Early development and allometric shifts during the ontogeny of a marine catfish

(Cathorops spixii-Ariidae)

By A. R. A. Lima1,2, M. Barletta1,2, D. V. Dantas1,2, F. E. Possato1, J. A. A. Ramos1,2 and M. F. Costa1,2

1Laboratory of Ecology and Management of Estuarine and Aquatic Ecosystems, Department of Oceanography, Federal Universityof Pernambuco, Recife, Pernambuco, Brazil; 2Instituto de Ecologia e Gerenciamento de Ecossistemas Aquaticos (IEGEA), Recife,Pernambuco, Brazil

Summary

This study assessed whether the developmental series of theariid Cathorops spixii (Agassiz, 1829) is related to growthpatterns during its early ontogeny. The main morphological

events of C. spixii were studied from the newly neurula embryo(6.99±0.69 mm TL) to juveniles (53.38±14.43 mm TL) inorder to characterize and corroborate patterns of ontogenetic

allometries. Prior to hatching, embryos were well-developed,with an ossified axial and appendicular skeleton. Embryosgrew slowly, but positive allometric growth was observed in

head width (b1 = 1.65) and eye diameter (b1 = 1.59). Thisseems to be related to the fast development of sensory organssuch as otoliths, Weberian apparatus, lenses, nostrils and

barbels during the embryonic period when eggs are under thecare of adult males. After hatching, mouth-brooding free-embryos grew horizontally isometric, except for the snoutlength that presented quick growth related to the end of

endogenous feeding (b1 = 1.73). Slow growth was observed inhead width (b1 = 0.44) and eye diameter (b1 = 0.26), takinginto account that sensory organs are formed in free-embryos.

The end of the yolk-sac period was characterized by a directchange from free-embryo to juvenile, without a true larvalperiod. Juveniles are characterized by growth patterns nearly

isometric in all body regions, suggesting that they already bearmost of characteristics of adult fish. The quick growth ofmorphometric variables that are related to sensorial organsbefore hatching and the increase in horizontal growth after the

first 6 weeks (hatched free-embryos) reflect developmentalpriorities during the earliest stages where important sensorialorgans are being developed for juvenile survival strategies.

Introduction

The yellow catfish Cathorops spixii (Agassiz, 1829) inhabitsshallow coastal waters and brackish estuaries, seeking outlagoons and river mouths for spawning (Acero, 2002). They

are distributed along the northeastern coast of South America,from Guiana to Brazil (Marceniuk and Menezes, 2007). Thisspecies belongs to the Order Siluriformes – Family Ariidae,which is characterized by the presence of the Weberian

apparatus that allows catfishes to have a better perception ofsounds and consequently a good adaptation to turbid waters(Rosen and Greenwood, 1970; Sanger and Mccune, 2002).

After spawning, the males incubate fertilized eggs in theirmouths until a young juvenile is developed (Rimmer andMerrick, 1983; Rimmer, 1985). A report for a tropical estuary

shows that C. spixii eggs develop to the hatching stage within

54 days at a temperature range of 29–33�C (Dantas et al.,2010).Research on systematics and phylogeny (Kailola, 2004;

Marceniuk and Menezes, 2007; Betancur-R., 2009), ecology(Barletta et al., 2005, 2008; Dantas et al., 2010), biology(Barbieri et al., 1992, Favaro et al., 2005) and ontogeny

(Merriman, 1940; Bamford, 1948; Rimmer and Merrick,1983; Rimmer, 1985; Menon et al., 1989) of Ariidae specieshas been expanding in recent years owing to their importance

to the environment and traditional communities (Barletta andCosta, 2009). Such studies are important not only to describemorphological adaptations that a species may develop toreduce vulnerability, but also to understand how different

developmental periods utilize the available habitats and whatare the requirements to complete their life cycle (Barletta-Bergan et al., 2002; Brown et al., 2004).

However, little is known about the ontogeny of C. spixii.This paper presents an overview concerning the earliestdevelopmental stages of this species in order to assess whether

its development is related to growth patterns as well as tocorroborate patterns of ontogenetic allometries.

Materials and methods

Specimens of C. spixii were collected in the Goiana Riverestuary (Northeast Brazil – 7�32¢–7�35¢S; 34�50¢–34�58¢W)

from 2005 to 2009. Fish samples were taken from three areas(upper, middle and lower) of the main channel by otter trawlnet following the methodology proposed by Barletta et al.

(2005, 2008). Eggs, free-embryos and juveniles were collectedfrom the oral cavity of the mouth-brooding adult malesprincipally in the upper reaches of the estuary during the late

dry season with water temperatures varying from 29 to 33�Cand salinity reaching almost 0 (Dantas et al., 2010). Theestimated age in terms of days after fertilization followed the

proposed by Tilney and Hecht (1993) for the ariid Galeichthysfeliceps Valenciennes, 1840, taking into account that theauthors found a similar mouth-brooding period reported byDantas et al. (2010) for C. spixii in the Goiana River estuary.

Embryos were anesthetized using tricaine methanesulfonate(MS 222) and stored in 4% buffered formalin.For the analyses, 80 eggs, 60 free-embryos and 55 juveniles

were used. C. spixii development was described following thehierarchy of intervals proposed by Balon (1990). The embry-onic period comprises the egg stage (Ø < 1 cm), ranging from

a newly neurula streak-shaped embryo to hatching (<2.3 cmTL). The yolk-sac period (>2.3–3.5 cm TL), characterized by

J. Appl. Ichthyol. 28 (2012), 217–225� 2011 Blackwell Verlag, BerlinISSN 0175–8659

Received: September 30, 2010Accepted: August 26, 2011

doi: 10.1111/j.1439-0426.2011.01903.x

U.S. Copyright Clearance Centre Code Statement: 0175–8659/2012/2802–0217$15.00/0

Applied IchthyologyJournal of

the nutritional contribution of the yolk-sac, ends whenexternal feeding is initiated. The juvenile period (>3.5–

8.2 cm TL), immediately after the yolk-sac total consumption,is characterized by the beginning of autonomous feeding.Digital measurements were made with the aid of a digital

camera (Canon-Powershot G10) attached to a trinocularstereo microscope (ZEISS-STEMI 2000-C) and the softwareAXIOXIOVISIONISION Release 4.7.2 (image capturer calibrated with amillimeter scale in all micrometer zooms that converts the

image pixels in millimeter) for small specimens. A digitalcaliper (799 Starrett ⁄ range: 6 ⁄ 150 mm) was used for largerspecimens (>2.3 cm TL). The morphometric variables mea-

sured were: total length (TL), eye diameter (ED), snout length(SNL), pre-pectoral length (PPL), pre-dorsal length (PDL),pre-pelvic length (PVL), pre-anal length (PAL), head length

(HL), head width (HW) (Fig. 1a,b). The angle (a�) between thebody axis and the upper lip surface was measured in allspecimens (Fig. 1c). Meristic data (number of hard and softrays of pectoral, dorsal, pelvic, anal and caudal fins; and the

number of pre- and post-anal myomeres) were also counted.The ontogenetic series was analyzed by clearing and staining toassure transparency of tissues revealing skeletal characters and

patterns of ossification (Dingerkus and Uhler, 1977; Potthoff,1984).Allometric growth was calculated as a power function of TL

according to the model Y = b0 TLb1 + � (Huxley, 1924).Linearization of the model was performed on log-transformeddata resulting in regressions curves of the type log Y = log

b0 + b1 log TL + log �, where Y is the dependent variable,TL the independent variable, b0 the intercept and b1 the slopeor growth coefficient. In isometric growth, the slope b1 is 1.When the slope b1 is smaller than 1, it is known as negatively

allometric; when higher, positively allometric (vanSnik et al.,1997). F-tests were performed to verify differences in growth

patterns between embryonic and yolk-sac periods; and yolk-sac and juvenile periods (Sokal and Rohlf, 1995).

Results

Embryonic period

Cathorops spixii eggs are spherical and with a diameter of8 ± 0.71 mm. The embryo is located on a large yolk masslocated in the center of each egg. This period was subdivided infive ontogenetic stages:

Stage I: Otic vesicle formation and notochord in pre-flexion:

±10–26 days. Embryos are 6.99 ± 0.69 mm TL and thenotochord is in pre-flexion (Fig. 2a). V-shaped myomeres are

present (Fig. 2a). Optic vesicles are recognizable. Otic vesiclesappear, but lack otoliths. Forebrain, midbrain and hindbrainare well-defined (Fig. 2a). Four branchiostegal arcs areobserved. The median fin is present. There are no skeletal

structures (Fig. 3a). The mouth is absent. Maxillary barbelbuds appear. The head angle (a�) has 12.89 ± 5.41�, indicat-ing that the snout is in the ventral position.

(a)

(b) (c)

Fig. 1. Morphometric variables. (a) TL, total length; ED, eye diam-eter; SND, snout length; PDL, pre-dorsal length; PPL, pre-pectorallength; PVL, pre-pelvic length; PAL, pre-anal length; HL, head length.(b) HW, head width. (c) a�, head angle

(a)

(b)

(c)

(d)

(e)

(f)

Fig. 2. Ontogenetic stages of embryonic period, C. spixii. ch, chorion;df, dorsal fin; ea, otic vesicle (ear); ey, optic vesicle (eye); fb, forebrain;fr, fin rays; ba, branchiostegal arcs; hb, hindbrain; l, lens; mb,midbrain; mi, myomeres; mt, mental barbel; mx, maxillary barbel; nc,notochord; o, operculum; ot, otolith; pf, pectoral fin; ys, yolk-sac.Scale bars: 1 mm. Arrow (fl) indicates moment of hatching

218 A. R. A. Lima et al.

Stage II: Anlage of skeletal structures and notochord flexion:

±27–31 days. Embryos are 8.3 ± 0.73 mm TL and thenotochord is in flexion (Figs 2b and 3b). The brain is furtherdeveloped (Fig. 2b). The operculum is developing. Maxillary

barbels elongate. The anlage of cartilaginous structuresappears at the head (Fig. 3b). Lenses begin to form. Thepectoral fin bud protrudes. The head angle is 31.11 ± 3.19�,indicating that the migration of the snout begins before mouthformation.

Stage III: Skeletal formation and mouth development: ±32–

42 days. Embryos are 11.8 ± 0.47 mm TL and notochord is

in post-flexion. The mouth appears. Single nostrils are present.The head angle increases to 37.43 ± 6.25�. Lenses are formed.Otic vesicles are developed, but otoliths remain absent

(Fig. 3c). The operculum and branchiostegal arcs are partiallydeveloped. Mental barbels appear. Cartilaginous structuresappear to initiate the skeletal formation. The anlage of the

Weberian apparatus appears as a bud (Fig. 3c). Pectoral finshave one hard and 4–5 soft rays (Table 1). Dorsal fin lacks

soft rays, but has a hard ray in formation. Caudal fin has 14–18 rays (Table 1). Hypural and para-hypural bones initiatetheir formation (Fig. 3a). Neural and haemal spines appear

(Fig. 3c).

Stage IV: Vertebrae formation and otolith appearance: ±43–

54 days. Embryos are 14.3 ± 0.43 mm TL. Myomereschange to W-shaped (Fig. 2d). Otoliths appear as conglom-

erates of small granules (Figs 2d and 3d). Head angle is60.92 ± 8.19�. The notochord begins to be replaced by bonyvertebrae. Neural and haemal spines are ossifying (Fig. 3d).

The Weberian apparatus, pectoral and dorsal fins areossifying (Fig. 3d and Table 1). The hard rays are stillflexible. Pelvic and anal fins are cartilaginous (Fig. 3d andTable 1). The cartilaginous caudal fin has hypural and para-

hypural bones formed (Fig. 4d). A cartilaginous epural bone

Fig. 3. Ontogenetic shifts in ossifica-tion patterns, C. spixii. (a–e) Stages Ito V, embryonic period; (f) newly-hatched embryo; (g) free-embryo; and(h) juvenile. afr, anal fin rays; ba,branchiostegal arc; cfr, caudal fin rays;d, dentary bone; dfr, dorsal fin rays;dfs, dorsal fin spines; ef, sphenoticbone; ep, epural bone; et, lateral eth-moid bone; fr, frontal bone; hs, haemalspine; hy, hypural bones; m, maxilla;met, mesethmoid bone; nc, notocordns, neural spine; ot, otolith; pd, pre-dorsal plate; pfr, pectoral fin rays; pfs,pectoral fin spine; phy, parahypuralbones; pm, pre-maxillary plate; pto,pterotico; sp, supraocciptal process; vt,vertebrae; w, Weberian apparatus

Development and growth of C. spixii 219

appears. The number of soft rays of pectoral (10), dorsal (7),and pelvic (6) fins do not vary in the following stages

(Table 1).

Stage V: Bifurcation and ossification of caudal fin and hatching:

± 55–75 days. Embryos are 20.33 ± 1.87 mm TL. Headbones are ossifying (Fig. 3e). Head angle is 88.04 ± 8.08�.Otoliths increase. Vertebrae and Weberian apparatus areossified (Fig. 3e). The premaxillary tooth plate appears.

Neural and haemal spines, the dentary bone (Fig. 3e), pelvicand anal fins are ossifying (Fig. 3e). The caudal fin bifurcates

(Fig. 2e). In larger specimens at this stage the dentary bonesare ossified (Fig. 3f). Hypural and para-hypural bones and softrays of the caudal fin initiate the ossification process (Fig. 3f).

At the end of this stage hatching occurs (Fig. 2f).

Free-embryo stage: ±75–100 days (yolk-sac period). Free-embryos (Fig. 6a) are 27.24 ± 3.57 mmTL. Nostrils separated

Fig. 3. (Continued)

220 A. R. A. Lima et al.

by a narrow septum. Pigmentation visible in newly-hatchedembryos. Head bones recognizable (Fig. 3g). Maxillary barbelsoverreach pectoral fin base. Premaxillary tooth plates well-

developed and dentary bone is ossified (Fig. 3g). Hatchedfree-embryos have a large yolk-sac and underdeveloped fins,whereas highly developed fins present only a trace of yolk-sac

and are almost completely developed. Head angle reaches114.822 ± 19.38�. Upper lip surface moved to a rostralposition (Fig. 5a). As the head angle is increasing, the yolk-

sac weight diminishes, emphasizing that autonomous feedingmust begin (Fig. 5b). At 30 mm TL, food particles started tobe observed in the stomach, marking the onset of exogenous

feeding.

Juvenile stage: ±100–140 days. Juveniles are densely pig-mented and 53.38 ± 14.43 mm TL. Head angle does notvary much (163.88 ± 4.76�) with TL. Soft and hard rays of

pectoral and dorsal fin, epural, hypural and para-hypuralbones as well as the axial skeleton are ossified (Fig. 3h).Head bones are fully differentiated (Fig. 3h). Mouth-

brooded juveniles (>3.5–4 cm TL) resemble most character-istics of free-embryos (Fig. 6b), whereas free-swimmingjuveniles (>4 cm TL) resemble characteristics of adult fish(Fig. 6c).

Growth patterns

Body proportions related to horizontal growth showedpatterns varying from negatively allometric (b1 < 1) to nearlyisometric (b1 » 1) (Fig. 4c–g). Pre-pectoral length (PPL)

growth differed between embryos and free-embryos(b1 = 0.43 and 0.93, respectively), and grew near isometry injuveniles (b1 = 0.91) (Fig. 4c and Table 2). Pre-dorsal length(PDL) growth was negatively allometric and did not differ

among periods (b1 = 0.81, 0.96 and 0.94) (Fig. 4d andTable 2). Pre-pelvic length (PVL) and head length (HL)growths differed among periods (Table 2), growing slowly in

embryos (b1 = 0.69 PVL and 0.75 HL) and nearly isometric infree-embryos (b1 = 1.17 PVL and 1.05 HL). During thejuvenile period HL grew relatively slowly (b1 = 0.90) and PVL

grew nearly isometric (b1 = 0.97). PAL growth was slow inembryos (b1 = 0.71), differing from the isometric pattern offree-embryos (b1 = 1.04), which in turn presented a similar

growth to that of juveniles (b1 = 1.06).

Eye diameter (ED) and head width (HW) growth differedamong periods, changing from fast growth (b1 = 1.59 ED and1.65 HW) in embryos to very slow patterns in free-embryos

(b1 = 0.26 ED and 0.45 HW) and accelerating again to near-isometric in juveniles (b1 = 0.95 ED and 1.16 HW) (Fig. 4hand Table 2). Snout length (SNL) showed accelerated growth

rates and did not differ among periods (Fig. 4b and Table 2).

Discussion

Cathorops spixii, as many other catfish species, hatches at anadvanced ontogenetic stage featuring a fully developed

juvenile (Merriman, 1940; Rimmer and Merrick, 1983;Rimmer, 1985; Menon et al., 1989; Tilney and Hecht, 1993;Geerinckx et al., 2007). This precocious development can beattributed to a large yolk mass and a long incubation time

under the care of mouth-brooding males (Rimmer, 1985;Tilney and Hecht, 1993). Its early ontogeny supports the ideathat a true larval period is absent, described by Balon (1990)

as a precocial (or direct) development. Examples from theliterature are the clariid Clarias gariepinus (Osman et al.,2008), the loricariid Ancistrus cf. triradiatus (Geerinckx et al.,

2007) and the ariid Galeichthys feliceps (Tilney and Hecht,1993).Studies on the ontogeny of both cranial and postcranial

skeleton of catfishes (Bamford, 1948; Menon et al., 1989;

Adriaens and Verraes, 1998) revealed that, in general,embryos form a well-developed chondocranium, but patternsof ossification are observed only at hatching such as in

C. gariepinus (Adriaens and Verraes, 1998), A. cf. triradiatus(Geerinckx et al., 2007) and Corydoras aeneus (Huysentruytet al., 2008). In C. spixii, however, the anlage of cartilaginous

skeletal structures appears during the second ontogeneticstage and patterns of ossification of the axial and appendic-ular skeleton are already noted long before hatching, such as

reported for Bagre marinus (Merriman, 1940), Tachysurusthalassinus (Menon et al., 1989) and G. feliceps (Tilney andHecht, 1993).Sensory organs of C. spixii were also reported to have a

fast development even during the embryonic period. Largeotoliths, lenses, nostrils, maxillary and mental barbels andthe Weberian apparatus are well recognizable in embryos

and they are completely developed before hatching. Similarpatterns were observed in G. feliceps, where the brain

Fig. 3. (Continued)

Development and growth of C. spixii 221

regions, otoliths, olfactory placodes (nostrils) and bran-chiostegal arcs form 22–23 days after fertilization (Tilney

and Hecht, 1993). However, in C. gariepinus, sensory organsstart to develop later in newly hatched larvae, different fromthat normally observed in ariids (Mukai et al., 2008; Osman

et al., 2008).The ontogeny of C. spixii is also marked by shifts in the

angle between the body axis and the upper lip surface, whichincreases while the fish grows and yolk-sac reduces. These

changes may be due to the need of a rostral mouth to initiatethe exogenous feeding when parental care is finished. For thisreason, a few shifts in the head angle were observed in the

feeding juveniles while they grow. In A. cf. triradiatus, thesame angle between the upper lip surface of the suckermouthand body axis decreases while the yolk-sac is reduced

(Geerinckx et al., 2008). This pattern differs significantlyfrom that observed for C. spixii, because the sub-terminalmouth migrates in loricariid catfishes from a rostral positionto a ventral position, which allows them to attach in the

substrata.During early ontogeny C. spixii body proportion growth

rates changed considerably. During the embryonic period head

width and eye diameter grew quickly and morphometricvariables related to horizontal growth showed slow growthpatterns. The head width and eye diameter grew very slowly in

free-embryos, whereas the horizontal growth rates were nearlyisometric. However, juveniles grew nearly isometrically in allbody regions. It is suggested that C. spixii embryos use a large

energy supply for the rapid development of sensory organssuch as the eyes, otic vesicle, and consequently otoliths at thehead, and that free-embryos, which already have developedsensory organs, must use the energy supply for horizontal

growth. At the end of the free-embryo stage the snout lengthgrowth showed a strongly accelerated pattern related to thetransition from endogenous to exogenous feeding. Similarly,

embryos of the suckermouth armoured catfish A. cf. triradi-atus showed quick growth in head width and snout length,although morphometric variables related to horizontal growth

grew nearly isometrically in both embryos and free-embryos(Geerinckx et al., 2008). Also, the snout length in free-embryosshowed a quick growth related not to shifts in feedingbehavior, but to the need of suckermouth attachment

(Geerinckx et al., 2008).The growth patterns exhibited by the yellow catfish

matched developmental events observed during the early

ontogeny of this species. The quick growth of sensorymorphometric variables at initial stages and the increase inhorizontal growth after the first 6 weeks possibly reflect

developmental priorities during early development whenimportant organs are being developed for juvenile survival.Such analysis may provide a framework of functional shifts

in developing fish, useful for both comparative studies of theontogeny with other species as well as for ecologicalapplications.

Acknowledgements

Authors acknowledge financial support from Conselho Nac-

ional de Desenvolvimento Cientıfico e Tecnologico (CNPq)through grants (Proc. 500267 ⁄ 2007-3, 552896 ⁄ 2007-1,482921 ⁄ 2007-2; CT-Hidro 29 ⁄ 2007 ⁄ CNPq Nº

552896 ⁄ 2007-1), Fundacao de Apoio a Pesquisa do Estadode Pernambuco (FACEPE) through grants (Proc. APQ-0586-1.08 ⁄ 06). Thanks to F. A. Sedor (Museu de CienciasT

able

1Meristicfrequency

ofC.spixiiontogenetic

stages

Ontogenetic

stages

Estim

atedagein

term

sofdaysafter

fertilization(Tilney

andHecht,1993)

Incubation

temperature

N�ofmyomeres

(range

and

mean±

SD)

N�ofhard

andsoftrays,

pectoralfin

N�ofhard

andsoftrays,

dorsalfin

N�ofsoft

rays,pelvic

fin

N�ofsoft

rays,anal

fin

N�ofsoft

rays,caudal

fin

Embryonic

period

Pre-anal

Post-anal

StageI(n

=30)

±10–26

29–33�C

18–21

18.8

±0.66

27–29

27.2

±0.91

––

––

–

StageII

(n=

10)

±27–31

29–33�C

18–20

19.1

±0.57

26–32

28.1

±1.59

––

––

–

StageIII(n

=10)

±32–42

29–33�C

18–19

18.2

±0.42

26–27

26.4

±0.52

I⁄4–5

I–

–14–18

StageIV

(n=

10)

±43–54

29–33�C

15–17

16±

0.47

26–27

26.3

±0.48

I⁄10

I⁄7

619–22

22–26

StageV

(n=

20)

±55–75

29–33�C

15–17

16.3

±0.57

25–27

26±

0.51

I⁄10

I⁄7

622–25

31–46

Free-em

bryos(n

=60)

±75–100

29–33�C

14–19

16.7

±1.68

23–29

25.7

±1.97

I⁄10

I⁄7

623–25

43–60

Juveniles

(n=

55)

±100–140

29–33�C

*(>

3.5–4cm

TL)

14–15

14.5

±0.5

27–29

27.9

±0.68

I⁄10

I⁄7

621–25

48–62

Hard

rays=

Romannumerals,softrays=

Arabic

numerals.

*Length

rangeformouth-bredjuveniles

222 A. R. A. Lima et al.

Naturais, Universidade Federal do Parana - UFPR) forshowing the clearing and staining technique. Additional

thanks are addressed to the anonymous referees who revisedthe first draft of this study. MB and MFC are CNPq fellows.

0

1

2

3

4

5

6

SNL

(b)

0

4

8

12

16

20

24

PDL

(d)

(f)

(h)

0

1

2

3

4

5

ED

(a)

02468

10121416

0 10 20 30 40 50 60 70 80 90

HL

(g)

Total length (mm)

05

1015202530354045

PAL

0

2

4

6

8

10

12

14

PPL

(c)

0

5

10

15

20

25

30

35

PVL

(e)

0

3

6

9

12

15

0 10 20 30 40 50 60 70 80 90

HW

β1 = 1.59r2 = 0.93

β1 = 0.26r2 = 0.17

β1 = 0.95r2 = 0.89 β1 = 1.27

r2 = 0.81

β1 = 1.73r2 = 0.42

β1 = 1.27r2 = 0.88

β1 = 0.43r2 = 0.73

β1 = 0.93r2 = 0.80

β1 = 0.91r2 = 0.94

β1 = 0.81r2 = 0.89

β1 = 0.96r2 = 0.82

β1 = 0.94r2 = 0.97

β1 = 0.69r2 = 0.91

β1 = 1.17r2 = 0.91

β1 = 0.97r2 = 0.98

β1 = 0.71r2 = 0.94

β1 = 1.06r2 = 0.98

β1 = 1.04r2 = 0.92

β1 = 0.75r2 = 0.94

β1 = 1.05r2 = 0.76

β1 = 0.90r2 = 0.96

β1 = 1.65r2 = 0.91

β1 = 0.44r2 = 0.64

β1 = 1.16r2 = 0.92

Fig. 4. Relationships of morphometric variables with total length (TL) for embryos (h), free-embryos (s) and juveniles (4). (a) ED, eyediameter; (b) SNL, snout length; (c) PPL, pre-pectoral length; (d) PDL, pre-dorsal length; (e) PVL, pre-pelvic length; (f) PAL, pre-anal length; (g)HL, head length; (h) HW, head width. Arrows indicate moment of hatching and yolk-sac depletion, respectively. Growth coefficients [slope (b1)]and r2 values of morphometric variables presented for each stage

020406080

100120140160180

0 10 20 30 40 50 60 70 80 90

αº

(a)

0.00

0.05

0.10

0.15

0.20

0.25

0.30

0 10 20 30 40 50 60 70 80 90

YSD

(b)

Total length (mm)

Fig. 5. Scatter plots of angle between upper lip surface and body axis (a�) (a) and yolk sac depletion (YSD) (b) of C. spixii regressed with TL forembryos (h), free-embryos (s) and juveniles (4). Arrows (fl) indicate moment of hatching and total yolk-sac consumption, respectively

Development and growth of C. spixii 223

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Table 2Significance values of regression slope(b1) (in relation to TL) comparison ofmorphometric variables betweenembryonic and yolk-sac periods andyolk-sac and juvenile periods inC. spixii

Variables

Embryo and yolk-sac periods Yolk-sac and juvenile periods

F-test F-test

ED F1,134 64.4195*** F1,109 56.8992***SNL F1,134 2.5259NS F1,109 3.7752NS

PPL F1,95 44.1289*** F1,109 0.0917NS

PDL F1,95 3.7498NS F1,109 0.1386NS

PVL F1,95 59.7367*** F1,109 15.4451***PAL F1,95 44.5753*** F1,109 0.3804NS

HW F1,134 65.0952*** F1,109 79.7347***HL F1,95 14.9013*** F1,109 4.3870*

ED, eye diameter; SNL, snout length; PPL, pre-pectoral length; PDL, pre-dorsal length; PVL, pre-pelvic length; PAL, pre-anal length; HW, head width; HL, head length; NS, non-significant(P > 0.05).Model: Y = b0 TL

b1 + �.*P < 0.05; **P < 0.01; ***P < 0.001

(a) (b)

(c)

Fig. 6. (a) Free-embryo and (b) young-juvenile (c) juvenile of C. spixii. adf, adipous fin; anf, anal fin; cfr, caudal fin rays; dfr, dorsal fin rays; dfs,dorsal fin spine; l, lens; mi, miomer; mt, mental barbel; mx, maxilary barbel; n, narine; o, operculum; pfr, peitoral fin rays; pfs, peitoral fin spine;pvf, pelvic fin; ys, yolk-sac. Scale bars: 1 cm

224 A. R. A. Lima et al.

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Author�s address: Mario Barletta, Federal University of Pernambuco,50740-550, Recife, Pernambuco, Brazil.E-mail: mario.barletta@pq.cnpq.br

Development and growth of C. spixii 225