desarrollo embrionario - pez monja- gymnocorymbus ternetzi.pdf
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Embryonic and larval development of black skirt tetra
(Gymnocorymbus ternetzi,Boulenger, 1895) under
laboratory conditions
Ihsan Celik1, Pnar Celik1, Sukran Cirik1, Mert Gurkan2 & Sibel Hayretdag2
1 Department of Aquaculture, Fisheries Faculty, Canakkale Onsekiz Mart University, Canakkale, Turkey2Department of Biology, Faculty of Science, Canakkale Onsekiz Mart University, Canakkale, Turkey
Correspondence: I Celik, Department of Aquaculture, Fisheries Faculty, Canakkale Onsekiz Mart Universi ty, Terzi oglu Campus,
17100 Canakkale, Turkey. E-mail: celik_ihsan@ yahoo.com
Abstract
The embryonic and larval development of black
skirt tetra, Gymnocorymbus ternetzi, are described
under controlled laboratory conditions. In addition,
major histomorphological changes and the allomet-
ric growth patterns during larval development have
been described. The laboratory-reared broodstock,
that is 1 year of age, were spawned. Hatching
occurred 2021 h after spawning at 24 0.5C.
The cleavage was finished in 2 h and the early blas-
tula stage occurred at 2:04 hours after spawning.
The gastrulation started at 3:20 hours and 30%
epiboly was observed at 3:34 hours after spawning.
Eight-somite stage was observed at 08:33 hours.And embryonic developmental stage was completed
at 21 h after spawning. The newly hatched larvae
were 1442 14.3 lm in mean total length (TL).
The mouth opened at 3 days after hatching (DAH).
The yolk sac had been totally absorbed and the
larvae started to swim actively within 34 days.
Notochord flexion began at 11 DAH. The metamor-
phosis was completed and the larvae transformed
into juveniles at 32 DAH. In this paper, the full
developmental sequence from egg to juvenile of
G. ternetziis described for the first time.
Keywords: Gymnocorymbus ternetzi, embryonic
development, larval development, morphological
characteristics, allometric growth
Introduction
Characidae is a family of freshwater subtropical
and tropical fish, found in southwestern Texas,
Mexico, Central and South America and it is a
large family that comprises about 152 genera and776 species (Nelson 1994). The black skirt tetra
(Gymnocorymbus ternetzi) is just one of many fish
in the group of tetras, Characins, is traded in the
ornamental fish industry. It is a popular species in
the trade of freshwater ornamental fish, since it is
attractive in appearance, undemanding in mainte-
nance and easily bred (Frankel 2004; Uma &
Chandran 2008). Information on embryonic and
larval development of fish is a fundamental key
which enables a closer approach to their biology
and taxonomy (Reynalte-Tataje, Zaniboni-Filho &
Esquivel 2004). Morphological features are very
important as they furnish information of life his-tory of fish and they provide critical parameters to
hatchery production (Martinez & Bolker 2003;
Silva 2004). Early life history characters of fish
can be used in assessing phylogenetic relationships
(Richards & Leis 1984; Stiassny & Mezey 1993;
Britz 1997; Meijide & Guerrero 2000)). In addi-
tion, studies on embryonic and larval development
of any fish species can be useful in directing the
husbandry efforts of fish breeder to the specific
state and requirements of each development
stage (Marimuthu & Haniffa 2007). There is vast
literature on embryonic and larval stages of fish,distributed among the fields of aquaculture,
applied ecology, behavioural ecology, biological
oceanography, comparative functional morphology
and physiology, fisheries science, limnology and
systematic ichthyology (Takeshita, Onikura,
Matsui & Kimura 1997; Webb 1999; Arvedlund,
McCormick & Ainsworth 2000; Borges, Faria, Gil,
Goncalves & Almada 2003; Martell, Kieffer &
2011 Blackwell Publishing Ltd1260
Aquaculture Research, 2012, 43, 12601275 doi: 10.1111/j.1365-2109.2011.02930.x
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Trippel 2005; Marimuthu & Haniffa 2007; Du,
Wang, Jiang, Liu, Wang, Li & Zhang 2010). How-
ever, detailed study about the embryonic and lar-
val development of characins is scarce. In
addition, information is lacking concerning ontog-
eny of black skirt tetra from egg to juvenile. In thepresent study, the embryonic and larval develop-
ment of laboratory-reared black skirt tetra (G.
ternetzi) from egg to juvenile are described in
detail for the first time. In addition, major histo-
morphological changes and the allometric growth
patterns during larval development have been
identified.
Materials and methods
Broodstock maintenance
One-year-old black skirt tetras (G. ternetzi) were
used as broodstock in the experiment. They were
fed with commercial ornamental fish feeds (Tetr-
amin Granulat, Tetra, Germany; Protein: 46%, Oil:
12%, Fibre: 3%, Ash: 11%, Moisture: 8%), three
times a day. During broodstock culture, water
temperature, pH and conductivity were monitored
daily at 24 0.5C, between 6.0 and 6.5 and
between 100 and 200 lS respectively. Water
temperature was controlled with additional sub-
merged heaters. The photoperiod was maintained
at 9L/15D by fluorescent lighting (lights on;
07:00
18:00 hours). Broodstocks were kept in40 L glass aquariums. Three pairs (3 males/3
females) were randomly selected from broodstock
tank and were placed into a 15 L spawning tank
late in the afternoon. Spawning was observed the
next day around dawn and lasted 13 h. Eggs and
larvae were obtained from three pairs of brood-
stocks.
Observations and measurements of embryos and
larvae
Fertilized eggs were collected immediately after
spawning and maintained at 24 0.5C. Some of
them were transferred into a beaker (500 mL) forembryonic development observations. The others
were maintained in 15 L aquaria at 24 0.5C.
Eggs were observed from spawning to hatching
under an Olympus BX51 research microscope
(Hatagaya, Shibuya-ki, Tokyo, Japan) and photo-
graphed using a colour video camera (Q Imaging,
Micropublisher 3.3 RTV, Burnaby, BC, Canada).
Embryonic development stages were identified
according to Kimmel, Ballard, Kimmel, Ullman
and Schilling (1995).
Larvae were fed once a day with Artemia sp.
(INVE Aquaculture Inc., Dendermonde, Belgium)
until the end of the experiment at 32 days after
hatching (DAH). They were randomly sampled
(n = 5) daily from hatch to 18 DAH and at 1-day
interval from 18 to 32 DAH. These specimens were
observed under an Olympus SZX7 zoom stereomi-
croscope, photographed by a colour video camera
and measured using image analysis program (Q
Capture Pro, version 5.1.1.14, Dendermonde, Can-
ada). On the other hand, they were used for obser-
vations on general morphology and for the
following morphometric measurements (mm): body
depth (BD), eye diameter (ED), head length (HL),
pre-anal length (PAL), Pre-anal myomer length(PrAM), post-anal myomer length (PoAM), snout
length (SnL), tail length, total length (TL), trunk
length (Fig. 1) Larval developmental stages were
identified according to Kendall, A.W., Ahlstrom
and Moser (1984) and differentiated into four peri-
ods I: yolk-sac larva, II: preflexion larva, III: flexion
larva and IV: postflexion larva.
Figure 1 Morphometric characters measured in the black skirt tetra larvae.
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Allometric growth patterns were calculated as a
power function of TL (Fuiman 1983) with the
exponent and intercept obtained from linear regres-
sions on log-transformed data (Gisbert, Merino,
Muguet, Bush, Piedrahita & Conklin 2002). The al-
lometric equation Y = aXb
of BD, ED, HL, PAL,PrAM, PoAM, SnL, tail length and trunk length on
TL was estimated. Here Y is the dependent variable
(measured character), X is the independent vari-
able (TL), a is the intercept and b is the growth
coefficient. When isometric growth occurred,
b = 1, a positive allometric growth occurred when
b > 1 and a negative one when b < 1.
Histological observations
For histological evaluations, larvae were randomlycollected (n = 10) daily from hatch (0 DAH) to 10
and every 2 days from 10 to 32 DAH. These speci-
mens were fixed in Bouins solution and 70% alco-
hol, dehydrated through a series of alcohol
concentrations, cleared in xylene and embedded in
(a) (b) (c)
(d) (e) (f)
(g) (h) (i)
(j) (k) (l)
(m) (n) (o)
(p) (r) (s)
Figure 2 The stages of embryonic development Gymnocorymbus ternetzi: (a) 2-blastomere stage; (b) 4-blastomere
stage; (c) 8-blastomere stage; (d) 16-blastomere stage; (e) 32-blastomere stage; (f) early blastula stage; (g) late blas-
tula stage; (h) early gastrula stage; (i) 30% epiboly; (j) 50% epiboly; (k) 75% epiboly; (l) 8-somite stage; (m) 11-
somite stage; (n) 13-somite stage; (o) otic capsule; (p) muscular effect; (q) otolith appearance; (r) hatching, 3 h after
hatching. Developmental stages were determined by comparison with standard zebrafish embryonic stages as
described by Kimmel et al. (1995). Scale bars, ar: 500 micron, s: 1mm.
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paraffin wax. Wax blocks were cut using a micro-
tome (Slee, Cut5062, Germany) at 5lm. Sagittal
sections were stained with Gills haematoxylin/
eosin (HE) procedures for general histology. Sec-
tions were observed under a light microscope
(Olympus BX50) to describe the larval developmentand photographed using a colour video camera.
Results
Embryonic development
The eggs were adhesive, demersal and spherical in
shape. The eggs ranged in diameter from 930.23
to 1063.95 lm, with a mean of 977.36
45.86 lm (n = 19). The egg capsule was transpar-
ent, while the yolk was brownish. The cleavage
of eggs was meroblastic and the first cleavage
(two-celled stage) occurred within 0:30 hours after
spawning (Fig. 2a). Blastodisc divided to form two
equal cells. The second cleavage occurred 0:43
hours and four blastomeres are clearly observed
(Fig. 2b). Blastodisc divided via meridional cleav-
age to form four equal cells The third and fourth
cleavages define 8 and 16 respectively (Fig. 2c
and d). The eggs cleaved into 8 and 16 cells
respectively. The third cleavage is horizontal and
results in a 2 9 4 array (Fig. 2c). The forth cleav-
ages occur in two separate planes, cleavage furrow
parallel to second cleavage plane and results in a
4 9 4 array (Fig. 2d). Eight and 16 cell stages
were observed at 0:50 hours and 1:04 hours
respectively (Fig. 2c and d). The fifth cleavage
took place after 1:10 hours from spawning
(Fig. 2e). Blastoderm divided via meridional cleav-
age into 32 cells and the 32 blastomeres arealready formed. The cells became smaller and were
arranged irregularly. The early blastula stage
occurred at the vegetal pole 2:04 hours after
spawning (Fig. 2f). At this stage, the crowded cells
expanded over the yolk and the blastomeres were
divided asynchronously. The late blastula stage
consists of a multicellular blastomere (Fig. 2g) and
fully completed at approximately 2:303:00 hours.
The gastrulation started at 3:20 hours after
spawning (Fig. 2h). Blastoderm cells spread over
the yolk and epibolic cells increased at this stage.
The embryo reached 30% epiboly at 3:34 hours
after spawning and the blastoderm covered 30% of
the yolk (Fig. 2i). 50% and 75% epiboly stages
were completed at 4:10 hours and 5:30 hours
respectively (Fig. 2j and k). The segmentation
stage was characterized by the sequential forma-
tion of the somites and lasted till just prior to
hatching. Eight-somite stage in black skirt tetra
was observed in the central part of the embryo at
08:33 hours (Fig. 2l). Eleven pairs of somites
formed at 09:00 hours and the number of somites
from stage 11 to stage 13 increased within 1 h
(Fig. 2m and n). The formation of the otic capsule
Table 1 Embryonic development stages of Gymnocorymbus ternetzi at 24 0.5C
Main stages Substages Time (h:min) Description Figure
Zygote 2 cells 0:30 First cleavage, blastodisc divided via meridional
cleavage to form two equal cells
1a
4 cells 0:43 Second cleavage, dividing the blastodisc into 4 blastomeres 1b
8 cells 0:50 Third cleavage 1c
16 cells 1:04 Fourth cleavage, 16 blastomeres can be seen 1d
32 cells 1:10 Fifth cleavage 1e
Blastula Early Blastula 2:04 Blastomeres continued to divide but they were less
synchronously
1f
Late Blastula 2:26 Epibolic cells increase 1g
Gastrula Early Gastrula 3:20 Blastoderm cells begin to spread over the yolk 1h%30 Epiboly 3:34 Germ ring epiboled 1/3 of yolk sac 1i
%50 Epiboly 4:10 Germ ring epiboled 1/2 of yolk sac 1j
%75 Epiboly 5:30 75% coverage of the yolk cell by the blastoderm 1k
Segmentation 8 Somite 8:33 1l
11 Somite 9:00 1m
13 Somite 10:01 1n
Pharyngula Otic capsule 13:15 Otic capsule formed 1o
Muscular effect 15:30 Embryo begins to spin 1p
P re-hatching s tage 18:35 The embry o shows conspic uous m usc ular contract ions 1q
Hatching 3 h after hatching 24:00 Pre-larva is 3 h after hatching 1r
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started at 13:15 hours and embryo began to spin
at 15:30 hours after spawning (Fig. 2o and p).
The eye development and brain differentiation
(forebrain, midbrain and hindbrain) has taken
place (Fig. 2q). Hatching rates were 8590% in
aquarium at 20 h after spawning. The embryonicdevelopment completed at 21 h (Table 1).
(a)
(b)
(c)
(d)
(e)
(f)
Figure 3 Larval development of Gymnocorymbus terne-
tzi. (a) Post-hatching stage (7 h); (b) yolk-sac stage (1
DAH); (c) yolk-sac stage, the gas bladder was formed but
not completely filled (2 DAH); (d) opened-mouth stage
(3 DAH); (e) preflexion larva, exogenous feeding (5
DAH); (f) preflexion larva (7 DAH). Scale bars =1 mm.
(a)
(b)
(c)
(d)
(e)
(f)
Figure 4 Larval development of Gymnocorymbus terne-
tzi. (a) Flexion stage, Notochord flexion started (11
DAH); (b) flexion stage, the notochord was completely
flexed (12 DAH); (c) postflexion larva, swim bladder
with two chambers was visible (17 DAH); (d) postflex-
ion larva (19 DAH); (e) postflexion larva (26 DAH); (f)
end of metamorphosis (30 DAH). Scale bars (fig. a, b,
c, d, e) =1 mm; Scale bar (fig. f) = 500lm.
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Larval Development
Morphological observations
Newly hatched larvae
Newly hatched larvae in the post-hatching stagewere laterally compressed and initially elongated.
The TL of newly hatched larvae was
1442 14.3 lm. The mouth was closed and the
yolk sac was 30% of the total body length
(Fig. 3a). Two otoliths which were like black dots
within the otic vesicles were visible (Fig. 3a). The
body of the newly hatched larvae was transparent
but pigmentation has started in the posterior part
of the yolk sac (Fig. 3a). The eyes were still unpig-
mented.
1DAH (TL: 3.03 0.02 mm)
The mouth and anus were closed and the undiffer-
entiated alimentary tract appeared as a straight
tube (Fig. 3b). Eyes were not pigmented and sev-
eral stellate melanophores were scattered over the
surface of body and the yolk sac. The primordial
fin fold was well developed in the sagittal plane
but no fins were differentiated (Fig. 3b). The yolk
sac was ovoid and 20% the total body length
(Fig. 3b).
2 DAH (TL: 3.50 0.09 mm)
The yolk sac has become smaller (12% the TL)
(Fig. 3c). Initial inflation was observed; the oval-
shaped swim bladder was first seen in 2 DAH. Pig-
mentation has increased over the eyes and the
body but they are still translucent. Black melano-
phores were scattered on the head region, ventral
and dorsal side of the body (Fig. 3c). The urinary
bladder is visible and seen near the anus. The pri-
mordial fin was slightly differentiated but, no anal
and dorsal fins were differentiated but pectoral fin
bud was present (Fig. 3c). The larvae could not
swim actively but short periods of swimming were
observed.
34 DAH (TL: 3.64 0.124.03 0.06 mm)
At 3 DAH, the mouth and anus opened (Fig. 3d).
The yolk sac has been completely absorbed and
Figure 5 The main events of larval development in black skirt tetra ( Gymnocorymbus ternetzi).
y= 3.0053e0.0531x
R2 = 0.9694, n= 112
0
5
10
15
20
25
30
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34
Age (DAH)
Totallength(mm)
Yolk sac Preflexion Postflexion
Flexion
Juvenile
Figure 6 Growth of black skirt tetra larvae from hatch to 32 DAH. Each point represents the mean total
length SD.
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the larvae started to swim actively at 34 days.
The larvae started to feed exogenously within
3 days at 24 1C. The eyes were pigmented.
The larvae have a one-chambered swim bladder.
The notochord end is not flexed (Fig. 3d).
57 DAH (TL: 4.29 0.074.37 0.05 mm).
The eyes became very prominent and were fully
pigmented (Fig. 3e). Second inflation of swim
bladder did not occur. It formed as a single cham-
ber, increased in size and extended posteriorly. The
larvae have still primordial fins (Fig. 3e and f).
The notochord end was not flexed (Fig. 3e and f).
The larvae could swim very well. Pigmentation
has increased on the head and lateral parts of the
body, black pigments were dominant, but yellow
pigments were also present (Fig. 3f).
11
12 DAH (TL: 4.97 0.15
5.78 0.23 mm).
Primordial fin was still present (Fig. 4a). Pectoral
fins were well developed. Dorsal and anal fins have
begun early differentiation (Fig. 4a and b). The
caudal-fin rays begin to form. At 11 DAH, the
notochord end was slightly flexed but flexion is
more obvious at 12 DAH. Swim bladder increased
in size and extended posteriorly (Fig. 4b). The lar-
vae could swim very well. There were clusters of
pigment over the body but pigmentation was more
concentrated on head region (Fig. 4b).
1517 DAH (TL: 5.75 0.166.09 0.27 mm).
Second inflation of swim bladder occurred between
15 DAH and 17 DAH. Swim bladder with two
chambers completely filled (Fig. 4c). Anal and dor-
sal fins begin to develop but have no rays but cau-
dal fin rays were more developed (Fig. 4c). Body
shape and pigmentation pattern were not similar
to the adult fish. The stomach of larvae contained
food, ventral region of larvae was swollen and
orange.
1926 DAH (TL: 7.83 0.8211.67 1.37 mm).
At 1922 DAH, dorsal and anal fins have differen-
tiated (Fig. 4d and e). Adipose fin began to form
between the dorsal and caudal fins at 22 and 23
DAH. Pigmentation has increased over the body
but the ventral trunk region was still translucent
and food particles (Artemia) could be seen in the
digestive tract. The adipose fin was more obvious
at 25 and 26 DAH (Fig. 4e). Dorsal and anal fins
were more developed with the separated rays and
caudal fin was forked (Fig. 4e). Body depth was
more than triple that of the previous stage and the
body shape of larvae has approached an adult
shape.
3032 DAH (TL: 14.67 0.9220.40 1.30 mm).
The body shape of larvae and pigmentation pat-tern were similar to those of the adult (Fig. 4f).
The body was almost completely covered with pig-
ment (Fig. 4f). Larvae have a dark grey to silver
body with black vertical bars but black and grey
pigments were dominant. Two characteristic black
vertical bars were visible on posterior side of the
gills (Fig. 4f). Morphological metamorphosis was
completed and the larvae had completely trans-
formed into juveniles. The main events during
larval development of black skirt tetra are summa-
rized inFig. 5.
Figure 7 Growth coefficients of head, trunk and tail
length during larval development stage. Each graph
represents the growth coefficients during a total length
(TL) interval.
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y= 0.3783x1.1261
R2= 0.9807, n= 107
02468
10121416
0.00 5.00 10.00 15.00 20.00 25.00 0.00 5.00 10.00 15.00 20.00 25.00
0.00 5.00 10.00 15.00 20.00 25.000.00 5.00 10.00 15.00 20.00 25.00
0.00 5.00 10.00 15.00 20.00 25.00
Total length (mm)
Taillength(mm)
y= 0.6101x0.9197
R2= 0.9808, n= 107
02468
1012
Total length (mm)
PAL(mm)
y= 0.3635x0.9329
R2= 0.9611, n= 107
0
2
4
6
8
10
Total length (mm)
PrAM(
mm)
y= 0.0296x1.2008
R2= 0.8903,n= 112
00.20.40.60.8
11.21.4
Total length (mm)
SnL(mm
)
y= 0.4388x0.9477
R2= 0.9732, n= 107
02468
1012
Total length (mm)
PoAM(
mm)
Figure 9 Allometric growth equations and relationship between five body segments and total length in black skirt
tetra during larval development period (from hatch to 32 DAH). PAL, Pre-anal length; PrAM, Pre-anal myomer
length; PoAM, Post-anal myomer length; SnL, snout length.
y= 0.4333x0.8191
R2= 0.9391, n= 107
0123456
Total length (mm)
Trunklength(mm)
y= 0.1644x1.1588
R2= 0.9525, n= 112
0
1234567
0.00 5.00 10.00 15.00 20.00 25.00
0.00 5.00 10.00 15.00 20.00 25.00 0.00 5.00 10.00 15.00 20.00 25.00
0.00 5.00 10.00 15.00 20.00 25.00
Total length (mm)
H
eadlength(mm)
y = 0.0639x1.1215
R2= 0.9737,n= 112
0
0.5
1
1.5
2
2.5
Total length (mm)
Ey
ediameter(mm)
y= 0.1124x1.3751
R2= 0.9584, n= 112
0
2
4
6
8
10
Total length (mm)
Bodydepth(mm)
Figure 8 Allometric growth equations and relationship between four body segments and total length in black skirttetra during larval development period (from hatch to 32 DAH).
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Allometric growth
Growth of the black skirt tetra larvae followed an
exponential curve during the larval stages and is
represented by the equation y = 1.79e0.051x
(R2
= 0.97, n = 112) where y is total length (TL)mm and x is DAH (Fig. 6). Four larval development
stages were observed after hatching; yolk-sac
larvae, preflexion larvae, flexion larvae and postflex-
ion larvae. The yolk sac has been completely con-
sumed at 4 DAH, when TL was 4.03 0.14 mm.
Notochord has been flexed between 10 DAH and
12 DAH, at 5.34 0.57 mm. All the meristic char-
acters were completely developed and juvenile stage
(a)
(b)
(c)
Figure 10 Sagittal sections of black skirt tetra larvae.
(a) 2 DAH (Olympus BX51 1009), (b) 3 DAH (Olym-
pus BX51 409), (c) 4 DAH (Olympus BX51 409). at,
alimentary tract; e, eye; ga, gill arches; l, liver; n, noto-
chord; oe, oesophagus; ph, pharynx; s, stomach; sb,
swim bladder; t, teeth; ys, yolksac.
(a)
(b)
(c)
Figure 11 Sagittal sections of black skirt tetra larvae.
(a) 16 DAH (Olympus SZX7 zoom stereo microscope
209), (b) 24 DAH (Olympus SZX7 zoom stereo micro-
scope 12.5x), (c) 32 DAH (Olympus SZX7 zoom stereo
microscope 89). df, dorsal fin rays; e, eye; g, gill; ga,
gill arches; gl, gill lamellae; i, intestine; l, liver; m,
mouth; n, notochord; oe, oesophagus; ph, pharynx; s,
stomach; sb, swim bladder; sb1, first chamber of swim
bladder; sb2, second chamber of swim bladder; t, teeth.
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started at 32 DAH, TL was 20.40 2.25 mm at
32 DAH.
In the yolk-sac stage, the head, trunk and tail
length had negative allometric growth in relation
to TL (b = 0.41, b=0.02, b = 0.25 respectively)
(Fig. 7). During the preflexion stage, they stillshowed negative allometric growth (b = 0.45,
b = 0.39, b = 0.15 respectively) (Fig. 7). The head,
trunk and tail length were positively allometric in
the flexion stage (b = 2.43, b = 3.29, b = 2.21
respectively) (Fig. 7). In the postflexion stage,
growth of trunk length was negatively allometric
(b = 0.87), while growth in the head and tail
length were positively allometric (b = 1.16,
b = 1.5 respectively) (Fig. 7).
Allometric growth equations between nine mea-
sured body segments and total length during lar-
val development stage (032 DAH) are presented
(Figs 8 and 9). Growth of trunk in length was
negatively allometric from hatch to 32 DAH
(a = 0.43, b = 0.82, R2 = 0.94, n = 107), while
the growth coefficients of HL, ED and BD were pos-
itively allometric (a = 0.16, b = 1.16, R2 = 0.95,
n = 112; a = 0.06, b = 1.12, R2 = 0.97, n = 112
and a = 0.11, b = 1.38, R2 = 0.96, n = 112
respectively) (Fig. 8).
The characters PAL and PrAM showed negative
allometry (a = 0.61, b = 0.92, R2 = 0.98, n = 107
and a = 0.36, b = 0.93, R2 = 0.96, n = 107
respectively), while tail length and SnL exhibited
positive allometric growth (a = 0.38, b = 1.13,R2= 0.98, n = 107 and a = 0.03, b = 1.20,
R2 = 0.98, n = 112 respectively) (Fig. 9). PoAM
showed isometric allometric growth (a = 0.44,
b = 0.95, R2 = 0.97, n = 107).
Histological observations
At 2 DAH; the mouth was closed, the alimentary
tract was distinct as a straight tube. The yolk sac
has become smaller (Fig. 10a). The swim bladder
was formed and initial inflation was observed at 2
DAH (Fig. 10a). At 3 DAH; the yolk was not
totally consumed. The mouth and anus were open
(Fig. 10b). Gill lamellae were observed in filaments
carried by gill arches (Fig. 10b). The swim bladder
increased in size and extended posteriorly. Larvae
began to feed exogenously before complete resorp-
tion of the yolk sac (Fig. 10b). 4 DAH; yolk has
been completely consumed (Fig. 10c). The larvae
were capable of feeding on Artemia and there was
presence of food material in the stomach. The
swim bladder with one chamber increased in size.
Eye pigment was concentrated and opaque. The
liver could be seen on the ventral side of the swim
bladder (Fig. 10c). Four pairs of gill arches with
filaments were obvious (Fig. 10c). The swim blad-
der increased in size and extended posteriorly andsecond inflation of swim bladder in larvae
occurred between 15 and 18 DAH (Fig. 11a). No
histological difference was observed between the
anterior intestine and the posterior intestine
(Fig. 11a). 24 DAH; the dorsal and anal fin rays
formed. The swim bladder with two chambers
could be seen (Fig. 11b). 3032 DAH; Metamor-
phosis was completed and the larvae completely
transformed into juveniles. Large sized food parti-
cles were observed in the stomach and intestine
(Fig. 11c). The body depth increased.
Discussion
In this study, the embryonic and larval develop-
ment of the laboratory-reared black skirt tetra (G.
ternetzi) are described. For the first time, the full
developmental sequence from egg to juvenile in
controlled aquarium conditions is also stated. In
addition, allometric growth of some body parts
was studied. Embryonic development lasted 21 h
and larval development lasted about 3032 days
at 24 0.5C.
Egg size is an important consideration for egg
and larval quality during incubation and rearingin aquaculture. The average diameter of most
ornamental fish eggs are around 0.8 mm, how-
ever, the size range is wide (Watson & Chapman
2002). Egg diameters of some aquarium fish were
reported as; 0.4 mm for gobies (Watson & Chap-
man 2002), 0.740.90 mm for Hyphessobrycon ser-
pae (Characidae) (Cole & Haring 1999), 0.9 mm
for Microgeophagus ramirezi (Cichlidae) (Coleman &
Galvani 1998), 1.1 mm for Symphysodon discus
(Cichlidae) (Coleman & Galvani 1998), 1.01.6 mm
for Symphysodon spp. (Celik 2008), 4.0 mm for
Tropheus moori (Cichlidae) (Coleman & Galvani
1998), 2.9 mm for Cyathopharynx fucifer (Cichli-
dae) (Coleman & Galvani 1998), 1.65 0.5 for
Cichlasoma dimerus (Cichlidae) (Meijide & Guerrero
2000), 1.18 0.05 mm for Capoeta tetrazona (Cyp-
rinidae) (Tamaru, Cole, Bailey & Brown 2001),
1.41.6 mm for Carassius auratus (Cyprinidae)
(Savas, Sener & Yldz 2006), 0.75 mm for Puntius
conchonius (Cyprinidae) (Bhattacharya, Zhang &
Wang 2005), 0.7 mm for Danio rerio (Cyprinidae)
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(Kimmel et al. 1995), 1.47 0.20 mm for Corydo-
ras aeneus (Callichthyidae) (Huysentruyt & Adria-
ens 2005), 1.799 0.0214 mm for Corydoras
paleatus (Callichthyidae) (Unal & Aral 2006), 1.5
2.0 mm for some ornamental catfish (Watson &
Chapman 2002) and from 0.89 0.97 mm to1.03 0.06 mm for Trichogaster pectoralis(Osphro-
nemidae) (Morioka, Ito & Kitamura 2010). The egg
size and fecundity depend on several factors, for
example broodstock age, broodstock size, feed and
water quality. The variety of reproductive strate-
gies of fish can cause great differences among
species in the number of eggs, egg size (Andrade-
Talmelli, Kavamoto, Romagosa & Fenerich-Verani
2001) but the eggs of a fish species are in a com-
mon size range. The eggs of black skirt tetra are
spherical, adhesive, demersal and have approxi-
mately 0.98 0.05 mm average diameter. The
number of eggs per spawn, per female was around
150200 and fertilization rate was about 90%.
In most fish species the blastomeres are regular
in size and shape (Hall 2008). In the black skirt
tetra, first five cleavages divided the blastodisc into
32 equal-sized blastomeres at the animal pore and
horizontal cleavage occurred between 64 and 128
cell stages (after the fifth divison). In the zebrafish
Danio (Brachydanio) rerio (Kimmel et al. 1995), in
the Atlantic cod Gadus morhua (Hall, Smith &
Johnston 2004; and in the Cichlasoma dimerus
(Meijide & Guerrero 2000) the first horizontal
cleavage occurs at the sixth cleavage, between the32 and the 64 cell stages. In the medaka Oryzias
latipes, it occurs between the 16 and 32 cell stages
(Iwamatsu 1994). It occurs even earlier in the
Holostean fish Amia calva (between the 8 and the
16 cell stages) (Ballard 1986; Nakatsuji, Kitano,
Akiyama & Nakatsuji 1997). and in the ice goby
Leucopsarion petersii (between the 4 and the 8 cell
stages) (Nakatsuji et al. 1997). Theoretical knowl-
edge of embryonic development stages might be
useful for incubation management with regard to
environmental variables, thus larvae malformation
and low productivity in captivity can be prevented
(Alves & Moura 1992). Furthermore, the studies
on embryonic and early larval development are
important to the successful rearing of larvae for
large-scale seed production and aquaculture (Khan
& Mollah 1998; Koumoundouros, Divanach &
Kentouri 2001; Borcato, Bazzoli & Sato 2004;
Rahman, Rahman, Khan & Hussain 2004). In
addition, it was reported that information on egg
characteristics was important for the fitness of lar-
vae (Saillant, Chatain, Fostier, Przybyla & Fauvel
2001).
Early blastula was observed 2:04 hours later.
Teleost gastrulation was morphologically charac-
terized by the presence of a germ ring (Arezo,
Pereiro & Berois 2005). In this study, gastrulationwas observed at 3:20 hours and 30% epiboly
began 3:34 h. G. ternetzi embryo reached the
eight-somite stage at 8:33 hours and reached the
pre-hatching stage at 18 h with the otic capsule,
head, primordial fin, tail. All the embryos had
hatched after 2122 h after the fertilization at
24 0.5C. It was reported that small differences
in temperature ( 2C) was important on larval
survival of lemonpeel angelfish Centropyge flavissi-
mus (Olivotto, Holt, Carnevali & Holt 2006). This
rule is the same for G. ternetzi larvae and for many
ornamental fish. G. ternetzi can spawn between
23C and 30C, eggs were obtained from adult
broodstock maintained at 24 0.5C in this
study. So, the water temperature was kept con-
stant during larval rearing (24 0.5C). Fish
embryos and larvae are generally more sensitive
to temperature change than older fish (Wood &
Mc Donald 1996). It is known that temperature
affects growth (Hunt von Herbing & Boutilier
1996; Wood & Mc Donald 1996; Mommsen 2001;
Martell et al. 2005), metabolic activity, embryonic
and larval mortality (survival) (Hanel, Karjalainen
& Wieser 1996; Bermudes & Ritar 1999; Martell
et al. 2005), energy utilization (Finn, Rnnestad,van der Meeren & Fyhn 2002), yolk-sac consump-
tion (Fukuhara 1990), enzyme activity (Papout-
soglou & Lyndon 2005) on embryonic and larval
development in fish. For example, while G. ternetzi
eggs hatch within 2021h after fertilization at
24 0.5C, the incubation time can be shorter at
28C (1617 h). On the other hand, most of the
eggs and larvae died under 22C and above 30C.
Minimum, maximum and optimum temperature
levels for growth and survival of G. ternetzi larvae
must be determined by future studies.
At hatching, the larva was 1.44 mm in total
length. The larva reached a size of 1420 mm
between 30 and 32 days and larval development
had completed. Eggs and larvae are not guarded
by the parents; within the first 3 days of hatching,
the larvae were inactive but short periods of swim-
ming were observed. They started swimming freely
within 34 days. On the other hand, it was
reported that G. ternetzi larvae hatched 2024 h
after spawning and were free-swimming 4872 h
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after hatching at 24C (Frankel 2004). While
many marine fish larvae had two kinds of energy
reserves, yolk and oil globule (Bjelland & Skiftesvik
2006), black skirt tetra has only yolk sac. The
yolk sac is depleted within 34 days and the lar-
vae start to feed exogenously before completeabsorption of the yolk sac. Mouth opening was
formed on the third day. Compared to other fresh-
water ornamental fish species (Nandini & Sarma
2000), larvae ofG. ternetzi have small mouth and
consume a small size range of prey. So, rotifer and
infusoria must be preferred as first feed. In this
study, infusoria that is the smallest of live foods
for fish larvae was used for first food until 7 DAH.
Black skirt tetra larvae can catch and eat Artemia
at 5 DAH, so Artemia nauplii has been used from
5 DAH to 32 DAH.
There are two types of swim bladders, physost-
omous and physoclistous (Moyle & Cech 2000;
Trotter, Pankhurst & Battaglene 2004; Govoni &
Forward 2008). According to Moyle and Cech
(2000), characins that include black skirt tetras,
cyprinids, salmonids, pike, catfish, mormyrids and
eels are fish species with physostomous swim blad-
der. Physostomous swim bladders are connected to
the alimentary tract and physostomous larvae
inflate their swim bladder with atmospheric air
(Moyle & Cech 2000; Trotter et al. 2004; Govoni
& Forward 2008; Perlberg, Diamant, Ofir & Zilberg
2008). In this study, the swim bladder was first
discernible at 2 DAH. Larvae could not start free-swimming and anus was closed at that time. Mor-
phological and histological findings indicated that,
the swim bladder was filled with a little air or
fluid. It was reported that larvae inflate the swim
bladder with gas from the digestion of organic
material in the gut. Although this has been ruled
out, it is possible (Pelster 2004). In larval culture,
swim bladder inflation requires special attention as
it affects feeding activity (Onal, Celik & Cirik
2010). It was reported that swim bladder inflation
coincided with yolk sac depletion and the start of
feeding activity in most species such as discus
(Symphysodonspp.,), Nile tilapia (Oreochromis niloticus),
Mozambique tilapia (Oreochromis mossambicus), Dover
sole, Solea solea and striped trumpeter, Latris line-
ata (Boulhic & Gabaudan 1992; Marty, Hinton &
Summerfelt 1995; Trotter, Pankhurst & Hart
2001; Onal et al. 2010). In contrast, it was
reported that yolk depletion and the start of feed-
ing activity did not appear to correlate distinctly
with swimbladder inflation in some species such as
freshwater angelfish (Pterophyllum scalare) (Zilberg,
Ofir, Rabinski & Diamant 2004), zebrafish (Danio
rerio) (Kimmel et al. 1995) and black skirt tetra
(present study). The timing of inflation in black
skirt tetra larvae was earlier than in many other
species; for example, in discus, D. Rerio, O. mos-sambicus, Stizostedion vitreum, Latris lineata, swim
bladder inflates at 45 DAH, 5 DAH, 79 DAH,
612 and 1120 DAH respectively (Boulhic &
Gabaudan 1992; Marty et al. 1995; Trotter et al.
2001; Onal et al. 2010). In contrast, inflation in
freshwater angelfish occurred at 12 DAH (Zilberg
et al. 2004).
In the present study, the morphological develop-
ment and allometric growth patterns in the black
skirt tetra larvae were studied. The allometric
growth formula is the most widely used method
of analysis for relative growth during early
larval development (Osse & van den Boogaart
2004; Pena & Dumas 2009). Teleostean larval
period was characterized by a high degree of allo-
metric growth patterns (Fuiman 1983; Osse, van
den Boogaart, van Snik & van der Sluys 1997;
Geerinckx, Verhaegen & Adriaens 2008). These
patterns can contribute to aquaculture and fisher-
ies management by characterizing normal growth
patterns (Pena & Dumas 2009). Allometric
growth during larval development was studied in
different teleost groups (Osse & van den Boogaart
2004). But allometric growth of many ornamental
fish has not been reported. We described the allo-metric growth patterns of G.ternetzi larvae from
hatching to day 32. The growth coefficients of
head, trunk and tail during larval periods (Period
I: yolk-sac larva, period ii: preflexion larva, period
iii: flexion larva, period iv: postflexion larva) were
similar to results that have been reported in
other teleosts (Osse & van den Boogaart 1999;
Geerinckx et al. 2008; Huysentruyt, Moerkerke,
Devaere & Adriaens 2009). The allometric changes
chronology would be related to the chronology of
important early life history events (Huysentruyt
et al. 2009) and positive allometry of head and tail
length during this period reflects the early priority
to develop organs related to vital functions such as
feeding and swimming (Osse & van den Boogaart
2004).
In conclusion, our findings indicated that black
skirt tetra eggs are demersal, adhesive and their
larvae are altricial. Hatching occurred after an
incubation period of 2022 h at 24 0.5C.
The cleavage pattern of G.ternetzi is the same as
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