Sex Ratio, Spawning Period, and Sexual Group Maturity of the Largehead Hairtail Trichiurus japonicus (Teleostei: Trichiuridae) in Korean Waters

Abstract

This study was performed to obtain information on the sex ratio, spawning period, and size at sexual maturity for fishery management of the largehead hairtail Trichiurus japonicus in Korean waters. The overall sex ratio (female, F; male, M) was 1:0.46 (n = 1274 females:589 males, 68.4% female) and as fish increased in length, the proportion of females increased. The oocyte development pattern was group-synchronous development, for which oocyte groups at different stages can be identified within the same ovary. The average gonadosomatic index (GSI) showed two peaks in June (3.03) and August (3.10) in females and in May (1.81) and September (2.24) in males. The median value of GSI showed two peaks in May (2.65F, 1.78M) and September (2.55F, 1.87M) for both females and males. As a result of analyzing the GSI and the monthly gonadal developmental stages, the main spawning season was estimated to be bi-annual (May–June and September–October). The anal length of fish at 50% sexual maturity was analyzed using a logistic regression model and was determined to be 16.38 cm (female) and 18.31 cm (male).

Full text

Citation: Shin, S.R.; Kim, H.J.; Kim,
J.W.; Kwon, D.-H.; Choi, J.; Park, J.J.;
Lee, J.S. Sex Ratio, Spawning Period,
and Sexual Group Maturity of the
Largehead Hairtail Trichiurus
japonicus (Teleostei: Trichiuridae) in
Korean Waters. Fishes 2023,8, 194.
https://doi.org/10.3390/fishes8040194
Academic Editors: Juan F. Asturiano
and Alberto Teodorico Correia
Received: 2 February 2023
Revised: 5 April 2023
Accepted: 6 April 2023
Published: 7 April 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
fishes
Article
Sex Ratio, Spawning Period, and Sexual Group Maturity of the
Largehead Hairtail Trichiurus japonicus (Teleostei: Trichiuridae)
in Korean Waters
So Ryung Shin 1, Hyeon Jin Kim 1, Jae Won Kim 2, Dae-Hyeon Kwon 3, Junghwa Choi 4, Jung Jun Park 5,*
and Jung Sick Lee 1, *
1Department of Aqualife Medicine, Chonnam National University, Yeosu 59626, Republic of Korea
2Department of Aquaculture, Gangwon State University, Gangneung 25425, Republic of Korea
3
West Sea Fisheries Research Institute, National Institute of Fisheries Science, Incheon 22383, Republic of Korea
4Fisheries Resources Management Division, National Institute of Fisheries Science,
Busan 46083, Republic of Korea
5Aquaculture Industry Research Division, East Sea Fisheries Research Institute, National Institute of
Fisheries Science, Gangneung 25435, Republic of Korea
*Correspondence: pjj515@korea.kr (J.J.P.); ljs@jnu.ac.kr (J.S.L.); Tel.: +82-33-660-8543 (J.J.P.);
+82-61-659-7172 (J.S.L.); Fax: +82-33-661-8515 (J.J.P.); +82-61-659-7179 (J.S.L.)
Abstract:
This study was performed to obtain information on the sex ratio, spawning period, and
size at sexual maturity for fishery management of the largehead hairtail Trichiurus japonicus in Korean
waters. The overall sex ratio (female, F; male, M) was 1:0.46 (n = 1274 females:589 males, 68.4%
female) and as fish increased in length, the proportion of females increased. The oocyte development
pattern was group-synchronous development, for which oocyte groups at different stages can be
identified within the same ovary. The average gonadosomatic index (GSI) showed two peaks in June
(3.03) and August (3.10) in females and in May (1.81) and September (2.24) in males. The median
value of GSI showed two peaks in May (2.65F, 1.78M) and September (2.55F, 1.87M) for both females
and males. As a result of analyzing the GSI and the monthly gonadal developmental stages, the main
spawning season was estimated to be bi-annual (May–June and September–October). The anal length
of fish at 50% sexual maturity was analyzed using a logistic regression model and was determined to
be 16.38 cm (female) and 18.31 cm (male).
Keywords: Trichiurus japonicus; sex ratio; GSI; spawning period; sexual group maturity
Key Contribution:
The spawning season of the largehead hairtail Trichiurus japonicus was estimated
to be bi-annual (May–June and September–October) in Korean waters. The anal length of fish at 50%
sexual maturity was 16.38 cm (female) and 18.30 cm (male).
1. Introduction
The hairtail, Trichiurus, is a migratory teleost belonging to the family Trichiuridae of
the order Scombriformes and is distributed in temperate and tropical zones around the
world [
1
]. In Northeast Asia, the hairtail mainly migrates from the south of Hokkaido to the
coastal waters of the East China Sea around Japan, the Korean Peninsula, and the Yellow
and Bohai Seas [2].
Trichiurus sp., which is mainly caught in Republic of Korea, was previously reported as
Trichiurus lepturus, but was later identified as T. japonicus as a result of molecular biological
analysis [
3
,
4
]. In Korea, Trichiurus is an important fishery resource, with the average catch
being 124,000 tons in the 1980s and approximately 68,000 tons in the early 2000s, though
the average catch in the last five years has decreased to 55,000 tons [
5
]. The reasons for
the continued decline in hairtail catch include the entry into force of The United Nations
Convention on the Law of the Sea, which was signed in 1994, and the entry into force of
Fishes 2023,8, 194. https://doi.org/10.3390/fishes8040194 https://www.mdpi.com/journal/fishes

Fishes 2023,8, 194 2 of 13
the agreement on fishing with Japan in 1999. As a result, many researchers continue to
study the ecology, reproduction, and fishing of hairtail to find a way to manage the reduced
fishing grounds [6–10].
The reproductive information, such as sex ratio, reproductive cycle, main spawning
period, and maturity of the teleost, is critical in terms of the conservation and management
of biological resources [
8
,
11
,
12
]. There have been many studies on the reproduction of
the hairtail, including those on fishery biology [
13
]; migration in the East China Sea
and Yellow Seas [
14
]; maturity and spawning in the Western Wakasa Bay [
15
]; stock
assessment of the Indian waters [
16
]; maturation and spawning in Korean waters [
6
,
7
,
17
];
reproduction in the South China Sea [
18
]; reproduction in the southern Brazil subtropical
convergence ecosystem [
19
]; age, growth, and reproduction in the southern East China
Sea [
20
]; fishery, reproductive biology, and stock status on the south-west coast of India [
21
];
and reproductive biology in south-eastern Australia [
22
]. The results on the main spawning
period and sexual maturity of T. japonicus migrating in Korean waters show differences
among these studies [6,7,17].
Various methods, such as morphology, anatomy, histology, and molecular biology,
are used to analyze biological indicators related to reproduction in teleosts. However, the
results obtained via morphological and anatomical methods can lead to serious errors;
in particular, when analyzing gonadal development and maturity using the histological
method, many errors can occur in the interpretation of the results, so caution is needed
regarding this [
11
,
12
,
23
]. In addition, immature individuals should be excluded from
the analysis of the frequency of gonadal development stage and gonadosomatic index
(GSI), which are essential parameters for main spawning period estimation. The sex ratio
analysis differs according to the fishing methods, age of the sample, and size, so caution is
required [7,18,19,24].
In this study, sex ratio, size at 50% sexual maturity, and main spawning period were
analyzed and compared with existing data to provide information for the efficient fishery
resource management of T.japonicus in Korea.
2. Materials and Methods
2.1. Sampling
Samples of Trichiurus japonicus were collected from January 2020 to December 2020
with a hairtail longline in Jeju Strait, Korea (Figure 1). About 150 specimens were collected
every month and the sex ratio was analyzed with 1863 specimens (Tables 1and 2). Among
this group, a total of 549 specimens (total length (TL): 81.7
±
11.3 cm; total weight (TW):
322.1
±
185.8 g) were analyzed with histological analysis of the gonads (approximately
40–50 specimens every month) (Figure 2, Table 1). For the analysis of the gonadosomatic
index (GSI), 531 specimens were used, excluding 18 immature specimens.
Fishes 2023, 8, x FOR PEER REVIEW 3 of 13
Figure 1. Sampling area of Trichiurus japonicus.
Figure 2. Morphometric characteristics of Trichiurus japonicus.
Table 1. Number of samples used in the analyses of the largehead hairtail Trichiurus japonicus.
Months (2020)
Number of Samples (Total Length, TL; Total Weight, TW)
Sex Ratio
Histological Analysis of the Gonads
January
30 (TL 85.5 ± 6.9 cm, TW 346.6 ± 128.0 g)
30 (TL 85.5 ± 6.9 cm, TW 346.6 ± 128.0 g)
February
30 (TL 77.1 ± 4.6 cm, TW 253.4 ± 57.1 g)
30 (TL 77.1 ± 4.6 cm, TW 253.4 ± 57.1 g)
March
70 (TL 83.8 ± 7.9 cm, TW 308.2 ± 126.8 g)
32 (TL 85.0 ± 8.7 cm, TW 343.3 ± 145.5 g)
April
185 (TL 79.1 ± 12.6 cm, TW 281.7 ± 204.1 g)
62 (TL 79.0 ± 15.3 cm, TW 300.8 ± 258.2 g)
May
95 (TL 78.3 ± 9.9 cm, TW 252.6 ± 130.1 g)
60 (TL 74.8 ± 19.0 cm, TW 279.0 ± 195.5 g)
June
108 (TL 80.3 ± 11.9 cm, TW 323.8 ± 172.8 g)
25 (TL 90.2 ± 12.9 cm, TW 420.9 ± 188.3 g)
July
70 (TL 78.8 ± 10.9 cm, TW 316.0 ± 179.2 g)
62 (TL 78.7 ± 11.4 cm, TW 206.7 ± 43.0 g)
August
228 (TL 79.6 ± 5.8 cm, TW 284.8 ± 92.4 g)
64 (TL 79.6 ± 7.4 cm, TW 294.5 ± 102.6 g)
September
209 (TL 83.1 ± 10.0 cm, TW 328.7 ± 163.8 g)
64 (TL 81.7 ± 10.4 cm, TW 317.7 ± 150.9 g)
October
272 (TL 84.9 ± 8.2 cm, TW 327.5 ± 159.7 g)
60 (TL 87.6 ± 10.9 cm, TW 388.9 ± 225.6 g)
November
286 (TL 83.6 ± 8.5 cm, TW 314.6 ± 197.4 g)
30 (TL 84.2 ± 11.1 cm, TW 320.1 ± 188.0 g)
December
280 (TL 83.7 ± 7.2 cm, TW 305.4 ± 120.5 g)
30 (TL 84.6 ± 9.3 cm, TW 322.4 ± 138.4 g)
Total
Average
1863
TL 81.9 ± 9.2 cm, TW 303.2 ± 155.3 g
549
TL 81.7 ± 11.3 cm, TW 322.1 ± 185.8 g
Figure 1. Sampling area of Trichiurus japonicus.

Fishes 2023,8, 194 3 of 13
Table 1. Number of samples used in the analyses of the largehead hairtail Trichiurus japonicus.
Months (2020)
Number of Samples (Total Length, TL; Total Weight, TW)
Sex Ratio Histological Analysis of the Gonads
January 30 (TL 85.5 ±6.9 cm, TW 346.6 ±128.0 g) 30 (TL 85.5 ±6.9 cm, TW 346.6 ±128.0 g)
February 30 (TL 77.1 ±4.6 cm, TW 253.4 ±57.1 g) 30 (TL 77.1 ±4.6 cm, TW 253.4 ±57.1 g)
March 70 (TL 83.8 ±7.9 cm, TW 308.2 ±126.8 g) 32 (TL 85.0 ±8.7 cm, TW 343.3 ±145.5 g)
April 185 (TL 79.1 ±12.6 cm, TW 281.7 ±204.1 g) 62 (TL 79.0 ±15.3 cm, TW 300.8 ±258.2 g)
May 95 (TL 78.3 ±9.9 cm, TW 252.6 ±130.1 g) 60 (TL 74.8 ±19.0 cm, TW 279.0 ±195.5 g)
June 108 (TL 80.3 ±11.9 cm, TW 323.8 ±172.8 g) 25 (TL 90.2 ±12.9 cm, TW 420.9 ±188.3 g)
July 70 (TL 78.8 ±10.9 cm, TW 316.0 ±179.2 g) 62 (TL 78.7 ±11.4 cm, TW 206.7 ±43.0 g)
August 228 (TL 79.6 ±5.8 cm, TW 284.8 ±92.4 g) 64 (TL 79.6 ±7.4 cm, TW 294.5 ±102.6 g)
September 209 (TL 83.1 ±10.0 cm, TW 328.7 ±163.8 g) 64 (TL 81.7 ±10.4 cm, TW 317.7 ±150.9 g)
October 272 (TL 84.9 ±8.2 cm, TW 327.5 ±159.7 g) 60 (TL 87.6 ±10.9 cm, TW 388.9 ±225.6 g)
November 286 (TL 83.6 ±8.5 cm, TW 314.6 ±197.4 g) 30 (TL 84.2 ±11.1 cm, TW 320.1 ±188.0 g)
December 280 (TL 83.7 ±7.2 cm, TW 305.4 ±120.5 g) 30 (TL 84.6 ±9.3 cm, TW 322.4 ±138.4 g)
Total
Average
1863
TL 81.9 ±9.2 cm, TW 303.2 ±155.3 g
549
TL 81.7 ±11.3 cm, TW 322.1 ±185.8 g
Table 2. Sex ratio with total length of largehead hairtail Trichiurus japonicus.
Total Length (cm) Number Sex Ratio
(F:M) Female (%)
Total Female Male
50.1–55.0 3 2 1 1:0.50 66.7
55.1–60.0 4 3 1 1:0.33 75.0
60.1–65.0 32 13 19 1:1.46 40.6
65.1–70.0 77 46 31 1:0.67 59.7
70.1–75.0 262 153 109 1:0.71 58.4
75.1–80.0 496 293 203 1:0.69 59.1
80.1–85.0 456 311 145 1:0.47 68.2
85.1–90.0 222 177 45 1:0.25 79.7
90.1–95.0 117 102 15 1:0.15 87.2
95.1–100.0 113 102 11 1:0.11 90.3
100.1–105.0 55 48 7 1:0.15 87.3
105.1–110.0 14 12 2 1:0.17 85.7
110.1–115.0 7 7 - - 100
115.1–120.0 5 5 - - 100
Total/Average 1863 1274 589 1:0.46 68.4
Fishes 2023, 8, x FOR PEER REVIEW 3 of 13
Figure 1. Sampling area of Trichiurus japonicus.
Figure 2. Morphometric characteristics of Trichiurus japonicus.
Table 1. Number of samples used in the analyses of the largehead hairtail Trichiurus japonicus.
Months (2020)
Number of Samples (Total Length, TL; Total Weight, TW)
Sex Ratio
Histological Analysis of the Gonads
January
30 (TL 85.5 ± 6.9 cm, TW 346.6 ± 128.0 g)
30 (TL 85.5 ± 6.9 cm, TW 346.6 ± 128.0 g)
February
30 (TL 77.1 ± 4.6 cm, TW 253.4 ± 57.1 g)
30 (TL 77.1 ± 4.6 cm, TW 253.4 ± 57.1 g)
March
70 (TL 83.8 ± 7.9 cm, TW 308.2 ± 126.8 g)
32 (TL 85.0 ± 8.7 cm, TW 343.3 ± 145.5 g)
April
185 (TL 79.1 ± 12.6 cm, TW 281.7 ± 204.1 g)
62 (TL 79.0 ± 15.3 cm, TW 300.8 ± 258.2 g)
May
95 (TL 78.3 ± 9.9 cm, TW 252.6 ± 130.1 g)
60 (TL 74.8 ± 19.0 cm, TW 279.0 ± 195.5 g)
June
108 (TL 80.3 ± 11.9 cm, TW 323.8 ± 172.8 g)
25 (TL 90.2 ± 12.9 cm, TW 420.9 ± 188.3 g)
July
70 (TL 78.8 ± 10.9 cm, TW 316.0 ± 179.2 g)
62 (TL 78.7 ± 11.4 cm, TW 206.7 ± 43.0 g)
August
228 (TL 79.6 ± 5.8 cm, TW 284.8 ± 92.4 g)
64 (TL 79.6 ± 7.4 cm, TW 294.5 ± 102.6 g)
September
209 (TL 83.1 ± 10.0 cm, TW 328.7 ± 163.8 g)
64 (TL 81.7 ± 10.4 cm, TW 317.7 ± 150.9 g)
October
272 (TL 84.9 ± 8.2 cm, TW 327.5 ± 159.7 g)
60 (TL 87.6 ± 10.9 cm, TW 388.9 ± 225.6 g)
November
286 (TL 83.6 ± 8.5 cm, TW 314.6 ± 197.4 g)
30 (TL 84.2 ± 11.1 cm, TW 320.1 ± 188.0 g)
December
280 (TL 83.7 ± 7.2 cm, TW 305.4 ± 120.5 g)
30 (TL 84.6 ± 9.3 cm, TW 322.4 ± 138.4 g)
Total
Average
1863
TL 81.9 ± 9.2 cm, TW 303.2 ± 155.3 g
549
TL 81.7 ± 11.3 cm, TW 322.1 ± 185.8 g
Figure 2. Morphometric characteristics of Trichiurus japonicus.
2.2. Environmental Conditions
Monthly averages of water temperature profiles of the study area were calculated
from daily measurements obtained from the Korea Hydrographic and Oceanographic
Administration [25].

Fishes 2023,8, 194 4 of 13
2.3. Histological Analysis
After measuring morphometric characteristics (TL, TW, AL, gonad weight), gonads
were prepared for examination under light microscopy. The samples were fixed in aqueous
10% neutral formalin for 24 h. The fixed sample was rinsed in running water for 48 h,
dehydrated through a graded ethanol series (70–100%), and then embedded in paraplast
(Leica, Wetzlar, Germany). Embedded tissues were serial-sectioned at a thickness of 4–6
µ
m using a microtome (RM2235, Leica, Wetzlar, Germany). Samples were stained with
Mayer’s hematoxylin—0.5% eosin (H–E) stain.
2.4. Sex Ratio
The sex ratio (female:male) and percentage of females in the population were calcu-
lated with the following Equations (1)and (2):
Sex ratio = Female (n):Male (n) (1)
Female frequency (%) = [Female (n)/Female (n) + male (n)] ×100 (2)
2.5. Gonadosomatic Index (GSI)
The gonadosomatic index (GSI) was calculated with the following Equation (3) [8,24,26,27]:
GSI (%) = Gonad weight (g)
Total weight (g)×100 (3)
2.6. Gonadal Developmental Stage
The oocytes were classified into six developmental stages: oogonium, previtellogenic,
initial vitellogenic, active vitellogenic, mature, and ripe [
28
]. The male germ cells were
classified into developmental stages of spermatogonium, spermatocyte, spermatid, and
sperm [
22
]. Gonadal development was classified into growing, mature, ripe, and spent and
degenerative stage for both males and females according to the degree of dominance of
each developmental stage of germ cells [29].
2.7. Sexual Group Maturity
In this study, the logistic regression model was used to estimate anal length at 50%,
75%, and 97.5% sexual maturity. Individuals were categorized based on their length into 2.0
cm class intervals. Afterwards, for each length group, we calculated 50%, 75%, and 97.5%
group maturity levels based on the size of the individuals corresponding to the mature,
ripe, and spent and degenerative stage. The mature individuals were evaluated based on
whether their ovaries were dominated by active vitellogenic oocytes, mature oocytes of
GVBD (germinal vesicle breakdown), or ripe oocytes, and only individuals that developed
ovaries after spawning were considered.
3. Results
3.1. Sex Ratio
The overall sex ratio (F:M) was 1:0.46. The female frequency was 68.4%, and as fish
increased in length, the proportion of females increased (Table 2).
3.2. Monthly Change of Gonadosomatic Index (GSI)
The average of the GSI showed two peaks in June (3.03) and August (3.10) for females
and May (1.81) and September (2.24) for males. In females, after increasing from January
to June, the GSI showed a rapid decrease in July. After showing a rapid increase again in
August, it continued to decrease until November. In males, after reaching 1.8 in May, the
GSI rapidly decreased in June, increased from July to September, and then decreased again
until November (Figure 3).

Fishes 2023,8, 194 5 of 13
Fishes 2023, 8, x FOR PEER REVIEW 5 of 13
germ cells were classified into developmental stages of spermatogonium, spermatocyte,
spermatid, and sperm [22]. Gonadal development was classified into growing, mature,
ripe, and spent and degenerative stage for both males and females according to the degree
of dominance of each developmental stage of germ cells [29].
2.7. Sexual Group Maturity
In this study, the logistic regression model was used to estimate anal length at 50%,
75%, and 97.5% sexual maturity. Individuals were categorized based on their length into
2.0 cm class intervals. Afterwards, for each length group, we calculated 50%, 75%, and
97.5% group maturity levels based on the size of the individuals corresponding to the
mature, ripe, and spent and degenerative stage. The mature individuals were evaluated
based on whether their ovaries were dominated by active vitellogenic oocytes, mature
oocytes of GVBD (germinal vesicle breakdown), or ripe oocytes, and only individuals that
developed ovaries after spawning were considered.
3. Results
3.1. Sex Ratio
The overall sex ratio (F:M) was 1:0.46. The female frequency was 68.4%, and as fish
increased in length, the proportion of females increased (Table 2).
3.2. Monthly Change of Gonadosomatic Index (GSI)
The average of the GSI showed two peaks in June (3.03) and August (3.10) for females
and May (1.81) and September (2.24) for males. In females, after increasing from January
to June, the GSI showed a rapid decrease in July. After showing a rapid increase again in
August, it continued to decrease until November. In males, after reaching 1.8 in May, the
GSI rapidly decreased in June, increased from July to September, and then decreased
again until November (Figure 3).
The median value of the GSI showed two peaks in May (2.65F, 1.78M) and September
(2.55F, 1.87M) for both males and females. Both males and females showed an increase
from January to May, followed by a rapid decrease in June and July. After showing a rapid
increase again in September, the GSI continued to decrease until November (Figure 3).
Figure 3. Monthly changes in gonadosomatic index (GSI) of largehead hairtail Trichiurus japonicus
and water temperature.
3.3. Histological Change with Gonadal Developmental Stage
3.3.1. Ovary
The oocyte development pattern was of the group-synchronous type, for which
oocyte populations of various stages can be identified within the same ovary [30]. The
spawning pattern showed a multiple spawning histology in which growing oocytes
developed after spawning within the same ovary (Figure 4).
Figure 3.
Monthly changes in gonadosomatic index (GSI) of largehead hairtail Trichiurus japonicus
and water temperature.
The median value of the GSI showed two peaks in May (2.65F, 1.78M) and September
(2.55F, 1.87M) for both males and females. Both males and females showed an increase
from January to May, followed by a rapid decrease in June and July. After showing a rapid
increase again in September, the GSI continued to decrease until November (Figure 3).
3.3. Histological Change with Gonadal Developmental Stage
3.3.1. Ovary
The oocyte development pattern was of the group-synchronous type, for which oocyte
populations of various stages can be identified within the same ovary [30]. The spawning
pattern showed a multiple spawning histology in which growing oocytes developed after
spawning within the same ovary (Figure 4).
Fishes 2023, 8, x FOR PEER REVIEW 6 of 13
In the growing stage of the ovary, the spent and degeneration of oocytes was not
observed. In the early growing stage, the ovary was filled with oogonia and
previtellogenic oocytes (Figure 4A), and initial vitellogenic oocytes and active vitellogenic
oocytes were mainly observed in the late growing stage (Figure 4B). Some active
vitellogenic oocytes were seen in the mature stage, but these were mainly mature oocytes
with GVBD (germinal vesicle breakdown) (Figure 4C). At the ripe stage, ripe oocytes with
a diameter of approximately 350 μm and eosinophilic stain were mainly observed (Figure
4D). At the spent and degenerative stage, the evidence for the release of ripe oocytes and
the degeneration of undischarged oocytes, as well as the relocation of early oocytes, was
confirmed (Figure 4E,F).
Figure 4. Ovarian developmental stage of the largehead hairtail Trichiurus japonicus. H–E stain. (A,B)
growing stage, (C) mature stage, (D) ripe stage, (E,F) spent and degenerative stage. Avo: active
vitellogenic oocyte, Do: degenerative oocyte, Ef: empty follicle, Eyg: eosinophilic yolk granule, Fl:
follicular layer, Gv: germinal vesicle, Ivo: initial vitellogenic oocyte, Mo: mature oocyte, Og:
oogonia, Ol: ovarian lobule, Pvo: previtellogenic oocytes, Ro: ripe oocyte, Zr: zona radiata.
3.3.2. Testis
The testicular development pattern was group synchronous, as multiple stages of
germ cell populations within the same gonad were identified simultaneously (Figure 5).
In the early growing stage, spermatocytes and spermatids were mainly observed (Figure
5A), and in the late growing stage, spermatocytes with condensed nucleoplasm and
cytoplasm were mainly observed, compared to spermatogonia along with some
spermatids (Figure 5B). In the mature stage, basophilic spermatids in the H–E stain were
mainly identified (Figure 5C), and testis in the ripe stage were filled with sperm of
basophilic in the H–E stain (Figure 5D). In the spent and degenerative stage, degeneration
and resorption of the remaining sperm after being spent were observed in the medulla of
the testis, but spermatogonia and spermatocytes were rearranged in the cortex (Figure
5E,F).
Figure 4.
Ovarian developmental stage of the largehead hairtail Trichiurus japonicus. H–E stain.
(
A
,
B
) growing stage, (
C
) mature stage, (
D
) ripe stage, (
E
,
F
) spent and degenerative stage. Avo: active
vitellogenic oocyte, Do: degenerative oocyte, Ef: empty follicle, Eyg: eosinophilic yolk granule, Fl:
follicular layer, Gv: germinal vesicle, Ivo: initial vitellogenic oocyte, Mo: mature oocyte, Og: oogonia,
Ol: ovarian lobule, Pvo: previtellogenic oocytes, Ro: ripe oocyte, Zr: zona radiata.

Fishes 2023,8, 194 6 of 13
In the growing stage of the ovary, the spent and degeneration of oocytes was not
observed. In the early growing stage, the ovary was filled with oogonia and previtellogenic
oocytes (Figure 4A), and initial vitellogenic oocytes and active vitellogenic oocytes were
mainly observed in the late growing stage (Figure 4B). Some active vitellogenic oocytes
were seen in the mature stage, but these were mainly mature oocytes with GVBD (ger-
minal vesicle breakdown) (Figure 4C). At the ripe stage, ripe oocytes with a diameter of
approximately 350
µ
m and eosinophilic stain were mainly observed (Figure 4D). At the
spent and degenerative stage, the evidence for the release of ripe oocytes and the degener-
ation of undischarged oocytes, as well as the relocation of early oocytes, was confirmed
(Figure 4E,F).
3.3.2. Testis
The testicular development pattern was group synchronous, as multiple stages of germ
cell populations within the same gonad were identified simultaneously (Figure 5). In the
early growing stage, spermatocytes and spermatids were mainly observed (Figure 5A), and
in the late growing stage, spermatocytes with condensed nucleoplasm and cytoplasm were
mainly observed, compared to spermatogonia along with some spermatids (Figure 5B). In
the mature stage, basophilic spermatids in the H–E stain were mainly identified (Figure 5C),
and testis in the ripe stage were filled with sperm of basophilic in the H–E stain (Figure 5D).
In the spent and degenerative stage, degeneration and resorption of the remaining sperm
after being spent were observed in the medulla of the testis, but spermatogonia and
spermatocytes were rearranged in the cortex (Figure 5E,F).
Fishes 2023, 8, x FOR PEER REVIEW 7 of 13
Figure 5. Testicular developmental stage of the largehead hairtail Trichiurus japonicus. H–E stain.
(A,B) growing stage, (C) mature stage, (D) ripe stage, (E,F) spent and degenerative stage. Sc:
spermatocytes, Sd: spermatids, Sg: spermatogonia, Sp: sperm, Tc: testicular cyst, Tl: testicular
lobule, Uds: undischarged sperm.
3.4. Monthly Change of Gonadal Developmental Stage
3.4.1. Ovary
The annual frequencies (January 2020–December 2020) of the ovarian developmental
stages were 31.3% for the growing stage, 11.9% for the mature stage, 19.5% for the ripe
stage, and 37.5% for the spent and degenerative stage (Figure 6). The monthly frequencies
of the spent and degenerative stage (48.0%) and the growing stage (40.0%) dominated in
January, and the growing stage had a frequency of 92.0% in February. In March, the
growing stage decreased to a 55.6% frequency, but the mature stage increased to 33.3%.
The ripe stage was dominant in April at 29.7% frequency and in May at 54.8%. In June,
the ripe stage had a 54.2% frequency and the spent and degenerative stage had a
frequency of 29.2%. The ripe stage was not observed in July, and the spent and
degenerative stage reached 82.1% frequency. In August, the mature and ripe stages had a
frequency of 36.6% and 17.1%, respectively. In September, when the water temperature
dropped, the frequency of the ripe stage was 32.4% and that of the spent and degenerative
stage was 51.4%. The spent and degenerative stage (93.6%) dominated in October and the
growing stage dominated in November and December (Figure 7).
3.4.2. Testis
The annual frequencies (March 2020–December 2020) of the testicular developmental
stages were 15.3% for the growing stage, 28.2% for the mature stage, 20.3% for the ripe
stage, and 36.2% for the spent and degenerative stage (Figure 6). The monthly frequencies
of the testicular developmental stages, the ratios of the growing, mature, and ripe stages,
were 21.4%, 64.3%, and 14.3% in March, respectively. In April, the mature stage reached
a 40.0% frequency and the ripe stage reached 28.0%. In May, the mature stage and ripe
stage dominated at 20.8% and 62.5%, respectively. In June, the spent and degenerative
stage was at 100%. In July, the mature stage and ripe stage were not confirmed, and the
spent and degenerative stage was at 73.7%. In August, the growing stage showed 21.7%
frequency and the mature stage 47.8%. In September, the mature stage was at 30.8% and
the ripe stage was at 23.1%. From October to December, the spent and degenerative stage
was dominant (Figure 7).
Figure 5.
Testicular developmental stage of the largehead hairtail Trichiurus japonicus. H–E stain.
(
A
,
B
) growing stage, (
C
) mature stage, (
D
) ripe stage, (
E
,
F
) spent and degenerative stage. Sc: sperma-
tocytes, Sd: spermatids, Sg: spermatogonia, Sp: sperm, Tc: testicular cyst, Tl: testicular lobule, Uds:
undischarged sperm.
3.4. Monthly Change of Gonadal Developmental Stage
3.4.1. Ovary
The annual frequencies (January 2020–December 2020) of the ovarian developmental
stages were 31.3% for the growing stage, 11.9% for the mature stage, 19.5% for the ripe
stage, and 37.5% for the spent and degenerative stage (Figure 6). The monthly frequencies
of the spent and degenerative stage (48.0%) and the growing stage (40.0%) dominated
in January, and the growing stage had a frequency of 92.0% in February. In March, the
growing stage decreased to a 55.6% frequency, but the mature stage increased to 33.3%. The

Fishes 2023,8, 194 7 of 13
ripe stage was dominant in April at 29.7% frequency and in May at 54.8%. In June, the ripe
stage had a 54.2% frequency and the spent and degenerative stage had a frequency of 29.2%.
The ripe stage was not observed in July, and the spent and degenerative stage reached
82.1% frequency. In August, the mature and ripe stages had a frequency of 36.6% and
17.1%, respectively. In September, when the water temperature dropped, the frequency of
the ripe stage was 32.4% and that of the spent and degenerative stage was 51.4%. The spent
and degenerative stage (93.6%) dominated in October and the growing stage dominated in
November and December (Figure 7).
Fishes 2023, 8, x FOR PEER REVIEW 8 of 13
Figure 6. Annual frequency of gonadal developmental stage in the largehead hairtail Trichiurus
japonicus.
Figure 7. Monthly change in frequency of gonadal developmental stage in the largehead hairtail
Trichiurus japonicus and water temperature.
3.5. Sexual Group Maturity
The histologically analyzed female (n = 368) and male (n = 181) maturities were 96.2%
and 80.7%, respectively (Table 3). In females, anal length (AL) at 50% maturity was 16.38
cm, and at 75% and 97.5% maturity, 19.39 cm and 26.42 cm, respectively. In males, AL at
50% maturity was 18.31 cm, and at 75% and 97.5% maturity, 23.91 cm and 36.97 cm,
respectively (Figure 8).
Figure 6. Annual frequency of gonadal developmental stage in the largehead hairtail Trichiurus japonicus.
Fishes 2023, 8, x FOR PEER REVIEW 8 of 13
Figure 6. Annual frequency of gonadal developmental stage in the largehead hairtail Trichiurus
japonicus.
Figure 7. Monthly change in frequency of gonadal developmental stage in the largehead hairtail
Trichiurus japonicus and water temperature.
3.5. Sexual Group Maturity
The histologically analyzed female (n = 368) and male (n = 181) maturities were 96.2%
and 80.7%, respectively (Table 3). In females, anal length (AL) at 50% maturity was 16.38
cm, and at 75% and 97.5% maturity, 19.39 cm and 26.42 cm, respectively. In males, AL at
50% maturity was 18.31 cm, and at 75% and 97.5% maturity, 23.91 cm and 36.97 cm,
respectively (Figure 8).
Figure 7.
Monthly change in frequency of gonadal developmental stage in the largehead hairtail
Trichiurus japonicus and water temperature.
3.4.2. Testis
The annual frequencies (March 2020–December 2020) of the testicular developmental
stages were 15.3% for the growing stage, 28.2% for the mature stage, 20.3% for the ripe
stage, and 36.2% for the spent and degenerative stage (Figure 6). The monthly frequencies
of the testicular developmental stages, the ratios of the growing, mature, and ripe stages,
were 21.4%, 64.3%, and 14.3% in March, respectively. In April, the mature stage reached a

Fishes 2023,8, 194 8 of 13
40.0% frequency and the ripe stage reached 28.0%. In May, the mature stage and ripe stage
dominated at 20.8% and 62.5%, respectively. In June, the spent and degenerative stage was
at 100%. In July, the mature stage and ripe stage were not confirmed, and the spent and
degenerative stage was at 73.7%. In August, the growing stage showed 21.7% frequency
and the mature stage 47.8%. In September, the mature stage was at 30.8% and the ripe stage
was at 23.1%. From October to December, the spent and degenerative stage was dominant
(Figure 7).
3.5. Sexual Group Maturity
The histologically analyzed female (n = 368) and male (n = 181) maturities were 96.2%
and 80.7%, respectively (Table 3). In females, anal length (AL) at 50% maturity was 16.38
cm, and at 75% and 97.5% maturity, 19.39 cm and 26.42 cm, respectively. In males, AL
at 50% maturity was 18.31 cm, and at 75% and 97.5% maturity, 23.91 cm and 36.97 cm,
respectively (Figure 8).
Table 3. Sexual group maturity with anal length of largehead hairtail Trichiurus japonicus.
Anal
Length
(cm)
Female Male
Examined
Individuals
Mature
Individuals
Maturity
(%)
Examined
Individuals
Mature
Individuals
Maturity
(%)
18.1–20.0 5 5 100 7 3 42.9
20.1–22.0 37 32 86.6 25 16 64.0
22.1–24.0 68 66 97.1 51 43 84.3
24.1–26.0 72 69 95.8 44 38 86.4
26.1–28.0 74 70 94.6 29 22 75.9
28.1–30.0 23 23 100 7 7 100
30.1–32.0 28 28 100 1 1 100
32.1–34.0 34 34 100 12 12 100
34.1–36.0 14 14 100 3 2 66.7
36.1–38.0 6 6 100 2 2 100
38.1–40.0 2 2 100 - - -
40.1–42.0 3 3 100 - - -
42.1–44.0 2 2 100 - - -
Total 368 354 96.2 181 146 80.7
Fishes 2023, 8, x FOR PEER REVIEW 9 of 13
Table 3. Sexual group maturity with anal length of largehead hairtail Trichiurus japonicus.
Anal
Length
(cm)
Female
Male
Examined
Individuals
Mature
Individuals
Maturity
(%)
Examined
Individuals
Mature
Individuals
Maturity
(%)
18.1–20.0
5
5
100
7
3
42.9
20.1–22.0
37
32
86.6
25
16
64.0
22.1–24.0
68
66
97.1
51
43
84.3
24.1–26.0
72
69
95.8
44
38
86.4
26.1–28.0
74
70
94.6
29
22
75.9
28.1–30.0
23
23
100
7
7
100
30.1–32.0
28
28
100
1
1
100
32.1–34.0
34
34
100
12
12
100
34.1–36.0
14
14
100
3
2
66.7
36.1–38.0
6
6
100
2
2
100
38.1–40.0
2
2
100
-
-
-
40.1–42.0
3
3
100
-
-
-
42.1–44.0
2
2
100
-
-
-
Total
368
354
96.2
181
146
80.7
Figure 8. Relationship between anal length (AL) and sexual group maturity of largehead hairtail
Trichiurus japonicus.
4. Discussion
The sex ratio of Trichiurus has been reported to be 1:1 or a high female ratio, but as
shown in Table 3, it showed differences depending on the region and researcher. These
discrepancies are thought to be due to differences in sample size according to the
sampling period and sampling method [19]. Therefore, for sex ratio analysis, analyzing
the same number of individuals in the same group size can reduce differences in the
interpretation of the results. The sex ratio of Trichiurus is generally high for males in small
groups and tends to increase for females with increasing size [19]. In the group collected
from the East China Sea, females were longer and heavier than males. These biological
differences between males and females are due to the difference in growth rate and
lifespan, because females, after two years of age, have a faster growth rate than males, and
females live more than four years longer than males [7,8].
In many studies on Trichiurus, even at the same stage of gonadal development, the
GSI differed among researchers. The average GSI peak in females in previous studies was
approximately 4.0 [6], 5.42 [7], and 3.5 [22,26], while in this study, it was 3.10. These
differences in the GSI are believed to be due to variations in nutritional status according
Figure 8.
Relationship between anal length (AL) and sexual group maturity of largehead hairtail
Trichiurus japonicus.

Fishes 2023,8, 194 9 of 13
4. Discussion
The sex ratio of Trichiurus has been reported to be 1:1 or a high female ratio, but as
shown in Table 3, it showed differences depending on the region and researcher. These
discrepancies are thought to be due to differences in sample size according to the sampling
period and sampling method [
19
]. Therefore, for sex ratio analysis, analyzing the same
number of individuals in the same group size can reduce differences in the interpretation of
the results. The sex ratio of Trichiurus is generally high for males in small groups and tends
to increase for females with increasing size [
19
]. In the group collected from the East China
Sea, females were longer and heavier than males. These biological differences between
males and females are due to the difference in growth rate and lifespan, because females,
after two years of age, have a faster growth rate than males, and females live more than
four years longer than males [7,8].
In many studies on Trichiurus, even at the same stage of gonadal development, the
GSI differed among researchers. The average GSI peak in females in previous studies
was approximately 4.0 [
6
], 5.42 [
7
], and 3.5 [
22
,
26
], while in this study, it was 3.10. These
differences in the GSI are believed to be due to variations in nutritional status according
to habitat and food [
19
,
30
,
31
], anatomical errors in the process of gonadal extraction, and
macroscopical classification of gonadal developmental stages [11,12,23].
Usually, the analysis of the GSI includes immature individuals and uses the average
value. The GSI may be underestimated when immature individuals are included. In the
GSI analysis, if the number of samples is small, a large difference in the average value may
occur due to some individuals having a very low or high GSI. Therefore, when a small
number of samples is used, it is recommended that the median value be used rather than
the average. In this study, the GSI analysis excluded immature individuals and showed
some differences when comparing the average and median values. When averages were
used, two peaks were observed in June and August for females and in May and September
for males. However, when the median value was applied, both males and females showed
two peaks in May and September.
Anatomical and histological methods are important in the analysis of the gonadal
developmental patterns, main spawning period, and sexual group maturity of teleosts.
The anatomical method has advantages over the histological method in terms of time
and cost, but has the disadvantage of low accuracy. Macroscopic staging for the ovarian
developmental stage of Trichiurus showed approximately 85% accuracy compared to micro-
scopic staging [
18
]. Care should be taken in microscopic interpretation for ovarian tissue
specimens from the ripe or spawning period of teleosts. In particular, care must be taken in
the interpretation of skipped spawning and the incidence of high-intensity atresia, because
these histological features can be interpreted as normal spawning objects [32–34].
Oocyte development patterns can be classified into synchronous, group-synchronous,
and asynchronous types according to the distribution patterns of dominant oocytes in the
ovary [
35
]. The group-synchronous pattern is the one in which at least two populations
of oocytes are distinct at the same time, and is a type mainly seen in teleosts, including
Leiognathus nuchalis [29,36].
Previous reports on oocyte developmental patterns have also reported that Trichiurus
are group synchronous and spawn more than twice during the spawning season once a
year [
6
,
7
,
17
,
18
]. In this study, the oocyte developmental pattern was also confirmed as
a group-synchronous type. However, in this study, the spawning season was observed
twice a year, in May–June and September–October, and it was different from the April–
October [
6
], June–November [
7
], and June–October [
17
] spawning seasons reported in the
same region.
This difference is believed to be due to the method of analysis used to determine
the maturity of the gonads. Cha and Lee [
6
] and Kim et al. [
7
] evaluated the spawning
period by means of the GSI and gonadal developmental stages by gonadal appearance.
In this study, the GSI increased again after the first spawning. In addition, as a result
of the histological analysis of the gonads, the degeneration of residual oocytes and the

Fishes 2023,8, 194 10 of 13
reappearance of early oocytes appeared simultaneously after the first spawning, and the
development of early oocytes was confirmed up to the second spawning period.
Histological evidence of ovarian maturation should be considered when evaluating
the maturity of females. In particular, in many studies on group-synchronous type fish,
mistakes are made in judging ovarian histological maturity due to the difficulty of dis-
tinguishing between the germ cell development and the ovarian developmental stage.
Oocytes of teleosts are laid in the primary oocyte stage of the first meiotic division. There-
fore, from the histological view, the oocyte developmental stage of the teleost is based
on morphological criteria including cell size, degree of yolk accumulation, and nuclear
changes from the oogonium to the primary oocyte that can be identified in the ovary [
28
].
Germ cell development is the differentiation and development process of germ cells, but the
ovarian developmental stage is classified based on the dominant germ cells in the gonads.
Therefore, determination of ovarian maturity in group-synchronous type fish should be
based on ovarian maturity, not in the developmental stage of germ cells.
The size at 50% sexual group maturity in Trichiurus has been reported differently by
researchers, as shown in Table 3, and these differences are believed to be due to differences
in the growth rate and analysis methods used. In the population collected from a sea area
similar to this study, the anal length (AL) at 50% sexual group maturity was 25.5 cm [
19
],
26.0 cm [
6
], 26.4 cm [
20
], and 25.0 cm [
7
]. These results are different from the 16.38 cm AL
found in this study. This difference is believed to be due to the difference in standards and
evaluation methods used for mature individuals (Table 4).
Table 4. Sex ratio and size of 50% sexual group maturity (L50) in Trichiurus sp.
Region Species Sampling Area Sex Ratio
(F:M) Size (cm) Citation
Tropical to
subtropical T. lepturus
Visakhapatnam Waters, India - TL 42.5 Reuben et al., 1997 [37]
All-India - TL 60 Thiagarajan et al., 1992 [16]
Karnataka Coast, India 1:0.85 TL 55.4 Rajesh et al., 2015 [21]
Arabian Sea, Oman 1:0.12 TL 79 Al-Nahdi et al., 2009 [24]
Northern Arabian Sea 1:0.75 TL 61.2 Ghosh et al., 2014 [27]
Northern Bay of Bengal 1:0.81 TL 52.9
South-eastern Brazil - TL 39 Bellini, 1980 [38]
Gulf of Mexico - TL 35 Sheridan et al., 1984 [39]
Southern Brazil 1:1 TL 69.3 Martins and Haimovici, 2000 [19]
Temperate
T. nanhaiensis South China Sea 1:1 AL 28.2 Kwok and Ni, 1999 [18]
T. lepturus
South China Sea 1:1 AL 25.5
South-eastern Australia 1:0.4 TL 108.0 Clain et al., 2023 [22]
Jeju Island, Korea - AL 26.0 Cha and Lee, 2004 [6]
T. japonicus
Southern East China Sea 1:1 PL 26.4 Shih et al., 2011 [20]
Jeju Island, Korea 1:0.38 AL 25.0 Kim et al., 2020 [7]
Jeju Island, Korea 1:0.46 AL 16.4 Present study
AL: anal length, PL: preanal length, TL: total length.
In the report of Cha and Lee [
6
], four stages of ovary development were macroscopi-
cally classified as immature, maturing, mature, and spent, based on the size and color of
the gonad, and the size and transparency of the egg. After the maturing stage, a fish was
classified as a mature individual. Kim et al. [
7
] classified five stages, immature, developing,
mature, spawning, and resting, under the same criteria as Cha and Lee [
6
], and considered
a fish to be a mature individual after the mature stage. Kwok and Ni [
18
] and Shih et al. [
20
]
classification methods seemed to be based on the oocyte developmental stage, not the
ovarian developmental stage (Table 4).

Fishes 2023,8, 194 11 of 13
The information on the main spawning season (May–June and September–October)
and size at 50% group sexual maturity (AL 16.38 cm) obtained in this study can be consid-
ered for the establishment of prohibited fishing size and seasons for resource management
of the T.japonicus in Korean waters.
5. Conclusions
This study was performed to obtain information on the exact reproductive ecology for
fishery management of the largehead hairtail Trichiurus japonicus in Korea. The overall sex
ratio (female:male) was 1:0.46 (n = 1274:589, 68.4% female) and the percentage of females
in the population tended to increase with length. The sex ratio was different from that
found in previous studies [
15
–
17
,
34
], and one of the methods employed to minimize this
difference was to use the same number of individuals in the same group size from the same
population. As a result of using the average and median values in the GSI analysis, both
peaks appeared twice, but there was a temporal difference (average: F, June and August,
M, May and September; median value: F and M, May and September). From these results,
it is also recommended that the median together with the average be used in the analysis
of the GSI. The spawning season was estimated to occur twice a year (May–June and
September–October), and the anal length at 50% sexual group maturity was 16.38 cm for
males and 18.31 cm for females. These results are different from those of previous studies,
and thus differences in maturity standards and interpretations should be considered. The
data on the main spawning season and size at 50% sexual group maturity can be considered
for the establishment of prohibited fishing size and seasons for resource management of
the Trichiurus japonicus in Korean waters.
Author Contributions:
Conceptualization, J.J.P. and J.S.L.; methodology, S.R.S.; software, H.J.K.;
validation, J.W.K. and D.-H.K.; formal analysis, J.C.; investigation, S.R.S. and H.J.K.; resources,
D.-H.K.
and J.C.; data curation, J.W.K.; writing—original draft preparation, S.R.S.; writing—review and
editing, S.R.S.; H.J.K. and J.S.L.; visualization, H.J.K.; supervision, J.J.P.; project administration, J.S.L.;
funding acquisition, J.C. All authors have read and agreed to the published version of
the manuscript
.
Funding:
This research was supported by a grant from the National Institute of Fisheries Science,
Korea (grant no. R2023057).
Institutional Review Board Statement:
The animal study protocol was approved by the Ethics
Committee of Chonnam National University (CNU IACUC-YS-2023-6).
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.
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