Journal of Survey in Fisheries Sciences 7(2) 49-62 2021
Backcross breeding between TGGG hybrid grouper
(Epinephelus fuscoguttatus  E. lanceolatus) and giant
grouper (E. lanceolatus)

Tan J.
*


Received: June 2020 Accepted: November 2020

Abstract
This paper reports on the first successful backcross breeding between TGGG hybrid
grouper and GG in captivity. To establish a seed production technique for this new
backcross grouper, eggs and larval development were observed. Three successful
spawning was observed in November 2018, September 2019 and November 2019. The
eggs were collected using stripping methods and the sperms were collected using
sperms collector. About 1.2 to 1.3 litres of eggs were collected in each spawning.
Eggs and larval development of backcross TGGG hybrid and GG were almost similar
to its parental species and other Epinephelus species. Fertilized eggs were measured
0.860 to 0.915 mm in diameter, with oil globule 0.190 to 0.214 mm in diameter.
Fertilization and hatching rate were in between 80 to 90 %. Newly hatched larvae range
from 1.64 to 1.99 mm and commenced feeding at 60 d AH. Larval dorsal and pelvic
spines started to develop from 9 d AH and fins were formed on 21 d AH. By the age of
30 d AH, the fish entered juvenile stage. At 60 d AH, the fry’s body shape and colour
resembled those of the adult. After more than 300 d AH, the fish reached 1 kg in weight.
The backcross between female TGGG and male GG is expected to perform even better
growth and survival rate than TGGG because the backcross carries more genetic
material from the GG, which would be ideal for mass production in the aquaculture
industry.

Keywords: Backcross breeding, Epinephelus lanceolatus, Epinephelus fuscoguttatus






*Bayu Aquaculture Sdn. Bhd. (BASB) is located at Kg. Serusop, Tuaran, Malaysia. BASB is
the anchor company for aquaculture development in the Sabah Agriculture Blueprint 2020.
BASB promotes production of quality fish for consumption without the use of chemical in the
process.
*
Corresponding author's Email: [email protected]
Mailing address: P. O. Box 22477, 88784 Luyang, Kota Kinabalu, Sabah, Malaysia. [ DOI: 10.18331/SFS2021.7.2.4 ]
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50 Tan, Backcross breeding between TGGG hybrid grouper …

Introduction
Grouper aquaculture is carried out in
tropical and subtropical areas throughout
the world, but most production is from
Asia (Rimmer and Glamuzina, 2017). In
the Southeast Asian region, the most
popular cultured groupers included the
tiger grouper (Epinephelus fuscoguttatus),
orange-spotted grouper (E. coioides) and
giant grouper (E. lanceolatus) (Luan et
al., 2016). The major grow-out sites for
grouper in Malaysia are in Sabah
(particularly Tuaran and Sandakan) and
Sarawak, where wild seeds are available
(Pomeroy, 2002). Groupers are high
quality marine fish with increasing
economic values. It was estimated almost
155 000 tonnes of groupers were
produced in 2015 with a total value of
USD 630 million (FAO, 2017). In order
to meet the growing market demand,
development of quality fish breeds can
contribute to the increase of fish
production.
In aquaculture, hybridization has
long been practiced in various species of
fishes to increase growth rate, improve
flesh quality, increase disease resistance
and environmental tolerance, and to
improve other quality traits to make the
fish more profitable (Rahman et al.,
2013). Hybridization has been practice in
groupers since 2006, with the first
production of TGGG, a crossbreed
between tiger grouper (TG;
E.fuscoguttatus) and giant grouper (GG;
E. lanceolatus) (Ch’ng and Senoo, 2008).
The TGGG hybrid grouper is known as
the most successful hybrid combination:
has a wide range of environmental
tolerance (Othman et al., 2015; De et al.,
2016; Shapawi et al., 2018), better
growth performance (Ch’ng and Senoo,
2008), and feeding performance (Othman
et al., 2015).
Generally, hybrids species are
consider sterile species because normally
inter-specific hybrids cannot produce
viable gametes (Bartley et al., 2001; Luin
et al., 2013). Even so, there are cases of
hybrids that show sexual maturation and
fertility (Na-Nakorn et al., 2004; Wang et
al., 2006), which indicates that producing
second generation (F2) of hybrids and
backcross breeding in fish is possible. In
fact, F2 generation (Argue et al., 2003;
Tymchuk and Devlin, 2005) and
backcross experiment (Sui et al., 2011;
Xu et al., 2011) in fish has been
conducted in some studies. According to
Shapawi et al. (2018), in comparison to
the hybrid species, the following
generation is characterized by greater
hybrid vigor or positive heterosis
characteristics.
In 2013, Luin et al. reported that
the TGGG hybrid grouper could reach
sexual maturation as evident from
development of their gonads, which
opened up the possibility to perform
backcross breeding in grouper. In 2016,
Luan et al. has successfully produce the
eggs of backcross between OGGG hybrid
grouper (orange spotted grouper, OG,
E.coioides x giant grouper, GG,
E.lanceolatus) and giant grouper (GG,
E.lanceolatus) in captivity. However,
fertilization and hatching rate were
recorded the lowest compared to other
hybrid groupers (Luan et al., 2016). In [ DOI: 10.18331/SFS2021.7.2.4 ]
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Journal of Survey in Fisheries Sciences 7(2) 2021 51

2018, Ching et al. reported the first
natural spawning and fertilized eggs of
F2 hybrid TGGG in captivity. Still, low
survival rate remains the bottleneck that
prevented the establishment of
production.
The above studies have motivated
the Bayu Aquaculture Sdn. Bhd. to
conduct the present study, in an attempt
to produce backcross bears close
resemblance to GG, which is fast
growing, has good organoleptic
properties, and would likely exhibit
higher resistance to common disease. To
the best of our knowledge, this study was
the first report on the successful
backcross breeding between TGGG and
GG in captivity. The backcross between
female TGGG and male GG (Fig. 1) is
expected to perform even better growth
and survival rate than TGGG because the
backcross carries more genetic material
from the GG, which would be ideal for
mass production in the aquaculture
industry. This will then help to boost the
fisheries sector in the country and also
satisfy the increasing demand for
grouper.


Figure 1: Concept of backcross breeding between female TGGG and male GG.

Materials and methods
Breeding and eggs incubation
The broodstock used in this study were
reared in net cages located in Gaya Island,
Sabah. The size of the net cages was 5 x
5 meter for GG and 4.5 x 4.5 meter for
TGGG, with the depth of 3.5 meter. The
broodstock were fed twice a week with
enriched prey fish (Sardinella sp.)
supplemented with fish oil, squid oil and
vitamin premixes. The total length of the
broods was in between 60 to 90 cm and
weight was ranged from 40 to 60 kg for
GG and 9 to 14 kg for TGGG. [ DOI: 10.18331/SFS2021.7.2.4 ]
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52 Tan, Backcross breeding between TGGG hybrid grouper …
In the present study, five male of GG and
three female of TGGG were involved in
the spawning. After the maturity of the
broods were checked and identified, the
eggs were collected using stripping
methods and the sperms were collected
using sperms collector. The eggs and
sperms were then mixed and washed.
Fertilized eggs were then transferred to
incubate at the fish farm of Bayu
Aquaculture Sdn. Bhd. in Tuaran, Sabah.
The size of eggs and development was
observed under microscope and
photographed using a digital camera. The
fertilized eggs were incubated in a 15 x 6
x 1.3 meter concrete pond with 24 hour
aeration. The water temperature, salinity,
DO and pH during eggs incubation were
28 to 32℃, 30 ppt, 5.0 to 7.0 mg/l, and
7.8 to 8.0 respectively.

Larval and juvenile rearing
Hatched larvae were reared in the same
pond where eggs incubated, and later
transferred to round tank filled with 4
tonne seawater when the dorsal and
pelvic spines began to retract. The
rearing water temperature, salinity, DO
and pH were 28 to 32℃, 30 ppt, 5.0 to
7.0 mg/l, and 7.8 to 8.0, respectively.
Cleaning of tank’s bottom was carried
out daily to remove excess feed and dead
larvae. Total length (TL) of larvae was
measured from 0 d AH and larval
development was observed under
microscope and photographs were taken
with a digital camera.
Different feeds were given at 3
times daily as shown in Figure 2. Larvae
rely on egg yolk sac on 1 to 2 day after
hatched (d AH). However, Chlorella sp.,
were added to the rearing pond as water
conditioner during that period. Rotifer
Brachionus sp. (150 um) were given to
larvae from 3 to 14 d AH. Commercial
brine shrimp Artemia salina nauplii were
introduced from 10 to 40 d AH, and
formulated powder feed, Otohime
(Marubeni Nisshin Food, Japan) was fed
from 20 to 55 d AH. Copepod harvested
from the sea was added into rearing tank
from 24 to 60 d AH. Minced fish was
added when the fish reached juvenile
stage and onwards.

Figure 2: Feeding sequences of TGGG x GG backcross grouper [ DOI: 10.18331/SFS2021.7.2.4 ]
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Journal of Survey in Fisheries Sciences 7(2) 2021 53

Results
Spawning and eggs development
First successful spawning was observed
in November 2018, followed by second
and third batch in September 2019 and
November 2019, respectively. About 1.2
to 1.3 litres of eggs were collected from
the female TGGG in each spawning.
Fertilization and hatching rate were in
between 80 to 90%. Fertilized eggs were
spherical, transparent, measured 0.860 to
0.915 mm in diameter, with oil globule
0.190 to 0.214 mm in diameter.
The eggs development is shown in Figure
3. At 10 hours after fertilized (h AF), the
head and myomere were formed, with
appearance of Kupper’s vesicle. At 12 h
AF, the tail has separated from the yolk
sac. At 15 h AF, lens vesicle becomes
visible and movement of embryo was
observed. Hatching began at 18 h AF.
Newly hatched larvae were measured
1.64 to 1.99 mm in total length (TL). The
newly hatched larvae would stay on
water surface, positioned upside down
due to the yolk sac and oil globule and
not swimming, but floating and drifting
around the water column.


Figure 3: Egg development of TGGG x GG backcross grouper. A. Fertilized eggs; B. Head and
myomere formed, Kupffer’s vesicle appeared; C. Tail separated from yolk, optic vesicle
appeared; D. Lens vesicle visible, embryo moving; E. Hatching commenced; F. Newly
hatched larvae; number at the left corner show hours after fertilization; all the scales are
same as shown in A at the right corner, except F.


Larval development and juvenile growth
The morphological changes in larvae and
juvenile stage are illustrated in Figures 4
and 5, respectively. The correspondence
between the morphological features and
behavioral changes is summarized in
Table 1. Total length (TL) changes of
larvae are shown in Figure 6.
The TL of newly hatched larvae
range from 1.64 to 1.99 mm. At 21 hour
after hatched (h AH), the larvae eyes
were formed but not pigmented. The
anus part formed but not opened. At 24 h [ DOI: 10.18331/SFS2021.7.2.4 ]
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AH, the yolk sac reduced in size and the
larvae started to perform vertical
swimming. At 38 h AH, eyes
pigmentation darken, anus part opened
and digestive tract were formed. At 60 h
AH, the yolk sac and oil globule were
completely absorbed. The larvae mouth
part opened, lower jaw and digestive
tract started mov ing, and
indicating that feeding process has begun.
At 3 days after hatched (d AH), black
pigmentation appeared at area above
intestine. The larvae were actively
swimming and fed on rotifer. At 5 d AH,
melanophores on the area above intestine
expanded and new spot of melanophores
also appeared on the area between anus
part and caudal fin.


Figure 4: Morphological changes of TGGG x GG backcross grouper in larval stage. A. 1 d AH,
2.57mm TL; B. 3 d AH, 2.71mm TL; C. 9 d AH, 4.06mm TL, D. 14 d AH, 7.01mm TL, E.
21 d AH, 18.5mm TL, F. 30 d AH, 23.0mm TL, G. 35 d AH, 28.0mm TL; H. 40 d AH,
30mm TL.
[ DOI: 10.18331/SFS2021.7.2.4 ]
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Journal of Survey in Fisheries Sciences 7(2) 2021 55




Figure 5: Morphological changes of TGGG x GG backcross grouper in juvenile stage. A. 60 d AH,
5.7cm TL; B. 80 d AH, 7.0cm TL; C. 120 d AH, 13.5cm TL; D. 170 d AH, above 20.0cm
TL; E. More than 200 d AH, above 25.0cm TL; F. More than 400 d AH, 30.0cm TL; G.
More than 300 d AH, reached 1kg in weight.

Dorsal pelvic spine started to develop
from 9 d AH and fully elongated at 14 d
AH. The spines were covered with
melanophores. At that moment, the
larvae were actively swimming and
Artemia salina nauplii were being
introduced into their diet. The larvae
started to congregate at the center bottom
of the tank. Dorsal and pelvic spines
slowly retracted and fins were formed on
21 d AH. The larvae responded well to
the formulated powder feed given. [ DOI: 10.18331/SFS2021.7.2.4 ]
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Table 1: Correspondence between morphological and behavioral changes backcrosses grouper
TGGG x GG larvae.
Morphological changes Day after hatched (d AH) Behavioral changes
Hatching commenced. 0 Floating and drifting around the
water column. Pelagic behaviour.
Eyes formed but not pigmented.
Anus formed but not opened.
1 Relying on yolk sac for nutrient.
Eyes pigmented. Mouth opened and
lower jaw moving. Movement in
digestive tracts. Yolk sac and oil
globule completely absorbed.
3 Swimming and started to feed on
rotifer.
Dorsal and pelvic spines started to
develop. Abdominal cavity deeply
pigmented.
9 Actively swimming and feed on
Artemia salina nauplii.
Dorsal and pelvic spines elongated,
covered with melanophore.
Pigmentation on head part. Coloured
abdominal cavity.
14 Actively fed on Artemia salina
nauplii. Congregated around
central part of tank.
Dorsal and pelvic spines retracted.
Dorsal and pelvic fins started to
develop.
21 Responding well to formulate
powder feed.
Body turned non-transparent.
Development of brown colouration
and dark patterns. Lateral line
clearly seen. Dorsal, pelvic, anal and
caudal fins well develop. Entering
juvenile stage.
30 Actively preyed on mixed live
feed of Artemia salina nauplii and
copepod, with formulated powder
feed.
Silvered abdomen. Juvenile stage. 40 Benthic habitat.


Figure 6: Growth of backcross grouper TGGG x GG larvae from 0 to 35 d AH.

By the age of 30 d AH, the larvae body
was no longer transparent. Brown
colouration and black stripes started to
develop and lateral lines can be clearly
seen. All the fins (dorsal, pelvic, anal and
caudal) were well developing. The fish
started to enter juvenile stage. At that
stage, they were actively preying on
combination of live feed consisting
Artemia salina and copepod, and
formulated powder feed. At 40 d AH, the
fry reached 35 mm in TL, shifted to [ DOI: 10.18331/SFS2021.7.2.4 ]
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Journal of Survey in Fisheries Sciences 7(2) 2021 57

benthic habitat and looked more
aggressive. After 60 d AH, the fry’s body
shape and colour resembled those of the
adult and actively fed on minced fish. At
150 d AH, the juvenile reached 20 mm in
TL, body colour and dark patterns turned
darker. After more than 300 d AH, the
fish reached 1 kg in weight.

Discussion
Eggs development
The fertilization and hatching rates in this
study were in the range of 80% to 90%.
The rates were similar with the F2 hybrid
TGGG study by Ching et al. (2018),
which reported the fertilization and
hatching rates at 80.7% and 91.5%, and
slightly higher than the maternal species,
recorded at 86.8% and 87.2%,
respectively by Ch’ng and Senoo (2008).
Hatching time of the eggs in this study
was 18 h AF, similar with the maternal
species (Ch’ng and Senoo, 2008) but
shorter than the paternal species, reported
at 30 h AF by Garcia-Ortega et al. (2013).
It is also shorter than the 19 h AF in TG
(Boonlipatanon et al., 2002) and slightly
longer than the 17:50 h AF in F2 hybrid
TGGG (Ching et al., 2018). Temperature
during eggs incubation in this study was
28 to 32 °C, more or less the same with
Ch’ng and Senoo (2008), Boonlipatanon
et al. (2002), and Ching et al. (2018) but
higher than in Garcia-Ortega et al. (2013),
which recorded at 28 to 29°C, 29 to 32°C,
29.5 to 30.5°C, and 27.6°C, respectively.
Fertilization and hatching rates are
important criteria used to assess the eggs
quality and often related to the nutritional
requirements of broodstock’s maturation
and fecundity (Kjørsvik et al., 1990;
Unuma et al., 2004; Ching et al., 2018).
Broodstock in this study were reared in
net cages, where the net mesh allows the
water to pass freely, thus maintaining
good water quality. The broodstock were
also well-fed with nutritionally balanced
diet with supplement. Physiologically,
when fish are given with the required
nutrient, they synthesize that nutrient for
maintenance and growth and support
various developmental processes
throughout their life span and resulted in
good quality of broodstock and
offsprings. Differences in hatching time
at similar water temperature are most
likely a characteristic of the species, but
most showed a close relationship with
water temperature (Park et al., 2014).
Diameter of eggs (0.86 to 0.915
mm) in this study was considered similar
to the paternal species (Garcia-Orgeta et
al., 2013) and the TG (Lim, 1993), both
recorded at 0.89 mm. Nevertheless, it
was relatively larger than the maternal
species, reported at 0.84 mm by Ch’ng
and Senoo (2008), and other hybrid
species (Koh et al., 2008; Koh et al.,
2010; Addin and Senoo, 2011). It was
also larger than the backcross between
OGGG and GG, reported at 0.755 mm in
diameter by Luan et al. (2016). It is
known that egg and larval sizes are
correlated and larger larvae tend to
survive longer without food than those
hatched from smaller eggs (Kjørsvik et
al., 1990). Bigger sized eggs are assumed
to have higher survival and growth
potential in subsequent stages (Colin et
al., 1996; Goncalves et al., 2011; Luan et
al., 2016).
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Larval and juvenile development
Total length (TL) of newly hatched
larvae in this study ranged from 1.64 to
1.99 mm, considered relatively similar
when compared to the maternal species,
reported at 1.99 mm by Ch’ng and Senoo
(2008). It was also similar to the TG,
reported at 1.80 to 1.90 mm by Lim
(1993). Growth of backcross TGGG x
GG was observed to be slower in the first
few days after hatched compared to the
parental species (Ch’ng and Senoo, 2008;
Garcia-Orgeta et al., 2013), but caught
up at later stage. TL of the backcross
TGGG x GG was 2.69 mm in 2 d AH
and 2.76 mm in 3 d AH, which was
smaller than the TGGG, recorded at 2.81
mm in 2 d AH (Ch’ng an Senoo, 2008)
and the GG, recorded at 2.9 mm in 3 d
AH (Garcia-Ortega et al., 2013).
However, in 20 d AH, TL of the
backcross TGGG x GG reached 17.1 mm,
while the size of TGGG was only 9.30
mm (Ch’ng and Senoo, 2008). In
addition, TL of the backcross TGGG x
GG reached 37.5 mm in 45 d AH, longer
than the 35.4 mm recorded in the GG by
Garcia- Ortega et al. (2013).
Backcrossed hybrids occasionally
outperform the F1 hybrid and the
parentals (Argue and Dunham, 1999).
Rapid growth through hybrid vigor is
observed in the F1 hybrid TGGG. Thus,
it is expected that the offspring from
backcross TGGG x GG may also inherit
desirable growth traits that promote even
faster growth than the parental species.
Hybridization merits tend to be more
affected by male parental species (Wang
et al., 2006). This was also suggested in
Koh et al. (2010), where TL of the hybrid
with GG as paternal parent has faster
growth than with TG as paternal parent.
The offspring of backcross TGGG x GG
is assumed to carry more genetic
materials from the male GG, which could
be the explanation of the faster growth of
larvae in this study. However, since this
is the first successful backcross breeding
of grouper, further details studies is
require to determine the growth-related
traits.
Morphological and behavioral
development of backcross TGGG x GG
larvae to juveniles is almost similar to its
parental species and other Epinephelus
species (Heemstra and Randal, 1993;
Tucker, 1999; Glamuzina et al., 2001;
Ch’ng and Senoo, 2008; Gracia-Ortega et
al., 2013). While the appearance of
pigmentation represents the basic
morphological characteristic of the
grouper in its early larval stage, there
were no distinct characteristic to
differentiate it from other species of
grouper larvae. In this study,
pigmentation on larvae can be clearly
observed at 3 d AH and the brown
colouration with dark pattern which was
similar to the parental species was
developed at 30 d AH. The development
of the dorsal and pelvic fin spines,
another basic morphological
characteristic of grouper larvae, were
observed as early as 9 d AH, with
melanophores on the tips. According to
Kawabe and Kohno (2009), the spines
play a role in maintaining position in the
water column and act as anti-predator
mechanism. When the length of dorsal
and pelvic fin spines shortens and
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Journal of Survey in Fisheries Sciences 7(2) 2021 59

becomes more obvious, the juveniles
enter the process of settling (Cunha et al.,
2013).
Larval period in present study was
about 30 d AH, which was similar to the
martenal species (Ch’ng and Senoo,
2008). During the transition of fish larvae
to juvenile stage, morphological,
physiological and ecological changes
occured (Powell et al., 1992; Chunha et
al., 2013; Jayadi et al., 2017), such as
scales covering the entire body (Kawabe
and Kohna, 2009), shifting habitat from
pelagic to benthic (Tucker, 1999), and
cannibalism (Jayadi et al., 2017). In this
study, behaviour of habitat preferences
and development of spines were similar
to the parental species and those of the
other grouper. At 61 d AH, the juveniles
backcross TGGG x GG reached 5 cm in
TL and showing the adult-like features.
At that stage, the juveniles exhibited
greater tolerance to va rious
environmental stress and can be used as
important indicator for transfer and
grading survivor (Kawabe and Kohno,
2009).
Major morphological deformities
and large-scale mortality were not
observed throughout the larvae and
juvenile rearing period of backcross
TGGG x GG. However, similar to other
grouper species, cannibalism is the main
factor responsible for the mortality in this
study. Cannibalism can be minimized by
feeding the fish well, weaning them as
soon as possible and grading the fish
regularly (Tucker, 2003). In the study by
Ruangpanit and Yashiro (1995), the
grading of fish is carried out once a week
to reduce cannibalism, a necessary
process which contributed to a 75%
survival rate.
This study concluded the first
record of backcross breeding in grouper
between TGGG and GG with remarkable
growth attained as fish has grown up to 1
kg in weight and reached nearly 30 cm in
total length within a year. This is an
important milestone achieved, especially
for grouper aquaculture. Even so,
survival rate remain as the main concern.
Others include the optimum rearing
condition and disease resistance which
requires further investigation to promote
better growth performance.

Acknowledgement
I thank Datuk Robert Tan and Bayu
Aquaculture Sdn. Bhd. for financing and
supporting this trial. My appreciation to
Ling Ming Woo and his team for
assistance in the trial and to Ong Fang
Sing for preparation of manuscript. I am
grateful to Associate Professor Dr.
Faihana Ching Fui Fui for her critical
comments on the manuscript.

References
Addin, M.A. and Senoo, S., 2011.
Production of hybrid groupers: spotted
grouper, Epinephelus polyphekadion x
tiger grouper, E.fuscoguttatus and
coral grouper, E.corallicola x tiger
grouper. In: International symposium
on grouper culture - technilogical
innovation and industrial development,
Taiwan.
Argue, B.J. and Dunham, R.A., 1999.
Hybrid Fertility, Introgression, and
Backcrossing in Fish, Reviews in
Fisheries Science, 7(3-4), 137-195. [ DOI: 10.18331/SFS2021.7.2.4 ]
[ Downloaded from sifisheriessciences.com on 2023-01-15 ]
11 / 14

60 Tan, Backcross breeding between TGGG hybrid grouper …
Argue, B.J., Liu, Z.J., Dunham, R.A.,
2003. Dress-Out and Fillet Yields of
Channel Catfish, Ictalurus Punctatus,
Blue Catfish, Ictalurus Furcatus, and
Their F1, F2 and Backcross Hybrids.
Aquaculture, 228, 81-90.
Bartlety, D.M., Rana, K. and Immunk,
A.J., 2001. The use of inter-specific
hybrids in aquaculture and fisheries.
Reviews in Fish Biology and Fisheries,
10, 325-337.
Boonlipatanon, P., Detsathit, S.,
Singhabun, A., 2002. Report of
natural spawning and larviculture of
tiger grouper, Epinephelus
fuscoguttatus (Forsskal, 1775), at
Krabi Coastal Aquaculture Station,
Thailand. Marine Finfifish
Aquaculture Newsletter. Network of
Aquaculture Centers in Asia-Pacifific
Publication, pp 1–3.
Ch’ng, C.L. and Senoo, S. 2008. Egg
and larval development of a new
hybrid grouper, tiger grouper
Epinephelus fuscoguttatus x giant
grouper Epinephelus lanceolatus.
Aquaculture Science, 56(4), 505-512.
Ching, F.F., Othman, N., Anuar, A.,
Shapawi, R. and Senoo, S., 2018.
Natural spawning, embryonic and
larval development of F2 hybrid
grouper, tiger grouper Epinephelus
fuscoguttatus x giant grouper
Epinephelus lanceolatus .
International Aquaculture Research,
10, 391-402.
Colin, P.L., Koenig, C.C. and Laroche,
W.A., 1996. Development from egg to
juvenile of the red grouper
(Epinephelus morio) (Pisces:
Serranidae) in the laboratory. In:
Arreguin-Sanchez, F., Munro, J.L,
Balgos, M.C. and Pauly, D. (eds.)
Biology, fisheries and culture of
tropical groupers and snappers.
ICLARM Conf. Proc. 48, 414 P.
Cunha, M.E., Re, P., Quental-Ferreira,
H., Gavaia, P.J. and
Pousao-Ferreira, P., 2013. Larval
and juvenile development of dusky
grouper Epinephelus marginatus
reared in mesocosms. Journal of Fish
Biology, 83, 448–465
De, M., Abdul Ghaffar, M., Bakar, Y.
and Das, S.K., 2016. Effect of
temperature and diet on growth and
gastric emptying time of the hybrid,
Epinephelus fuscoguttatus x
Epinephelus lanceolatus. Aquaculture
Reports, 4, 118-124.
FAO, 2017. FishStatJ, a Tool for Fishery
Statistics Analysis. FAO Fisheries and
Aquaculture Department, FIPS -
Statistics and information, Rome.
García-Ortega, A., Daw, A. and
Hopkins, K., 2013. Feeding
hatchery-produced larvae of the giant
grouper Epinephelus lanceolatus. In:
Rust, M.P., Olin, A., Bagwill and
Fujitani, M. (eds). Hatchery
Technology for High Quality Juvenile
Production: Proceedings of the 40th
U.S.- Japan Aquaculture Panel
Symposium, Honolulu, Hawaii,
October 22-23, 2012. U.S. Dept.
Commerce, NOAA Tech. Memo.
NMFS-F/SPO-136. pp. 36-42.
Glamuzina, B., Glavis, N., Skaramuca,
B., Kozul, V. and Tutman, P., 2001.
Early development of the hybrid
Epinephelus costae and Epinephelus
marginatus. Aquaculture, 198, 55-61. [ DOI: 10.18331/SFS2021.7.2.4 ]
[ Downloaded from sifisheriessciences.com on 2023-01-15 ]
12 / 14

Journal of Survey in Fisheries Sciences 7(2) 2021 61

Goncalves, I.B., Ahnesjo, I. and
Kvarnemo, C., 2011. The
relationship between female body size
and egg size in pipefishes. Journal of
Fish Biology, 78, 1847-1854.
Heemstra, P.C. and Randall, J.E., 1993.
FAO species catalogue. Vol. 16.
Groupers of the world (Family
Serranidae, Subfamily Epinephelinae).
An annotated and illustrated catalogue
of the grouper, rockcod, hind, coral
grouper and lyretail species known to
date. FAO Fisheries Synopsis, 125(16),
pp. 382.
Jayadi, Mallawa, A., Nessa, N.,
Djawad, I. and Ardiansyah, ??.,
2017. Growth patterns of camouflage
grouper (Epinephelus polyphekadion,
Bleeker, 1849) larvae. Journal of
Fisheries and Aquatic Science, 12,
12-21.
Kawabe, K. and Kohno, H., 2009.
Morphological development of larval
and juvenile blacktip grouper,
Epinephelus fasciatus. Fisheries
Science, 75, 1239–1251.
Kjørsvik, E., Mangor-Jensen, E. and
Holmefjord, I., 1990. Egg quality in
fishes. Advances in Marine Biology,
26, 71-113.
Koh, I.C.C., Shaleh, S.R.M. and Senoo,
S., 2008. Egg and larval development
of a new hybrid orange-spotted
grouper Epinephelus coioides x tiger
grouper Epinephelus fuscoguttatus.
Aquaculture Science, 56(3), 441-451.
Koh, I.C.C., Shaleh, S.R.M., Akazawa,
N., Ooota, Y., Senoo, S., 2010. Egg
and larval development of a new
hybrid orange-spotted grouper
Epinephelus coioides x giant grouper
Epinephelus lanceolatus. Aquaculture
Science, 58(1), 1-10.
Luan, G.H., Luin, M., Shapawi, R.,
Ching, F.F. and Senoo, S., 2016. Egg
development of backcrossed hybrid
grouper between OGGG (Epinephelus
coioides x Epinephelus lanceolatus)
and giant grouper (Epinephelus
lanceolatus). International Journal of
Aquatic Science, 7(1), 13-18.
Luin, M., .Fui, C.F. and Senoo, S.,
2013. Sexual maturation and gonad
development in tiger grouper
(Epinephelus fuscoguttatus) x giant
grouper (Epinephelus lanceolatus)
hybrid. Journal of Aquaculture
Research and Development, 5, 213.
Na-Nakorn, U., Rangsin, W. and
Boon-Ngam, J., 2004. Allotriploidy
increased sterility in the hybrid
between Clarias Macrocephalus and
Clarias Gariepinus. Aquaculture, 237,
73-88.
Othman, A.R., Kawamura, G., Senoo,
S. and Ching, F.F., 2015. Effects of
different salinities on growth, feeding
performance and plasma cortisol level
in hybrid TGGG (tiger grouper,
Epinephelus fuscoguttatus x giant
grouper, Epinephelus lanceolatus)
juveniles. International Research
Journal of Biological Sciences, 4(3),
15-20.
Park, J.Y., Han, K.H., Cho, J.K.,
Myeong, J.I. and Park, J.M., 2014.
Early osteological development of
larvae and juveniles in red spotted
grouper, Epinephelus akaara
(Pisces:Serranidae). Development and
Reproduction, 20(2), 87–707. [ DOI: 10.18331/SFS2021.7.2.4 ]
[ Downloaded from sifisheriessciences.com on 2023-01-15 ]
13 / 14

62 Tan, Backcross breeding between TGGG hybrid grouper …
Pomeroy, R.S., 2002. The status of
grouper culture in Southeast Asia.
SPC Live Reef Fish Information
Bulletin, (10), 22-26.
Powell, A.B. and Tucker, J.W.Jr., 1992.
Egg and larval development of
laboratory-reared nassau grouper,
Epinephelus striatus (Pisces,
Serranidae). Bulletin of Marine
Science, 50(1), 171-185.
Rahman, M.A., Arshad, A.,
Marimuthu, K., Ara, R. and Amin,
S.M.N., 2013. Inter-specific
hybridization and its potential for
aquaculture of fin fishes. Asian
Journal of Animal and Veterinary
Advances, 8(2), 139-153.
Rimmer, M.A. and Glamuzina, B.,
2017. A review of grouper (Family
Serranidae: Subfamily Epinephelinae)
aquaculture from a sustainability
science perspective. Reviews in
Aquaculture, 1–30.
Ruangpanit, N. and Yashiro, R., 1995.
A review of grouper (Epinephelus
spp.) and seabass (Lates calcarifer)
culture in Thailand. ln: Main, K.L.
and. Rosenfeld, C. (eds.) The Culture
of High- value Marine Fishes in Asia
and the United States. The Oceanic
Institute, Hawaii, pp. 167-183
Shapawi, R., Ching, F.F., Senno, S.
and Mustafa, S., 2018. Nutrition,
growth and resilience of tiger grouper
(Epinephelus fuscoguttatus) x giant
grouper (Epinephelus lanceolatus)
hybrid - a review. Reviews in
Aquaculture, 1-12.
Sui, J., Liu, Q., He, T., Xiao, Z.,, Xu, S.,
Ma, D., Xiao, Y., Lin F. and Li, J.,
2011. Analysis of early development
in first and backcross generation
between Paralichthys Olivaceus and
Paralichthys dentatus. African
Journal of Biotechnology, 10,
15438-15443.
Tucker, J.W.Jr., 1999. Species profile.
Grouper aquaculture. SRAC
Publication, pp. 721.
Tucker, J.W.Jr., 2003. Grouper Culture.
World Aquaculture, 34(3), 32-59.
Tymchuk, W.E. and Devlin, R.H., 2005.
Growth Differences among First and
Second Generation Hybrids of
Domesticated and Wild Rainbow
Trout (Oncorhynchus Myk iss).
Aquaculture, 245, 295-300.
Unuma, T., Kondo, S., Tanaka, H.,
Kagawa, H., Nomura, K. and Ohta,
H., 2004. Determination of the rates
of fertilization, hatching and larval
survival in the Japanese eel, Anguilla
japonica, using tissue culture
microplates. Aquaculture, 241,
345-356.
Wang, X., Ross, K.E., Saillant, E.,
Gatlin, D.M. and Gold, J.R., 2006.
Quantitative genetics and heritability
of growth-related traits in hybrid
striped bass (Morone Chrysops x
Morone Saxalitis). Aquaculture, 261,
535-545.
Xu, D.D., You, F., Li, J., Wu, Z.H.,
Xiao, Z.Z., Xhang, P.J., Xu, Y.L.
and Wang, B., 2011. First evidence
for hybrid breakdown in the backcross
of olive flounder, Paralichthys
olivaceus, and summer flounder,
Paralichthys dentatus. Journal of the
World Aquaculture Society, 42,
347-353.
[ DOI: 10.18331/SFS2021.7.2.4 ]
[ Downloaded from sifisheriessciences.com on 2023-01-15 ]
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