Fish Sci (2009) 75:1177–1188
DOI 10.1007/s12562-009-0147-4
ORIGINAL ARTICLE
Effects of temperature, food availability, and body size on daily
growth rate of Japanese anchovy Engraulis japonicus larvae
in Hiuchi-nada
Hiromu Zenitani Æ Naoaki Kono Æ Youichi Tsukamoto Æ
Reiji Masuda
Received: 16 January 2009 / Accepted: 30 June 2009 / Published online: 31 July 2009
Ó The Japanese Society of Fisheries Science 2009
Abstract With data sampled from 2003 to 2006, this
study presents the effects of temperature, food availability
(C), and body size on the somatic growth rate g^
(mm day-1) and on the size-specific growth rates G^
(day-1) of larval Japanese anchovy Engraulis japonicus
caught in Hiuchi-nada, Seto Inland Sea, Japan, a semi-
enclosed narrow sea. C was calculated using an individual-
based model, which is an encounter model between cope-
pods and anchovy where the anchovy resulted in a suc-
cessful capture of the copepod. g^ decreased with increasing
anchovy length, but increased with increasing C. No sig-
nificant relationship was found between g^ and temperature.
G^ decreased with increasing temperature, but anchovy
weight, on the other hand, increased with increasing C. In
the literature, the mechanism of growth determination for
larvae of pelagic fish species is considered to be primarily
determined by sea temperature and secondarily by food
availability. However, g^ and G^ were found to be dependent
on C rather than temperature. G^ was dependent on anchovy
weight rather than C and temperature. For forecasting the
number of days required for development from an arbitrary
pre-recruitment size to the recruitment size, we address not
only temperature but also food availability and the size
H. Zenitani (&)
N. Kono
National Research Institute of Fisheries and Environment
of Inland Sea, Fisheries Research Agency, Hastukaichi,
Hiroshima 739-0452, Japan
e-mail: zenitani@affrc.go.jp
Y. Tsukamoto
Seikai National Fisheries Research Institute, Fisheries Research
Agency, Nagasaki, Nagasaki 851-2213, Japan
R. Masuda
Field Science Education and Research Center, Kyoto University,
Maizuru, Kyoto 625-0086, Japan
Biology
effect when considering the mechanism of growth deter-
mination for larvae.
Keywords Engraulis japonicus
Japanese anchovy
larvae
Otolith growth analysis
Seto Inland Sea
Introduction
The Seto Inland Sea is well known for its high fishery
production and is one of the most productive areas of
enclosed or semi-enclosed waters in the world: Seto Inland
Sea 21 t km-2 yr-1; Chesapeake Bay 7 t km-2 yr-1;
Baltic Sea 2 t km-2 yr-1; North Sea 6 t km-2 yr-1;
Mediterranean sea 1 t km-2 yr-1 [1]. The Japanese
anchovy Engraulis japonicus is an important commercial
species in the Seto Inland Sea (2006 annual catch was
60 9 103 t, accounting for 36% of the total fish produc-
tion) [2]. Hiuchi-nada is located in the central part of the
Seto Inland Sea and is a major spawning and fishing
ground of Japanese anchovy (2005 annual catch in Hiuchi-
nada was 15 9 103 t, accounting for 27% of that in the
Seto Inland Sea) [3]. In this area, forecasting the recruit-
ment populations of shirasu (larval anchovy in Japanese) to
the fishery stock is required for efficient exploitation [4].
Recruitment forecasting, however, has generally not been
successful [5] because it is difficult to forecast the survival
rate (or mortality rate) from the pre-recruitment stage to the
recruitment stage.
Hiuchi-nada, located between Kurushima strait and Bi-
san strait, has a size of about 50 9 30 km and an average
depth of about 20 m. The water exchange between the bay
and straits in the summer is suggested to be important to
the density structure and nutrient supply in the bay [6, 7].
Water in Hiuchi-nada enters the Kurushima strait through
123
1178
the surface layer and moves into the Bisan strait through
the bottom layer, which can be considered as a compen-
satory effect for the intrusion of water from the two straits
[8]. There is a clockwise circular residual current in the
western part of Hiuchi-nada, whereas a counterclockwise
circular residual current occurs in the eastern part of Hiu-
chi-nada [9]. Hiuchi-nada could be regarded as a natural
test tank for larval anchovy growth and survival because of
its largely enclosed condition, as anchovy eggs and larvae
become entrained in the circular residual currents.
Mortality and growth rates of marine fishes are strongly
coupled during early life. Rapid growth reduces the stage-
specific mortality rate to a shorter time frame and increases
the survival potential [10]. In Zenitani et al. [4], the authors
attempted to estimate the survival rates of larval cohorts [3–
15 mm in standard length (SL)] of the Japanese anchovy
population in Hiuchi-nada [4] and examined the relationship
with their food availability. The estimated daily survival
rates increased with the increase in the mean concentration
of small copepod nauplii (less than 100 lm in body length)
sampled at 10 m depth. It might be possible to provide a
framework for forecasting larval abundance immediately
prior to recruitment size (10–15 mm SL) based on larval
abundance of the monitored size (3–8 mm SL) and the
survival rate which is estimated from the concentration of
small nauplii. Studies on the mechanisms determining
growth rates of larval Japanese anchovy in Hiuchi-nada
have not advanced although studies on growth are clearly
essential to allow for accurate recruitment forecasting.
Environmental factors such as sea temperature and food
availability have been concluded to determine early growth
rates [5]. Significant research effort has gradually clarified
the growth–environment relationships of pelagic fish spe-
cies in various regions and has focused on two major
factors, temperature and food availability [11–14]. How-
ever, growth rate is affected by not only exogenous factors
(sea temperature and food availability) but endogenous
factors (genetics, maternal contribution, and the body size
in relation to the fish’s previous growth history) [12, 15].
This manuscript presents the effects of temperature, food
availability, and body size on the daily growth rate of larval
Japanese anchovy in Hiuchi-nada.
Materials and methods
Oceanic survey
From spring to early summer, in 2003–2006, a total of 19
daytime cruises of the R.V. Shirafuji maru, National
Research Institute of Fisheries and Environment of Inland
Sea, were conducted to sample plankton at 13 stations over
4-day survey periods (Fig. 1, Table 1). At each station, a
123
Fish Sci (2009) 75:1177–1188
44˚N
39˚N
Seto Inland Sea
Japan
34˚N
Pacific Ocean
29˚N
128˚E 133˚E 138˚E 143˚E
Hiuchi - nada
Bisan strait
34º15’N
Kurushima
strait Kanonzi-port
34º00’N
133º0 0’E 13 3 º 30 'E
Fig. 1 Survey stations (filled circles) of plankton sampling in Hiuchi-
nada, Seto Inland Sea, Japan
hydrographic cast was made using a Niel Brown CTD
(Cataumet, MA, USA) in 2003 and a compact CTD (ACL
208-PDK Alec Electronics, Kobe, Japan) in 2004–2006.
Water samples for determining copepod nauplii density
were collected with a 20-l Van Dorn water sampler (Rigo,
Tokyo, Japan) from 10 m depth. Since previous studies in
the Seto Inland Sea [16, 17] have demonstrated that larval
anchovies are distributed mainly in the 5–20 m depth
strata, predominantly at 10 m, we selected 10 m as a rep-
resentative depth.
For copepod nauplii abundance, 1 l of the water sample
was filtered aboard with a cellulose nitrate membrane filter
(Toyo Roshi Kaisha, pore size 5.0 lm, Tokyo, Japan), and
copepod nauplii on the filters were resuspended and pre-
served in 5–10% formalin in a 10-ml test tube. After
nauplii were stained by adding 0.1–0.2 ml of Rose Bengal,
they were enumerated on a counting plate. The body length
was measured for all the nauplii.
Copepods (copepodites and adults) were collected with
a plankton net (mouth diameter 0.45 m, length 1.95 m,
mesh opening 100 lm, fitted with a Rigosha flowmeter;
Rigo), which was pulled vertically from 2 m above the sea
bottom to the surface. After the net was retrieved, the
zooplankton were immediately preserved in 5–10%
formalin-seawater solution. Later the sample was split
into 1/32–1/256 subsamples, from which copepods were
Fish Sci (2009) 75:1177–1188 1179

Table 1 Sampling date, temperature at 10 m depth, copepod nauplii abundance, small (0.25–0.50 mm in prosome length) copepod abundance,
and large (over 0.50 mm in prosome length) copepod abundance in Hiuchi-nada in 2003–2006
Cruise Date Temperature Copepod nauplii Small copepods Large copepods
(°C) Concentration
Concentration Size (mm) (103 individuals m-3) Concentration Size (mm)
(106 individuals m-3) (103 individuals m-3)

1 17–20 April 2003 12.4 (±0.4) 14.8 (±8.5) 0.20 (±0.01) 9.4 (±28.5) 4.2 (±22.7) 0.77 (±0.05)
2 7–10 May 2003 14.9 (±0.8) 48.2 (±27.4) 0.20 (±0.02) 11.4 (±35.8) 2.7 (±14.6) 0.83 (±0.08)
3 21–24 May 2003 16.3 (±0.5) 33.2 (±17.6) 0.19 (±0.03) 12.3 (±37.4) 3.4 (±18.5) 0.87 (±0.10)
4 11–14 June 2003 19.0 (±0.4) 22.8 (±12.9) 0.19 (±0.03) 19.8 (±62.5) 1.6 (±8.8) 0.82 (±0.08)
5 27–30 June 2003 20.8 (±0.8) 25.1 (±13.3) 0.19 (±0.03) 12.2 (±36.9) 2.2 (±12.1) 0.79 (±0.06)
6 22–25 July 2003 22.8 (±0.5) 51.2 (±27.4) 0.19 (±0.03) 16.3 (±49.6) 1.3 (±7.1) 0.75 (±0.02)
7 6–9 May 2004 15.9 (±0.6) 15.5 (±9.4) 0.19 (±0.04) 11.3 (±35.0) 2.9 (±15.8) 0.76 (±0.03)
8 18–21 May 2004 17.5 (±0.6) 23.8 (±12.7) 0.19 (±0.03) 14.7 (±44.8) 2.2 (±12.0) 0.77 (±0.04)
9 6–9 June 2004 19.8 (±0.6) 16.2 (±9.0) 0.19 (±0.03) 4.5 (±13.7) 0.4 (±2.0) 0.77 (±0.04)
10 1–4 July 2004 22.5 (±0.7) 18.9 (±9.8) 0.18 (±0.04) 5.0 (±15.5) 1.1 (±5.9) 0.75 (±0.01)
11 13–16 July 2004 24.3 (±0.9) 52.9 (±17.8) 0.17 (±0.04) 20.9 (±64.2) 2.1 (±11.1) 0.75 (±0.01)
12 18–21 April 2005 12.6 (±0.5) 25.8 (±15.1) 0.18 (±0.04) 10.6 (±32.0) 3.1 (±16.8) 0.81 (±0.06)
13 9–12 May 2005 15.7 (±0.6) 23.0 (±15.1) 0.19 (±0.03) 11.0 (±34.1) 2.4 (±12.9) 0.83 (±0.09)
14 19–22 May 2005 16.7 (±0.5) 34.6 (±20.5) 0.19 (±0.03) 13.3 (±41.4) 2.8 (±15.1) 0.79 (±0.06)
15 6–9 July 2005 18.3 (±0.5) 38.3 (±23.1) 0.19 (±0.04) 20.0 (±61.2) 3.6 (±19.2) 0.78 (±0.06)
16 22–25 July 2005 20.4 (±0.9) 25.1 (±13.3) 0.19 (±0.03) 19.8 (±60.3) 1.9 (±10.1) 0.76 (±0.04)
17 23–26 May 2006 15.6 (±0.6) 15.2 (±10.1) 0.20 (±0.02) 8.1 (±24.5) 2.4 (±12.6) 0.77 (±0.04)
18 13–16 June 2006 18.4 (±0.5) 16.6 (±9.7) 0.19 (±0.02) 10.4 (±31.9) 2.3 (±12.2) 0.77 (±0.04)
19 15–18 July 2006 21.7 (±0.6) 17.3 (±11.9) 0.19 (±0.02) 8.6 (±25.9) 0.8 (±4.6) 0.76 (±0.02)
Values are mean ± SD

enumerated under a stereoscopic microscope. In order to
estimate the length–frequency distribution from cruise i, up
to 100 copepods for each genus were selected at random
from each sample and their prosome length was measured
to the nearest 0.1 mm.
We classified the copepods into three stages
Wc(i, j, k) is the carbon weight of taxonomic group k of
stage j of copepod from cruise i (mg C individual-1). The
taxonomic groups were k = 1: Acartia, k = 2: Calanus,
k = 3: Centropages, k = 4: Microsetella, k = 5: Oithona,
k = 6: Paracalanus, and k = 7: others (Corycaeus, On-

8
<1 nauplii stage ð\0:25 mm in body lengthÞ
j¼ 2 small size stage ð0:25  0:50 mm in prosome length; mode 0:37 mmÞ ð1Þ
:
3 large size stage ð [ 0:50 mm in prosome lengthÞ

We calculated the mean body length [Lc(i, 1)] for a caea, etc.). a(k) and b(k) are parameters of the k taxonomic
copepod nauplii from cruise i, and then the carbon content group (Table 2).
[Wc(i, 1); mgC individual-1] was calculated from the mean We set the mean length in stage 2, Lc(i, 2, k), at 0.38 mm,
body length [18]: and calculated the mean length in stage 3, Lc(i, 3), and mean
weight in stages 2 and 3, Wc(i, j), by the following equation
Wc ði; 1Þ ¼ 1:51  1014  fLc ði; 1Þ  103 g2:94 ð2Þ P7
Lc ði; j; kÞ  Ac ði; j; kÞ
Prosome length of k taxonomic group of stage j of Lc ði; 3Þ ¼ k¼1 P7 ð4Þ
copepod from cruise i [Lc(i, j, k); mm] was converted to k¼1 Ac ði; j; kÞ
P7
body carbon weight using the length–weight regression Wc ði; j; kÞ  Ac ði; j; kÞ
equation [19–21]. Wc ði; jÞ ¼ k¼1 P7 ðj ¼ 2; 3Þ ð5Þ
k¼1 Ac ði; j; kÞ
Wc ði; j; kÞ ¼ 10aðkÞ  103
Ac(i, j, k) is the mean abundance of taxonomic group k of
 ðLc ði; j; kÞ  103 ÞbðkÞ ðj ¼ 2; 3Þ ð3Þ stage j of copepod from cruise i (103 individuals m-3).

123
1180
Table 2 Parameters of regression equations of carbon weight against
length for copepods collected in the Seto Inland Sea
k Taxonomic groups a(k) b(k)
1 Acartia 8.51 3.08
2 Calanus 7.00 2.64
3 Centropages 8.19 2.97
4 Microsetella 5.58 1.95
5 Oithona 3.90 1.13
6 Paracalanus 8.45 3.13
7 Others (Corycaeus, Oncaea, etc.) 8.37 3.07
Otolith growth analysis
The metamorphosing stage of Japanese anchovy, based
on the period of guanine deposition on the peritoneal
surface in relation to guanine deposition on the trunk
surface, occurs from 31 to 37 mm SL, while the juvenile
stage occurs starting from ca. 40 mm SL [22]. Based on
previous studies of anchovy development stages, we
assessed the growth rate in the larval stage (5.6–
40.0 mm SL).
The size-specific growth rate of an individual anchovy l
is determined by otolith growth analysis as follows:
Anchovy were sampled from commercial catches (seine
net fishery) at Kanonzi-port in Hiuchi-nada (Fig. 1) on 18
July 2003, 6 July and 6 August 2004, 27 June 2005, and 24
June 2006. A subsample of ca. 50–100 anchovy larvae and
juveniles was taken randomly from each commercial catch
and preserved in 99% ethanol. Each fish was measured for
SL to the nearest 0.1 mm with digital calipers. Sagittal
otoliths of the larvae and early juveniles (18.0–65.0 mm)
were dissected out, cleaned under a binocular dissecting
microscope, and mounted on a glass slide with epoxy resin.
The possible effect of SL shrinkage due to ethanol pres-
ervation on SL measurements was ignored [23]. Measure-
ment of otolith increments was conducted along a core–
posterior axis, from the core to the posterior edge, using the
otolith measurement system (Ratoc System Engineering,
Tokyo, Japan) on a light microscope at 100–2009
magnification.
When the relation between otolith radius and fish size is
predictable, growth rates can be calculated based on otolith
increment widths [11, 24–26]. According to previous
experimental studies on Japanese anchovy, the daily
growth increment is deposited at the start of external
feeding, 3–4 days after hatching [27]. SL at completion of
yolk absorption is 5.6 mm [28]. Daily age of each anchovy
was calculated, therefore, as the number of rings plus 3. SL
at each daily age was back-calculated by the biological
123
Fish Sci (2009) 75:1177–1188
intercept method [29, 30], with SL at the first deposition of
the daily growth increment fixed at 5.6 mm as the bio-
logical intercept at the individual level. The relationship
between SL and otolith radius at sampling day of indi-
vidual l, ds(l), was examined for anchovy collected in
Hiuchi-nada. Plot of SL against otolith radius for both the
larvae and juveniles was expressed by an allometric rela-
tionship (see ‘‘Results’’).
We assumed that the relationship of otolith radius
[OR(l,m)] and SL [La(l,m)] of individual anchovy l of the
mth ring formation can be expressed by an allometric
formula. Hence, La(l,m) of each anchovy was back-calcu-
lated by substituting OR(l,m) with La(l, m) using the allo-
metric relationship
La ðl; mÞ ¼ cðlÞ  ORðl; mÞdðlÞ ð6Þ
c(l) and d(l) are parameters determined for each anchovy
by solving the two equations,
La ðl; 1Þ ¼ c ðlÞ  ORðl; 1ÞdðlÞ ð7Þ
and
La ðl; mmax ðlÞÞ ¼ cðlÞ  ORðl; mmax ðlÞÞdðlÞ ð8Þ
La(l, 1), 5.6 mm, OR(l, 1), La(l, mmax(l)), and OR(l,
mmax(l)) are SL at the first daily growth increment depo-
sition, measured radius of the first daily ring, SL at sam-
pling day ds(l), and measured radius at sampling day s(l),
respectively. mmax(l) is the maximum number of rings of
individual anchovy l.
An allometric formula was fitted to the otolith radius–
SL relationship, but a growth effect may occur with
slower-growing larvae tending to have larger otoliths
than faster-growing conspecifics at the same somatic size
[31]. The growth effect could lead to the possibility of
biases in the back-calculation processes based on the
otolith radius–SL relationship. The biological intercept
method and its modifications, using an allometric radius–
SL relationship at the individual level, would be useful
to reduce biases, although further consideration of the
growth effect in the back-calculations may add to the
precision in growth analysis in future studies.
The relationship between body weight [Wa(l, m); mg
C individual-1] and SL of Japanese anchovy larvae [19,
32] has been found to be
Wa ðl; mÞ ¼ 2:045  104  La ðl; mÞ3:38532  0:43 ð9Þ
The somatic growth rate, g^ ðl; mði; lÞÞ (mm day-1),
and size-specific growth rates, G^ ðl; mði; lÞÞ (day-1), for
individual anchovy l at m(i, l)th ring formation were
estimated from the change in the back-calculated length
and weight for individual anchovy l from cruise i,
Fish Sci (2009) 75:1177–1188
La ðl; mði; lÞ þ DtÞ  La ðl; m ði; lÞÞ
g^ ðl; mði; lÞÞ ¼ ð10Þ
Dt
Wa ðl; mði; lÞ þ DtÞ  Wa ðl; mði; lÞÞ
G^ ðl; mði; lÞÞ ¼
Dt
 Wa ðl; mði; lÞÞ1 ð11Þ
m ði; lÞ ¼ mmax ðlÞ  ds ðlÞ þ dc ðiÞ ð12Þ
dc(i) is the first day of cruise i. The simplest measure of an
individual’s growth over a period of time, Dt, is the dif-
ference in length, i.e., the absolute somatic growth rate.
This provides a first-order estimate of growth and can be
used to compare with previous studies’ somatic growth
rates. In our study, Dt was the period of time for a cruise,
Dt = 3 days. Based on the importance of current body size,
there are obvious advantages to expressing the absolute
somatic growth rate in proportion to the growth already
achieved as the proportional growth rate, i.e., the size-
specific growth rate. Calculation of specific growth
improves our ability to compare growth among fish in
different stages [15].
Food availability
The size-specific rate of maximum food consumption
(food availability) was determined with an individual-
based model for each individual anchovy of a given size
at a temperature and the abundance of prey, as follows.
Copepods are the main prey items for the anchovy lar-
vae. At first feeding stage, larval anchovy eat mainly
naupliar copepods, then with increasing size, the larvae
eat copepodites and adult copepods [33, 34]. The max-
imum rate of feeding of individual anchovy l on cope-
pods at m(i, l)th ring formation, Cc[l, m(i, l)], was
calculated as
X
3
Cc ðl; mði; lÞÞ ¼ ðEm ði; j; lÞ  Wc ði; jÞÞ ð13Þ
j¼1
Em(i, j, l) was the average number of encounters between
stage j copepods and individual anchovy l that resulted in
the successful capture of stage j copepods during cruise i.
The mean number of encounters, E(i,j,l), between stage j
copepods and individual anchovy l in cruise i was based on
the Gerritsen and Strickler [35] model for randomly mov-
ing organisms in a 3-D space such that:
8

< p  DE  CE  Ac ði; jÞ  RT ði; j; lÞ2  3Va ði; lÞ þVc ðjÞ
3Va ði; lÞ
Eði; j; lÞ ¼
2
: p  DE  CE  Ac ði; jÞ  RT ði; j; lÞ2  3Vc ðjÞ þVa ði;lÞ
3Vc ðjÞ
1181
DE is the proportion of daylight hours in a day (12 h/24 h),
CE is a conversion factor (8.64 9 10-4 s day-1), Ac(i, j) is
the abundance of stage j copepods from cruise i
(individuals m-3),
X
7
Ac ði; jÞ ¼ Ac ði; j; kÞ ð15Þ
k¼1
RT(i, j, l) is the total encounter radius (mm). Va(i, l) and
Vc(j) are the swimming speeds of individual anchovy l in
cruise i and stage j copepods (mm s-1), respectively. The
total encounter radius was assumed to be equal to the sum
of the mean encounter radius of stage j, Rc(i, j), and the
mean encounter radius of individual anchovy l, Ra(i, l), in
cruise i, as Bailey and Batty [36] estimated
RT ði; j; lÞ ¼ Rc ði; jÞ þ Ra ði; lÞ ð16Þ
2  Lc ði; jÞ
Rc ði; jÞ ¼ ð17Þ
p2
2  La ðl; mði; lÞÞ
Ra ði; lÞ ¼ ð18Þ
p2
Within the temperature range 13–23°C, the average
swimming speed of anchovy larvae was dependent on
length and temperature [after Hunter [37] and Masuda R
unpubl. data, 2007; a fish was transferred to a glass
container (105–235 mm diameter depending on the size of
fish) covered with a black vinyl sheet and the movement of
the fish was recorded from above for 90 s using a digital
video recorder (DCR-PC100, Sony, Tokyo, Japan). Sound
stimuli were provided by releasing a string-hung metal nut
three times at 10-s intervals. This procedure was repeated
for 10 individuals. Cruise swimming speed was measured
starting 10 s before the sound stimulus by tracing the
movement of the fish on a TV monitor]. The swimming
speed of individual anchovy l in cruise i (Fig. 2) was
calculated as
Va ði; lÞ ¼ La ðl; mði; lÞÞ  ð0:076  T ðiÞ  0:52Þ ð19Þ
T(i) was mean water temperature at 10 m depth in cruise i
in Hiuchi-nada.
The average swimming speed of the copepod Temora
longicornis was 1.5 mm s-1 for nauplii and young co-
pepodid stage (\0.4 mm in body length), about 5 mm s-1
for the female adult stage, and 9 mm s-1 for the male adult
stage [38]. According to Yen [39], Euchaeta rimana has a
2 2

for Va ði; lÞ  Vc ðjÞ
2
 ð14Þ
for Vc ðjÞ [ Va ði; lÞ
123
1182 Fish Sci (2009) 75:1177–1188

Relative swimming speed (SL-1 s-1)

2
Results
y = 0.076x - 0.52
1.5 2
r = 0.60 Mean temperature at 10 m depth ranged from 12.4 to
24.3°C. Mean abundance of copepod nauplii, small cope-
1 pods, and large copepods ranged from 14.8 9 106 to
52.9 9 106, 4.5 9 103 to 20.9 9 103, and 0.4 9 103 to
4.2 9 103 individuals m-3, respectively (Table 1). Mean
0.5
abundance of large copepods decreased with increasing
mean temperature:
0
10 15 20 25 Ac ði; 3Þ ¼ 0:21  TðiÞ þ 6:08
Temperature (°C) ðr 2 ¼ 0:52; n ¼ 19; F test; P\0:001Þ ð25Þ
Fig. 2 Relationship between relative swimming speed of anchovy Mean size of copepod nauplii and large copepods ranged
and temperature. Open circles are Engraulis mordax [29] and filled
circles are Engraulis japonicus (after Masuda R, unpubl. data 2007).
from 0.17 to 0.20 mm in body length and 0.75 to 0.87 mm in
SL Standard length prosome length, respectively. For small copepods, Acartia,
Corycaeus, Microsetella, Oithona, and Paracalanus were
predominant throughout the study periods. For large
typical swimming speed of roughly 7 mm s-1. We assumed copepods, Acartia, Calanus, Corycaeus, and Paracalanus
that the swimming speed in the nauplii, small copepods, and were predominant throughout the study periods (Fig. 3).
large copepods was 1.5, 1.5, and 7 mm s-1, respectively. Mean sizes of both copepod nauplii and large copepods
The number of encounters between stage j copepods decreased with increasing mean temperature. The
and individual anchovy l in cruise i, in which individual relationship between Lc(i, 1) and T(i) and between Lc(i, 3)
anchovy l successfully captured stage j copepods, was and T(i) was expressed as
determined from a binominal distribution, BN(E(i, j, l),
P(i, j, l)), and the mean number of encounters is Lc ði; 1Þ ¼ 0:21  exp ð0:0049  TðiÞÞ
Em ði; j; lÞ ¼ Eði; j; lÞ  P ði; j; lÞ ð20Þ ðr 2 ¼ 0:26; n ¼ 19; F test; P\0:05Þ ð26Þ

P(i, j, l) is the capture success probability of individual Lc ði; 3Þ ¼ 0:88  exp ð0:0064  TðiÞÞ
anchovy l for stage j copepods in cruise i: ðr 2 ¼ 0:28; n ¼ 19; F test; P\0:05Þ ð27Þ

1 for Lmin ði; lÞ  Lc ði; jÞ  Lmax ði; lÞ The age and size of anchovy larvae and juveniles col-
Pði; j; lÞ ¼
0 for Lc ði; jÞ\Lmin ði; lÞ or Lmax ði; lÞ\Lc ði; jÞ lected in 2003, 2004, 2005, and 2006 were in the ranges
ð21Þ 30–71, 56–114, 21–65, and 30–50 days, respectively, and
30–45, 34–65, 18–33, and 25–31 mm SL, respectively
The minimum and maximum length of copepods that (Fig. 4). The plot of La(l, mmax(l)) for SL under 40 mm
anchovy larvae were able to capture, Lmin(i, l) and Lmax(i, against OR[l,mmax(l)] (Fig. 5) showed an allometric
l), was relationship:

0:15 for 5:6 mm  La ðl; mði; lÞÞ\9:0 mm La ðl; mmax ðlÞÞ ¼ 2:23  ORðl; mmax ðlÞÞ0:48
Lmin ði; lÞ ¼
0:20 for 9:0 mm  La ðl; mði; lÞÞ
ðr 2 ¼ 0:83; n ¼ 151; F test; P\0:001Þ ð28Þ
ð22Þ
We carried out the back-calculation of La(l, m(i, l)) for
and data from cruises 3–5 in 2003, 7–11 in 2004, 13–16 in
Lmax ði; lÞ ¼ 0:434  exp ð0:105  La ðl; mði; lÞÞÞ ð23Þ 2005, and 17–18 in 2006 (Table 3).
There was no relationship between g^ ðl; mði; lÞÞ and T(i)
after Fig. 5-1 in Yokota et al. [33] and Fig. 6 in Uotani (Fig. 6a). g^ ðl; mði; lÞÞ increased with increasing C(l,m(i,l))
[40]. (Fig. 6b):
The specific rate of food consumption of individual
anchovy l on copepods at m(i, l)th ring formation, C(l, g^ ðl; mði; lÞÞ ¼ 0:46  C ðl; mði; lÞÞ þ 0:44
ð29Þ
m(i, l)), is defined as a function of the feeding rate on ðr 2 ¼ 0:12; n ¼ 486; F test; P\0:001Þ
copepods,
On the other hand, g^ ðl; mði; lÞÞ decreased with increasing
C ðl; m ði; lÞÞ ¼ Cc ðl; mði; lÞÞ  Wa ðl; mði; lÞÞ1 ð24Þ La(l, m(i, l)) (Fig. 6c)

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Fish Sci (2009) 75:1177–1188 1183

Small surface temperature (SST) but not with food availability for
100 anchovy larvae in the Kuroshio Extension and Kuroshio-
Oyashio transition regions of the western North Pacific
75 [41]. At the same time, larval growth rates in the shirasu
fishing ground in Sagami Bay, central Japan, were shown
50 to be variable under the influences of both SST and food
availability [14]. In Sagami Bay, the growth rate of
25 anchovy larvae was dependent on food availability rather
than temperature. The somatic or size-specific growth rate
of anchovy larvae in Hiuchi-nada was also dependent on
0
1 3 5 7 9 11 13 15 17 19 food availability rather than temperature (Figs. 6, 7).
%

Mechanism of determination of the growth rates in Hiuchi-

Large nada was close to that in coastal regions, such as the
100 shirasu fishing ground in Sagami Bay, where a circular
residual current occurs [42]. At the end of May, the lowest
75 temperature in the surface layer was in Kurushima strait,
the highest temperature in the eastern part of Hiuchi-nada,
50 and an intermediate temperature in the Bisan strait and
northern part of Hiuchi-nada. This distribution pattern was
25 unchanged in June and July [8]. Data variation in tem-
perature at 10 m depth layer was small in each cruise in our
study; the coefficient of variation was 0.02–0.05 (Table 1).
0
1 3 5 7 9 11 13 15 17 19 Data variation in copepod density for each cruise in our
study was 0.34–0.67 for copepod nauplii, 3.02–3.16 for
Cruise No. small copepods, and 5.35–5.56 for large copepods
Others Oithona Centropages (Table 1). High spatial variation in food availability might
Paracalanus Microsetella Calanus cause the phenomenon that the growth rate of anchovy
Oncaea Corycaeus Acartia larvae in Hiuchi-nada was dependent on food availability
rather than temperature.
Fig. 3 Compositions of small (0.25–0.50 mm in prosome length, It is stated that the systematic mechanism of growth
mode 0.37 mm) and large (0.50 mm in prosome length) copepods for determination for larvae of pelagic fish species larvae is
each cruise
primarily determined by sea temperature and secondarily
g^ ðl; mði; lÞÞ ¼ 1:30  La ðl; mði; lÞÞ0:28 by food availability [14]. In the Seto Inland Sea, recruit-
ment of anchovy tends to decrease with increasing tem-
ðr 2 ¼ 0:12; n ¼ 486; F test; P\0:001Þ ð30Þ peratures (16–19°C), even though egg production is at a
^ mði; lÞÞ decreased with increasing T(i) and Wa(l, m(i,
Gðl; high level [43]. The size-specific growth rate of anchovy in
l)) (Fig. 7a, c), but on the other hand, increased with Hiuchi-nada in April–July decreased with increasing tem-
increasing C[l, m(i, l)] (Fig. 7b): perature. In contrast, the growth rate in Kuroshio-Oyashio
transition regions, the East China Sea, and shirasu fishing
G^ ðl; mði; lÞÞ ¼ 267:39  TðiÞÞ2:67 ground in Sagami Bay increased with an increase in tem-
ðr 2 ¼ 0:23; n ¼ 486; F test; P\0:001Þ ð31Þ perature between 14 and 22°C, while copepod size and
abundance decreased with increasing temperature. In the
G^ ðl; mði; lÞÞ ¼ 0:46  C ðl; mði; lÞÞ  0:022 Seto Inland Sea, temperature might affect recruitment
ðr 2 ¼ 0:43; n ¼ 486; F test; P\0:001Þ ð32Þ through the growth rate. Therefore, the mechanism of
growth determination for anchovy in Hiuchi-nada also may
G^ ðl; mði; lÞÞ ¼ 0:15  Wa ðl; mði; lÞÞ0:42
be primarily determined by sea temperature. However, the
ðr 2 ¼ 0:75; n ¼ 486; F test; P\0:001Þ ð33Þ food availability would be a synthetic index for prediction
of anchovy larval growth in Hiuchi-nada because it is
related not only to temperature but also to the abundance of
Discussion copepods, size of anchovy, and relative size of copepods to
size of anchovy.
In a previous study, recent 3-day mean growth rates Measurement width of the ring at the edge of the otolith
directly before capture were positively related with sea using the recent 3-day growth rates was more difficult than

123
1184 Fish Sci (2009) 75:1177–1188

Fig. 4 Frequency distribution 2003

of age and standard length of the 60 60
anchovy for growth analysis in
40 40
2003, 2004, 2005, and 2006
20 20
0 0
0 20 40 60 80 100 120 5 15 25 35 45 55 65

60 60 2004
40 40

20 20
0 0
0 20 40 60 80 100 120 5 15 25 35 45 55 65

%
60 60 2005

40 40

20 20

0 0
0 20 40 60 80 100 120 5 15 25 35 45 55 65

60 60 2006

40 40

20 20

0 0
0 20 40 60 80 100 120 5 15 25 35 45 55 65
Age (days) Standard length (mm)

y = 2.23x
0.48 although our analysis period of otolith growth was
50
2
r = 0.83
restricted to May–July.
We could only collect surviving anchovy larvae but not
Standard length (mm)

40
dead anchovy larvae in field, since the point of no return
30
(PNR: time when starved larvae have lost the capability to
recover after subsequent feeding) is short, between 1 and
20 2 days after the first feeding day under conditions of 20–
25°C [46]. Previous research in Hiuchi-nada has shown the
10 importance of food abundance for survival of larval
anchovy, i.e., massive mortalities of larval anchovy after
0 the first feeding day [4]. The main cause of mortality in
0 200 400 600
marine fish larvae is considered to be predation [47, 48],
µm)
Otolith radius (µ
and the predatory loss is related to larval growth [49–51].
Fig. 5 Relationship between otolith radius and standard length of the Slower-growing larvae remain in the stage vulnerable to
anchovy for growth analysis predators for a longer period of time and have lower sur-
vival rates. Whether the cause of mortality is starvation or
that on the inner side of otolith because of difficulties in predatory loss, the survivors might be derived from faster-
focusing on the ring due to the structure of the otolith [44]. growing cohorts. The mean growth rate of faster-growing
However, our method can reduce the difficulty because we cohorts was larger than that of the origin cohort in the field
measured the width of the otolith ring on the inner side of where the survival rate was low [52], i.e., a positive bias
otolith. The growth trajectory of the main cohorts of occurs in the distribution of the growth rate. This bias
anchovy in Hiuchi-nada in spring [45] could be traced, effect tends to overestimate the growth rate for small

123
Fish Sci (2009) 75:1177–1188 1185

Table 3 Sampling or back-calculation date, back-calculated standard length (SL), somatic growth rate as length increment, and size-specific
growth rate as weight increment per unit of weight for anchovy with SL \ 40 mm in Hiuchi-nada in 2003–2006
Cruise Date Back-calculated Somatic growth rate Size-specific growth rate Sample size (n)
SL (mm) as length increment as weight increment
(mm day-1) per unit of weight (day-1)

3 Back-calculation 21–24 May 2003 12.0 (±2.2) 0.76 (±0.08) 0.27 (±0.05) 5
4 Back-calculation 11–14 June 2003 18.4 (±4.8) 0.67 (±0.17) 0.17 (±0.11) 38
5 Back-calculation 27–30 June 2003 25.1 (±4.9) 0.57 (±0.16) 0.09 (±0.06) 58
Sampling 18 July 2003 58
7 Back-calculation 6–9 May 2004 19.0 (±6.8) 0.60 (±0.15) 0.15 (±0.09) 10
8 Back-calculation 18–21 May 2004 21.1 (±7.1) 0.65 (±0.15) 0.14 (±0.08) 22
9 Back-calculation 6–9 June 2004 22.6 (±9.0) 0.67 (±0.19) 0.15 (±0.11) 54
10 Back-calculation 1–4 July 2004 31.6 (±5.5) 0.58 (±0.16) 0.07 (±0.03) 41
Sampling 6 July 2004 14
11 Back-calculation 13–16 July 2004 35.5 (±4.0) 0.58 (±0.19) 0.06 (±0.03) 29
Sampling 6 August 2004 50
13 Back-calculation 9–12 May 2005 11.8 (±6.3) 0.59 (±0.04) 0.26 (±0.17) 2
14 Back-calculation 19–22 May 2005 12.0 (±3.6) 0.66 (±0.16) 0.27 (±0.15) 18
15 Back-calculation 6–9 July 2005 18.6 (±4.4) 0.55 (±0.15) 0.13 (±0.09) 46
16 Back-calculation 22–25 July 2005 25.4 (±4.4) 0.44 (±0.14) 0.07 (±0.03) 50
Back-calculation 27 July 2005 50
17 Back-calculation 23–26 May 2006 12.6 (±3.2) 0.52 (±0.08) 0.18 (±0.06) 15
18 Back-calculation 13–16 June 2006 22.3 (±1.8) 0.55 (±0.08) 0.09 (±0.02) 98
Sampling 24 June 2006 98
Values are mean ± SD or number

Fig. 6 Relationship between 1.2 (a) 1.2

somatic growth rate and (b)
temperature (a), food
availability for anchovy (b), and
standard length of the anchovy 0.8 0.8
(c)

0.4 0.4
Somatic growth rate (mm day-1)

y = 0.46x + 0.44
2
r = 0.12
0 0
15 20 25 0 0.2 0.4 0.6 0.8 1
Temperature (°C) Food availability (day-1)

1.2 (c)

0.8

0.4

y = 1.30x-0.28
2
r = 0.12
0
0 10 20 30 40 50
Standard length (mm)

123
1186 Fish Sci (2009) 75:1177–1188

Fig. 7 Relationship between -2.67 y = 0.46x - 0.022

size-specific growth rate and 0.8 (a) y = 267.39x 0.8 (b) 2
2
r = 0.23 r = 0.43
temperature (a), food
availability for anchovy (b), and
body weight of the anchovy (c)
0.6 0.6

0.4 0.4

Size specific growth rate (day-1)

0.2 0.2

0 0
15 20 25 0 0.2 0.4 0.6 0.8 1
Temperature (°C) Food availability (day-1)
0.8 (c)

0.6
-0.42
y = 0.15x
2
0.4 r = 0.75

0.2

0
0 10 20 30
Body weight (mgC individual-1)

anchovy larvae, although endogenous factors (related to the
body size or development stage of anchovy) affected the
relationship between size-specific growth rate and body
weight (Eq. 33).
The size-specific growth rate of an individual for non-
reproducing fish is determined as the difference between
the size-specific rate of food consumption and the sum of
size-specific energy output rate, such as metabolism,
egestion, and excretion. Metabolic processes such as res-
piration are dependent upon body weight and ambient
temperature [53]. Elliott [54] demonstrated that waste
losses due to egestion and excretion vary as functions of
the feeding level and temperature. Since the feeding level
is dependent upon body weight and temperature, energy
output rate varies as a function of body weight and tem-
perature. The variations in temperature, abundance of
copepods, size of anchovy, and relative size of copepod to
size of anchovy might change with food availability and
metabolic loss, and subsequently the variation in growth
rate was considered to be induced by their variations. The
size-specific growth rate of anchovy larvae in Hiuchi-nada
was also dependent on body size rather than temperature
and food availability (Fig. 7). Body size was a major factor
for determining early growth rates. For forecasting the
number of days required for development from an arbitrary
pre-recruitment size to the recruitment size, i.e., one factor
for forecasting the recruitment population, we should
address not only temperature and food availability but also
the size effect when considering the mechanism of growth
determination for larvae.
Acknowledgments We thank Mrs. A. Iguchi, Mrs. H. Yoshida, and
Mrs. M. Tani for their kind assistance. We are also indebted to the
captain and crew of the R.V. Shirafuji maru and company executives
and staff of the Mekachi Suisan Ltd. for their assistance with the
sampling. This work was supported in part by Research for Assess-
ment and Prediction of Production Rate in Fishery Ground, from the
Fisheries Agency.
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