LIFE C Y C L E STUDIES ON T H E
I N T R O D U C E D SPIDER CRAB PYROMAIA TUBERCULATA
(LOCKINGTON) ( B R A C H Y U R A : MAJIDAE).
I. E G G A N D L A R V A L STAGES
Toshio Furota
A B S T R A C T
T h e introduced spider crab P y r o m a i a t u b e r c u l a t a has recently colonized eutrophic bays in
Japan. In Tokyo Bay, this crab annually recolonizes an area o f the u p p e r bay w h i c h is subjected
to severe hypoxic and anoxic water and s u b s e q u e n t extinction of benthic animal populations
e v e r y summer. This research was designed to clarify e g g and larval g r o w t h characteristics of
P. tuberculata, and to shed light on h o w this species is able to effectively colonize such
eutrophic areas. Three sets o f experiments, incubation time, egg growth, and larval development, were conducted. Incubation time decreased with rising temperature, ranging from 3
m o n t h s at 8°C to 7 days at 26°C. Egg g r o w t h was classified in 4 stages by structure as noted
from external observation, and eye spots appeared in the final stage (last quarter o f the incubation period). T h e larvae passed through first and second zoeal and megalopal stages. T h e
experimental results, c o m b i n e d with field observations, indicate that P. t u b e r c u l a t a is capable
of breeding, incubating, hatching, and m e t a m o r p h o s i n g to first crab throughout the year in
Tokyo Bay. These reproductive and larval growth characteristics allow this species to annually
recolonize the u p p e r areas o f Tokyo Bay.
The spider crab P y r o m a i a tuberculata
(Lockington) was originally distributed
along the American Pacific coast from California south to Colombia (Rathbun, 1925;
Garth, 1958). Colonization by introduced
populations of P. tuberculata have been
found in East Asia and N e w Zealand (Webber and Wear, 1981; Carlton, 1987; Furota
and Furuse, 1988). In Japanese coastal waters, populations o f this spider crab have
been established in large eutrophic polluted
embayments: Tokyo Bay, Ise-Mikawa Bay,
and the eastern Seto Inland Sea (including
Osaka Bay), where hypoxic water develops
on a stagnant bottom during the s u m m e r
stratification period (Furota and Furuse,
1988). This distribution suggests that population maintenance of this spider crab in
Japanese coastal waters might depend on a
fluctuating environment, where a significant
part of the bottom is subject to seasonal extinction o f benthic populations (Furota and
Furuse, 1988).
In the upper part o f Tokyo Bay, catastrophic benthic defaunation occurs in late
summer, due to the development of hypoxic
and anoxic bottom water. A large population of the spider crab, however, recolonizes
this area from midfall to early summer o f
the following year, when a rich oxygen con-
tent is maintained in the bottom water layer
(Furota, 1988, 1990). Juvenile spider crabs
recruit in midfall when the s u m m e r hypoxic
period is over and the bottom environment
has improved. They reach maturity by early
spring, and then continue to breed until
killed by the hypoxic water in early summer. Early research (Furota, 1990) has suggested that the quick recovery o f the crab
population in the upper bay may be supported by intrusion o f larvae which are released from parent crabs living on healthy
bottoms in adjacent areas. To test the hypothesis, however, more detailed research
on reproduction and larval transport process
o f the spider crab is necessary.
Larval development series of the family
Majidae generally have 2 zoeal and 1 megalopal stages (Hartnoll, 1963, 1965). In P.
tuberculata, however, only the first and second zoeae have been described (Webber
and Wear, 1981; Terada, 1983), and no data
on duration of larval development is available. Furthermore, egg growth and egg size
have not been studied in detail. The laboratory experiments described in this paper
were designed to fill these gaps in our understanding of this species. The results provide data on egg growth and larval development, including the megalopal stage. A
detailed
analysis
of
the
entire
life
cycle,
f r o m e g g t h r o u g h r e p r o d u c t i o n , is p r o v i d e d
in the f o l l o w i n g p a p e r (Furota, 1996).
M A T E R I A L S AND M E T H O D S
E g g I n c u b a t i o n T i m e . - O n e to 10 adult female crabs
were reared in a 4-1 tank containing aerated Tokyo Bay
sea water (=30%o salinity) with half to equal n u m b e r
o f males, u n d e r constant temperature ( ± 1 ° C ) a n d an
artificial 12:12 day-night cycle. E g g incubation time
was estimated as duration in days f r o m e g g deposition
to hatching. M e a n daily temperature was used as the
incubation temperature for experimental analysis. In a
previous e x p e r i m e n t (Furota, 1988), incubation time
was o b s e r v e d at various temperatures b e t w e e n 8°C and
26°C. In this paper, additional experiments were conducted at 10°, 17°, 24°, and 27°C, temperatures for
w h i c h no data had been obtained in the previous study.
G r o w t h o f E g g s . - G r o w t h (increase in volume) and
d e v e l o p m e n t o f eggs during the incubation period were
e x a m i n e d at 17°C (±1°C). Ten eggs were r e m o v e d daily from the pleopods o f a female using fine tweezers.
T h e eggs were preserved in 5 % neutralized sea-water
Formalin. Since the eggs s h o w e d an oval to spherical
shape, the m a x i m u m and m i n i m u m diameters o f the
eggs were estimated using an optical micrometer. Egg
v o l u m e ( m m ' ) was calculated as irab2/6 where a and
b are the m a x i m u m and m i n i m u m diameters in m m ,
respectively.
Surface structure o f the collected eggs was o b s e r v e d
u n d e r a stereomicroscope during the incubation period.
L a r v a l G r o w t h . - O v i g e r o u s females carrying n e w l y
deposited eggs were kept in a 10-1 tank with nearly
the same n u m b e r o f males. Temperature was kept constant t h r o u g h o u t the experiment. Experiments were
conducted at 4 temperatures (10°, 15°, 20°, and 25°C,
± 1 ° C ) w h i c h represent almost the full range of bottom
temperatures in the collection area o f Tokyo Bay.
W h e n the e g g yolks had been c o n s u m e d , the females
were isolated individually in 1-1 tanks.
I m m e d i a t e l y after hatching, zoeae were r e m o v e d to
1 of 3 types o f experimental container: (1) 4-1 glass
tank; (2) 1-1 plastic-tube cage covered with 0 . 5 - m m
nylon mesh a n d suspended in a 20-1 tank; and (3) 500ml beaker. The m a x i m u m n u m b e r o f larvae in each
type o f c o n t a i n e r was 300, 50, and 10, respectively.
Filtered T o k y o B a y sea water (=30%o salinity) was
used for this part of the experiment. Gentle aeration
was provided, except for the 500-ml beaker. The containers were kept at constant temperature ( ± 1 ° C ) and
a 12:12 day-night cycle was artificially created with a
fluorescent light. Sea water was c h a n g e d every 1-3
days except for the plastic-tube cage, in w h i c h the tank
water was constantly filtered with bottom sand. The
larvae w e r e fed with either a single food item or mixture o f items, c o m p o s e d o f artificial feed for cultured
p r a w n larvae (Artificial Plankton, p r o d u c e d by N i h o n
N o s a n K o g y o , Inc.), the brackish water rotifer B r a chionus plicatili.s Miiller, w h i c h was cultured on Chlorella (produced by N i p p on Chlorella K o g y o Co., Inc.),
n e w l y hatched California brine shrimp (distributed by
Bio-Marine, Inc.), as well as natural plankton collected
f r o m Tokyo B a y with a 70-wm m e s h plankton net. The
n u m b e r o f surviving larvae was c o u n t e d daily, a n d the
Fig. 1. Relationship between water temperature and
egg incubation time of the introduced spider crab Pyromaia tuberculata under laboratory conditions. Redrawn from Furota (1988) (0), with results of this
study added ( · ) .
growth of the larvae was carefully observed and recorded.
All crabs used in this study were collected in upper
Tokyo Bay (35°30'N, 139°50'E) using a trawl or SCUBA diving.
RESULTS
Egg Incubation T i m e . - F o u r ovigerous females were reared at 27°C, but none of
these were able to hatch their eggs, and two
females died during the experiment. Data
from nine other trials, at temperatures at
24°, 17°, and 10°C, can be combined with
results of the previous egg experiment (Furota, 1988) to yield a preliminary relationship between temperature and incubation
time, which is shown in double logarithmic
plot (Fig. 1).
Incubation time decreased from 80 days
at 8°C to 7 days at 26°C, as shown by the
following equation:
y = 7833.5x-212,
r = 0.993, N = 63
where y = incubation time (days); x = temperature (°C).
E g g G r o w t h . - F i g u r e 2 shows changes in
egg volume during the entire period o f egg
incubation at 17°C. The egg volume increased from 0.027 mm3 (0.39 m m in mean
diameter) to 0.045 mm3 (0.44 m m in mean
diameter). Egg volume increased steadily
from day 5 to day 10, then sharply from
Fig. 2. C h a n g e in egg v o l u me o f the introduced spider crab P y r o m a i a t u b e r c u l a t a through incubation period
f r o m e g g deposition to hatching at 17°C. E g g s hatched at 18 days after deposited.
day 10 to day 15, while no substantial
change was observed at the initial and final
phases o f development. Based on surface
structure observations conducted during
this experiment, egg development was classified into 4 stages, shown in Table 1. Eye
spots appeared during the final stage (the
final quarter o f the incubation period).
L a r v a l G r o w t h . - T a b l e 2 shows experimental conditions and results for larval proTable 1. Developmental stages of eggs of the introduced spider crab Pyromaia tuberculata during a total
incubation period (18 days) at 17°C.
gression. The values for first zoea indicate
the initial number o f larvae used in each
trial, and the following three figures indicate the frequency o f the number of larvae
which reached each successive stage. A total of 189 megalopae and 43 first crabs
were obtained.
First crabs were obtained only at 20° and
25°C. No clear influence on larval survival
was observed for the various experimental
containers and feed items. Figure 3 shows
molting schedules o f larvae o f P. tuberculata at four temperatures. At 20° and 25°C,
the l a r v a e m o l t e d at r e g u l a r i n t e r v a l s
throughout the experiment, with total larval
stage durations o f 17.5 days and 14.0 days,
respectively. For 15°C and 10°C, on the other hand, not only were durations for the
zoeal stage much longer, but development
was terminated, respectively, at the megalopal and second zoeal stages.
Table 2. R e a r i n g conditions and frequency (%) o f survived individuals through molting growth in laboratory
experiments on larval growth o f the introduced spider crab P y r o m a i a tuberculata. In the first zoea c o l u m n the
n u m b e r in ( ) indicates the initial n u m b e r o f the zoeae used for each experimental series.
* C o n t a i n e r : 4 L = 4-1 glass a q u a r i u m ; b e a k e r = 5 0 0 - m l b e a k e r ; c a g e = 1-1 c a g e d tube.
* * F o o d : m i x t u r e of: AP, Artificial P l a n k t o n ; Ar, A r t e m i a ; NP, N a t u r a l p l a n k t o n ; Rt, Rotifer.
DISCUSSION
The experiments described here have
clarified several aspects of egg and larval
development for P. tuberculata. Incubation
time was shown to decrease with rising
temperature, with an upper limit on egg development at 26°C (Fig. 1). Volume o f eggs
throughout development, measured at 17°C
over an 18-day incubation period, was
shown to increase from 0.028-0.046 mm3.
Growth increment was steady from day 5
to day 10, but increased sharply from day
10 to day 15 (Fig. 2). Eye spots appeared
Fig. 3. Influence of temperature on larval developm e n t of the introduced spider crab P y r o m a i a tuberculata. Points indicate m e d i a n time o f molting, bars
indicate time range.
in the final stage of the incubation period
(Table 1).
Mean diameter of the egg at the final
stage was 0.44 m m . The size o f the eggs o f
P. tuberculata demonstrates that P. tuberculata falls in the smallest egg-volume
group among spider crabs (Hartnoll, 1965).
Hines (1982) noted that egg volume tends
to be smaller in smaller species o f spider
crabs. Body weight of adult female P. tuberculata ranges from 0.23-1.25 g with a
mean o f about 0.7 g in live weight (Furota,
1996). The egg volume of P. tuberculata
measured here is close to the egg volume
of Californian spider crabs, such as Mimulus foliatus Stimpson and P u g e t t i a richii
Dana, which are the same size as P. tuberculata (see Hines, 1982). The results generated here confirm Hines' conclusion.
Wear (1974) compared egg volume and
tolerance of high temperatures a m o n g British crustacean decapods, showing that only
smaller eggs (less than 0.02 m m ' when deposited), such as these of portunid crabs,
Carcinus m a e n a s (L.) and Macropipu.s spp.,
can develop in high temperatures higher
than 25°C. Although original egg volume
(0.028 m m ' ) of P. tuberculata is greater
than those o f these portunid crabs, the eggs
o f P. tuberculata show an equivalent tolerance to high temperatures.
Hartnoll (1963) stated that spider crabs
pass through first and second zoeal stages
and a megalopal stage. Results o f this study
confirm this 3-stage larval development for
P. tuberculata as well. Durations o f larval
development were observed at 25° and
20'C, varying from 14-17.5 days. The larvae molted at regular intervals throughout
larval development. Based on this characteristic, and on the the results o f first zoeal
durations at each temperature (Fig. 3),
planktonic durations at 15° and 10°C were
extrapolated at about 1 and 2 months, respectively.
Female P. tuberculata had already been
observed breeding continuously throughout
the year in Tokyo Bay (Furota, 1988). Data
from incubation experiments clearly indicate that females are able to hatch their eggs
from 8 to 26°C, which covers the annual
bottom temperature fluctuation in their Tokyo Bay habitat (Furota, 1995). W h e n combined, these observations and experimental
results demonstrate that larvae o f P. tuberculata can be produced throughout the
year in Tokyo Bay.
In the larval growth experiments, P. tuberculata failed to reach first crab at temperatures of 15° and 10°C. Field observations in Tokyo Bay, however, indicate that
megalopae are present throughout the year,
including winter months when temperatures
are as low as 8°C (Furota, unpublished).
There is thus a strong possibility that the
inability to molt as seen in the rearing experiment was due to some aspect o f the
food or container environment.
Grassle and Grassle (1974) discussed
life-cycle characteristics o f the polychaete
Capitella capitata (Fabricius), commonly
found in organic polluted marine environments. They stated that this polychaete can
quickly colonize disturbed bottoms, after
recovery of the environment, by opportunistic recruitment that is supported by yearround larval supply. The results o f this
study demonstrate that P. tuberculata is
able to breed, incubate, hatch, and metamorphose to first crab throughout the year
in Tokyo Bay, and is also capable o f yearround larval supply which could possibly
support opportunistic recruitment. These reproductive and larval growth characteristics
allow juvenile P. tuberculata to annually
recolonize that portion o f Tokyo Bay which
is s u b j e c t e d t o s e a s o n a l b e n t h i c e x t i n c t i o n .
They
m a y also be related to the ability of
this species to quickly recolonize the u p p e r
areas of Tokyo
Bay
by
recruitment of ju-
venile crabs soon after the hypoxic a n d anoxic
water period
is o v e r .
The
entire
life
cycle, including crab stage and reproduct i o n , o f P . t u b e r c u l a t a is d i s c u s s e d i n t h e
following paper (Furota, 1996).
ACKNOWLEDGEMENTS
I a m grateful to Dr. Taiji Kikuchi for his critical
c o m m e n t s on the m a n u s c r i p t and his helpful suggestions. Miss Akiko Iijima and m a n y students in the Laboratory o f Marine Biology, Toho University, are
thanked for their assistance in the experiments. Mr.
Yoshifumi M i y a m a of C h i b a Prefecture Tokyo Bay
S e a F a r m i n g Center, and Mr. Hiroyuki Suzuki o f Chiba
Prefecture S e a Farming Center, kindly provided the rotifer and Chlorella. I also thank Dr. Kevin Short for
editing the English.
LITERATURE C I T E D
Carlton, J. T. 1987. Patterns o f transoceanic marine
biological invasions in the Pacific O c e a n . - B u l l e t i n
o f M a r i n e Science 41: 452�465.
Furota, T. 1988. T h e ecology o f the introduced spider
crab P y r o m a i a t u b e r c u l a t a in an organically polluted bay (preliminary r e p o r t ) . - B e n t h o s R e s e a r c h 33/
34: 7 9 - 8 9 . [In Japanese with English abstract.]
�
â ��
â ��
â ��
â �. 1990. Population structure of the introduced
spider crab P y r o m a i a t u b e r c u l a t a in t h e innermost
region of Tokyo B a y . - B e n t h o s Research 39: 1-7.
[In Japanese with English abstract.]
�
â ��
â ��
â ��
â �. 1996. Life cycle studies on the introduced
spider crab P y r o m a i a tuberculata (Lockington)
(Brachyura: Majidae), II. Crab stage a n d reproduct i o n . - J o u r n a l o f Crustacean Biology 16: 7 7 - 9 1 .
�
â ��
â ��
â ��
â �. and K. Furuse. 1988. Distribution of the introduced spider crab, P y r o m a i a tuberculata, along
the coast o f J a p a n . - B e n t h o s Research 33/34: 75�
78. [In J a p a n e s e with English abstract.]
Garth, J. S. 1958. B r a c h y u r a o f the Pacific Coast o f
America, O x y r h y n c h a . - A l l a n H a n c o c k Pacific Expedition 2 1 ( 1 - 2 ) : 1-854.
Grassle, J. E, and J. P. Grassle. 1974. Opportunistic
life histories and genetic systems in marine benthic
p o l y c h a e t e s . - J o u r n a l o f Marine R e s e a r c h 32: 253�
284.
Hartnoll, R. G. 1963. T h e biology of M a n x spider
c r a b s . - P r o c e e d i n g s o f the Zoological Society of
L o n d o n 141: 445�496.
�
â ��
â ��
â ��
â �. 1965. The biology o f spider crabs: a comparison o f British and J a m a i c a n species.â��Crustac e a n a 9: 1â��16.
Hines, A. H. 1982. Allometric constraints and variables of reproductive effort in b r a c h y u r a n crabs.�
M a r i n e Biology 69: 3 0 9 - 3 2 0 .
Rathbun, M. J. 1925. The spider crabs o f America.�
United States National M u s e u m Bulletin 129: 1�
â�
613.
Terada, M. 1983. Preliminary notes on the zoeae o f
brachyuran Crustacea f r o m the Sea o f Enshunada,
S h i z u o k a P r e f . - Z o o l o g i c a l M a g a z i n e 92: 10-13.
[In Japanese with English abstract.]
Wear, R. G. 1974. Incubation in British d e c a p o d Crustacea, and the effects o f temperature on the rate and
success o f e m b r y o n i c d e v e l o p m e n t . - J o u r n a l o f the
M a r i n e Biological Association of the United Kingd o m 54: 7 4 5 - 7 6 2 .
Webber, W. R., and R. G. Wear.
1981. Life history
studies on N e w Zealand Brachyura 5. L a r v a e of the
family M a j i d a e . - N e w Zealand Journal o f Marine
and Freshwater Research 15: 3 3 1 - 3 8 3 .
RECEIVED: 28 D e c e m b e r 1994.
AccEprED: 16 May 1995.
Address: Laboratory o f Marine Biology, Faculty of
Science, Toho University, M i y a m a 2-2-1, Funabashi,
Chiba, 274 Japan.
ANNOUNCEMENT
A n International Conference on Integrated Management and Sustainable Development
in Coastal Zones will be held at Rimouski, Quebec, Canada, 12-17 August 1996. The
conference will have the following objectives: (1) to review current knowledge since the
Coastal Zone C a n a d a ' 9 4 Conference held at Halifax in September 1994, (2) to provide
a forum by bringing together representatives o f governmental, academic, business, and
coastal communities and other interest groups involved in the management, development,
and use o f coastal zones, and (3) to frame recommendations arising from the deliberations
o f the conference and to outline new research and management directions.
Papers and case study presentations are invited from national and international coastal
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and primary resource users, industry and business. The international conference will feature oral and poster presentations, plenary panel sessions, and round-table discussions.
For more information or in order to receive the second announcement please write to:
Professor M o h a m m e d EI-Sabh
Coordinator Coastal Zone Canada ' 9 6 International Conference
Groupe de recherche en environmant cotier (GREC)
Universite du Quebec
310, allee des Ursulines
Rimourski, Quebec, Canada G 5 L 3A11
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