JOURNAL OF CRUSTACEAN BIOLOGY, 22(3): 601–606, 2002
RELATIVE GROWTH PATTERN OF WALKING LEGS
OF THE JAPANESE MITTEN CRAB ERIOCHEIR JAPONICA
Satoshi Kobayashi
3-36-36-404, Hakozaki, Higashi-ku, Fukuoka City, Japan (e-mail: [email protected])
ABSTRACT
I quantified relative growth of the walking legs of the Japanese mitten crab Eriocheir japonica (de
Haan) in the Saigo River, Fukuoka Prefecture, Japan. By plotting the third walking leg merus length
(LML) against carapace width (CW), I could distinguish four growth phases for both sexes; I then fitted a
regression line of allometry (Log Y ¼ a Log X þ b) to each phase. In the first phase (not sexed, CW < 4
mm), growth was positively allometric, and relative length of legs increased (a ¼ 1.37). In the second
phase (4 mm £ CW < 20 mm), growth was nearly isometric, and legs remained relatively longer (a ¼
1.05 for males and 1.04 for females). In the third phase (20 mm £ CW < 40 mm for male, and 20 mm £
CW < 37 mm for female), growth was negatively allometric, and relative leg length decreased (a ¼ 0.82
for males and 0.70 for females). In the fourth phase (CW ‡ 40 mm for males and CW ‡ 37 mm for
females) including adult crabs, growth was negatively allometric, and the legs become relatively shorter;
for males, relative growth was more negative than for females (a ¼ 0.82 for males and 0.92 for females).
These patterns reflect the migratory habit in the life cycle of E. japonica. The first phase occurred just
after settlement and metamorphosis (instars 1–3) before starting upstream migration and was preparatory
for the migration. The second phase coincided with the period of upstream migration and dispersal.
Relatively longer legs increase locomotor activity against the flow and help crab dispersion to the wide
area along the river. The third phase is the growth phase after active migration until crabs attain maturity.
The fourth phase is the maturity phase, during which adults participating in reproduction emerge and
sexual dimorphism becomes evident. There was a morphological variation in fourth phase males
(relatively long legs in smaller males and relatively short legs in larger males). The possibility of variation
of mating strategy is discussed.
Among Crustacea, growth pattern has so far
been investigated with reference to the relative
growth of particular organs. Their hard integument facilitates accurate measurement, the process of ecdysis enables the clear subdivision of
ontogeny, and there are frequently wide differences in growth rates between male and female
specimens. Inflections or discontinuities in the
relative growth pattern can be indications of
several growth phases in each species. As for
brachyuran crabs, marked growth of the cheliped in males (chela height, meral spread,
chelar weight, etc.) or abdominal segments in
females (abdominal width) as a secondary sexual character often coincides with gonadal development. Thus, the minimum size at maturity
can be estimated by the study of relative
growth for each species (Huxley, 1932;
Hartnoll, 1974, 1978, 1982; Lee, 1995; Tessier,
1935, 1960). However, walking legs have
rarely been measured. Because walking legs
dictate locomotor activity, understanding
growth patterns provides insight into migratory
patterns during the life cycle.
The Japanese mitten crab Eriocheir japonica
(de Haan, 1835) is a grapsid crab distributed in
rivers and shallow marine areas throughout Japan, Sakhalien, east Korea, and Taiwan
(Sakai, 1976). This catadromous crab migrates
downstream to the sea (including brackish
water) for mating and oviposition (Kobayashi
and Matsuura, 1995a). As juveniles, crabs migrate upstream and disperse within the river.
High locomotor activity is considered to be necessary during this life stage. Particularly, young
crabs must crawl upstream. Walking legs of the
crabs are relatively longer in juveniles than in
adults, and there is high variability associated
with size and sex, suggesting that the morphology is strongly related to crab life cycle.
Species belonging to genus Eriocheir are
known for their active life style related with
their catadromous habit, especially for E. sinensis H. Milne Edwards, 1854. Eriocheir sinensis
is an alien animal in many European countries
and United States of America, where it has
actively moved along the rivers and sea coast
and has widely spread in these areas since the
601
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 3, 2002
beginning of the 20th century (Clark et al.,
1998; Cohen and Carlton, 1997; Peters and
Panning, 1933). During the 1990s, this species
underwent active population growth and dispersion, and investigations into the dispersion
process and the impacts on native ecosystems
have been conducted in the invaded countries
(Clark et al., 1998; Cohen and Carlton, 1997).
The settlement of megalopa larvae and metamorphosis to crab stage in the estuary, and the
upstream migration to freshwater areas by
young crabs has been presumed from the results of a rearing experiment of larval stages
(Anger, 1991). However, there have been few
studies of the migration process and the change
of morphs in relation to locomotor activity in
the river phase of mitten crabs.
Here, I relate crab morphology to their migratory habit and quantify sexual differences in
the reproductive behavior as factors leading to
the change of relative leg length.
MATERIALS AND METHODS
Eriocheir japonica were collected with hand nets in the
Saigo River, Munakata County, Fukuoka Prefecture, Japan
(3346¢N, 18030¢E) during July 1996 through September
1997. The length of the main stream of this river is nearly 7
km, and the collection site was within 2 km from the river
mouth including both the freshwater area (growth area) and
tidal area (reproductive area). For crabs > 9 mm CW, sex
was determined; females, juveniles, and adults were
identified by the shape of pleopods and abdominal segments. For the females, abdomens are nearly triangular and
the edges of the thoracic sterna are exposed in juveniles,
and the abdomen is nearly oval and all parts of the thoracic
sterna are covered in adults (Kobayashi and Matsuura,
1992). To represent the body size and length of the walking
legs, widest carapace width (CW) and the merus length of
the third walking legs, which are the longest segment of the
longest walking legs, (leg merus length, LML) were
measured using vernier calipers (nearest 0.1 mm) for crabs
<10 mm CW or using a ruler from a magnified image using
a profile projector to the nearest 0.01 mm (Fig. 1). Values
measured on the same samples of crabs around 10 mm CW
were not different between the two methods (n ¼ 10, < 0.1
mm). This species is symmetrical under normal conditions
(no autotomy and regeneration); thus, only right legs of
symmetrical animals were measured. The relative length of
the walking leg was represented by the ratio of the leg
merus length to carapace width (LML/CW). The growth
phase was divided by the distribution pattern of LML/CW
ratio in relation to increase of CW. In addition, regression
lines were fitted using the least squares between CW and
LML for each growth phase after log (base 10) transformation: Log Y ¼ aLogX þ b, where X ¼ CW, Y ¼ LML.
Allometric growth type was categorized by the value of a:
negative allometry (a < 1), isometric allometry (a ¼ 1), and
positive allometry (a > 1) after the method reviewed by
Tessier (1960) and Hartnoll (1982).
Fig. 1. Positions of Eriocheir japonica measurements:
CW, carapace width; LML, third walking leg merus length.
RESULTS
I collected and measured 74 unsexed juveniles, 122 juvenile and 74 adult females, and
146 males. The LML/CW ratios varied widely
according to the carapace width (Fig. 2). Four
growth phases occurred per sex. In the first
phase, the LML tended to increase within the
range of 0.57 to 0.80 (about CW < 4 mm). In the
second phase, LML had relatively higher values
within the range of 0.62 to 0.89 (about 4 mm <
CW < 20 mm), and in the third phase decreasing within the range of 0.82 to 0.56 (about
CW < 38 mm). In the fourth phase, the leg
lengths were relatively shorter, within the range
of 0.72 to 0.59 in males and 0.65 to 0.53 in
females, but males were larger than females,
and LML tended to decrease in larger males
(about CW > 38 mm).
Allometric regression lines were fitted after
arbitrarily being divided into the four phases in
each sex according to the distribution of data
points in Fig. 3 as follows: 2–4-mm CW for the
first phase (n ¼ 28); 4–20-mm CW for the second phase (n ¼ 70 for males and n ¼ 78 for
females); 20–38-mm CW (males, n ¼ 63) and
20–37-mm CW (females, n ¼ 65) for the third
phase; CW ‡ 38 mm (males, n ¼ 59) and CW
‡ 37 mm (females, n ¼ 99) for the fourth
phase. The unsexed juveniles were used in the
first phase and partly in the second phase equally
for both sexes. Three male phases (first to third
phases) were divided by inflection, and the
fourth phase was divided from third phase by
a discontinuity. The four phases among females
were all divided by inflection. All regressions
were significant (F-tests, all were P < 0.01).
KOBAYASHI: RELATIVE GROWTH OF LEGS OF JAPANESE MITTEN CRAB
603
Fig. 2. Relationship between carapace width and third leg merus length/carapace width ratio of Eriocheir japonica, with
the division of four growth phases.
I compared regression lines among different
phases with analysis of covariance (Table 1).
In both sexes, differences existed between adjacent phases in the slope and/or Y-intercept. For
the fourth phase of females, juveniles and
adults did not differ, and these two types were
combined. Between sexes, significant differences only occurred for phases 3 and 4 in slope
and/or Y-intercept. Phase 1 exhibited positive
allometric growth during which the legs grew
relatively longer (a ¼ 1.369). Phase 2 was
nearly isometric, during which the legs remained relatively longer (a ¼ 1.052 for males;
1.041 for females). Phase 3 had negative allometry, during which the legs become relatively shorter and females were more negative
than males (a ¼ 0.822 for males; 0.702 for females). Phase 4 had negative allometry, during
which the legs become relatively shorter, and
males were more negative than females
(a ¼ 0.823 for males; 0.918 for females).
DISCUSSION
I have already described an outline of the
migratory process of Eriocheir japonica (see
Kobayashi, 1999a), and this migratory habit is
closely similar to that of E. sinensis (see Peters
and Panning, 1933; Panning, 1938). The relative growth of walking legs reflects the migratory habit. Megalopa larvae swim in the
estuary using pleopods, settle, and metamorphose to the postlarval stage (about CW ‡ 2
mm) in the upper tidal area of rivers where
mostly fresh water flows. The first phase (about
2–4 mm in CW) coincides with the crabs just
after settlement and metamorphosis (instars 1–
3), prior to upstream migration. Megalopa larvae usually move by swimming with pleopods,
but not by crawling with walking legs. The first
phase may be a transition phase of the main locomotive method and preparation for migration. The second phase (about 4–20 mm in
CW) coincides with upstream migration and
dispersal. Young crabs (about 4–11 mm in CW)
begin their upstream migration to the freshwater area, dispersing over the river from the
lower region to the upper region (Kobayashi,
1998). They continue to migrate in swarms,
during which they grow to 20 mm or more.
Relatively longer legs increase locomotor activity upstream. Crabs often climb on vertical
concrete walls in the fishway and weir and
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 3, 2002
Fig. 3. Regression lines for the third leg merus length
relative to carapace width of Eriocheir japonica. Axes are
normal logarithmic.
sometimes invade the terrestrial environment,
but concentrate in the area of rapid flows (Kobayashi, unpublished data). These juvenile
crabs grow larger until attaining maturity in the
wide area of the freshwater area. The third
phase (about 20–38 mm in CW) is the growth
phase after active migration until attaining maturity. They may not be so active as during the
second phase. Adults (sexually mature phase)
are about CW ‡ 37 mm in both sexes, but the
largest juveniles are about CW ¼ 60–65 mm,
and there is a wide range of overlapping sizes;
maturity size tends to be larger in the upper
region of the river (Kobayashi and Matsuura,
1995b). The fourth phase (about CW ¼ 38
mm) is the maturity phase in which adults participating in reproduction emerge and sexual
dimorphism becomes evident. The minimum
sizes of adults are within 35–40-mm CW in
both sexes in each local population (Kobayashi
and Matsuura, 1995b), and nearly agree with
the transition from the third phase to the fourth
phase of walking legs. Adults (hard-shell condition after puberty and terminal molt) migrate
downstream to the estuary and sea coast areas
for copulation and oviposition. However, for
adults, it may be much easier to migrate over
the long distance than it is for juveniles migrating upstream; adults have increased locomotor
activity after growing to a larger size and only
need to flow downstream when the river is rising. After reaching the tidal area, they can also
easily invade the sea during ebb tides. They become widely dispersed along the sea coast and
die without molting after reproduction (females
oviposit at most three times within a single season) (Kobayashi and Matsuura, 1995a). Thus,
the relative leg length may not reflect the migratory habit in this phase.
Sexual dimorphism in walking legs reflects
reproductive behavior, and partly agrees with
growth of the chelae (Kobayashi and Matsuura,
1993, 1996). Walking legs of adult males are
relatively longer than those of adult females,
and chelae are also relatively larger in males
(Kobayashi, 1999b; Kobayashi and Matsuura,
1993). Relatively long legs and large chelae in
males are useful during mating. After crabs migrate downstream from the freshwater area to
the tidal area, males actively wander in the
coastal area and search for mates (Kobayashi
and Matsuura, 1994). Mating is initiated by the
active behavior of males grasping and mounting the females. After copulation, males cradle
and guard females to protect their paternity
(Kobayashi, 1999c). Longer legs in males
likely are useful for successful guarding. Additionally, there is a chela dimorphism within the
adult males in the sea area; smaller males have
smaller chelae with thin hair, and larger males
have larger chelae with dense hair, and both
types are in an equally mature phase in which
crabs die after one reproductive season without
molting growth (Kobayashi, 1999b). Such a
morphological variation with present results in
adult males (smaller males with relatively small
chelae and relatively long legs and larger males
with large chelae and relatively short legs) suggests the presence of a different mating strategy
or tactics. Polymorphism in mature males
has been recorded in several species among
arthropods and explained to be caused by
sexual selection (Otte and Stayman, 1979;
605
KOBAYASHI: RELATIVE GROWTH OF LEGS OF JAPANESE MITTEN CRAB
Table 1. Results of the analysis of covariance between growth-phase regression lines of Eriocheir japonica collected from
the Saigo River, Japan during July 1996 through September 1997.
d.f.
Male–Male
Phase 1, Phase 2
Phase 2, Phase 3
Phase 3, Phase 4
Female–Female
Phase 1, Phase 2
Phase 2, Phase 3
Male–Female
Phase 4 (juvenile),
Phase 4 (adult)
Phase 3, Phase 4
(juvenile and adult)
Phase 2, Phase 2
Phase 3, Phase 3
Phase 4, Phase 4
Slope
Y-intercept
Slope
Y-intercept
Slope
Y-intercept
Slope
Y-intercept
Slope
Y-intercept
Slope
Y-intercept
Slope
Y-intercept
Slope
Y-intercept
Slope
Y-intercept
Slope
Y-intercept
Eberhard, 1980, 1982; Ra’anan and Sagi, 1985;
Shuster, 1987; Sagi and Ra’anan, 1988; Shuster
and Wade, 1991; Andersson, 1994). Larger
body and weapon size is profitable in male–
male competition. However, the development
of this competitive advantage may require a
greater quantity of energy and/or a longer time,
and such development may require uncommonly good environmental conditions. Conversely, individuals with smaller bodies and
weapons may be disadvantaged in competition;
however, they may be able to attain maturity
earlier or use alternative mating behaviors, such
as female mimicry, sneak matings, or searching
for females away from larger males, to compensate for their competitive disadvantages and increase their fitness. Disadvantages may not
always be compensated for, but smaller animals
may be more successful under poor conditions
(Eberhard, 1982; Andersson, 1994). Trade-offs
such as this may occur among males in E. japonica; however, how morphology interacts with mating patterns is still unknown. Further observations
and experiments are needed to solve the problem.
ACKNOWLEDGEMENTS
I thank the staff of the Laboratory of Marine Biology
and the Fisheries Research Laboratory, Faculty of Agriculture, Kyushu University for their kind assistance. I also
thank Dr. C. P. Norman, for the comments that improved
this paper.
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
1,
94
95
129
130
118
119
102
103
139
140
95
96
160
161
144
145
124
125
154
155
F-value
23.009
0.390
26.196
39.153
0.129
47.728
20.601
0.664
57.750
4.905
1.554
0.348
29.227
3.408
0.102
0.004
12.838
-0.730
7.655
178.911
P
<0.001
N.S.
<0.001
<0.001
N.S.
<0.001
<0.001
N.S.
<0.001
<0.05
N.S.
N.S.
<0.001
N.S.
N.S.
N.S.
<0.001
N.S.
<0.01
<0.001
LITERATURE CITED
Andersson, M. 1994. Sexual Selection. Princeton University
Press, Princeton, New Jersey.
Anger, K. 1991. Effects of temperature and salinity on the
larval development of the Chinese mitten crab Eriocheir
sinensis (Decapoda: Grapsidae).—Marine Ecology Progress Series 72: 103–110.
Clark, P. F., P. S. Rainbow, R. S. Robbins, B. Smith, W. E.
Yeomans, M. Thomas, and G. Dobson. 1998. The alien
Chinese mitten crab, Eriocheir sinensis (Crustacea:
Decapoda: Brachyura), in the Thames catchment.—Journal of the Marine Biological Association of the United
Kingdom 78: 1215–1221.
Cohen, A. N., and J. T. Carlton. 1997. Transoceanic
transport mechanisms: introduction of the Chinese mitten
crab, Eriocheir sinensis, to California.—Pacific Science
51: 1–11.
Eberhard, W. G. 1980. Horned beetles.—Scientific American 242: 166–182.
———. 1982. Beetle horn dimorphism: making the best of a
bad lot.—American Naturalist 119: 420–426.
Hartnoll, R. G. 1974. Variation in growth pattern between
some secondary characters in crabs (Decapoda, Brachyura).—Crustaceana 27: 131–136.
———. 1978. The determination of relative growth in
Crustacea.—Crustaceana 34: 281–293.
———. 1982. Growth. Pp. 111–196 in L. G. Abele, ed. The
Biology of the Crustacea. Vol. 2. Academic Press, New
York.
Huxley, J. S. 1932. Problems of Relative Growth. Menthuen, London. 276 pp.
Kobayashi, S. 1998. Settlement and upstream migration of
the Japanese mitten crab Eriocheir japonica (de Haan).
—Ecology and Civil Engineering 1: 21–31.
———. 1999a. Reproductive ecology of the Japanese
mitten crab Eriocheir japonica (de Haan): a review.—
Japanese Journal of Benthology 54: 24–35.
———. 1999b. Dimorphism in adult male Japanese mitten
crab Eriocheir japonica (de Haan).—Crustacean Research 28: 24–36.
606
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 3, 2002
———. 1999c. Mating behaviour of the Japanese mitten crab
Eriocheir japonica (de Haan). Pp. 231–247 in T. Okutani,
S. Ohta, and R. Ueshima, eds. Updated Progress in Aquatic
Invertebrate Zoology. Tokai University Press, Tokyo.
———, and S. Matsuura. 1992. Morphological changes of
the exoskeleton of the female Japanese mitten crab,
according to growth and maturity.—Research on Crustacea 21: 159–168.
———, and ———. 1993. Ecological studies on the
Japanese mitten crab Eriocheir japonicus De Haan-III.
Relative growth of the chela and soft-hair distribution on
the chela.—Benthos Research 45: 1–9.
———, and ———. 1994. Occurrence pattern and behavior
of the Japanese mitten crab Eriocheir japonicus De Haan in
the marine environment.—Benthos Research 46: 49–58.
———, and ———. 1995a. Reproductive ecology of the
Japanese mitten crab Eriocheir japonicus (De Haan) in its
marine phase.—Benthos Research 49: 15–28.
———, and ———. 1995b. Population structure of the
Japanese mitten crab Eriocheir japonicus (De Haan)–
clinal variations in size of maturity.—Crustacean Research 24: 128–136.
———, and ———. 1996. Relative growth of the Japanese
mitten crab Eriocheir japonica (De Haan) during the
juvenile stages.—Crustacean Research 25: 1–6.
Lee, S. Y. 1995. Cheliped size and structure: the evolution
of a multifunctional decapod organ.—Journal of Experimental Marine Biology and Ecology 193: 161–176.
Otte, D., and K. Stayman. 1979. Beetle horns: some patterns
in functional morphology. Pp. 259–292 in M. S. Blum
and N. A. Blum, eds. Sexual Selection and Reproductive
Competition in Insects. Academic Press, New York.
Panning, A. 1938. The Chinese mitten crab.—Smithonian
Institution Annual Report 3508: 361–378.
Peters, K., and A. Panning. 1933. Die Chinesische Wollhandkrabbe (Eriocheir sinensis H. Milne Edwards) in Deutschland.—Zoologische Anzeiger (Suppliment) 104: 1–180.
Ra’anan, Z., and A. Sagi. 1985. Alternative mating
strategies in male morphotypes of the freshwater prawn
Macrobrachium rosenbergii (de Haan).—Biological
Bulletin 169: 592–602.
Sagi, A., and Z. Ra’anan. 1988. Morphotypic differentiation
of males of the freshwater prawn Macrobrachium rosenbergii: changes in the midgut gland and the reproductive system.—Journal of Crustacean Biology 8: 43–47.
Sakai, T. 1976. Crabs of Japan and Adjacent seas.
Kodansha, Tokyo.
Shuster, S. M. 1987. Alternative reproductive behaviors:
three discrete male morphs in Paracerceis sculpta, an
intertidal isopod from the northern Gulf of California.—
Journal of Crustacean Biology 7: 318–327.
———, and M. J. Wade. 1991. Equal mating success
among male reproductive strategies in a marine isopod.—Nature 350: 608–610.
Tessier, G. 1935. Croisssance des variants sexuels chez
Maia squinado L.—Travaux de la Station Biologique de
Roscoff 13: 93–130.
———. 1960. Relative growth. Pp. 537–560 in T. H.
Waterman, ed. The Physiology of Crustacea. Vol. 1.
Academic Press, New York.
RECEIVED: 19 May 2001.
ACCEPTED: 29 November 2001.