ORIGINAL ARTICLE Biology

Growth of juvenile chub mackerel Scomber japonicusin the western North Pacific Ocean: with applicationand validation of otolith daily increment formation

Masanori Takahashi • Michio Yoneda •

Hajime Kitano • Atsushi Kawabata •

Mami Saito

Received: 31 May 2013 / Accepted: 26 December 2013

� The Japanese Society of Fisheries Science 2014

Abstract The growth of juvenile chub mackerel Scomber

japonicus collected in the western North Pacific Ocean in

2007 and 2009 was examined based on the evidence of

otolith daily increment formation in captive specimens.

There was a significant difference in the relationship

between known age and number of increments in the frontal

and sagittal planes. Repeated markings on the otolith using

Alizarin complexone and the coefficient of variation in

number of increments suggest that the increments in the

frontal plane of the otolith are more suitable for age esti-

mation than those in the long and short axes of the sagittal

plane. The increments in the frontal plane formed daily, and

the first ring was usually deposited 3 days after hatch. Age of

wild juveniles ranged from 24 to 211 days after hatch based

on the frontal plane method. The estimated hatching periods

of specimens ranged from February to June, but the April-

hatched specimens were collected throughout the sampling

periods of 2007 and 2009. The Gompertz growth model

showed a difference in growth pattern in specimens between

2007 and 2009. The juveniles in 2009 appeared to grow more

quickly than those in 2007 until summer, but thereafter the

2009 specimens seemed to grow more slowly.

Keywords Alizarin complexone � Growth � Otolith �Scomber japonicus � Validation � Western North Pacific

Ocean

Introduction

Chub mackerel Scomber japonicus is one of the most

important commercial fishes around the coastal waters of

Japan, and it has been managed by the total allowable catch

system since 1997. Among the Pacific stock of chub

mackerel, spawning mainly occurs from April to June in

the waters around the Izu Islands, central Japan [1–4]. The

larvae and juveniles drift northeast into the Kuroshio-Oy-

ashio transition area, which functions as a nursery ground,

and then they migrate to the feeding ground around the

waters off the Kuril Islands from June to October [1, 5–8].

The size of the Pacific stock of chub mackerel has

decreased dramatically since the 1980s, and has remained

low over the last few decades [8]. The higher fishing

mortality rates found in younger chub mackerel and the

lower abundance of recruits were considered to prevent

recovery of the population, although relatively large year

classes occurred in several years in the 1990s and 2000s.

M. Takahashi � A. Kawabata

National Research Institute of Fisheries Science, Fisheries

Research Agency, 2-12-4 Fukuura, Kanazawa-Ku, Yokohama,

Kanagawa 236-8648, Japan

Present Address:

M. Takahashi (&)

National Research Institute of Fisheries and Environment of

Inland Sea, Fisheries Research Agency, 2-17-5 Maruishi,

Hatsukaichi, Hiroshima 739-0452, Japan

e-mail: mtaka8@affrc.go.jp

M. Yoneda

Hakatajima Station, National Research Institute of Fisheries and

Environment of Inland Sea, Fisheries Research Agency,

2780 Kinourakou, Hakatachou, Imabari, Ehime 794-2305, Japan

H. Kitano

Fisheries Research Institute of Karatsu, Department of Joint

Research, Faculty of Agriculture, Kyushu University,

6-10-1 Hakozaki, Higashi-Ku, Fukuoka 812-8581, Japan

M. Saito

Environmental Science Laboratory, JAPAN NUS Co. Ltd,

1-1 Fukuura, Kanazawa-Ku, Yokohama,

Kanagawa 236-0004, Japan

123

Fish Sci

DOI 10.1007/s12562-013-0698-2

The long-term trend in the relationship between fish size at

age 0 (about 6 months old) and the abundance of recruit-

ment have indicated that the growth pattern during the

early life stage could be one of the key factors for under-

standing the mechanisms of recruitment fluctuation in the

Pacific stock of chub mackerel [9]. However, little infor-

mation on growth characteristics and survival process of

juvenile chub mackerel in these waters was available.

Microstructural increments (ring marks) in the otolith are

widely used for age determination and to estimate the

growth pattern of fish species during early life stages [10,

11]. In many cases, it has been assumed that microstructural

increments on the otolith are formed daily (e.g., Ma et al.

[12]). However, this assumption may be invalid, as the

otolith increment deposition may not be daily, or easily

discernible in some species [13, 14]. For chub mackerel,

estimates of spawning dates and growth pattern of juveniles

[15, 16] were based on an examination of microstructural

increments on the sagittal otolith, using evidence from

captive Atlantic mackerel Scomber scombrus [17] (Migoya,

unpublished, 1989) or spotted mackerel S. australasicus

[18]. However, no study of the validation of daily-based

formation of microstructural increments on the otolith has

been made in chub mackerel. Also, the microstructure of the

sagittal otolith of chub mackerel shows the occurrence of

accessory primordia (AP) at a specific time in the early life

stage [15]. Thereafter, the otolith grows rapidly from the

AP, giving the otolith a fan-like morphology in the sec-

ondary growth layers. These morphometric characteristics

would make it difficult to obtain a single plane of sectioning

through the core of the otolith to its edge. It is therefore

reasonable to assume that the interpretation and validation

of the microstructural growth pattern on the sagittal otolith

should be a prerequisite to estimating the age and growth of

chub mackerel during the early life stage.

The main purpose of this study is to standardize the

method of juvenile chub mackerel otoliths for the purposes

of age estimation. The microstructural increments on the

different planes of the otolith of captive individuals were

compared through rearing experiment, accompanied by

repeated marking of the otolith using Alizarin complexone

(ALC) at set intervals. The hatch dates and growth patterns

of juveniles were also examined, using specimens collected

from the Kuroshio-Oyashio transition area to the Oyashio

area in 2007 and 2009.

Materials and methods

Experimental set up

Juvenile chub mackerel were caught from the waters off

western Shikoku Island, Ehime Prefecture, and maintained

in the sea cages of a fish-farming company under natural

photoperiod and sea temperature from autumn 2007. In

April 2009, the 2-year-old fish in sea cages were trans-

ferred to the Fishery Research Laboratory of Kyushu

University, Fukuoka Prefecture, and kept in circular tanks

(3 t) under ambient temperature and a natural photoperiod.

After anesthetizing the specimens with 2-phenoxyethanol

(0.02 %), females with oocytes greater than 600 lm in

diameter and spermiating males were injected intramus-

cularly with GnRHa [des Gly10-(D-Ala6) LHRH ethyla-

mide; Sigma-Aldrich, St. Louis, MO, USA] [400 lg/kg

body weight (BW)], combined with coconut oil [19]. After

GnRHa injection, specimens to be returned into the circular

tanks were fed about 1 % BW per day of commercial dry

pellets (Higashimaru Co. Ltd., Tokyo, Japan). Fertilized

eggs were able to be collected every day from 2 days after

GnRHa injection, for about a month [19]. About 1,000 eggs

were transferred into 0.5 t circular tanks under ambient

temperature and a natural photoperiod, and larvae were

hatched out 3 days after spawning. They were fed with

rotifers, type S, enriched with docosahexaenoic acid

(DHA)-enriched fresh-water chlorella (Super Fresh Chlo-

rella-V12; Pacific Trading Co. Ltd., Fukuoka, Japan) from

2 days after they hatched. Artemia nauplii, enriched with a

commercial emulsion of n-3 polyunsaturated fatty acids

(Marine Alfa; Nisshin Marine Tech Co. Ltd., Tokyo,

Japan), were also fed to juveniles from 13 days after

hatching. Fish were fed formula feed (New Alteck;

Marubeni Nisshin Feed Co. Ltd., Tokyo, Japan) 15 days

after hatching.

ALC marking

Three repeated luminescent markings were made to vali-

date the periodicity of microstructural increments on the

sagittal otolith [17, 20]. Specimens were exposed to

25 ppm ALC solution, buffered to rearing pH with NaOH,

for 5.5 h 28 days after hatching. Second and third ALC

treatments were conducted 48 and 68 days after hatching.

Eighty-nine days after they hatched, all specimens were

collected and measured to the nearest 0.1 mm fork length

(FL) and BW. Identification of the developmental stage of

the individuals followed Watanabe [1]. Otoliths of speci-

mens were removed and cleaned by removing tissue frag-

ments, and stored dry until mounting.

Otolith preparation

To determine the optimal plane of sagitta (henceforth ot-

oliths) to observe the microstructural increments, the left

side of the otolith was used to analyze increments in the

frontal plane, while the right side was used for the sagittal

plane (Fig. 1). In both otoliths of a specimen, the rostrum

Fish Sci

123

side was folded to avoid loss by polishing of the curved

otolith edge. The left otolith was embedded in epoxy resin

(Petropoxy 154, Maruto Instrument Co. Ltd., Tokyo,

Japan) and mounted on a glass slide with hot water-soluble

wax (Aqua wax 80, Maruto Instrument Co. Ltd., Tokyo,

Japan), with the ventral side up. The otoliths were polished

with waterproof sandpaper (#600-2000) and alumina pol-

ishing suspension (Baikalox 3.0CR, Baikowski Japan Co.

Ltd., Chiba, Japan) until the nucleus became visible, and

thenthe wax was removed from the glass slide using hot

water. The otolith was turned over and mounted on a glass

slide with epoxy resin, with the dorsal side up. The dorsal

side was polished again with waterproof sandpaper and

alumina polishing suspension above the nucleus. The right

otolith was mounted in clear fingernail enamel, distal side

up, on a glass slide, and polished with waterproof sand-

paper and alumina polishing suspension until the nucleus

became visible.

The number of microstructural increments and ALC

luminescent markings on each plane of the otolith were

counted using an otolith measurement system (Ratoc Sys-

tem Engineering, Tokyo, Japan), comprising a transmitting

light or reflected UV light microscope at 200–400 magni-

fication. To validate daily-based increment deposition on

the otolith, the cumulative number of increments marked

ALC on the otolith and days after hatching ALC treatments

(ages 28, 48 and 68 days) were compared. Also, to deter-

mine the microstructural increments on the optimal planes

of the otolith for age estimation, the number of increments

in three different planes—frontal plane (postrostrum

direction), long axis (postrostrum direction) of sagittal

plane, and short (posterior or anterior direction) axis of

sagittal plane—were compared.

Field collection

Specimens were collected during eight research cruises

conducted to cover the distribution area of juveniles of the

Pacific stock of chub mackerel at the Kuroshio-Oyashio

transition zone and the Oyashio area, between May and

October in 2007 and 2009 (Table 1). A mid-water trawl net

was used (27–30 m mouth opening, 8–17 mm mesh cod-

end, 30–60 min duration at 3.5–5.0 knots). All samples

were frozen on board. If the catch was too numerous (more

than about 100 specimens), about 60 specimens were ran-

domly sampled. A total of 450 field samples of chub

mackerel were used for otolith microstructure analysis.

After measuring FL and wet BW, otoliths were removed

from these samples at a laboratory, and the increment count

was examined using the sagittal and frontal plane method.

Mann–Whitney U test was conducted to compare FL in

each sampling period of both years.

Hatch date and growth analyses

The number of growth increments in individual specimens

in the frontal plane of the otolith were counted and mea-

sured. Daily age of individuals was determined by calcu-

lating the total number of growth increments, plus 2, since

the microstructural increments usually appeared to start

forming 3 days from hatch (see ‘‘Results’’). Hatch date was

calculated by subtracting daily age from sampling date.

The estimated hatch dates were classified into three periods

of a given month: early (days 1–10), middle (days 11–20)

and late (days 21–31).

Prior to the estimate of growth trends of wild fishes,

Gompertz, Logistic and von Bertalanffy equation models

dorsal

ventral

rostrum postrostrumN

short axis

long axis

N

ventral

dorsal

rostrum postrostrum

Fig. 1 Overview of different

plane otolith (sagitta) of chub

mackerel. Upper sagittal plane

of right otolith from the distal

side. Lower frontal plane of left

otolith polished from dorsal

side. Dotted arrows indicate the

direction of increment counting.

N nucleus of otolith

Fish Sci

123

fitted to the observed FL at the age were compared using

Akaike’s Information Criterion (AIC) to select the best

model in this study. Of the three models, the Gompertz

growth model has the lowest AIC, indicating an appropri-

ate growth trend of specimens collected. This agrees with

the studies on growth of Atlantic mackerel S. scombrus

[21–24]. The Gompertz growth model [25] was expressed

as:

Lt ¼ L1e�e�kðt�t0Þ

where Lt is FL at age t (days from hatch), L? is asymptotic

FL at the end of the first growth year (0-year-class), k is a

growth coefficient, t is age (days from hatch) and t0 is point

of inflection (age of maximum growth). The biological

intercept followed Watanabe (L0 = 3.0) [1]. The parame-

ters were estimated by non-linear least-squares fitting using

MS Excel Solver (Microsoft, Redmond, WA, USA). A

measure of goodness of fit was provided by calculating a

coefficient of determination (r2) [26].

Results

Otolith microstructure

At the end of the experiment, specimens (n = 9) at age of

89 days were identified as young stage, and the mean

(±SD) FL and BW were 139.2 ± 9.7 mm and

28.7 ± 6.8 g, respectively. The otoliths of the specimens

showed a rectangular shape with a wide, postrostrum-like

wedge. Clear-and-dense and dark-and-wide increments

were alternately observed from the nucleus to the edge of

the otolith in the frontal plane, together with AP (Fig. 2a).

Increments on the secondary growth layer outside the AP

showed broad width and an irregular growth axis, with

some vague rings (Fig. 2a). Three distinct ALC lumines-

cent checks were clearly observed in the frontal plane

(Fig. 2b). The otolith on the postrostrum part of the sagittal

plane appeared to grow rapidly, but the direction of the

growth axis was more warped than in the frontal plane

(Fig. 2c). Also, this became thickened and curved after the

AP, with a fan-like morphology in the secondary growth

layer, where the vague rings were often observed (Fig. 2c).

Three ALC luminescent checks were observed on the

sagittal plane, but they tended to become obscure in the

outer margin of the otolith (Fig. 2d).

Validation of daily increment of the otolith

The relationship between the cultivated number of incre-

ments of three ALC luminescent checks or the edge of

otolith in different planes of otoliths and age from hatch are

shown in Fig. 3. The regression equations shown as fol-

lows (n = 9):

Y = 1.01x - 2.22 (r2 = 0.99, frontal plane)

Y = 0.97x - 2.23 (r2 = 0.97, long axis of sagittal

plane)

Y = 0.82x - 3.32 (r2 = 0.97, short axis of sagittal

plane).

Of the three regressions, the r2 of the relationship

between the cultivated number of increments on the

frontal plane and age from hatch was the highest. Slopes

of the regression of the relationship counted from the

frontal and long axes of the sagittal planes were about

1.0, indicating that the microstructural increment on both

planes forms daily and can be easily recognized. On the

other hand, the slope of the relationship on the short axis

of the sagittal plane was significantly lower than that of

the other two planes’ regressions (ANCOVA, p \ 0.01).

The estimated intercept of the regressions on the frontal

and long axis of the sagittal planes was 2.2, while that on

the short axis was 3.3. The observed data on the culti-

vated number of increments on the long axis of the sag-

ittal plane on the days of the third ALC luminescent

treatment and at the end of the experiment were more

variable than those on the frontal plane (Fig. 3, CV = 6.1

and 1.5 % at the 3rd ALC, 7.0 and 1.5 % at the end of

the experiment).

Table 1 Source of specimens of juvenile chub mackerel collected in the western North Pacific Ocean in different years of sampling

Year Period Hauls Location n

Latitude Longitude

2007 10–30 May 43 35�02–39�09 N 143�06–162�03 E 151

3 June–1 July 72 34�15–44�32 N 154�57–165�55 E 40

10 June–11 July 83 37�10–45�18 N 142�56–179�06 E 22

13 September–7 October 44 38�58–46�00 N 141�48–165�00 E 58

2009 8–26 May 49 35�07–39�19 N 142�58–160�03 E 50

2 June–2 July 76 34�45–45�55 N 150�57–165�56 E 25

9 June–11 July 92 37�29–46�59 N 147�01–175�05 E 41

23 September–17 October 49 37�39–47�50 N 141�58–169�01 E 63

Fish Sci

123

Hatch period and growth of wild fish

The mean FL and the range in hatch period of specimens

collected in May, June/July and September/October in

2007 and 2009 are shown in Table 2. In May and June/

July, the FL in 2009 was significantly larger than that in

2007 (U test, p \ 0.01). In September/October there was

no significant difference in FL of specimens between the

two sampling years (U test, p = 0.34). The estimated hatch

period ranged from February to June in the two sampling

years. The specimens hatched in April were found

throughout the sampling periods in both years.

Specimens were 22.0–246.0 mm FL and 24–193 days

old in 2007, and 37.8–248.9 mm FL and 31–211 days old

in 2009. The Gompertz growth curve was computed with

length at age (Fig. 4). There were significant differences in

the parameters of the Gompertz growth model between

specimens in 2007 and 2009 (F test, p \ 0.05; Table 3).

This indicated that juveniles in 2009 appeared to grow

faster than those in 2007 until about age 90 days, but

thereafter the 2009 year-class of specimens grew more

slowly (Fig. 4).

Fig. 2 Otolith (sagitta) of reared chub mackerel (young stage,

89 days after hatch). a Postrostrum side of otolith in frontal plane.

b Postrostrum side of otolith in frontal plane under reflected UV

lighting. c Postrostrum side of otolith in sagittal plane. d Postrostrum

side of otolith in sagittal plane under reflected UV lighting. White

arrows indicate ALC luminescent checks. Black arrow indicates

accessory primordia (AP). N nucleus of otolith. Scale bar shows

200 lm

10

20

30

40

50

60

70

80

90

20 40 60 80

10

20

30

40

50

60

70

80

90

20 40 60 80

10

20

30

40

50

60

70

80

90

20 40 60 80 100

Num

ber

of in

crem

ents

from

nuc

leus

Days after hatching

Frontal planen = 9

Long axis of sagittal planen = 9

Short axis of sagittal planen = 9

Fig. 3 Relationship between days after hatching and the number of

increments from nucleus to three ALC luminescent checks (28, 48,

and 68 days) or the edge (89 days) in different planes of otolith. Plots

and bars represent average and standard deviation, respectively.

n number of fish examined

Fish Sci

123

Discussion

The morphometric characteristics of juvenile chub mack-

erel otoliths were similar to those of the Atlantic mackerel

[16, 17, 21], as found in the previous study [15]. However,

there were some differences in the patterns of daily-formed

increments in different planes of the otolith and the timing

of onset of increment formation. In Atlantic mackerel, the

validation of daily-formed increments in the short axis of

the sagittal plane of juvenile otoliths was carried out using

known-age fishes in captive condition and recaptured

specimens marked with calsein, fluorescein complex [16,

17]. D’Amours et al. [17], however, suggested that the

counts of growth rings on the short axis of the otolith may

have the potential to underestimate the age of the fish.

Since the rings at the outer margin of the short axes of the

otolith tend to become indiscernible as the fish grows, age

estimation of Atlantic mackerel using microstructural

increments of the otolith can only be applied to specimens

B 40 days from hatch [27]. In this study, the number of

increments in the short axis of the sagittal plane at the time

of ALC treatments was significantly lower than in the

frontal plane and in the long axis of the sagittal plane. Of

the two planes, the increments in the frontal plane were

more accurate and discernible than those in the long axis of

the sagittal plane, although the increment in both planes

appeared to form daily over about 90 days from hatch.

Additionally, in fishes at age[90 days, the microstructural

increment in the outer margin of frontal plane also forms

daily and can be recognized as found in otoliths of speci-

mens with ALC markings. This suggests that there would

not be a serious bias in the increment count after 90 days

from hatch. From these observations and assumptions, a

maximum total of 211 increments in the frontal plane of

the otolith were able to be successfully counted using a

specimen collected in the western North Pacific Ocean.

The timing of the first increment of chub mackerel

otolith collected around the coastal waters off southern

Korea [15] matched the evidence found in Atlantic mack-

erel, indicating that the first ring in the short axis of the

sagittal plane of the otolith forms on the day of hatching

[16, 17]. Our findings on the relationship between number

of increments in the frontal plane of otolith and fish age,

however, suggest that the first ring of chub mackerel could

usually deposit 3 days from hatch. The first increment may

also have a different physiological basis among fish spe-

cies, and may be formed in association with a particular

Table 2 Mean (±SD) fork length (FL, mm) and estimated hatch period of specimens collected during the three periods in 2007 and 2009

Sampling

year

May June–July September–October

n FL Hatch period n FL Hatch period n FL Hatch period

2007 151 38.2 ± 7.0 Late March–late

April

62 104.1 ± 22.0 Late February–late

April

58 205.3 ± 20.0 Late March–early

June

2009 50 68.6 ± 13.1* Late March–mid

April

66 125.3 ± 28.9* Mid March–early

May

63 203.7 ± 20.3 Mid March–late

May

Results of U test are shown; values with * differ significantly from each other (p \ 0.05)

0

50

100

150

200

250

0 50 100 150 200 250

May

Jun-Jul

Sep-Oct

0

50

100

150

200

250

0 50 100 150 200 250

May

Jun-Jul

Sep-Oct

Days after hatching

Fo

rk le

ng

th (m

m)

For

k le

ngth

(mm

)

2007n = 271

2009n = 179

Fig. 4 Gompertz growth curve (solid line) fitted to length-at-age data

of chub mackerel collected from the western North Pacific Ocean in

2007 and 2009. n number of fish examined

Table 3 Results of parameters of Gompertz growth curves for

juvenile chub mackerel collected from the western North Pacific in

2007 and 2009

Year n Parameter r2

L? k

2007 271 245.6 0.023 0.979

2009 179 208.9 0.030 0.932

Biological intercept (L0 = 3.0) follows Watanabe [1]

Fish Sci

123

developmental stage [28]. For example, in Clupea haren-

gus, the first prominent increment of the otolith was formed

well after hatching and towards the end of the yolk-sac

stage [13]. In our experiment, the yolk-sac absorption and

mouth opening of chub mackerel were found about 2 days

from hatch, and first feeding was observed at age 3 and

4 days, as found in a previous study of captive fish [1].

Although the cause of the timing of onset of increment

formation on chub mackerel otolith needs to be clarified,

the first increment can be used as the reference point for

age estimation of this species during the early life stage.

The estimated hatch period of wild juveniles ranged

from February to June in 2007 and 2009. This is consistent

with the spawning period of the Pacific stock of chub

mackerel [1, 29]. In 2007 and 2009, the April-hatched

specimens were found throughout the sampling periods,

although the range of hatch period differed between sam-

pling periods. Watanabe [29] showed that a relatively

higher abundance of chub mackerel eggs collected in the

spawning grounds has been found between May and June

in recent years. Further research of the relationship

between the abundances of eggs and surviving cohort in

these waters needs to clarify the mechanism of recruitment

of this species.

The growth pattern of specimens differed significantly

between the two year classes. The specimens in 2009 grew

faster than those in 2007 until about 90 days from hatch.

This is likely to reflect a difference in FL of specimens in

May and June/July between the two sampling years,

although the ranges of hatch periods were almost identical.

In chub mackerel, the effect of temperature on growth was

evident, with higher temperature resulting in acceleration

of growth rate of larvae and early juveniles under captive

condition [30, 31]. On the other hand, Watanabe and Yatsu

[9] hypothesized that improved feeding conditions may

result in acceleration of juvenile mackerel growth. Thus the

temperature and prey availability that larvae and juveniles

have experienced could affect their growth rate during the

early life stage, although the cause of variation in growth

pattern between specimens in 2007 and 2009 remains

unknown.

In conclusion, our findings showed for the first time that

the daily-formed increments in the frontal plane of the

otolith of chub mackerel were more suitable for estimating

the age of juveniles than those in the short and long axes of

the sagittal planes. The first increment in the frontal plane

of the otolith was usually deposited 3 days from hatch.

These findings led us to estimate the hatch period and

growth pattern of wild juveniles collected in the western

North Pacific Ocean. The range of the estimated hatch

period of specimens was consistent with the previously

reported spawning period of chub mackerel in these waters

[1, 29], but specimens hatched in April were found

throughout the sampling periods in 2007 and 2009. Also,

there was a significant difference in growth pattern of

specimens between the two year classes. Recent field sur-

veys indicate a positive relationship between the mean FL

of juveniles collected in the Kuroshio-Oyashio transition

area and the abundance of recruits in a given year class [8].

Kawabata et al. [8] have suggested that this may be

attributable to variations in the hatch date and growth rates

during larval and early juvenile stages among the year-

classes. Our findings could assist in the proper assessment

of their life history traits to clarify the mechanism of

recruitment dynamics of the Pacific stock of chub

mackerel.

Acknowledgments We thank the staff and students of the Fishery

Research Laboratory and the Laboratory of Marine Biology at Kyu-

shu University for their support in rearing and measuring the speci-

mens. We are grateful to Drs. K. Mori and N. Yamashita of the

Hokkaido National Fisheries Research Institute, Fisheries Research

Agency of Japan (FRA); Drs. Y. Ueno and S. Honda of the National

Research Institute of Fisheries Science, FRA; and Drs. S. Suyama and

M. Nakagami of the Hachinohe Station, Tohoku National Fisheries

Research Institute, FRA, for sample collection; and to the captain,

officers and crews of the training vessels Hokuho-Maru and Omi-

Maru for helping with collection and measurement. We also thank Dr.

T. Akamine for critical comments on the statistical analysis. This

research was funded by a sub-project on studies on the prediction and

application of fish species alternation (SUPRFISH), financed by the

Agriculture, Forestry and Fisheries Research Council of Japan as part

of the Population Outbreak of Marine Life (POMAL) Project, and

financially supported by the Fisheries Agency of Japan. The Fisheries

Agency is not responsible for the content of this paper.

References

1. Watanabe T (1970) Morphology and ecology of early stages of

life in Japanese common mackerel, Scomber japonicus HOU-

TTUYN, with special reference to fluctuation of population. Bull

Tokai Reg Fish Res Lab 62:1–283 (in Japanese with English

abstract)

2. Usami S (1973) Ecological studies of life pattern of the Japanese

mackerel, Scomber japonicus HOUTTUYN, on the adult of the

Pacific sub-population. Bull Tokai Reg Fish Res Lab 76:71–178

(in Japanese with English abstract)

3. Murayama T, Mitani I, Aoki I (1995) Estimation of the spawning

period of the Pacific mackerel Scomber japonicus based on the

changes in gonad index and the ovarian histology. Bull Jpn Soc

Fish Oceanogr 59:11–17 (in Japanese with English abstract)

4. Watanabe C, Hanai T, Meguro K, Ogino R, Kubota Y, Kimura R

(1999) Spawning biomass estimated of chub mackerel Scomber

japonicus of Pacific subpopulation off central Japan by a daily

egg production method. Nippon Suisan Gakkaishi 65:695–702 (in

Japanese with English abstract)

5. Odate K (1994) Zooplankton biomass and its long-term variation

in the western north Pacific ocean, Tohoku sea area, Japan. Bull

Tohoku Natl Fish Res Inst 56:115–173 (in Japanese with English

abstract)

6. Kawasaki T (1966) Structure of the Pacific population of the

mackerel. Bull Tokai Reg Fish Res Lab 47:1–34 (in Japanese

with English abstract)

Fish Sci

123

7. Watanabe C, Nishida H (2002) Development of assessment

technique for pelagic fish stocks: applications of daily egg pro-

duction method and pelagic trawl in the northwestern Pacific

ocean. Fish Sci 68:97–100

8. Kawabata A, Watanabe C, Nishida H, Honda S (2012) Stock

assessment and evaluation for the Pacific stock of chub mackerel

(fiscal year 2011). In: Marine fisheries stock assessment and

evaluation for Japanese waters (fiscal year 2011/2012). Fisheries

Agency and Fisheries Research Agency of Japan, Tokyo,

pp 151–186 (in Japanese)

9. Watanabe C, Yatsu A (2004) Effect of density-dependence and

sea surface temperature on interannual variation in length-at-age

of chub mackerel (Scomber japonicus) in the Kuroshio-Oyashio

area during 1970–1997. Fish Bull 102:196–206

10. Campana SE, Neilson JD (1985) Microstructure of fish otoliths.

Can J Aquat Sci 42:1014–1032

11. Campana SE (2005) Otolith science entering the 21st century.

Mar Freshw Res 56:485–495

12. Ma T, Miller MJ, Shinoda A, Minagawa G, Aoyama J, Tsu-

kamoto K (2005) Age and growth of Saurenchelys (Nettastom-

atidae) and Dysomma (Synaphobranchidae) leptocephali in the

East China Sea. J Fish Biol 67:1619–1630

13. Geffen AJ (1982) Otolith ring deposition in relation to growth

rate in herring (Clupea harengus) and turbot (Scophthalmus

maximus) larvae. Mar Biol 71:317–326

14. Morales-Nin B (1992) Determination of growth in bony fishes

from otolith microstructure. FAO Fish Tech Paper 322:51

15. Hwang S, Lee TW (2005) Spawning dates and early growth of

chub mackerel Scomber japonicus as indicated by otolith

microstructure of juveniles in the inshore nursery ground. Fish

Sci 71:1185–1187

16. Takahashi M, Takagi K, Kawabata A, Watanabe C, Nishida H,

Yamashita N, Mori K, Suyama T, Nakagami M, Ueno Y, Saito M

(2010) Estimated hatching season of the Pacific stock of chub

mackerel Scomber japonicas and spotted mackerel S. austral-

asicus in 2007. Fish Biol Oceanogr Kuroshio 11:49–54 (in

Japanese)

17. D’Amours D, Landry JG, Lambert TC (1990) Growth of juvenile

(0-group) Atlantic mackerel (Scomber scombrus) in the gulf of St.

Lawrence. Can J Fish Aquat Sci 47:2212–2218

18. Watanabe C, Kobayashi K, Kawabata A, Nashida K (2002) Age

and growth of chub mackerel and spotted mackerel. Kaiyo Mon

34(4):261–265 (in Japanese)

19. Shiraishi T, Ohta K, Yamaguchi A, Yoda M, Chuda H, Ma-

tsuyama M (2005) Reproductive parameters of the chub mackerel

Scomber japonicus estimated from human chorionic gonadotro-

pin-induced final oocyte maturation and ovulation in captivity.

Fish Sci 71:531–542

20. Tsukamoto K (1988) Otolith tagging of Ayu embryo with fluo-

rescent substances. Nippon Suisan Gakkaishi 54:1289–1295

21. Simard P, Castonguay M, D’Amours D, Magnan P (1992)

Growth comparison between juvenile Atlantic mackerel

(Scomber scombrus) from the two spawning groups of the

Northwest Atlantic. Can J Fish Aquat Sci 49:2242–2248

22. Kendall AW Jr, Gordon D (1981) Growth rate of Atlantic

mackerel (Scomber scombrus) larvae in the middle Atlantic

Bight. Rapp P v Reun Cons Int Explor Mer 178:337–341

23. Ware DM, Lambert TC (1985) Early life history of Atlantic

mackerel (Scomber scombrus) in the southern Gulf of St. Law-

rence. Can J Fish Aquat Sci 42:577–592

24. Gluyas-Millan MG, Castonguay M, Quinonez-Velazquez CQ

(1998) Growth of juvenile Pacific mackerel, Scomber japonicus,

in the Gulf of California. Sci Mar 62:225–231

25. Ricker WE (1973) Growth rates and models. In: Hoar WS et al

(eds) Fish physiology, vol. 8. Acadmic Press, New York,

pp 677–743

26. Sokal RR, Rohlf FJ (1981) Biometry: the principles and practice

of statistics in biology research, 2nd edn. WH Freeman and Co.,

New York

27. Robert D, Castonruay M, Fortier L (2007) Early growth and

recruitment in Atlantic mackerel Scomber scombrus: discrimi-

nating the effects of fast growth and selection for fast growth.

Mar Ecol Prog Ser 337:209–219

28. Wright PJ, Panfili P, Morales-Nin B, Geffen AJ (2002) Types of

calcified structures. In: Panfili J et al (eds) Manual of fish scle-

rochronology. IRD Editions, Paris, pp 29–88

29. Watanabe C (2010) Change in the reproductive traits of the

Pacific stock of chub mackerel Scomber japonicus and their

effects on the population dynamics. Bull Jap Soc Oceanogr

74:46–50 (in Japanese with English abstract)

30. Hunter JR, Kimbrell CA (1980) Early life history of Pacific

mackerel, Scomber japonicus. Fish Bull 78:89–101

31. Murata O, Yamamoto S, Ishibashi R, Oka Y, Yoneshima H, Kato

K, Miyashita S, Kumai H (2005) Egg development and growth of

larval and juvenile cultured chub mackerel Scomber japonicus

(Perciformes: Scombridae) in a captive spawning experiment.

Aquacult Sci 53:319–324

Fish Sci

123