New Zealand Journal of Marine and Freshwater Research

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Age, growth and reproductive characteristics of

gold striped amberjack 1 Seriola lalandi in the
waters off western Kyushu, Japan

T Shiraishi , S Ohshimo & R Yukami

To cite this article: T Shiraishi , S Ohshimo & R Yukami (2010) Age, growth and reproductive
characteristics of gold striped amberjack 1 Seriola�lalandi in the waters off western Kyushu,
Japan, New Zealand Journal of Marine and Freshwater Research, 44:2, 117-127, DOI:
10.1080/00288330.2010.488787

To link to this article: https://doi.org/10.1080/00288330.2010.488787

Published online: 10 Aug 2010.

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New Zealand Journal of Marine and Freshwater Research
Vol. 44, No. 2, June 2010, 117127

Age, growth and reproductive characteristics of gold striped amberjack 1 Seriola

lalandi in the waters off western Kyushu, Japan
T Shiraishi, S Ohshimo* and R Yukami
Seikai National Fisheries Research Institute, Fisheries Research Agency, Taira, Nagasaki, Japan
(Received 6 October 2010; final version received 9 April 2010)

Growth and reproductive characteristics of gold striped amberjack Seriola lalandi collected in
the waters off western Kyushu from April 2003 to March 2008 were determined based on
vertebral centrum readings and gonad histology, respectively. Translucent and opaque zones on
vertebral centrum were identified, and the number of opaque rings counted. Von Bertalanffy
growth parameters did not significantly differ between males and females (F
0.28, P
0.05),
and transformed value for the von Bertalanffy growth parameter FL  and K were 1108 and
0.3091, respectively. The spawning period was evaluated to be from April to June for S. lalandi,
based on the results from monthly changes in the gonadosomatic index and histological
observations. Based on the relationships between the fork length and the developmental stage of
testes and ovaries, the smallest fork length of male and female with mature gonads was 624 and
662 mm, respectively. The first maturation age was estimated to be 2 years old for both sexes.
Keywords: centrum; gold striped amberjack; growth; reproduction; Seriola

Introduction fluctuated from 400 to 600 metric tonnes

Gold striped amberjack Seriola lalandi is widely from 1990 to 2000 (Gillanders et al. 1999b),
distributed in temperate and subtropical waters although this level has fallen dramatically in
of the world. In Japan, this species is distributed recent years (Stewart et al. 2004). This species is
important commercially in many areas of the
in the Pacific Ocean off the south coast of
world.
Honshu and throughout the Sea of Japan to the
As gold striped amberjack have been man-
East China Sea, and is caught as commercially
aged as a part of the resources of the genus
important species and grouped in fisheries landing Seriola by the government of Japan, it is
statistics with yellowtail Seriola quinqueradiata, necessary to clarify how the biological char-
greater amberjack Seriola dumerili and almaco acteristics of each species in the genus Seriola
jack Seriola rivoliana. The main methods of differ. Many studies on the biological charac-
fishing for the genus Seriola in the East China teristics of yellowtail, S. quinqueradiata, have
Sea is by set nets and purse seines, and the annual been reported in Japan. Age was determined
catch has ranged from 7000 to 16,000 tons since using various hard tissues (Mitani 1955,
1970. The catch of the gold striped amberjack is 1958; Mitani & Sato 1959), and distribution
less than that of the yellowtail; however, as and migration of yellowtail, ranging from
most of the catch has been previously grouped Hokkaido to the continental shelf margin,
and landings treated with other Seriola spp. have been investigated (Mitani 1960; Watanabe
without identification, accurate catch statistics 1979; Murayama 1992). The reproductive char-
for this species are not available. In New South acteristics of yellowtail have been reported for
Wales (NSW), Australia, annual catches have the spawning season, the maturity process of

*Corresponding author. Email: [email protected]

ISSN 0028-8330 print/ISSN 1175-8805 online
# 2010 The Royal Society of New Zealand
DOI: 10.1080/00288330.2010.488787
http://www.informaworld.com
118 T Shiraishi et al.

oocytes and the spawning ground (Mitani 1959; considered annual rings and were counted
Murayama 1992; Uehara et al. 1998). However, following the method of Gillanders et al.
there are no studies of biological (growth and (1999a) and Mitani (1958). The distance from
reproduction) characteristics of the gold striped the focus (F) along a straight line to the
amberjack, S. lalandi, around Japan. Conse- centrum margin was denoted the centrum
quently, the aims of the present study are to radius (CR; Fig. 2D), and the distance from
determine the age, growth and reproductive F to the outer edge of each opaque zones was
characteristics of the gold striped amberjack in the ring radius (rn). To define the period of the
the East China Sea. Then, we compared the formation of the ring marks (opaque zone), we
biological characteristics of S. lalandi in the examined monthly changes in the frequency of
East China Sea, Japan, with that of S. lalandi individuals with opaque zones on the outer
in NSW, Australia and that of S. lalandi in margin of the centrum and the marginal incre-
Northern New Zealand. ment (MI). The MI was determined according
to the equation:
MI
(CRrn)=(rnrn1);
Materials and methods
where CR represents the centrum radius (mm)
Collection of samples and general biological data and rn the ring radius (mm) of the nth outer
A total of 164 specimens of gold striped opaque zone of the centrum.
amberjack obtained from April 2003 to March Age was determined for each fish on the
2008 in the waters off western Kyushu were basis of the number of ring marks (annuli) on
analysed (Fig. 1). Specimens were caught by the centrum, assuming a hatch date of 1 May,
large-sized purse seines and set nets mainly in which approximately corresponded to the
the coastal waters off the Goto Islands. middle of the spawning period (see Results).
Specimens were measured to the nearest For some specimens sampled from May to
millimetre in total length and fork length June, which did not form a new translucent
(FL) and to the nearest gram of body weight zone on the outer margin, the age was
(BW). The gonad weight (GW) was measured calculated as the sum of the number of ring
to the nearest 0.1 g after determining the sex, marks plus 1 year. In order to describe the
and small pieces of the gonad were fixed in growth of males and females, von Bertalanffy
10% formalin for histological observations. growth equations were fitted to the observed
The vertebral centra were removed and FL values at age t by using non-linear least-
frozen for later analysis. The gonadosomatic square regression for both sexes. The growth
index (GSI) was calculated as the ratio of equation is:
GW/(BW-GW).
FLt
FL [1expfK(tt0)g];
where FLt represents the fork length (mm) at
Age determination age t, FL, K and t0 represents the asymptotic
The 17th vertebra was used for determining the fork length, the growth coefficient and the
age, or if the 17th vertebra was damaged, then hypothetical age at fork length equal to zero,
the 16th or 18th vertebra was used. The respectively. The difference of growth rate
vertebra was boiled in water for several min- between males and females was examined
utes, cleaned, sectioned along the longitudinal using analysis of covariance (ANCOVA) be-
axis, bleached with 10% solution of H2O2 and tween survey length value and theory length
dried for 1 day. Each centrum was examined by
value.
three readers, and ring marks on the posterior
face of the centrum were counted and directly
measured using calipers. Broad translucent
zones alternated with narrow opaque zones Histological observations
on the centrum surface (76; Fig. 2AC). The The fixed gonads were dehydrated and
opaque zones that encircled the centrum were embedded in paraffin, and sections (thickness;
 Age and reproduction of Seriola lalandi 119

Fig. 1 The location of Seriola lalandi commercially caught in the waters off western Kyushu. The size of circle
indicates the number of fish caught at each site in the present study. The total number of collected specimens
of gold striped amberjack was 164.

4 mm) were obtained and stained by the The five stages of testes were as follows:
Mayer’s haematoxylin and eosin method. The
stained sections were observed under an 1. The spermatogonial proliferation stage (Sp;
optical microscope and the most advanced Fig. 3A)*only spermatogonia are abundant
testes and oocyte stages were recorded. The in the seminal lobule.
developmental stages of testes and ovaries were 2. The early spermatogenesis stage (Es;
classified as five and six stages of maturity, Fig. 3B)*spermatogonia and spermatids
respectively, based on the development of the are organized in the seminal lobules.
most advanced testes and oocytes and their 3. The late spermatogenesis stage (Ls; Fig. 3C)
histological characteristics (Fig. 3 and 4). *spermatogenesis proceeds in the testis.
120 T Shiraishi et al.

Spermatids of the seminal lobules increase

and spermatozoa are found in the lumina of
the seminal lobules.
4. The functional maturation stage (Fm;
Fig. 3D)*spermatozoa are abundant in
the lumina of the seminal lobules and main
sperm duct. Spermatogonial division and
further spermatogenesis proceeds in the
seminal lobules.
5. The post-spawning stage (Ps; Fig. 3E)*
spermatogonia are found in the seminal
lobules, although spermatozoa occur in the
lumina of the seminal lobules.
The six stages of oocytes were as follows:
1. The immature stage (Im; Fig. 4A)*only
previtellogenic oocytes are present, including
those in the perinucleolus and yolk vesicle
stages.
2. The developing stage (D; Fig. 4B)*the most
advanced oocytes are at the early yolk or
mid-yolk stages.
3. The vitellogenic stage (Vi; Fig. 4C)*the
most advanced oocytes are at the late yolk
stage, which marks the end of vitellogenesis.
4. The mature stage (M; Fig. 4D, E), the most
advanced oocytes are at the germinal vesicle
127 migration or hydration stages. The de-
generated old postovulatory follicles appear
in some ovaries at the germinal vesicle
migration.
5. The spawning stage (Sp; Fig. 4F)*yolked
oocytes and newly postovulatory follicles
are present. Most postovulatory follicles
disappear from the ovaries before the devel-
oping oocytes attain the germinal vesicle
migration stage.
6. The resting stage (Re; Fig. 4G)*all yolked
Fig. 2 Photograph of centrum of Seriola lalandi with oocytes are degenerating (atretic stage) and
three ring marks (A, FL
758 mm, female), two ring non-yolked oocytes are present.
marks (B, FL
710 mm, female) and one ring mark
(C, FL
586 mm, male), and a schematic figure (D)
of the measurement region on the centrum shown in Sexual maturity
(A). Black arrows and grey areas in (D) indicate ring
marks and the opaque zone, respectively. F, focus; Estimates of size at maturity for 60 males
CR, centrum radius; rn, ring radius of the boundary and 78 females were based on the relationship
from an opaque zone to a translucent zone; MI, between gonad developmental stages and fork
marginal increment. length. Sexually mature males were defined
 Age and reproduction of Seriola lalandi 121

Fig. 3 Photomicrographs of testes at different developmental stages in Seriola lalandi: (A) spermatogonia
proliferation stage; (B) early spermatogenesis stage; (C) late spermatogenesis stage; (D) functional
maturation stage; (E) post-spawning stage. sg, spermatogonial; st, spermatid; sz, spermatozoon. Scale bar
equals 100 mm.

as individuals with testes at the Fm stage. 7 and 8 years old, respectively. One clear
Sexually mature females were defined as ring mark was observed on vertebrae of 29
individuals with ovaries with Vi, M or Sp individuals from 408 to 615 mm FL and
stage oocytes. validated by three independent readers (Fig.
2C), and individuals more than 630 mm FL
had the first ring mark at the same position
Results as the 1-year-old fish (Fig. 2A,B). All speci-
mens examined from July to December had a
Growth translucent zone on the outer margin of the
A total of 164 specimens (73 males ranging in centrum (Fig. 5A), and the frequency with an
size from 404 to 1121 mm FL, 91 females opaque zone was high from January to June.
ranging in size from 399 to 1235 mm FL) of Some specimens examined from April to June
gold striped amberjack were sampled, and the had only minimal translucent zones (Fig. 5B),
ages of 162 specimens could be identified. and the MI values gradually increased from
The largest specimens (1121 and 1235 mm July to January.
FL) were excluded from the analysis because The hatch date of all the individuals
it was too difficult to read the ring marks. was assumed to be 1 May for gold striped
For the other specimens, the estimated amberjack (see below), and the age of each
maximum ages for male and female were individual was decided as the monthly age
 122 T Shiraishi et al.
Fig. 4 Photomicrographs of ovaries at different developmental stages in Seriola lalandi: (A) immature stage; (B) developing stage; (C) vitellogenic
stage; (D-E) mature stage; (F) spawning stage; (G) resting stage. at, atretic oocyte; ey, early yolk oocyte; gvm, germinal vesicle migration oocyte; hy,
hydration oocyte; ly, late yolk oocyte; my, mid-yolk oocyte; pn, perinucleolus oocyte; pof, postovulatory follicle. Scale bar equals 100 mm.
 Age and reproduction of Seriola lalandi 123

using the results of age determination. The GSI values of female individuals were less than
relationship between age and FL of gold 1.1 in the immature (Im) stage, and the values
striped amberjack is shown in Fig. 6. As for the oocytes ranged from 0.8 to 1.7 in the
there were no significant differences in the developing (D) stage (Fig. 9C). GSI values for
growth between males and females (F
0.28, females in the Vi, M and Sp stages ranged from
P
0.05), all the individuals were pooled for 2.4 to 7.6, and most of these individuals
the estimation of the growth model. Growth exceeded 3.0. The minimum fork length of
model of gold striped amberjack was esti- females in the mature (from Vi to Sp) stages
mated as follows: was 662 mm FL (Fig. 9D).
FLt
1108[1expf0:3091(t0:5881)g]
(1 5t58; r2
0:94; n
162): Discussion
where FLt is the fork length at age t. There have been no studies on age, growth and
reproduction of this species in the northern
hemisphere. In the southern hemisphere, the
Annual reproductive cycle growth pattern of S. lalandi in NSW, Australia,
The mean GSI value of the gold striped amber- was reported by Gillanders et al. (1999a) using
jack was high from April to June and peaked in several structures (scales, otoliths and vertebrae)
May for both sexes (Fig. 7A,B). The maximum and length frequency data. They reported that
values of the mean GSI in males and females in the otoliths, scales and vertebrae can be used for
May were 2.0 and 3.3, respectively. The mean age determination, although it is necessary to
GSI values decreased rapidly in July and were determine the position of the first zone and to
less than 1.0 from July to March. validate estimates for all age classes. In the
The gonads of all males collected from present study, a clear ring mark was observed
August to March were at the Sp stage (Fig. 8A). on vertebrae and validated by three independent
Individuals at the Fm stage appeared from readers, and the first ring mark on vertebrae of
April, and c. 70% of specimens in May and larger fish was clearly observed at the same
c. 30 % in June had abundant spermatozoa in position as that of individuals with one
the lumina of the seminal lobules and main ring mark only. Moreover, there was a clear
sperm duct. Specimens in the Ps stage appeared periodicity in the formation of ring marks based
from June, and only Ps stage specimens (n
2) on monthly changes in MI and the frequency of
were observed in July. appearance of an opaque zone on the outer
No maturing (Vi, M and Sp stages) females margin. Therefore, it is considered that the
of the gold striped amberjack were collected vertebrae can be used for age determination in
from July to March (Fig. 8B). Maturing S. lalandi as shown by Gillanders et al. (1999a).
females appeared from April, and c. 70% of Gillanders et al. (1999a) reported that aver-
specimens in May exhibited the maturing age fork lengths were about 485 mm FL at age 1
condition, although specimens with hydrated and 788 mm FL at age 5, and the maximum age
oocytes were not observed. Half of the speci- of fish was 11 years old (approximately 900 mm
mens collected in June had atretic oocytes, but FL) based on age determination using verte-
females with ovaries in M and Sp stages were brae. In the present study, the maximum age
also observed. estimated was estimated at 8 years old
(1083 mm FL), and the predicted fork lengths
at age 1 and 5 were 430 and 911 mm FL,
Size at maturation respectively. The sizes of S. lalandi in NSW
GSI values of male individuals were less than and East China Sea were approximately equal
0.9 in immature (Sp and Es) stages, 1.2 in the at age 1, but the size in the East China Sea was
Ls stage, and from 1.4 to 4.1 in the Fm stage larger than that in NSW at age 5.
(Fig. 9A). Individuals with testes at the Fm There are no reports regarding gold
stage were larger than 624 mm FL (Fig. 9B). striped amberjack maturation in Japan using
124 T Shiraishi et al.

2001). The peak gonad activity of S. lalandi

from NSW was in December suggesting an
early summer spawning period, and the smal-
lest mature male and female were 360 mm FL
(0 years old) and 698 mm FL (3 years old),
respectively (Gillanders et al. 1999b). GSI of
S. lalandi from NNZ was high from November
1998 to January 1999, and from October 1999
to January 2000, suggesting spawning during
the spring and summer period (Poortenaar
et al. 2001). Poortenaar et al. (2001) reported
that the smallest mature males and females
S. lalandi in NNZ were 750 mm FL (4 years
old) and 775 mm FL (4 years old), respectively.
McGregor (1995) reported that NNZ popula-
tion of S. lalandi mature between 580 and
670 mm FL. In the present study, the spawning
period of this species is estimated to occur in
Fig. 5 Monthly changes in (A) frequency of appear-
ance of an opaque zone on the outer margin of the late spring/early summer (April to June; peak
centrum and in the (B) marginal increments (MI) of May) based on seasonal changes in the GSI and
centrum in Seriola lalandi. Open and closed circles in maturation stage. Individuals under 500 mm
indicate the specimens with translucent and with FL (1 year old) had immature testes and
opaque zones on the outer margin, respectively. oocytes. The minimum size of males and
Number of fish examined each month is indicated. females with mature gonads is approximately
620 mm and 660 mm FL, respectively, and the
histological techniques, but size and age at estimated age at maturity is 2 years old for both
sexes. Differences in size and age of sexual
maturity, and seasonal changes in gonad activ-
maturity among waters or year class would be
ity have been reported for S. lalandi using
attributed to different environmental condition
histological techniques from NSW (Gillanders
(water temperatures, food condition, etc), or
et al. 1999b) and from Northern New Zealand
behavioural and physiological differences
(NNZ) (McGregor 1995; Poortenaar et al.
among populations.
In a previous study for S. quinqueradiata, it
was reported that they stay around same sea
area from 1 to 2 years old, then migrate over a
wider range after 3 years old (Mitani 1960;
Murayama 1992), and the growth rates were
different in the habitat attributed to water
temperature (Murayama 1992). Although
migration of S. lalandi is not clarified, it
is considered that S. lalandi make a similar
migration to the S. quinqueradiata, and differ-
ences in the growth rates will occur between
water regions. Seasonal changes in GSI and
maturation stage of female giant yellowtail
showed that the spawning season of this species
was from April to June, which is slightly late
Fig. 6 Relationship between age and fork length. compared with the Japanese amberjack (from
Fitted curve indicates the von Bertalanffy growth March to May). Maturity age of both S.
curve for Seriola lalandi. quinqueradiata and S. lalandi was 2 years old.
 Age and reproduction of Seriola lalandi 125

Fig. 7 Monthly changes in the gonadosomatic index (GSI) of male (n
60) and female (n
78) Seriola
lalandi. Vertical bars denote the standard error.

Fig. 8 Monthly changes in the frequency of occurrence of various maturity stages of (A) testes and (B)
ovaries in Seriola lalandi. For males, Sp, spermatogonial proliferation stage; Es, early spermatogenesis stage;
Ls, late spermatogenesis stage; Fm, functional maturation stage; Ps, post-spawning stage, and for females,
Im, immature stage; D, developing stage; Vi, vitellogenic stage; M, mature stage; Sp, spawning stage; Re,
resting stage. The numbers over each column represent the number of fish examined.
126 T Shiraishi et al.

Fig. 9 Relationships between (A) the five maturation stages of testes and gonadosomatic index (GSI); (B) the
five maturation stages of testes and fork length; (C) the six maturation stages of ovaries and GSI; (D) the six
maturation stages of ovaries and fork length of Seriola lalandi. Refer to Figs. 3 and 4 for each testis and
ovarian stage, respectively. n, number of fish examined.

The growth and reproductive parameter is Acknowledgements

different in habitation area or year class. It is The authors thank Dr Yamamoto of the Tsukuba
not clear whether these differences in growth Office, Agriculture, Forestry and Fisheries Research
(estimated sizes for
1-year-old fish) and re- Council Secretariat Ministry of Agriculture, Forestry
production (age and size of first spawning) and Fisheries for advice on the method of age
occur because of the geographic differences in determination using vertebral centrum.
the distribution (i.e. respective latitudes and
physical conditions) or are genetic differences.
In the present study, the biological charac-
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