Fisheries Science
63(1), 15-21 (1997)
Spawning Cycle of Two Dragonet Species, Calliurichthys japonicus and
Repomucenus huguenini, in Tosa Bay, Southern Japan
Benjamin
Jareta
Gonzales,*1,*3
*1Department
of Fisheries
*2Department
of Biology
*3State
, Faculty
of Agriculture,
Taniguchi,*1,•õ
and
Kochi
Nankoku,
University,
Osamu
Okamura*2
Kochi
, Faculty
of Science,
Kochi University,
2-5-1 Akebono-cho,
College of Palawan
-Institute
of Marine
Sciences ,
Polytechnic
Puerto
Nobuhiko
Princesa
City
5300,
783, Japan
Kochi
780,
Japan
Philippines
(Received February 9, 1996)
The
from
japonicus
spawn
the
spawning
March
was
during
cmSL
bution
peak
occur
the
in
male.
range
of
at
its
from
Key
peak
season
34.4-34.6in
words:
of
in
Calliurichthys
February
1993
spawner,
90-120m
peak
japonicus
in a wild
having
water
reproductive
high
depth
huguenini
water
depth
during
in July.
Corresponding
author.
(May)
This
species
matures
and reproduces
in both
sexes.
The temperature
in
July,
ranged
of R.
huguenini
15
spawning,
to
30m
from
17.4-21.6•Ž
water
length
at
the
Kochi
of
females
and
an
salinity
temperature
early
when
from
ranged
at
within
(October
to
age with
the GI of
12.5cm
appears
waters
in
SL
its normal
to
of
and
distri
December
with
a
maturity
estimated
to
C. japonicus
samples
34.6-35.0.
from
investigated
Calliurichthys
The species
to shallower
occurs
spawning
autumn
was
Prefecture.
summer.
ground
spawner,
from
45-120m
and
in November,
huguenini
Bay,
activity
in
its spawning
Maturity
is a biannual
spring
Repomucenus
in Tosa
reproductive
and
extends
During
22.4-22.8•Ž
the
and
peak
salini
depth.
maturity,
dragonet,
Information on the ecological interactions of fish spe
cies is a prerequisite for their effective management and
conservation. Conservation efforts for fish species should
consider not only those species of fishery or of economic
importance, but other ecologically important species as
well.1) Fish catch compositions during trawling surveys in
Tosa Bay reveal a high catch percentage of a diverse array
of dragonet
fishes. Calliurichthys
japonicus
and
Repomucenus huguenini are the two dragonet species
which predominantly occur among these fish catches.
Because of their abundance, these two species are likely to
play an important ecological role in the benthic communi
ty of the Bay.
Life history strategies of fishes can be deduced by
studying or comparing similar species in the same or simi
lar environments.2) It is also important to understand
which of the life history characteristics and environmental
factors covary. In the present paper, we detail the spawn
ing season and length at maturation of C. japonicus and
R. huguenini to clarify the dynamics of the benthic com
munity of Tosa Bay. In addition, since C. japonicus and
R. huguenini are both abundant and are benthic ver
tebrates in the Bay, they can also be useful as biological in
dicators to detect environmental changes that may occur
in the Bay. Therefore, any basic information on the
seasonal reproductive timing and length at maturation of
both species may assist in detecting or forecasting the vari
ous impacts of human-induced changes on the benthic
ecosystem of Tosa Bay.
•õ
and
population
period
Repomucenus
15-30m
in November).
at 4.5cm
SL
reproductive
ty
to
is an annual
mainly
between
Bay
17.7
cycle
1992
Tosa
Bay
Research on dragonets has determined the age and
growth of Callionymus lyra;3) the general biology and ecol
ogy of Foetorepus altivelis,4) Callionymus belcheri,5) and
Diplogrammus xenicus;6) the life-history of Repomucenus
beniteguri;7) and the spawning of Repomucenus valencien
nei and R. richardsonii8) and Paradiplogrammus enneac
tis.9) However, no reports are available on the spawning of
two predominant dragonets Calliurichthys japonicus and
Repomucenus huguenini occurring in Tosa Bay.
Materials
and
Methods
Samples were collected monthly in Tosa Bay from eight
depth zones of 15, 30, 45, 60, 90, 120, 150, and 190m dur
ing the period from March 1992 to February 1993 (Fig. 1).
Sampling of fish specimens was carried out using a beam
trawl (7m beam length, 10m total net length with 10mm
cod end mesh). The net was towed for about 30 minutes at
each depth zone. The gear was operated on board the 20
ton R/V Toyohata Maru of the Usa Marine Biological
Institute of Kochi University. The bottom water was sam
pled with a Nansen bottle sampler at each station. A revers
ing type thermometer mounted on the water sampling bot
tle and a conduction type salinometer were used to analyze
the proximate environmental parameters.
Fish specimens were temporarily stored on ice while on
board the vessel and were preserved in 10% formalin solu
tion immediately after sorting. In the laboratory, standard
length (SL) and body weight (BW) of the fish were meas
16
Gonzales
et al.
ured
to
the
nearest
gonads
were
The monthly
determined,
adult
and
fish
months
R.
sex
the
male
C.
organ
by
of
the
color)
GI
was
The
(g) •~
specimens
?17.0cm
Fig. 1. Map of study area and location of trawling survey sites (dotted
portion).
depth
the
2.
Monthly
collected
In
dotted
changes
from
C. japonicus,
lines).
Tosa
in gonad
Bay,
no
March
female
indices
(GI)
of
1992-February
specimens
? 12.1
Calliurichthys
1993
or
japonicus
(A,
were
(Fig.
female;
B, male)
(Fig.
and
To
male
R.
female
specimens
while
depths
R.
sizes
discern
has
huguenini,
in
length
accurately
which
different
dark
Gl=gonad
with
japonicus,
than
from
and
only
analysis,
2).
confirmed
formula:
specimens
C.
length
white).
japonicus,
GI
R.
genital
finally
milky
SL
of
male
body
(elongated
the
C.
for
range
to
such
length
in
elongated
was
testis
and
female
of
collected
length
12.1cm
used
ground
distribution
samples
separately
Fig.
SL
tail
fin
SL;
by
longer
dorsal
Sex
the
In
used
and
of
spawning
<9cm
relatively
using
SL3(cm).
oocytes
initially
relatively
(rounded
were
male
in
of
the
peak
japonicus,
first
species.
length ?
spawning
the
calculated
104/
SL
? 4.5cm
the
longer
both
of
the
determined
as the
on
color
ovary
of
huguenini,
the
in
the
(C.
and
and
The
a microscope.
was
relatively
males
and
weight
SL)
janonicus,
shape
stage
under
finrays
respectively.
during
individuals
characters
filamentous
huguenini,
of
maturation
<6cm
morphological
0.1g,
weighed
to the nearest
0.01mg.
index
(GI)
of both
species
were
collected
small
huguenini,
the
the
observed
of
and
and
gonad
specimens
were
The
0.1cm
removed
mean
a wider
we
analyzed
and
months
4).
and
Repomucenus
huguenini
(C
, female;
D,
male)
(Mean•}SE).
male
specimens ?
17.0cm
in
SL
were
collected
in
March,
May,
and
October
(indicated
by
Spawning
in Two
Results
Spawning Season of C. japonicus
The mean monthly GI of female C. japonicus started to
increase from January (Fig. 2A). No large individuals
(? 12.0cm in SL) were caught in either March or May, but
in April, the mean GI value showed a continuation of this
trend. A significant increase in female GI was observed it
June (Fig. 2A), and the mean monthly GI of female C,
japonicus (? 12.0 cm in SL) peaked in July, having high
values over the summer, from June to September (Fig. 2A).
No large male C. japonicus (? 17.0cm in SL) were col.
lected in March or May. The mean monthly GI of male C.
japonicus was relatively high in April (Figs. 2B, 3). The
male GI increased in June, while a slight decrease was ob
served in July (Fig. 2B). The GI of large males (? 17.cm.
SL) increased significantly in August reaching the peak it
September (Fig. 2B). Mean monthly GI values of both sex.
es were low in winter (Figs. 2A, B and 3).
A sligt
males
increase
(>
smaller-sized
SL)
male
SL)
cohorts
As
larger
were
increase
females
(13.0-17.0
These
tinued
in
until
and
year
3).
GI
SL.
(Fig.
value
Of
was
the
(5.0-10.8),
Samples
depths
were
distributed
of
throughout
the
the
collected
also
with
with
high
depths.
Large
males
depths
in
collected
males
depth
in
The
males
high
GIs
GIs
of
July
high
and
collected
and
almost
and
a few
GIs
were
at 45-120m,
at its
from
of
the
collected
(Fig.
in 45
males
However,
only
in
90m
of
C. japoni
4D).
when
peak
year
large
January.
(Fig.
60m
in deep
observed
relatively
in
large
and
collected
also
July
water
July,
45
months
were
depths
September
salinity
45-120m
In
were
all
also
was
in
were
and
were highest
While
speci
between
however,
45-60m
with
June
September.
C. japonicus
depth.
45 and
(90-120m),
in
observed
appeared
in
in
August
were
through
17.7
values
however,
depths
the
GI
in July,
ranged
34.4-34.6
at
season
range
15 to
of R.
was
huguenini
in
22.4-22.8•Ž
30 m depths,
where
and
samples
of
the
oocytes
observed
in July,
and
R.
were characterized
(vitellogenic
in
adult
huguenini
by a very
specimens
during
narrow
of
C.
May
and
previtelline
stage).
Discussion
a
individuals
waters
females,
60m
was
GI
female
the
with
water
between
of these
fish samples
in August
(Fig.
4B).
males,
temperature
samples
17.4-21.6•Ž
of
reproductive
temperature
collected.
japonicus
November
space
peak
the
GI
of
females
with
Large
con
their
February
of
that
deeper
large
and
June
large
4).
Some
(90-120m)
Some
large
cus
in
high
females
er waters
(Fig.
values
zone
during
were
and
specimens
Bay
45
depths
- 60m
SL
till
in
GIs
17
the
salinity
were
Most
occurred
high
size
the
a
larger
thereafter
low
GIs.
June,
and
values
while
smallest
mostly
year.
between
(Fig. 4A).
The GI
in the 120m
depth
4C).
GI
During
November,
Individual
GI
relatively
remained
female
3).
highest
high
fe
Species
All females were reproductively inactive, having low GI
values from March to April, while from May larger ones
(approximately 10.0 cm mean SL) with a maximum GI
value of 10.2 appeared (Fig. 5). Smaller females (7.0-9.0
cm in SL) began to show higher GIs in July, and these in
creased continuously until the peak in November. The
most active female spawning cohort in November had a
mean SL of 7.0cm, while a larger cohort with a mean SL
of 12.0cm showed a decreasing GI in the same month.
Testes began to ripen earlier than the ovaries in April (Fig.
5). Comparatively high male GI values occurred from
April to May and from September to November. The male
GI gradually decreased from December to February of the
following year. During the high spawning activity of R.
huguenini from October to December, 26% of the total fe
male specimens with relatively high GI values (10.3-17.9)
had a size range of 4.5-7.2cm SL, while in males, 24% of
the total specimens with relatively high GI values (0.3-0.9)
had a size range of 4.1 to 7.3cm SL. The smallest length
size with a high GI value was 4.5cm SL for both male and
female R. huguenini.
Only
low
in
(Fig.
with
The
showed
74%
were
collected
from
90m
of C. japonicus
were
collected
120m
mens
with
12.5cm
total
all
and
3).
(8.0-11.9cm
sampled
the
September,
decreased
female
and
with
individuals
to appear
(Fig.
occurred
SL)
SL)
large
males
were
GI
following
cm
in May
cm
of both
in April
and
individuals
markedly
high
valuu
observed
collected
(17.0-21.7cm
July.
GI
was
(8.5-12.6cm)
female
marked
males
in the
14.0cm
Dragonet
from
34.6-35.0.
Spawning Season of R. huguenini
The mean monthly GI values of R. huguenini (?4.5cm
SL) in both sexes were relatively low from March to Sep
tember, but a significant increase occurred from Septem
ber to October, reaching a peak in November (Fig. 2C, D).
Thereafter, it markedly decreased until February.
Spawning of Calliurichthys japonicus
Although we lack data for March and May, the GI
values of C. japonicus increase from February to June,
reaching a peak in July. The mean monthly GI value (Fig.
2A) and the presence of large individuals with high GI
values (Fig. 3) suggest that female C. japonicus spawn in
the summer, from June to September with the highest
reproductive condition being in July.
Calliurichthys japonicus may be classified with the
group of dragonets that spawn once a year (annual
spawner). The peak of its reproductive effort is the same as
that of Callionymus enneactis, spawning in July.9) The an
nual reproductive frequency of C. japonicus is similar to
Callionymus belcheri, spawning once a year. However, C.
belcheri spawns between March and May,5) occurring earli
er than C. japonicus. These two species were described by
Fricke10) as belonging to the same genus-Callionymus.
The annual reproductive frequency occurrence of C.
japonicus coincides with that of Synchiropus altivelis,
which spawns annually between late winter and early
spring.4) However, the spawning season of the former
differs from that of the latter by occurring in summer. The
Synchiropus species groups are easily distinguished from
the Callionymus species by their generic differences.11)
Furthermore, Fricke10)classified Calliurichthys japonicus,
Callionymus enneactis (Paradiplogrammus enneactis in
Nakabo,12)) and Callionymus belcheri in one genus-Cal
lionymus. In our result, these three species are separated
from Synchiropus altivelis by spawning annually in either
spring or summer, while the latter species spawns during
18
Fig. 3.
Gonzales
et al.
Relationship between standard length (SL) and gonad index (GI) of Calliurichthys japonicus
the colder months of late winter and early spring. Added
to this, Synchiropus altivelis is distributed in relatively
deeper water (180m) than C. enneactis (0-1m),9,13) C. bel
cheri (3-33 m),5) and C. japonicus (45-120). On the other
hand, Synchiropus altivelis, Callionymus enneactis, and
C. belcheri have a similar geographic distribution (from
the waters of Australia to the waters around Japan, 5,12,14))
while Calliurichthys japonicus has a relatively wider ge
ographical distribution, occurring from the Western
Pacific to Western Australia and the Southeast coast of
Africa.10,15)Despite their taxonomic and geographical or
bathymetrical distribution differences, these dragonets all
in Tosa Bay for March 1992 to February 1993.
spawn once a year.
Spawning of Repomucenus huguenini
The mean monthly GI value shows that R. huguenini
spawned from October to December with a peak in Novem
ber. The appearance of individuals with high GI values
(Fig. 5) indicates that spawning also occurs in May.
Repomucenus huguenini is therefore a biannual spawner,
which also includes species such as Callionymus sublaevis;
spawning in March and October; C. calcaratus, May
through June and from October to November;16) and
Repomucenus
richardsonii,
April and November.17)
Spawning
in Two
Dragonet
Species
19
Fig. 4. Monthly average standard length (top) and average GI (bottom) of all samples of female (A, B) and male (C, D) Calliurichthys japonicus
collected from different zones within its distributional range (45-120m depth).
Repomucenus huguenini, besides belonging in the same ge
nus with R. richardsonii, also has a similar geographic dis
tribution, the former from Hokkaido to the Fast China
Sea and the latter from Niigata, Sendai Bay, southward to
the South China Sea.14)On the other hand, the congeneric
species Callionymus sublaevis and C. calcaratus are also
similarly distributed in Australia.16) Despite their taxonom
ic and geographical distribution differences, these drago
nets all spawn twice a year and have a very similar
reproductive timing, occurring either in spring and au
tumn, or in summer and autumn. In contrast, though C.
enneactis, C. belcheri, C. sublaevis, and C. calcaratus are
congeneric species, they exhibit different annual reproduc
tive frequencies and seasons. These facts suggest that the
seasonal reproductive timing and frequency of breeding
per year in dragonets may not be influenced by their taxo
nomic relationships and geographical or bathymetrical dis
tributions, but may depend on an endogenous reproduc
tive cycle, which is under genetic control, synchronized to
the environmental conditions of their respective habitats.
The oocytes in the vitellogenic stage observed in adult
specimens of C. japonicus in July, and R. huguenini dur
ing May and November, also suggest that both species
were ready to spawn during those periods. In other fish,
like Nibea mitsukurii, actual spawning in a tank occurred
two months later than the spawning period estimated from
GI and microscopic observations of oocytes sampled from
the wild.18) This finding is inconsistent with those of the
dragonets
Callionymus
belcheri and Repomucenus
huguenini. In C. belcheri, the first discharge of follicles oc
curred during the peak of the female GI.5) Repomucenus
huguenini spawned spontaneously in a tank from late Sep
tember to late November,19) coinciding with the significant
increase of male and female GI in the present study. Fur
thermore, Takita et al.,9) based on ovarian histological ex
aminations, confirmed that the (predicted) spawning
period in nature of the dragonet Paradiplogrammus en
neactis and that which occurred in the tank were syn
chronous. These results support the validity of our esti
mates of the spawning seasons of C. japonicus and R.
huguenini in the wild, using the GI method.
Spawning grounds
The depth distribution of C. japonicus has a tendency
for larger specimens to occur in deeper waters (Fig. 4A, C).
Such phenomena are widespread in the demersal fishes of
Tosa Bay.20)Both large male and female C. japonicus were
collected from the deeper part of its distributional range,
90-120m, throughout the year. The high GI values (Fig.
4B, D) of large individuals (Fig. 4A, C) between 90-120m
depths indicate that this depth range is their main spawn
ing ground. The appearance of large males and females
with high GIs in 45 and 60m depths in July, during the
peak reproductive period, suggest that some of the spawn
ing individuals migrate to shallower waters (45-60m) to
spawn. Such spawning migration may occur to allow the
exploitation of wider habitat ranges. On the other hand,
the narrow depth distribution (15-30m) of the R. hugueni
20
Gonzales
Standard
Fig. S.
et al.
length
(cm)
Relationship between standard length (SL) and gonad index (GI) of Repomucenus
ni implies that no spawning migration occurs and that the
species spawn within its distributional range: in the shal
low waters of Tosa Bay. Adult male and female R.
huguenini collected from 15m and 30m water depths of
Tosa Bay spawned in a tank from late September through
late November. 19)
The difference in the seasonal reproductive timing and
the spawning depth between C. japonicus and R. hugueni
ni show that there is no space competition during spawn
ing between these two species.
huguenini in Tosa Bay for March 1992 to February 1993.
Length at Sexual Maturity
The relative size at maturation between sexes of C.
japonicus was similar to that of other dragonets;4,16,17,21)
smaller in females and larger in males. In R. huguenini,
the relative size at maturation was similar to that of C. bel
cheri 5)being the same in both sexes. Early life-history theo
ry suggests that high mortality caused by density-indepen
dent effects selects for early reproduction and this strategy
would be expected in harsh or unpredictable environ
ments.22)The early maturation of R. huguenini, is presuma
bly influenced by the environmental changes in the shallow
Spawning
in Two
waters of Tosa Bay and is therefore environmentally less
stable. On the contrary, C. japonicus thrives in deeper
waters, which are a relatively stable environment, and
shows a more delayed maturation.
Life history traits are relative to the productivity of their
habitats; in high-productivity streams, there tends to be
several spawnings in a season, early age at maturity and a
short life span. In low-productivity streams, the tendency
is for a single spawning in a breeding season, delayed
maturity and long life spans.22) These circumstances agree
with the results of our study. Repomucenus huguenini,
presumably living in a high productivity environment,
spawned twice a year, matured early, and has a short life
span (about 1 year and 4 months*4). In contrast, C. japoni
cas lives in an environment with lower productivity,
spawns once a year, and has a delayed maturation and lon
ger life span (?3 years; Gonzales, unpublished).
Acknowledgments
Thanks are due to Associate Professor Kunio Sasaki
and his students, and the captain and crew of Toyohata Maru for the
field assistance. We also thank Associate Professor Tetsuji Nakabo of
Kyoto University for providing us with valuable references. We are grate
ful to Dr. Ambok Bolong Abul Munafi for his assistance on fish maturi
ty, to the anonymous reviewers and Chris Norman for their helpful com
ments on this manuscript.
Dragonet
7)
8)
9)
10)
11)
12)
13)
14)
15)
16)
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17)
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22)
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21
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