LABORATORY OBSERVATIONS ON THE EARLY LIFE STAGES OF
THE DIAMOND SQUID THYSANOTEUTHIS RHOMBUS
KAZUTAKA MIYAHARA 1 , KATSUYA FUKUI 2 , TARO OTA 3
AND TAKASHI MINAMI 4
1
Hyogo Tajima Fisheries Technology Institute, 1126-5 Sakae, Kasumi, Kami, Hyogo 669-6541, Japan;
Shimane Prefectural Fisheries Experimental Station, 25-1 Setogashima, Hamada, Shimane 697-0051, Japan;
3
Tottori Prefectual Fisheries Research Center, Ishiwaki, Yurihama, Tohaku, Tottori 689-0602, Japan;
4
Graduate School of Agricultural Science, Tohoku University, 1-1 Tsutsumidori, Amamiya-machi, Aoba, Sendai, Miyagi 981-8555, Japan
2
(Received 8 June 2005; accepted 2 November 2005)
ABSTRACT
The early life stages of the diamond squid Thysanoteuthis rhombus from early embryogenesis to
post-hatching (0 – 7 days old) were observed through laboratory incubation using egg masses collected
in the southern Sea of Japan. The egg diameter and mantle length increased during embryonic development through hatching. Mantle-length growth was linear over time, and the growth rate was
significantly higher at 258C than at 208C. The inner yolk was located on the dorsal side of the
mantle cavity and increased in volume through hatching. Immediately after they hatched, the hatchlings remained on the bottom of culture plates with their ventral sides facing up, but 2– 3 days after
hatching they began to swim with their dorsal sides facing up. Feeding experiments were conducted,
but none of the hatchlings fed. Statolith growth increments were shown to form daily. Ontogenetic
changes that occur from fertilization through post-hatching are discussed.
INTRODUCTION
The diamond squid Thysanoteuthis rhombus Troschel, 1857 is a
large nektonic squid (maximum dorsal mantle length ¼ 100 cm,
maximum body weight ¼ 30 kg) distributed worldwide in
tropical to temperate waters (see reviews in Nigmatullin &
Arkhipkin, 1998; Bower & Miyahara, 2005). It spawns large
(60 – 180 cm in length, 11 – 30 cm in diameter), oblong, freefloating egg masses (Nigmatullin & Arkhipkin, 1998), and is
one of the few oceanic cephalopods whose egg masses are
commonly observed (Okutani, 1982). Recently, new records of
T. rhombus egg masses were reported from the eastern Atlantic
Ocean and Mediterranean Sea (Guerra et al., 2002), and
waters around Japan (Watanabe et al., 1998; Ando et al., 2004;
Miyahara et al., 2006).
Embryonic development of T. rhombus has been well described
(Arnold & O’Dor, 1990; Watanabe et al., 1998; Guerra et al.,
2002), but there are few ecological studies on the early life
stages. Sabirov et al. (1987) suggested that the buoyancy of egg
masses allows the embryos to undergo fast development in the
warm surface waters, but they did not examine the relationship
between development time and temperature. Watanabe et al.
(1998) noted that hatchlings can survive without feeding for
4 – 5 days using the large volume of yolk inside the mantle
cavity, and that 4- to 5-day-old hatchlings have undeveloped
beaks and undifferentiated clubs, which suggests that their first
prey might be inactive. Suspension feeding has been proposed
for some ommastrephid paralarvae (O’Dor, Helm & Balch,
1985; Vidal & Haimovici, 1998), but feeding experiments
have not been conducted for T. rhombus to identify their first
prey. Nigmatullin, Arkhipkin & Sabirov (1995) derived a
growth formula for T. rhombus in tropical to subtropical waters
based on statolith analysis, but there is little information on
the early life stages, and the periodicity of growth increments
that occur in the statoliths after hatching remains assumptive.
Correspondence: K. Miyahara; e-mail: [email protected]
In this paper, we provide results of laboratory observations on
the eggs, embryos and hatchlings of T. rhombus using egg masses
collected in the Sea of Japan during late October to early
November, 2004 (Miyahara et al., 2006). Embryonic development and changes in ML were investigated at 208C and 258C.
The periodicity of statolithincrement formation and possible
first food for hatchlings were also examined, and the early life
stages are discussed from an ecological viewpoint.
MATERIALS AND METHODS
From the southern Sea of Japan, which is a major fishing
ground for Thysanoteuthis rhombus in Japan (Miyahara & Gorie,
2004; Miyahara et al., 2005; Bower & Miyahara, 2005), four
egg masses (EM1 – 4) were collected during 29 October to
5 November 2004 and transported to onshore laboratories
immediately or on the day after collection using a 20- or 80-l
tank filled with seawater (Fig. 1). Incubation started 11, 3, 8
and 22 h after collection (EM1 – EM4, respectively). A total of
120– 150 eggs were removed from each egg mass together with
a very small volume of the surrounding gelatinous substance
and put into sterilized 6-well culture plates (Becton Dickenson
Falcon 3046, 10 – 20 eggs per well until hatching, 1 – 3 eggs per
well after hatching) filled with 12 ml of filtered seawater
(salinity: 32.9– 33.4). Two thirds of the seawater was manually
exchanged once or twice a day (except for the first three days
for EM3, during which there was no water exchange), and
dead or deteriorated eggs were removed. The water temperature
at collection was about 208C, so the incubation temperature was
maintained at this temperature for all egg masses. In addition,
another set of the eggs from the same part of EM4 was incubated
at 258C, which corresponds to the optimum temperature for
spawning (.23 – 248C, Nigmatullin & Arkhipkin, 1998).
Eggs and embryos were assigned to the developmental stages
described in Watanabe et al. (1998) for T. rhombus and in
Watanabe et al. (1996) for the Japanese common squid,
Todarodes pacificus Steenstrup, in which stages 4 – 10 are in cleavage, 11 – 15 are in segregation of the germ layers and growth
Journal of Molluscan Studies (2006) 72: 199– 205. Advance Access Publication: 23 February 2006
# The Author 2006. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved.
doi:10.1093/mollus/eyi068
K. MIYAHARA ET AL.
et al., 1998). The inner yolk is visible through the mantle
(Ando et al., 2004), and has a spheroidal shape with a major
axis (A) and two minor axes (B). We approximated the
volume of the inner yolk (mm3) as (4pAB2)/3, after measuring
the length of the axes (A and B) from the dorsal and/or
ventral sides using a video micrometer.
To examine the possible first food of hatchlings, three
phytoplankton species (Skeletonema costatum, Bacillariophyceae;
Chaetoceros glacilis, Bacillariophyceae; and Pavlova lutheri,
Haptophyceae) and the nauplii of one crustacean (Artemia sp.)
were fed to T. rhombus hatchlings as a prey (Table 1). They
were preliminarily cultured, and added to 12 – 250 mL filtered
seawater (208C) containing 5 – 10 T. rhombus hatchlings in
dupli- or triplicated culture plates or beakers. After 6 – 48
hours, the hatchlings were removed from the seawater, and
their stomachs were dissected under a stereomicroscope to
determine if they had fed.
Statoliths were analysed using the methods of Natsukari
(1998) and Nakamura (2000). They were extracted under a
stereomicroscope from frozen or preserved (in 90% ethanol)
hatchlings incubated at 208C (0 – 6 days after hatching, n ¼ 5
on each day, total ¼ 35). The length (maximum radius) and
width (minimum radius) of each statolith were measured using
a light microscope under 200X magnification. The number of
growth increments was counted excluding the outline of the statoliths, and linear regressions (number of increments against
age) were obtained by the least-squares method. To determine
if the growth increments formed daily, the slope of this regression
was tested against 1 using a t-test for both the right and left
statoliths. Difference in the growth rate between right and left
statoliths was also examined using a t-test.
Figure 1. Sites where four diamond squid Thysanoteuthis rhombus egg
masses (EM1–4) were collected.
of the blastoderm, 16 – 26 are in organogenesis and 27 – 34 are
post-hatching. Eggs in EM1– 4 began the incubation in stages
15 –18, 24 – 25, 6 –9 and 4 – 6, respectively. The hatching day
was defined as the day when more than half of the existing
embryos hatched. Since hatchlings were also used for prey
experiments and statolith analysis, survival rates were not
estimated in our study. The egg diameter (ED, diameter of the
egg chorion) and dorsal mantle length (ML) of developing
embryos were measured using a video micrometer (Olympus
VM-60) under 10 – 45X magnification. Differences in the ED
and ML at hatching among the egg masses (208C) were compared using one-way ANOVA after testing the homogeneity of
variances using Bartlett’s test, and then Tukey’s test was used
for a multiple comparison of the means. In EM4, differences in
the mean ED and ML between the 208C and 258C incubation
conditions were examined using a t-test. A regression of ML
on time was run using the least squares method, and the
growth rate was estimated. In EM4, difference in the growth
rate between the 208C and 258C incubation conditions was
also examined using a t-test. While sepioid and myopsid
embryos have a large external yolk (Watanabe et al., 1996),
T. rhombus embryos in early organogenesis have a small domeshaped external yolk sac in the cephalic region (outer yolk
sac), from which yolk is transferred to the inner yolk sac
located within the mantle cavity before hatching (Watanabe
RESULTS
The egg diameter (ED) and dorsal mantle length (ML) of
embryos increased during embryonic development (Fig. 2).
The mean ED for each egg mass increased from 1.5 – 2.0 mm
at the beginning of incubation to 1.7 – 2.4 mm just before hatching (EM1 – 4, n ¼ 10 – 30). The mean ED at hatching (stages
26 – 28) differed significantly among EM1– 4 (208C) except
between EM1 and EM4 (P , 0.05, Tukey’s test), and was
smallest in EM3. In EM4, there was no significant difference
in ED between 208C and 258C (P . 0.05, Welch’s t-test).
The mean ML was 0.7 – 0.8 mm in early organogenesis (stages
15 – 18, measured in EM3 and EM4; n ¼ 30) and 1.3 – 1.5 mm
at hatching (measured in EM1– 4, n ¼ 10 – 30). Hatching
occurred 3 – 8 days after the egg masses were collected from
the sea and was completed within two days for each egg mass.
The mean ML at hatching differed significantly (P , 0.05)
among EM1– 4 (208C) except between EM1 and EM2, and
between EM1 and EM4 (Tukey’s test), and was smallest in
EM3. In EM4, no significant difference was observed in MLs
between 208C and 258C (P . 0.05, t-test).
Table 1. Feeding experiments for T. rhombus hatchlings. None of the four prey items was found in the stomachs of the hatchlings.
Prey (cultured plankton)
Size of prey
Initial no.
No. of
Vol. of
(mm)
of prey
T. rhombus
seawater (ml)
Skeletonema costatum (Bacillariophyceae)
0.050 –0.150a
1.0 103
5
12
Chaetoceros glacilis (Bacillariophyceae)
0.006 –0.008b
4.3 107
10
250
Pavlova lutheri (Haptophyceae)
0.007 –0.010b
1.0 108
10
250
10 2 20
5
12
Nauplii of Artemia sp. (Crustacean)
a
b
0.450 –0.550
c
c
length of colony; length of cell; total length.
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EARLY LIFE STAGES OF THYSANOTEUTHIS RHOMBUS
cavity. The mean yolk volume was largest at around
1.3 – 1.5 mm in ML and age 0, and then decreased with time
after hatching (Fig. 4). The colour of the yolk changed from
dark purple to light pink, especially in the post-hatching stages.
During the first two days after hatching, hatchlings remained
on the bottom of the wells without swimming and with the
ventral-side facing up (Fig. 5A). Two or three days after hatching, they began swimming with the dorsal-side facing up
(Fig. 5B). When touched, they often withdrew their head into
the mantle cavity for about 10 – 20 s, and inking behavior was
observed for the first time in hatchlings .2 days old. Numerous
cilia around the mouth of hatchlings (0 – 7 days old) were
observed to beat continuously, but no active movement of the
tentacles was observed, and their clubs were not differentiated.
No prey was found in the stomachs of the hatchlings in the
feeding experiment (Table 1). All hatchlings died within seven
days of hatching.
Statoliths became visible in the anterior part of the statocysts
one day before hatching (Fig. 6). The statoliths increased from
0.038 – 0.067 mm in length and 0.021 – 0.034 mm in width at
hatching (n ¼ 10) to 0.094 – 0.110 mm in length and
0.045 – 0.052 mm in width at 6 days after hatching (Fig. 7).
All relationships between age (days after hatching) and sizes
(length or width) of the statoliths (Fig. 7), between the
number of increments and sizes (Fig. 7), and between age and
number of growth increments (Fig. 8) were linear (R 2 ¼ 0.69–
0.89, P , 0.001). Slopes of the regressions of growth-increment
number on age were 0.88 for the left statoliths and 0.92 for the
right statoliths, and neither significantly differed from 1.0
(P . 0.1, t-test, Fig. 8). Growth rates of the right and left
statoliths did not differ significantly (P . 0.05, t-test, Fig. 8).
Figure 2. Changes of egg diameter (ED, diameter of chorion) and
mantle length (ML) before hatching (mean + SD, n ¼ 30). Numbers
show the embryonic stages of Watanabe et al. (1996). The eggs were
incubated at 208C (EM1–4, closed circle) and 258C (EM4, open
square).
The ML increased linearly over time between stage 18 and
hatching (Fig. 3). The growth rate ( ¼ slope of the regressed
line assigned for stages after 18) was 0.07 – 1.12 mm d21 at
208C (EM1 –4) and 0.20 mm d21 (EM4) at 258C. In EM4,
the difference of the growth rates between 208C and 258C was
significant (P , 0.001, t-test), and as a result, hatching occurred
later at 208C (7.4 days after collection) than at 258C (4.4 days).
Yolk was visible at both the dorsal side of mantle cavity (inner
yolk) and the cephalic region (outer yolk) from early organogenesis to hatching. As in Watanabe et al. (1996, 1998), we observed
that the dome-shaped outer yolk was transferred to the mantle
DISCUSSION
The egg diameter (ED) and dorsal mantle length (ML)
increased during embryonic development in all the egg masses
(Fig. 2). Sakurai & Ikeda (1994) and Sakurai et al. (1995)
pointed out that an increase in the ED (i.e. chorion expansion)
is needed to allow space for the embryos to revolve and respire.
Figure 3. Changes of mantle length (ML) during incubation
(mean + SD, n ¼ 30 before hatching and 6–20 for hatchlings). Closed
marks show hatching day. Linear regressions by least-squares method
were applied to stages after 18 of Watanabe et al. (1996). Growth rate
(¼slope of the lines) was 0.09, 0.07, 0.12 and 0.12 mm d21 for EM1–4
(under 208C) and 0.20 mm d21 for EM4 (258C), respectively.
Figure 4. Changes of the inner yolk volume (mean + SD) with mantle
length (ML) and age (days: from one day before hatching (age 21) to six
days after hatching (age 6)).
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K. MIYAHARA ET AL.
Figure 5. Posture of hatchlings in a spectrophotometer cell. For the first two days after hatching, hatchlings remained on the cell bottom with the
ventral side facing up (age 0 –2 days, A). Several days after hatching, they began swimming with the dorsal side facing up and started to display defensive reflexes, such as inking (B).
Figure 6. Statocysts (ST) and statoliths (SL). A. One-day old hatchling (ventral view with funnel removed). Scale bar: 1 mm. B. Statoliths extracted
from a 6-day old hatchling; the right statolith (R) measured 0.105 mm in length (a) and 0.047 mm in width (b), and the left one (L) measured
0.108 mm in length (a) and 0.052 mm in width (b). Six growth increments (closed triangles) were counted in each statolith (outline of the statolith
was excluded).
In the four egg masses maintained at 208C (EM1 – 4), the
growth rate was highest in EM3 and EM4, followed by EM1
and EM2. This may have been due to differences in the initial
stage(s) at which incubation was started. Embryonic development occurs quicker at a constant water temperature (such
as in an incubator) than at a fluctuating temperature (such as
in the sea) even when the mean temperature is the same
(observation in Sepioteuthis lessoniana, Segawa, 1994).
Eggs of oceanic squids are characterized by their small size,
short hatching period and large volume of inner yolk, which
possibly reflect a reproductive strategy for dispersion in the
open sea (Watanabe et al., 1996). In T. rhombus, the inner yolk
sac occupies a large part of the mantle cavity, especially along
the dorsal side, at hatching (Watanabe et al., 1998). The yolk
volume inside the mantle cavity peaked around hatching,
when yolk was transferred from the outer yolk. This large
inner yolk caused the hatchings to be positioned with the
ventral-side facing up for 1 – 2 days after hatching until
the yolk was consumed. The egg masses (EM1 – 4) were floating
at the time of hatching (Miyahara et al., 2006), but Sabirov
The ED and ML at hatching both differed among egg masses,
and were smallest in EM3. Seawater was not exchanged
during the early incubation period of EM3, which may have
restricted growth due to a lack of oxygen. However the sizes at
hatching were within the ranges of previous reports based on
eggs collected from the sea (Nigmatullin & Arkhipkin, 1998;
Guerra et al., 2002), suggesting that the embryonic development
in our experiment was normal. Since no difference was observed
under different temperatures using the eggs from an identical egg
mass (EM4), differences in ED and in ML among egg masses at
hatching may have been due to differences in environmental
conditions before collection or to premature hatching,
which can be caused by external stimulation of the embryos
(Watanabe et al., 1996).
The embryonic development and growth of cephalopods is
highly temperature dependent (Boletzky, 1987; Forsythe,
2004). In T. rhombus, embryos grew significantly faster at 258C
than at 208C. Our result supports the suggestion of Sabirov
et al. (1987) that the positive buoyancy of the egg masses positions them where growth will be fastest in the water column.
202
EARLY LIFE STAGES OF THYSANOTEUTHIS RHOMBUS
Figure 7. Relationships of statolith sizes against age (days after hatching, top) and number of growth increments (bottom). Left (L) and right (R)
statoliths from 0- to 6-day-old hatchlings (n ¼ 5 for each day, total ¼ 35) were examined.
as has been proposed for some ommastrephid paralarvae
(O’Dor, Helm & Balch, 1985; Vidal & Haimovici, 1998).
However, the high growth rate of T. rhombus (Nigmatullin &
Arkhipkin, 1998) suggests that it probably begins to feed on
planktonic and/or micronektonic organisms soon after hatching.
In tropical and subtropical waters, the chlorophyll maximum
occurs near or below the depth of penetration of 1% of the
surface light (Ventric, McGowan & Mantyla, 1973), and near
Okinawa (Pacific Ocean), which is a spawning ground for
T. rhombus (Bower & Miyahara, 2005), copepod biomass and
primary productivity are also highest at subsurface depths
(Nakata et al., 2001).
Statoliths first appeared one day before hatching. Statoliths at
hatching were larger than the nuclei in statoliths from young to
adults (mean length ¼ 0.026 mm, mean width ¼ 0.018 mm,
Nigmatullin et al., 1995), suggesting that growth increments
begin forming 0 – 1 day before hatching. The statocyst is part
of the gravity and angular acceleration receptor system
(Budelmann, 1994), and statoliths of T. rhombus are relatively
large compared with those of various cephalopods in similar
stages (Arkhipkin & Bizikov, 1997; Shigeno et al., 2001). In
other oceanic squids, during the first several days after hatching,
increments are indistinct (e.g. Illex illecebrosus (Dawe et al., 1985),
Dosidicus gigas (Yatsu, Tafur & Maravi, 1999), T. pacificus
(Nakamura, 2000) and Ommastrephes bartramii (Yatsu & Mori,
2000)) or form sub-daily or aperiodically (e.g. I. argentinus
(Sakai et al., 1998; Sakai et al., 2004)). Development of sensory
organs such as the eye and statocyst is correlated with changes
in feeding behavior in T. pacificus (Shigeno et al., 2001),
and more detailed investigation of the ontogenetic development
of T. rhombus, especially after complete absorption of the yolk,
is needed.
The daily formation of statolith growth increments has been
directly validated in several oceanic squids (e.g. I. illecebrosus,
Dawe et al., 1985, and T. pacificus, Nakamura & Sakurai, 1991)
by marking the statoliths with tetracycline or strontium.
Although not a direct method, we used a statistical approach
similar to that of Uozumi & Ohara (1993), and Hatfield &
Rodhouse (1994) by comparing the number of increments in
the statoliths with the elapsed number of days and found that
the rate at which growth increments formed did not significantly
et al. (1987) observed that egg masses disintegrate by the end of
embryogenesis, and eggs just before hatching fall free from the
masses. In both cases, the hatchlings descend from the surface
(but possibly not deeper than the pycnoline) until the yolk is
absorbed, and swimming ability with normal posture (dorsalside facing up) and defensive reflexes such as inking are
acquired. Reduced visibility due to lower light levels below
the surface will presumably reduce the risk of predation. We
suggest that this descent is consistent with the distribution
patterns of later life stages. In summary, paralarvae occur in
the upper epipelagic and do not perform diurnal vertical
migration (Yamamoto & Okutani, 1975; Nigmatullin &
Arkhipkin, 1998); postlarvae and juveniles (15– 50 mm ML)
occur at depths .20 – 30 m (Nigmatullin & Arkhipkin, 1998);
and juveniles (.50 mm ML) probably occur in the upper
mesopelagic layers (Nesis, 1992).
The vertical distribution of possible prey organisms may be
related to the descent after hatching, though the first prey
remains unknown. Some gonatid paralarvae have been observed
to withdraw their heads into their mantle cavity (Arkhipkin &
Bizikov, 1996), which could be related to suspension feeding,
Figure 8. Relationship between age (days after hatching) and number of
growth increments. Left (L) and right (R) statoliths from 0- to 6-day-old
hatchlings (n ¼ 5 for each day, total ¼ 35) were examined. The growth
rates (slopes of the line) did not significantly differ from 1, indicating one
increment formed per day. Growth rates did not significantly differ
between the left and right statoliths.
203
K. MIYAHARA ET AL.
Figure 9. Summary of early life stages of T. rhombus from spawning to post-hatching.þ: present study, 1: Nigmatullin et al., 1995; 2: Nigmatullin &
Arkhipkin, 1998; 3: Sabirov et al., 1987; 4: Miyahara et al., 2006; 5: Yamamoto & Okutani, 1975; 6: Nesis, 1992.
manuscript. Thanks are also due to Dr Kumi Akaba (ne´e
Watanabe) for providing us helpful advice on observation of
squid development and Dr Chingis Nigmatullin (Atlantic
Research Institute of Marine Fisheries and Oceanography,
Russia) for his help to understand Russian references. Furthermore, we thank to the staff of the Hyogo Tajima Fisheries Technology Institute for their thoughtful cooperation, comments and
encouragement. This work was partly funded by the Agriculture, Forestry and Fisheries Research Council, Japan (Research
Project for Utilizing Advanced Technologies in Agriculture,
Forestry and Fisheries).
differ from one per day, suggesting that they formed daily.
There was no significant difference in the growth rates
between the right and left statoliths, and our study confirms
the validity of growth analysis using statoliths. Using this
method, Miyahara et al. (unpublished data) analysed the
growth of T. rhombus in the Sea of Japan and showed that
growth rates differ between groups with different hatching
seasons.
In conclusion, the early life history of T. rhombus based on the
results of this and previous studies is summarized in Figure 9.
During the 3 –4 months that a female is mature, it can
produce about 8– 12 egg masses (Nigmatullin et al., 1995).
Spawning occurs near the sea surface (Nigmatullin &
Arkhipkin, 1998) or at depth. The egg masses ascend to the
surface and may expand due to decreased water pressure. Eggs
within the egg masses develop quickly in the warm surface
waters. Hatching occurs 5 – 10 days after the eggs are spawned
(Sabirov et al., 1987; Miyahara et al., 2006), and hatchlings
descend from the egg masses with the ventral-side facing up.
After 2– 3 days, they begin to swim with their dorsal sides
facing up and develop defensive reflexes, but exhaust the inner
yolk after about a week. The first food of the hatchlings is not
known, but this descent will place them at depths where
potential prey is abundant. Statoliths first appear one day
before hatching, and growth increments within the statoliths
form daily after hatching.
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The egg masses were generously provided by the fishermen of the
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