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Fish Aquat Sci 18(3), 301-309, 2015
Ontogenetic Development of the Digestive System in Chub
Mackerel Scomber japonicus Larvae and Juveniles
Su-Jin Park1, So-Gwang Lee2 and Woo-Seok Gwak1*
Marine Bio-education and Research Center, Gyeongsang National University, Tongyeong 53064, Korea
Gyongsangnam-do Fisheries Resources Research Institute, Tongyeong 53080, Korea
1
2
Abstract
Chub mackerel, Scomber japonicus, larvae and juveniles were reared from hatching to 35 days after hatching (DAH), and the development of their digestive systems was histologically investigated. The larvae were initially fed on rotifers and Artemia nauplii
starting around 19 DAH, and thereafter on Artemia nauplii, fish eggs, and a formulated feed mixture. The primitive digestive system differentiated at 3 DAH; the digestive tract was distinctively divided into the buccopharyngeal cavity, esophagus, stomach, air
bladder, intestines, and rectum. The gastric gland and pyloric caeca first appeared at 5 and 7 DAH, respectively. The stomach was
divided into cardiac, fundic, and pyloric regions in the preflexion phase. The number of gastric glands and pyloric caeca, as well
as the volume of the gastric blind sac increased markedly, with development continuing into the juvenile stage. The precocious
development of the digestive system during the larval period might be related to the early appearance of piscivory, which is able
to support high growth potential. The organogenesis results obtained for this precocial species represent a useful tool to aid our
understanding of the physiological requirements of larvae and juveniles to ensure optimal welfare and growth under aquaculture
conditions, which will improve current rearing practices of this scombrid species.
Key words: Chub mackerel, Scomber japonicus, Digestive system, Larvae, Juveniles
Introduction
The chub mackerel, Scomber japonicus, has high growth
potential; it has a large head containing a large mouth and big
eyes, there is a posterior shift of the anus with growth, and it
has well-developed preopercular spines (Hunter, 1981). These
morphological traits are indicative of the survival strategy of
scombrid larvae, which includes large prey-fast growth. In addition, its feeding is opportunistic and non-selective, with the
adult diet ranging from copepods and other crustaceans to fish
and squid (FAO, 1983). The precocious digestive system of
scombrid larvae supports their fast growth during their early
life history. In common with marine fishes, the juvenile-type
digestive system is established at the same time as the transformation to the juvenile stage (Tanaka, 1973). In bluefin tuna
larvae, however, differentiation of the gastric glands, followed
by the appearance of pyloric caeca, was observed at the flexion phase, suggesting that the digestive system attained a juvenile-type structure long before metamorphosis (Kaji, 1996;
Miyashita, 1998). In addition, striped bonito (Harada et al.,
1974) and Japanese Spanish mackerel (Fukunaga et al., 1982)
larvae grew to 106 and 90 mm in length, respectively, during
the first 30 days after hatching (DAH). This growth was the
fastest among marine fish larvae hatched from pelagic eggs
and explained the development of the precocious digestive
system with a well-developed gastric blind sac (Tanaka et al.,
1996; Kaji, 2002).
The chub mackerel is a candidate for aquaculture develop-
Received 16 June 2014; Revised 13 May 2015
Accepted 28 June 2015
© 2015 The Korean Society of Fisheries and Aquatic Science
This is an Open Access article distributed under the terms of the Creative
Commons Attribution Non-Commercial Licens (http://creativecommons.
org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use,
distribution, and reproduction in any medium, provided the original work
is properly cited.
pISSN: 2234-1749 eISSN: 2234-1757
*Corresponding Author
E-mail: [email protected]
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Fish Aquat Sci 18(3), 301-309, 2015
Artemia nauplii
Formulated feed mixture, Pagrus major eggs
60
Total length (mm)
1,600
180
160
1,400
Wet weight (mg)
70
200
50
40
30
140
1,200
120
1,000
100
800
80
600
60
20
400
40
10
200
20
0
0
5
10
15
20
25
30
0
35
Dry weight (mg)
Rotifers
1,800
0
5
10
15
20
25
30
0
35
Day after hatching
Day after hatching
Fig. 1. Total length (mean ± S.D.) and feeding schedule of the chub
Fig. 2. Developmental changes in wet (▲) and dry weight (■) of
ment in Korea, with high market prices due to a strong demand
for live aquaculture products. Although artificial rearing techniques of the chub mackerel have recently been reported in
Korea, the early development of the scombrid larvae is poorly
understood, primarily due to difficulties in rearing the larvae.
Culturing of the early stages is considered the most critical
phase for successful aquaculture (Tanaka, 1973). In particular,
a lack of information of the nutritional requirements of the
fish larvae and the development of their digestive system is
thought to play a major role in the limited success of larval
culture of many species. Hence, to develop successful aquaculture methods, species-specific information on the early development of larvae is required to provide the best feeding regimes to match the ontogenetic status of the larvae. However,
there is no documented ontogeny of the digestive system in S.
japonicus. The aim of this study was to describe the histological changes and organogenesis of S. japonicus during early
ontogeny, from hatching to the early juvenile stages.
Sample collection
mackerel Scomber japonicus larvae and juveniles.
Scomber japonicus during larval and juvenile period.
Eighty individuals were collected from hatching on a daily
basis for 35 days from 31 May 2011 until 5 July 2011. Fifty
individuals were fixed in 10% natural formaldehyde for morphological investigation (Olympus DP20, Olympus Co., Japan). Total length (TL) and standard length (SL) were measured to the nearest 0.1 mm. The developmental phases were
classified into 5 stages (the yolk-sac larvae, 0–2 DAH; preflexion larvae, 3–12 DAH; flexion larvae, 13–16 DAH; postflexion larvae, 17–26 DAH; and juvenile, 27–35 DAH) based
on Kendall et al. (1984). The criteria for classification were as
follows: the yolk-sac larval stage, a transitional stage (from
hatching to yolk-sac absorption); the larval period, divided
into three phases (preflexion phase: first feeding to onset of
notochord flexion: flexion phase: to completion of notochord
flexion; postflexion phase: to completion of fin formation) depending on the flexion of the notochord that accompanied the
hypochordal development of the homocercal caudal fin, and
the juvenile stage (completion of fin ray counts and beginning
of squamation until the fish entered the adult population or attained sexual maturity).
Individual fish were placed on pre-weighted pieces of foil
and dried at 60°C for 48 h to obtain the dry weight measurements. The remaining fish were fixed in Bouin’s solution for
24 h and preserved in 80% ethanol for subsequent histological
preparation. The larvae were dehydrated and embedded in paraffin. Serial sections were made with a microtome at a thickness of 5–7 µm. Sections were stained with Mayer’s hematoxylin and eosin and then observed under a microscope system
(Olympus BX51, Japan, and Leica DM2500, Germany).
Materials and Methods
Rearing
Fertilized eggs of chub mackerel were obtained from a
broodstock maintained by Gyongsangnam-do Fisheries Resources Research Institute, Korea and stocked in a 20-ton rearing tank. The water was maintained at an average temperature
of 19.1 ± 2.2°C. Rotifers were fed immediately after hatching
until 19 DAH, and Artemia nauplii (3–4 individuals/mL) were
supplied from 15 to 27 DAH. Red sea bream (Pagrus major)
eggs and a formulated feed mixture (Otohime; 53% protein)
were supplied at a ratio of 1:3 from 20 to 35 DAH (Fig. 1).
http://dx.doi.org/10.5657/FAS.2015.0301
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Park et al. (2015) Development of the Digestive System in Chub Mackerel Larvae and Juvelines
A
B
Fig. 3. Photomicrographs of a Scomber japonicus larva on the day just after hatching. (A) Whole-body photograph. (B) Sagittal section of the body axis of
larva just after hatching showing large yolk. The scale bars indicate 1 mm for (A); 200 µm for (B). yo, yolk; no, notochord.
Results
Preflexion larvae
The mouth and anus were completely open, and the eyes
fully pigmented at 3 DAH (3.91 ± 0.20 mm TL). The primordial fin fold, which had developed by 3 DAH, formed the external structure that was able to find and consume food. The
digestive tract had expanded, with a rudimentary stomach
apparent between the esophagus and the intestines at 3 DAH
(Fig. 4A). The primitive structure of the digestive system was
divided into an oropharyngeal cavity, esophagus, rudimentary
stomach, swim bladder, intestines, and rectum. The gastric
gland and blind sac were not observed in the stomach mucosa.
Rotifers first appeared in the digestive tract at 3 DAH, and the
basic structure of the digestive system, which enabled the larvae to ingest and digest exogenous nutrients, was established
(Fig. 4B). The yolk was mostly absorbed, and the intestinal
epithelium had thickened (Fig. 4C). The rectum epithelium
was composed of columnar absorptive cells, with well-developed, striated borders (Fig. 4D). By 5 DAH (4.11 ± 0.23
mm TL) the intestines had become increasingly inflated, and
the epithelium was composed of vacuoles. The rectum epithelium from which the mucosal fold does not develop, became
thick, and acidophil granules were observed in great numbers.
The rectum was completely separated from the intestines by a
well-developed rectal valve. The first appearance of the gastric gland was noted at 5 DAH. By 7 DAH (4.67 ± 0.29 mm
TL) the intestines had enlarged, and the mucosal fold of the
rectum had started to developed. The mucosal folds of the
stomach developed, the dorso-posterior section had enlarged
to form the blind sac, and the pyloric caeca was differentiated.
The mucosal folds of the intestines and rectum developed,
and the intestines were divided into the anterior and posterior
intestines by 9 DAH (5.24 ± 0.37 mm TL). The esophagus
was differentiated at 11 DAH (5.53 ± 0.37 mm TL), with the
Growth
The total length of larval fish averaged 3.35 ± 0.14 mm just
after hatching, 3.91 ± 0.20 mm at first feeding (3 DAH), 5.91
± 0.45 mm at the flexion phase (13 DAH), 7.09 ± 0.61 mm at
the postflexion phase (17 DAH), 21.46 ± 2.45 mm at the juvenile phase (27 DAH), and 56.64 ± 9.27 mm at the experimental end date (35 DAH). The total length of the chub mackerel
larvae increased markedly from the postflexion phase to the
juvenile phase (Fig. 1). The wet and dry weights were 4.6 and
0.4 mg, respectively, at 17 DAH; by 27 DAH, the wet and dry
body weights had increased >60 fold, to 277.1 mg and 59.1
mg, respectively (Fig. 2). The average growth rate during 35
days of rearing was approximately 1.52 mm/day.
Development of the Digestive System
Yolk-sac larvae
At 0 DAH (3.35±0.15 mm TL), the mouth and anus were
unopened, and the melanosome in the eyes was not yet colored (Fig. 3A). Most of the body cavity was occupied with
yolk (Fig. 3B). The digestive tract was a simple straight tube
observed along the dorsal wall of the yolk. At 1 DAH (3.69 ±
0.16 mm TL), the lumen of the gut was slightly enlarged, and
the digestive system of the chub mackerel was opened to the
anus, although the mouth had not yet opened. The intestines
and rectum were differentiated, and the mouth opened completely. The rudimentary swim bladder began to differentiate
from the dorsal wall of the anterior gut at 2 DAH (3.91 ± 0.17
mm TL).
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Fish Aquat Sci 18(3), 301-309, 2015
A
B
C
D
Fig. 4. Photomicrographs of Scomber japonicus larva at first feeding stage on 3 DAH. (A) Whole-body photograph. (B) Sagittal section of the body axis
showing the differentiated digestive tract. (C) Sagittal section of the rudimentary stomach, oil globule, intestine and air bladder. (D) Sagittal section of
the rectum. The scale bars indicate 1 mm for (A); 100 µm for (B)-(D). st, stomach; og, oil globule; in, intestine; ab, air bladder; re, rectum; no, notochord; oe,
oesophagus.
stratified squamous epithelium in the front and simple squamous epithelium in the back. The number of gastric glands
increased, and the stomach elongated posteriorly to form the
blind sac at 11 DAH.
Postflexion larvae
At 17 DAH (7.09 ± 0.61 mm TL), the notochord tip upturn
was complete, along with a nearly complete caudal fin (Fig.
6A). The stomach had separated into the cardiac and pyloric
portions and the blind sac. The blind sac extended posteroventrally (Fig. 6B). The number of gastric glands had increased
(Fig. 6C). The number of jaw and pharyngeal teeth, gastric
glands, and pyloric caeca had also increased. The pyloric caeca were well formed at the anterior-most part of the intestines.
There were few mucous cells on the oral cavity epithelium
(Fig. 6D).
Flexion larvae
The head became larger, and the body depth increased. The
notochord tip began to turn upward with the appearance of
urophysial bones at 13 DAH (5.91 ± 0.45 mm TL) (Fig. 5A).
Development of the digestive system as a whole took place at
this time. The mucosal folds of the stomach in particular were
developed (Fig. 5B). The mucosal epithelium became thicker
and noticeably developed (Fig. 5C, D).
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Park et al. (2015) Development of the Digestive System in Chub Mackerel Larvae and Juvelines
A
B
C
D
Fig. 5. Photomicrographs of a Scomber japonicus larva at the flexion phase on 13 DAH. (A) Whole-body photograph. (B) Sagittal section of the body axis
showing the development of stomach, intestine and rectum. (C) Sagittal section of stomach showing the early appearance of the gastric glands. (D) Sagittal
section of the rectum and intestine. The scale bars indicate 2 mm for (A); 500 µm for (B); 100 µm for (C) and (D). st, stomach; in, intestine; re, rectum; gg,
gastric glands; no, notochord.
Discussion
Juveniles
At 27 DAH, all the fins were fundamentally established
(Fig. 7A), and the histological characteristics of the digestive
organ were similar to those of adult chub mackerel (Fig. 7B).
The gastric glands had increased in number (Fig. 7C) and were
distributed throughout the stomach, with the exception of the
pyloric portion (Fig. 7D). The gastric lumen contained a large
volume of food, resulting in the expansion of the blind sac
toward the posterior edge of the abdominal cavity. Intestinal
epithelial cells were stained dark with hematoxylin in all the
fish examined.
The development of the digestive system in S. japonicus
larvae is similar to that reported for other scombrid species,
particularly the striped bonito Sarda orientalis (Kaji et al.,
2002), the bluefin tuna Thunnus thynnus, and the yellowfin
tuna Thunnus albacares (Kaji et al., 1996; 1999). These all
possessed an undifferentiated and rudimentary digestive system, which later differentiated into the buccopharynx, esophagus, intestines, and rectum at 3 DAH. Tanaka (1973) reported
that Japanese sea bass (Lateolabrax japonicus), red sea bream,
and black sea bream (Acanthopagrus schlegelii) formed a
primitive larval-type digestive system at 4 DAH. These early
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Fish Aquat Sci 18(3), 301-309, 2015
A
B
C
D
Fig. 6. Photomicrographs of Scomber japonicus larva at the postflexion phase on 17 DAH. (A) Whole-body photograph. (B) Sagittal section of the body
axis showing the development of stomach, intestine and rectum. (C) Sagittal section of the stomach showing the gastric glands. (D) Pyloric caecum
differentiated from the anterior intestine. The scale bars indicate 3 mm for (A); 1 mm for (B); 100 µm for (C) and (D). st, stomach; in, intestine; re, rectum; gg,
gastric glands; pc, pyloric caecum; no, notochord.
larval-type digestive systems are established to enable the larvae to ingest, digest, and assimilate its first exogenous food
when the yolk reserves have been completely absorbed. However, the assimilation efficiency may be lower in larvae than
that in adult fish due to the lack of a morphological and functional stomach in the larvae.
Pinocytosis has been suggested as an alternative pathway
for the digestion of proteins in teleost larvae, as their enzymatic digestive system is poorly developed (Watanabe, 1982).
This study showed that vacuoles appeared evenly on the intestinal epithelium of chub mackerel larvae, and acidophil granules were observed in the rectal epithelium at 3 DAH. Iwai
and Tanaka (1968) and Tanaka (1973) reported that the vacuoles and acidophil granules were indicative of larval digestion
and absorption mechanisms that existed before the development of the functionality of the early divided stomach and
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gastric gland of larval fish. In most marine fishes, the development of a digestive system consisting of a functional stomach
with well-developed gastric glands and pyloric caeca occurs
in association with the transformation to the juvenile stage.
Accordingly, the typical development pattern of marine fishes
involves a mechanism for digestion, and absorption changes
from pinocytosis and intracellular digestion to extracellular
digestion and membrane transport with the development of
the gastric gland (Govoni et al., 1986).
The first appearance of the gastric gland was reported at
21 DAH in red sea bream, 15 DAH in rainbow trout (Oncorhynchus mykiss), 25 DAH in black sea bream, and 90–120
DAH in Plecoglossus altivelis (Tanaka, 1973). However, in
chub mackerel larvae, the gastric gland appeared at 5 DAH
during the preflexion phase. Interestingly, the striped bonito
(Kaji et al., 2002) and Spanish mackerel Scomberomorus ni-
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Park et al. (2015) Development of the Digestive System in Chub Mackerel Larvae and Juvelines
A
B
C
D
Fig. 7. Photomicrographs of Scomber japonicus at early juvenile phase on 27 DAH. (A) Whole-body photograph. (B) Sagittal section of the body axis
showing the development of stomach, intestine, pyloric caecum and rectum. (C) Densely distributed gastric glands. (D) Pyloric caecum differentiated from
the anterior intestine. The scale bars indicate 7 mm for (A); 2 mm for (B); 100 µm for (C) and (D). st, stomach; in, intestine; re, rectum; gg, gastric glands; pc,
pyloric caecum.
phonius (Tanaka et al., 1996), which are both members of the
Scombridae, developed gastric glands at 3 and 4 DAH, respectively. In contrast, in bluefin and yellowfin tuna, the gastric
glands emerged at 11 and 14 DAH, which was 2–3 times later
than in chub mackerel (Kaji et al., 1996; 1999). The appearance of pyloric caeca followed a similar pattern to the gastric
glands in the scombrid larvae. In the striped bonito (Kaji et al.,
2002) and Japanese Spanish mackerel (Fukunaga et al., 1982),
pyloric caeca appeared earlier (at 7 DAH) than in the chub
mackerel, and these emerged at 14 and 16 DAH in bluefin and
yellowfin tuna, respectively (Kaji et al., 1996; 1999).
Although five scombrid larvae, including the chub mackerel, showed species-specific timing in the appearance of the
gastric glands and pyloric caeca, their digestive system attained the juvenile-type structure long before metamorphosis.
On the other hand, a juvenile-type digestive system formed
during the juvenile period, at 35 DAH, in black sea bream and
false kelpfish (Sebastiscus marmoratus), at 135 DAH in sweet
fish (Tanaka, 1973), and at 21 DAH in large yellow croakers (Mai et al., 2005). Consequently, the development of the
digestive system of chub mackerel larvae can be considered
precocious compared to common marine fishes.
Scombrids can grow very rapidly during their early life
stages, and this may be related to the precocious development
of the digestive system in this group of fishes (Tanaka et al.,
1996). In chub mackerel, the total length and body weight increased gradually from 17 DAH; thereafter, there was a rapid
increase from 25 DAH. As in other scombrids, chub mackerel
larvae also undergo marked, rapid growth during the early life
stages, which is supported by their precocious digestive system. In addition, Shoji et al. (2001) reported that the absolute
growth of wild chub mackerel increased from 0.298 mm/day
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References
(post-first-feeding stage) to 0.712 mm/day (later larval and
early juvenile stages), suggesting that the increase in growth
rate of the chub mackerel may result from the shift in feeding
to piscivory.
Tanaka et al. (1996) suggested that the precocious development of the digestive system with differentiation of the
functional stomach in scombrid larvae also supported the
appearance of piscivory. The increase in pepsin-like enzyme
activity measured from the whole body extract is likely to be
concomitant with gastric gland differentiation in the scombrid
larvae, as in many other species (Govoni et al., 1986). This
physiological advancement, as well as the formation of a blind
sac that enables the larvae to store larger prey items, would
support the appearance of piscivory in scombrid larvae, including chub mackerel larvae.
The peak occurrence of wild Spanish mackerel larvae is
synchronized with the peak abundance of their prey larvae,
suggesting the ecological advantage of early piscivory with
the precocious development of the digestive system (Shoji et
al., 1999). In contrast, the bluefin and yellowfin tuna larvae
attained juvenile-type digestive systems during the flexion
phase and underwent a larval period of planktivory with a
larval-type digestive system, suggesting that they may have
adapted to their offshore feeding habitat where the density of
prey fish larvae may be low (Tanaka et al., 1996). Kohno et al.
(1984) reported that swimming and feeding abilities develop
rapidly after the development of the jaw and pharyngeal teeth,
as well as the caudal fin formation in chub mackerel larvae of
5–7 mm SL. In addition, 25% of wild chub mackerel larvae
measuring 5–6 mm SL contained fish in their stomachs; this
increased to 80% at 9–10 mm SL (Shoji et al., 2001). As in
the Spanish mackerel, the early morphological developments
and precocious digestive system in chub mackerel larvae were
likely associated with the early onset of piscivory. Stomach
contents analysis of wild chub mackerel larvae of 4–9 mm TL
showed that the main prey were the larvae of the sea squirt,
crustaceans, Evadne sp., and water fleas (Ozawa et al., 1991).
However, as the chub mackerel larvae grew, the amount of fish
larvae in the diet increased, as the consumption of crustacean
larvae and Evadne decreased. The size range (4–9 mm TL) of
wild chub mackerel was estimated between 6 and 18 DAH in
this study; this period coincides with the establishment of the
juvenile-type digestive system during the larval period. Therefore, it could be predicted that the precocious development of
the digestive system during the larval period of chub mackerel
is related to the early appearance of piscivory, which is able to
support the high growth potential of the larvae. Consequently,
the precocious digestive system in chub mackerel larvae described in this study will provide useful information to improve current larval rearing practices and feeding protocols,
and will reduce weaning costs for this fish species.
http://dx.doi.org/10.5657/FAS.2015.0301
FAO Species Catalogue. 1983. Scombrids of the world - An annotated
and illustrated catalogue of tunas, mackerels, bonitos and related
species known to date. 125, 56-57.
Fukunaga T, Ishibashi N and Mitsuhashi N. 1982. Artificial fertilization and seeding production of Spanish mackerel. Saibai-giken 11,
29-48.
Govoni JJ, Boehlert GW and Watanabe Y. 1986. The physiology of digestion in fish larvae. Environ Biol Fish 16, 59-77.
Harada T, Murata O, and Miyashita S. 1974. On the artificial fertilization and rearing of larvae in bonito. Mem Fac Agri Kinki Univ 7,
1-4.
Hunter JR. 1981. Feeding ecology and predation of marine fish larvae.
In: Marine Fish Larvae. Lasker R, ed. University of Washington
Press, Seattle, US, pp. 33-77.
Iwai T and Tanaka M. 1968. The comparative study of the digestive
tracts of teleost larvae-III. Epithelial cells in the posterior gut of
halfbeak larvae. Bull Japan Soc Sci Fish 34, 44-48.
Kaji T, Tanaka M, Takahashi Y, Oka M and Ishibashi N. 1996. Preliminary observations on development of pacific bluefin tuna Thunnus
thynnus (Scombridae) larvae reared in the laboratory, with special
reference to the digestive system. Mar Freshwater Res 47, 261-269.
Kaji T, Tanaka M, Oka M, Takeuchi H, Ohsumi S, Teruya K and Hirokawa J. 1999. Growth and morphological development of laboratory-reared yellowfin tuna Thunnus albacares larvae and early
juveniles, with special emphasis on the digestive system. Fish Sci
65, 700-707.
Kaji T, Kodama M, Arai H, Tagawa M and Tanaka M. 2002. Precocious
development of the digestive system in relation to early appearance
of piscivory in striped bonito Sarda orientalis larvae. Fish Sci 68,
1212-1218.
Kendall AW, Ahlstrom EH and Moser HG. 1984. Early life stages of
fishes and their characters. In: Ontogeny and Systematics of Fishes.
Moser HG, Richards WJ, Cohen DM, Fahay MP, Kendall AW and
Richardson SL, eds. Allen press, Lawrence, US, pp. 11-22.
Kohno H, Shimizu M and Nose Y. 1984. Morphological aspects of the
development of swimming and feeding functions in larval Scomber
japonicus. Nip Sui Gak 50, 1125-1137.
Mai K, Yo H, Ma H, Duan Q, Gisbert E, Zambonino-Infante JL and
Cahu CL. 2005. A histological study on the development of the
digestive system of Pseudosciaena crocea larvae and juveniles. J
Fish Biol 67, 1094-1106.
Miyashita S, Kato K, Sawada Y, Murata O, Ishitani Y, Shimizu K, Yamamoto S and Kumai H. 1998. Development of digestive system
and digestive enzyme activities of laeval and juvenile bluefin tuna,
Thunnus thynnus, reared in the laboratory. Suisanzoshoku 46, 111120.
Ozawa T, Kawai K and Uotani I. 1991. Stomach content analysis of
chub mackerel Scomber japonicus by quantification I method. Bull
Jap Soc Sci Fish 57, 1241-1245.
Shoji J, Maehara T and Tanaka M. 1999. Short-term occurrence and
rapid growth of Spanish mackerel larvae in the central waters of
the Seto Inland Sea, Japan. Fish Sci 65, 68-72.
308
Park et al. (2015) Development of the Digestive System in Chub Mackerel Larvae and Juvelines
Shoji J, Tanaka M and Maehara T. 2001. Comparative diets and growth
of two Scombrid larvae, chub mackerel Scomber japonicus and
Japanese Spanish mackerel Scomberomorus niphonius in the central Seto Inland Sea, Japan. UJNR Technical Report 30, 93-103.
Tanaka M. 1973. Studies on the structure and function of the digestive
system of teleost larvae. Ph.D. Dissertation, Kyoto University,
Kyoto, Japan.
Tanaka M, Kaji T, Nakamura Y and Takahashi Y. 1996. Development
strategy of scombrid larvae: high growth potential related to food
habits and precocious digestive system development. In: Survival
Strategies in Early Life Stages of Marine Resources. Watanabe Y,
Yamashita Y and Oozeki Y, eds. Balkema, Amsterdam, Netherlands, pp. 125-139.
Watanabe Y. 1982. Intracellular digestion of horseradish peroxidase by
the intestinal cells of teleost larvae and juveniles. Bull Japan Soc
Sci Fish 48, 37-42.
309
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