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.

2011 Blackwell Publishing Ltd, Aquaculture Research, 43, 12601275 1261

Aquaculture Research, 2012, 43, 12601275 Embryonic and larval development of black skirt tetra I Celik et al.


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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.

2011 Blackwell Publishing Ltd, Aquaculture Research, 43, 126012751262

Embryonic and larval development of black skirt tetra I Celik et al. Aquaculture Research, 2012, 43, 12601275


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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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do cardinal tetra, Paracheirodon axelrodi Schultz, 1956

(Characiformes: Characidae), em laboratorio. Boletim do

Instituto de Pesca, Sao Paulo32 (2), 151160.

Faustino F., Nakaghi L.S.O. & Neumann E. (2010) Bry-

con gouldingi (Teleostei, Characidae): Aspects of the

embryonic development in a new fish species with aquacul-

ture potential Zygote: pp. 1

13. Cambridge University

Press, doi:10.1017/S0967199410000535.

Finn R.N., Rnnestad I., van der Meeren T. & Fyhn H.J.

(2002) Fuel and metabolic scaling during the early life

stages of Atlantic cod Gadus morhua. Marine Ecology

Progress Series 24, 217234.

Frankel J.S. (2004) Inheritance of Trunk Banding in the

Tetra (Gymnocorymbus ternetzi Characidae). Journal of

Heredity 95 (2), 262264.

Fuiman L.A. (1983) Growth gradients in fish larvae.

Journal of Fish Biology23, 117123.

Fukuhara O. (1990) Effects of temperature on yolk utili-

zation, initial growth, and behaviour of unfed marine

fish-larvae. Marine Biology 106 (2), 169

174.Geerinckx T., Verhaegen Y. & Adriaens D. (2008) Onto-

genetic allometries and shape changes in the sucker-

mouth armoured catfish Ancistrus cf. triradiatus

Eigenmann (Loricariidae, Siluriformes), related to suck-

ermouth attachment and yolk-sac size. Journal of Fish

Biology 72, 803814.

Gisbert E., Merino G., Muguet J.B., Bush D., Piedrahita R.

H. & Conklin D.E. (2002) Morphological development

and allometric growth patterns in hatchery-reared

California halibut larvae. Journal of Fish Biology 61,

12171229.

Govoni J.J. & Forward R.B Jr (2008) Buoyancy. In: Fish

Larval Physiology (ed. by R.N. Finn & B.G. Kapoor), pp.

495

522. Science Publishers, Enfield, NH, USA.

Hall T.E. (2008) Pattern formation In: Fish larval physiol-

ogy, (eds.R.N. Finn & B.G. Kapoor) pp. 325. Science

Publishers, Enfield, New Hampshire, USA.

Hall T.E., Smith P. & Johnston I.A. (2004) Stages of

embryonic development in the Atlantic cod Gadus mor-

hua. J. Morphology 259, 255270.

Hanel R., Karjalainen J. & Wieser W. (1996) Growth of

swimming muscles and its metabolic cost in larvae of

whitefish at different temperatures. Journal of Fish Biol-

ogy 48, 937951.

Hunt von Herbing I. & Boutilier R.G. (1996) Activity and

metabolism of larval Atlantic cod (Gadus morhua)

from Scotian Shelf and Newfoundland source popula-tions. Marine Biology 124, 607617.

Huysentruyt F. & Adriaens D. (2005) Adhesive structures

in the eggs of Corydoras aeneus (Gill, 1858; Callich-

thyidae).Journal of Fish Biology 66, 871876.

Huysentruyt F., Moerkerke B., Devaere S. & Adriaens D.

(2009). Early development and allometric growth in

the armoured catfish Corydoras aeneus (Gill, 1858).

Hydrobiologia627, 4554.

Iwamatsu T. (1994) Stages of normal development

in the medaka Oryzias latipes. Zoological Science 11,

825839.

Kendall A.W., Ahlstrom E.H. & Moser H.G. (1984). Early

life history stages of fishes and their characters. In

Ontogeny and systematics of fishes: American Society of

Ichthyologists and Herpetologists, Special Publication

No. 1 (ed. by Moser H.G., Richards W.J., Cohen D.M.,

Fahay M.P., Kendall A.W. & Richardson S.L.), pp. 11

22. Allen Press Inc, Lawrence, Kansas, U.S.A.

Khan M.M.R. & Mollah M.F.A. (1998) Embryonic and

larval development of African catfish, Clarias gariepinus

(Burchell). Bangladesh Journal of Fisheries 21, 9197.

Kimmel C.B., Ballard W.W., Kimmel S.R., Ullman B. &

Schilling T.F. (1995) Stages of embryonic development

of the zebrafish.Developmental Dynamics 203, 253310.

Koumoundouros G., Divanach P. & Kentouri M. (2001)

Osteological development of Dentex dentex (Osteichth-

yes:Sparidae): dorsal, anal, paired fins and squamation.

Marine Biology 138, 399

406.Marimuthu K. & Haniffa M.A. (2007) Embryonic and lar-

val development of the striped snakehead Channa stria-

tus. Taiwania 52 (1), 8492.

Martell D.J., Kieffer J.D. & Trippel E.A. (2005) Effects of

temperature during early life history on embryonic

and larval development and growth in haddock.

Journal of Fish Biology66, 15581575.

Martinez G.M. & Bolker J.A. (2003) Embryonic and stag-

ing of summer flounder (Paralichthys dentatus). Journal

of Morphology 255, 162176.

Marty G.D., Hinton D.E. & Summerfelt R.C. (1995) Histo-

pathology of swimbladder noninflation in walleye (Stiz-

ostedion vitreum) larvae: role of development and

inflammation.Aquaculture 138, 35

48.

Meijide F.J. & Guerrero G.A. (2000) Embryonic and

larval development of a substrate-brooding cichlid

Cichlasoma dimerus (Heckel, 1840) under laboratory

conditions.Journal of Zoology 252 (4), 481493.

Mommsen T.P. (2001) Paradigms of growth in fish.

Comparative Biochemistry and Physiology B 129, 207

219.

Morioka S., Ito S. & Kitamura S. (2010) Growth and

morphological development of laboratory-reared larval

and juvenile snakeskin gourami Trichogaster pectoralis.

Ichthyological Research 57, 2431.

Moyle P.B. & Cech J.J. (2000) Fishes: An Introduction to

Ichthyology, Fourth Edition. Prentice-Hall, Upper SaddleRiver, NJ, 6978.

Nakatsuji T., Kitano T., Akiyama N. & Nakatsuji N.

(1997) Ice goby (Shiro-uo), Leucopsarion petersii, may

be a useful material for studying teleostean embryo-

genesis. Zoological Science 14, 443448.

Nandini S. & Sarma S.S.S. (2000) Zooplankton prefer-

ence of two species of freshwater ornamental fish

larvae. Journal of Applied Ichthyology 16, 282284.




15/16

Nelson J.S. (1994) Fishes of the world. Third edition. John

Wiley & Sons, Inc., New York. 600 p. Characidae).Jour-

nal of Heredity 95 (3), 262264.

Olivotto I., Holt S.A., Carnevali O. & Holt G. J. (2006)

Spawning, early development, and first feeding in the

lemonpeel angelfish Centropyge flavissimus. Aquaculture

253, 270

278.

Osse J.W.M., van den Boogaart J.G.M., van Snik G.M.J. &

van der Sluys L. (1997) Priorities during early growth

of fish larvae. Aquaculture 155, 249258.

Osse J.W.M. & van den Boogaart J.G.M. (1999) Dynamic

morphology of fish larvae, structural implications of

friction forces in swimming, feeding and ventilation.

Journal of Fish Biology 55 (Supplement A), 156174.

Osse J.W.M. & van den Boogaart J.G.M. (2004) Allo-

metric growth in Fish Larvae: Timing and Function.

In: The Development of Form and Function in Fishes and

the Question of Larval Adaptation, (ed. by J.J. Govoni),

pp. 167194. American Fisheries Society, Symposium

40, Bethesda, MD, USA.Onal U., Celik I. & Cirik S. (2010) Histological develop-

ment of digestive tract in discus, Symphysodon spp. Lar-

vae. Aquaculture International 18, 589601.

Pan X., Zhan H. & Gong Z. (2008) Ornamental expres-

sion of red fluorescent protein in transgenic founders

of white skirt tetra (Gymnocorymbus ternetzi). Marine

Biotechnology 10, 497501.

Papoutsoglou E.S. & Lyndon A.R. (2005) Effect of incu-

bation temperature on carbohydrate digestion in

important teleosts for aquaculture. Aquaculture

Research 36, 12521264.

Pelster B. (2004) The development of the swim bladder:

structure and performance. In: The Development of Form

and Function in Fishes and the Question of Larval Adapta-

tion (ed. by J.J. Govoni), American Fisheries Society Sym-

posium 40, 3746. Bethesda.

Pena R. & Dumas S. (2009) Development and allomet-

ric growth patterns during early larval stages of the

spotted sand bass Paralabrax maculatofasciatus (Percoi-

dei: Serranidae).Scientia Marina 73(Special issue), 183

189.

Perlberg S.T., Diamant A., Ofir R. & Zilberg D. (2008)

Characterization of swim bladder non-inflation (SBN)

in angelfish, Pterophyllum scalare (Schultz), and the

effect of exposure to methylene blue. Journal of Fish

Diseases 31, 215228.

Rahman M.R., Rahman M.A., Khan M.N. & Hussain M.G. (2004) Observation on the embryonic and larval

development of silurid catfish, gulsha (Mystus cavasius

Ham). Pakistan Journal of Biological Sciences 7 (6),

10701075.

Reynalte-Tataje D., Zaniboni-Filho E. & Esquivel J.R.

(2004) Embryonic and larvae development of pira-

canjuba,BryconorbignyanusValenciennes, 1849 (Pisces,

Characidae).Acta Scientiarum. Biological Sciences Maringa

26(1), 6771.

Richards W. J. & Leis J. M. (1984) Labroidei: develop-

ment and relationships. In Ontogeny and Systematics of

Fishes: American Society of Ichthyologists and Herpetolo-

gists. Spec. Publ. No. 1, (ed. by Moser H.G., Richards

W.J., Cohen D.M., Fahay M.P., Kendall A.W. & Rich-

ardson S.L.), pp. 542547. Allen Press Inc, Lawrence,

Kansas, USA.

Romagosa E., Narahara M.Y. & Fenerich-Verani N.

(2001) Stages of embryonic development of the

Matrnxa, Brycon cephalus (Pisces, Characidae). Bole-

tim do Instituto de Pesca, Sao Paulo 27 (1), 2732.

Saillant E., Chatain B., Fostier A., Przybyla C. & Fauvel C.

(2001) Parental influence on early development in the

European sea bass.Journal Fish Biology58, 15851600.

Savas E., Sener E. & Yldz M. (2006) Japon balklarnda

(Carassius sp.) embriyolojik ve larval gelismenin ince-

lenmesi. Istanbul Universitesi Vet erinerlik Faultesi Der gisi

32 (3), 719.

Silva L.V.F. (2004) Morphology and early development of

silver catfish, Rhamdia quelen, (Siluriforme, Pimelodi-dae) embryos and larvae. In: Physiology of Fish Eggs

and Larvae Symposium Proceedings, ( ed. by D. MacKin-

lay), 8994. International Congress on the Biology of

Fish Manaus, Brazil.

Stiassny M.L.J. & Mezey J.G. (1993) Egg attachment sys-

tems in the family Cichlidae (Perciformes: Labroidei),

with some comments on their significance for phyloge-

netic studies. American Museum Novitates3058, 111.

Takeshita N., Onikura N., Matsui S. & Kimura S. (1997)

Embryonic, larval and juvenile development of the

roughskin sculpin, Trachidermus jasciatus (Scorpaenifor-

mes: Cottidae). Ichthyological Research 44 (3), 257

266.

Tamaru C.S., Cole B., Bailey M.S.R. & Brown B.A.C.

(2001) A manual for commercial production of the tiger

barb, Capoeta tetrazona, a temporary paired tank spawner.

Center for Tropical and Subtropical Aquaculture Publi-

cation Number 129. Hawaii.

Trotter A.J., Pankhurst P.M. & Hart P.R. (2001) Swim-

bladder malformation in hatchery-reared striped trum-

peter Latris lineata (Latridae). Aquaculture 198, 4154.

Trotter A.J., Pankhurst P. M. & Battaglene S.C. (2004)

Morphological development of the swim bladder in

hatchery-reared striped trumpeter Latris lineata. Journal

of Applied Ichthyology 20, 395401.

Uma B. & Chandran M.R. (2008) Induction of Triploidy

in Gymnocorymbus Ternetzi (Boulenger). Research Jour-nal of Fisheries and Hydrobiology3 (2), 4147.

Unal H. & Aral O. (2006) Copcu balklar (Corydoras

spp.) ve yetistiriciligi. Journal of Fisheries and Aquatic

Sciences 23(1-2), 311318.

Watson C.A., ChapmanF.A. (2002). Artificial incubation of

fish eggs. Fact Sheet FA-32, Institute of Food and

Agricultural Science, University of Florida Exten-

sion. Available at http://edis.ifas.ufl.edu/pdffiles/FA/

FA05100.pdf (accessed 03 February 2011).




16/16

Webb J. (1999)Larvae in fish development and evolution.

In The Origin and Evolution of Larval Forms(ed. by B.K.

Hall & M.H. Wake), pp. 109158. Academic Press,

San Diego, CA, USA.

Wood C.M. & Mc Donald D.G. (1996) Global warning:

Implications for freshwater and marine fish. Society for

Experimental Biology Seminar Series 61. Cambridge Uni-

versity Press, Cambridge, pp. 177223.

Zilberg D., Ofir R., Rabinski T. & Diamant A. (2004)

Morphological and genetic characterization of swim-

bladder non-inflation in angelfish Pterophyllum scalare

(Cichlidae).Aquaculture 230, 1327.



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