japonica is considerably large (ca. 1030 mm vs 30-90 mm CW in adult size) among the varunid
crabs inhabiting the intertidal coastal regions of temperate
areas, e.g., Hemigrapsus sanguineus (de Haan, 1835), H.
penicillatus (de Haan, 1835), and Gaetice depressus (de
Haan, 1833). This crab has evolved to invade the freshwater
river environments where competitive species are rare, and
to utilize a new habitat as growth area. Consequently, it
has achieved a much larger adult size compared with other
species after several molts (over 15) over long period (>2
years) spent in the river phase. In addition, the high fecundity
owing to the large size compensates the cost of catadromous
migration and loss of post-puberty molting growth after
reaching the tidal area (Kobayashi, 2001).
Eriocheir japonica is a unique brachyuran species in
terms of its loss of the post-puberty molt in marine environment. Although adult crabs eat similarly large amount
of food as in the freshwater river (Kobayashi, 2009), they
become exhausted after reproduction and die within one reproductive season without molting growth (Kobayashi and
Matsuura, 1995b, 1997). Thus, two common theories for
growth patterns are not applicable to E. japonica. A change
in growth rate does not determine the limits of growth, but
theoretically boundless growth is also impossible under normal conditions. The cost of osmoregulation and reproduction after downstream migration substantially restricted their
further growth after the puberty molt.
In some majid crabs, the puberty molt is equivalent
to the terminal molt, e.g., Maja squinado (Herbst, 1788),
Passano, 1960; Libinia emarginata Leach, 1815, Hinsch,
1972; Chionoecetes bairdi Rathbun, 1924, Donaldson et al.,
1981. However, this is usually applicable only in females,
and the adult size range differs considerably between sexes.
Sexual differences in the energy invested into reproduction
can explain the difference in growth patterns. Reproductive
investment, e.g., ovarian development, is much higher in
females. In E. japonica, it is different from these species
because the puberty molt is generally the terminal molt
in both sexes. Adult body size ranges generally overlap
between sexes collected in the reproductive area (Kobayashi
and Matsuura, 1995b).
In the present study, a single adult female molted again
after the puberty molt. In natural conditions, adult crabs
after puberty molt between August and November are
exhausted because of reproduction, and they die in the
sea latest by the following June. Thus they live for at
760
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 32, NO. 5, 2012
longest 10 months (300 days) after puberty molt without
further molting (Kobayashi, 1999a, 2003). In contrast, the
continuous rearing of adults in freshwater showed that adult
crabs could live much longer in freshwater (591 days)
with one molting growth occupying 300 days after the
puberty molt. This result suggests that if adult crabs remain
in a freshwater area without downstream migration and
overwinter in the upper regions, they can grow larger to some
degrees through a post-puberty molt, with a low growth rate
and a long intermolt period. In addition, these crabs probably
exhibit early gonad maturation and can begin reproduction
earlier in the next reproductive season than normal crabs that
begin their maturation process after puberty molt in summer.
Early reproducing large-size crabs are present in small
numbers in Fukuoka (Kobayashi and Matsuura, 1995b). The
potential of post-puberty molting in freshwater also suggests
that the growth limitation after maturity of E. japonica in
the sea is not caused by the same possible molting growth
pattern commonly found among brachyuran species, but it
might instead be an ecological outcome of the high energy
costs of migration and reproduction.
ACKNOWLEDGEMENTS
I wish to thank the members of Marine Biological Laboratory, Kyushu
University for their kind assistance. I also wish to thank Dr. Akira Asakura,
Kyoto University for comments on the manuscript.
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R ECEIVED: 12 September 2011.
ACCEPTED: 7 May 2012.