Early development of the head skeleton in Brycon moorei(Pisces, Ostariophysi, Characidae)

Early development of the head skeleton in Bryconmoorei (Pisces, Ostariophysi, Characidae)

P. VANDEWALLE*†, G. GERMEAU*, P. BESANCENET‡,E. PARMENTIER* AND E. BARAS§

*Universite de Liege, Departement des Sciences et Gestion de l’Environnement,Laboratoire de Morphologie fonctionnelle et evolutive, Institut de Chimie B6,

Sart Tilman, B-4000 Liege, Belgium, ‡Laboratoire d’Ethologie et dePsychologie animale, Centre de Recherche et d’Education en Aquaculture,Chemin de la Justice, B-4500 Tihange, Belgium and §IRD, UR-175, Avenue

J.-F. Breton 361, F-34033 Montpellier, Cedex O1, France

(Received 12 December 2002, Accepted 30 November 2004)

At hatching (15 h post fertilization), Brycon moorei possesses no skeletal structure. Thereafter,

development is very rapid. The first oral teeth appear no later than 3 h post-hatching, but they

remain covered with epithelium until c. 45 h. At 7 h, the trabecular bars and part of the

cartilaginous visceral arches are visible and at 15 h, the dentaries and premaxillaries are present.

At 25 h, i.e. the onset of piscivory and cannibalism (the yolk sac is only fully resorbed after

36 h), the oral teeth are fully developed, the first pharyngeal teeth are formed, and some head

movements already appear synchronized, but the mouth cavity is not completely isolated from

the neurocranium by bony structures. Thereafter, no new buccal or pharyngeal bony structure

is visible until 45 h, when the maxilla and opercula appear, along with a new type of cannibal-

istic behaviour. Cartilage resorptions also start at 45 h, but with no concomitant replacement by

formation of calcified structures. Later, development gradually becomes similar to that of many

previously studied teleosts. The developmental pattern of B. moorei is thus extremely rapid in

comparison with other teleosts, i.e. it prioritizes feeding structures that permit the expression of

piscivory at a very early age. The uniqueness of this pattern is discussed in relation to ecological

constraints on early feeding and fast growth. # 2005 The Fisheries Society of the British Isles

Key words: Brycon moorei; cannibalism; cephalic development; Characidae; skeleton.

INTRODUCTION

Developmental patterns in teleosts are assumed to reflect environmentalconstraints leading to the need to acquire, more or less rapidly, structuresenabling an individual to breath, feed and grow. Some species produce feweggs of large size, with abundant yolk reserves; the species may also displayvarious degrees of parental care that contribute to protecting the young duringthe most critical early stages. Other species invest in a greater number of smalleggs with fewer endogenous reserves, and little or no parental care apart from

†Author to whom correspondence should be addressed. Tel.: þ32 4 366 50 40; fax: þ32 4 366 37 15;

email: [email protected]

Journal of Fish Biology (2005) 66, 996–1024

doi:10.1111/j.1095-8649.2005.00656.x,availableonlineathttp://www.blackwell-synergy.com

996# 2005TheFisheries Society of theBritish Isles

selection of the spawning habitat and of the time of year at which theyreproduce. For these latter species that reproduce late during the spawningseason, time is short before the onset of more harsh seasonal conditions, andit is imperative that their young attain a minimum size to survive the harshenvironmental conditions or heavy predation. Thus, fast developmental rates,and possibly more extreme developmental patterns might be anticipated in thesespecies.Species displaying piscivory at a young age and small size are good examples

of such extreme strategists. Tunas and other scombrids, which possess a largehead and high ingestion capacities at a young age and small size, belong to thiscategory. One example is Scomberomorus niphonius (Cuvier) (Shirota, 1970;Shoji & Tanaka, 2001), but the record-holder for early piscivory is apparentlythe freshwater teleost Brycon moorei Steindachner, a characid that can bepiscivorous from the very start of exogenous feeding (no later than 24 h post-hatching and <40 h post-fertilization, Baras et al., 2000a, b). Additionally,B. moorei is among the fastest growing fish species, since it can grow from0�5mg to >30 g within 1 month (Baras & Jobling, 2002). These traits make it agood candidate for the study of developmental patterns, especially with respectto feeding structures. Yet there has been no complete description of the devel-opment of the head and feeding structures in B. moorei (or any closely relatedspecies), nor of how markedly this development might differ from those of otherspecies confronted with less severe environmental constraints. The aim of thisstudy was to fill this gap in knowledge by describing the ontogeny of headmorphology in B. moorei. This should help improve knowledge about thedevelopmental patterns of characiforms. Such knowledge is still extremelyfragmentary and scarce (Bertmar, 1959), despite the fact that this order repre-sents >10% of all freshwater fishes (Froese & Pauly, 2002).

MATERIALS AND METHODS

REPRODUCTION

The specimens studied were the offspring of wild breeders captured as juveniles inNovember 1995 in the Magdalena River, Colombia, and raised at the AquacultureStation of the University of Liege (Tihange, Belgium) at a temperature between 26 and28� C. Male and female breeders were selected according to their maturity and generalhealth status, and reproduction was induced by injections of carp pituitary extract,according to the protocol proposed by Baras et al. (2000b). Artificial fertilization wascarried out 7 h after the last injection, then the eggs were incubated at 27�5� C in Zuggerjars. Hatching occurred c. 15 h after fertilization. The larvae were then placed in 50 laquaria in a recirculating system at 27� C under 12L : 12D. Twenty-four hours afterhatching, the larvae were fed live Artemia salina nauplii supplied in excess so as to reducecannibalism and growth heterogeneity. Weaning to formulated feed began 8 days post-hatch and ended on day 14. The food distributed was Sea Bream from Nippai, followedby Ecostart 1 and 2 from Biomar.

SAMPLING, OBSERVATIONS AND STAINING

Batches of c. 50 larvae, then fry were sampled at 1, 3, 7, 11, 15, 21, 25, 31, 35, 45, 63,87, 95, 131, 175, 199, 271, 319 and 572 h post-hatch. Specimens were sampled at random,but the largest and smallest individuals were rejected. Individual specimens from each

HEAD SKELETON DEVELOPMENT IN BRYCON MOOREI 997

# 2005TheFisheries Society of theBritish Isles, Journal of FishBiology 2005, 66, 996–1024

batch corresponding to ages 1 to 25h were then placed alive in a graduated Petri dish toallow observation and filming with a JVC TK-C1381 colour video camera mounted on aOlympus SZ40 binocular and connected to a Panasonic AG6124 video recorder. Theclearest sequences of mouth-part movements were digitized and analysed. Biometric mea-surements of the mouth and gape were performed. The filmed fish were then returned totheir respective batches and each batch was fixed in buffered formalin for at least 5 days.

In the different batches, some individuals were stained with alcian blue to reveal thecartilaginous structures, and others were stained with alizarin red (Taylor & Van Dyke,1985), to reveal the calcified structures. Stained fry were observed with a Leica M10binocular microscope, and the most relevant features of the skeletal structures weredrawn using a mounted camera lucida. Not all stages have been illustrated or described.Only the more interesting morphological details of these are noted here. It was possible toidentify the skeletal elements by determining their topographical position, and by com-paring the structures formed in adult fish (Weitzman, 1962) with those of older fry, thencomparing the structures of these older fry with those of younger ones and so on to theyoungest fry.

The jaws and teeth of individuals aged 21h (6�3mm total length, LT), 45h (8�0mm), 199 h(15�5mm), and 572h (33�0mm) were observed and photographed with a Jeol JSM840Ascanning electron microscope after fixation for 2 h in 2�5% glutaraldehyde in sodiumcacodylate buffer (0�1M) and dehydration with alcohol by the critical-point method.

RESULTS

SKELETAL STRUCTURES

At hatching (c. 15 h post-fertilization)No skeletal structure is visible in the head.

Three hours post-hatchingOsteocranium: small oral uncoloured teeth appear in an almost circular

mouth.

Seven hoursChondrocranium [Fig. 1(a)]: several cartilaginous elements have appeared.

The neurocranium shows a pair of trabecular bars distinct from the parachordalplates. The splanchnocranium consists of Meckel’s cartilages (left and right) andthe first four pairs of ceratobranchials.Osteocranium: the uncoloured oral teeth are more developed.

Eleven hoursChondrocranium [Fig. 1(b), (c)]: the trabecular bars broaden out anteriorly

and the parachordal plates occupy their final positions below the chord. Thelateral walls of the otic capsules have appeared dorsal and lateral to the para-chordal plates.Meckel’s cartilages are more developed. They curve toward each other. The

palato-quadrates have appeared.

Fifteen hoursChondrocranium [Fig. 1(d), (e)]: the splanchnocranium now possesses

hyosymplectics and hyoid bars. The interhyals have appeared between thehyosymplectics and hyoid bars.

998 P . VANDEWALLE ET AL .


CBR3

CBR4(a)

CBR2CBR1

CBR1

CBR4 CBR4CBR2

CBR

CBR3

(b)

(d)

(e)

(c)

OT.CAP

OT.CAP

OT.CAP

OT.CAP

PAL.Q

PAL.Q

PAL.Q

PAL.Q

CBR4

PC

TR

TR

TR

TR TR

PC

PC IH

HSY

H.B

PC

M.CA

M.CA M.CA

M.CA

M.CA

0·5 mm

DENT

PMAX

FIG. 1. Brycon moorei. (a) Lateral view of the chondrocranium at 7 h post-hatch, (b) lateral and (c) dorsal

views of the chondrocranium at 11 h, and lateral views of the (d) chondrocranium and (e)

osteocranium at 15 h. � � �, the locations of the eye, yolk sac and chord. CBR, ceratobranchials;

DENT, dentary; H.B, hyoid bar; HSY, hyosymplectic; IH, interhyal; M.CA, Meckel’s cartilage;

OT.CAP, otic capsule; PAL.Q, palato-quadrate; PC, parachordal plate; PMAX, premaxilla; TR,

trabecula.



Osteocranium: the dentaries and premaxillae are present, but not visiblyconnected to the oral teeth.

Twenty one hours (end of the embryonic period)Chondrocranium [Fig. 2(a), (b), (c)]: the trabecular bars are joined anteriorly

with a massive ethmoid plate. The otic capsules are connected to the parachor-dal plates by two commissurae basicapsulares anteriores. The palato-quadratehas lengthened upward and curved forward. The foramen of the truncus hyoi-deomandibularis is visible in the upper part of the hyosymplectic; the latterpossesses a posterior extension articulating with the interhyal. The fifth cerato-branchials, the hypohyals, and the first three pairs of hypobranchials haveappeared. Epibranchials 1, 2, 3 and 4 have begun to form.

PC TR

TR

PCBCA

ETHM.P

OT.CAP

PHAR.T

PMAX

DENT0·5 mm

ETHM.P

M.CA

M.CAHBR1 HBR1H.B H.B

CBR1 CBR1

CBR2CBR2PAL.Q

PAL.Q

HSY HSY

IH IH

HBR3 HBR3CBR3 CBR3

CBR4 CBR4CBR5 CBR5

HBR2 HBR2

M.CAHH HH

HHPAL.QH.B

IH

CBR

HSYOT.CAP(a)

(c) (d)

(b)

EBR

FIG. 2. Brycon moorei. (a) Lateral view of the chondrocranium, (b) ventral view of the cartilaginous

splanchnocranium, (c) dorsal view of the chondroneurocranium and (d) lateral view of the osteo-

cranium (D) at 21 h post-hatch. BCA, commissura basicapsularis anterior; CBR, ceratobranchial;

DENT, dentary; EBR, epibranchials; ETHM.P, ethmoid plate; H.B, hyoid bar; HBR, hypobran-

chial; HH, hypohyal; HSY, hyosymplectic; IH, interhyal; M.CA, Meckel’s cartilage; OT.CAP, otic

capsule; PAL.Q, palato-quadrate; PC, parachordal plate; PHAR.T, pharyngeal teeth; PMAX,

premaxilla; TR, trabecula.



Osteocranium [Fig. 2(d)]: the oral teeth are larger and more numerous. Mostof them appear lodged in alveoli of the premaxillae and dentaries, which shouldmake them fully functional. As visualized with the scanning electron micro-scope, the teeth appear to be covered by an epithelium [Fig. 3(a)]. A few teethare visible at the level of the pharyngeal jaws.

Twenty five hoursChondrocranium [Fig. 4(a), (b), (c)]: the taeniae marginales are present and

connected to each other by the epiphyseal bridge. They are attached at theethmoid plate by the commissurae sphenoseptales. Posteriorly, Meckel’s carti-lages now bear a depression corresponding to the articulation with the palato-quadrate. The articular process for the opercular has appeared behind thehyosymplectic. The latter articulates with the neurocranium.A copula anterior (basibranchial) and a fourth pair of hypobranchials is present;

the epibranchials have developed and a small cartilaginous part (possibly the fifthepibranchial) is conspicuous, attached to the fourth epibranchials. In addition, acartilaginous plate corresponding to the third and fourth infrapharyngobranchialshas appeared at the medial tip of the third and fourth epibranchials.Osteocranium [Fig. 4(d)]: the dentaries and premaxillae are more developed.

More teeth are visible, both on the buccal pieces and on the pharyngeal jaws.

Thirty one hoursChondrocranium: the trabecular bars have become longer and thinner. The

commissurae basicapsulares posteriores have appeared, on either side of the head,so delimiting with the commissurae basicapsulares anteriores a large fenestrabasicapsularis. The acrochordal cartilage is present, connecting the parachordals.

(a) (b)

(c) (d)

FIG. 3. Bryconmoorei. Scanning electronmicroscope pictures of (a) the teeth of the lower jaw at 21h post-hatch,

(b) the premaxilla at 45h, (c) the maxilla at 199h and (d) the premaxilla at 512h. Scale bars¼ 100mm.



The dorsal and ventral extremities of the palato-quadrate are joined anddelimit a pterygoid fenestra. They are extended anteriorly by a pterygoidprocess, the anterior part of which (the pars palatina) broadens out. The secondinfrapharyngobranchials have appeared.

Forty five hoursChondrocranium [Fig. 5(a), (b), (c)]: the chondrocranium is almost complete,

except in the ethmoid region where the laminae orbitonasales are not yet

HSYOT.CAP

(a)

(c)

(b)

(d)

PT.PR TRT.M

SPSE

COP.AM.CA M.CA

HH HH

H.B H.B

HSY

HBR1

HBR2

HBR3

HBR2

HBR1

PAL.Q

CBR3

IHEBR1 EBR2

HBR4

EBR4EBR3

CBR5

PHAR.T

PMAX

DENT

CBR4

CBR2

PBR3,4

CBR1ETHM.PL

M.CAHH

HBR1HBR2

ETHM.P SPSEE.B

TRT.M

BCA

PC OT.CAP

0·5 mm

HBR3PAL.QH.B

IH

CBR

EBR 5?

EBR

PBR3,4


splanchnocranium, (c) dorsal view of the chondroneurocranium and (d) lateral view of the

osteocranium at 25 h post-hatch. BCA, commissura basicapsularis anterior; CBR, cerato-

branchial; COP.A, copula anterior; DENT, dentary; E.B, epiphyseal bridge; EBR, epibranchial;

ETHM.P, ethmoid plate; H.B, hyoid bar; HBR, hypobranchials; HH, hypohyal; HSY, hyosym-

plectic; IH, interhyal; M.CA, Meckel’s cartilage; OT.CAP, otic capsule; PAL.Q, palato-quadrate;

PBR, pharyngobranchial; PC, parachordal plate; PHAR.T, pharyngeal teeth; PMAX, pre-

maxilla; PT.PR, pterygoid process; SPSE, commissura sphenoseptalis; T.M, taenia marginalis; TR,

trabecula.



formed. The left and right parts of the rear of the skull are joined dorsally bythe tectum posterius. Anteriorly, the pilae laterales or commissurae lateraleslimit the sphenoid fenestrae; the pilae occipitales are present next to the vagusnerve.

TC.P HSY TRPT.PR E.B

T.M

SPSE

PCRB

M.CA

M.CA

M.CA

BHHH

HBR1

HBR2

HBR3

PBR1

EBR1HBR4

PAL.Q

PBR2

EBR3EBR2

IH

HSYCBR4

CBR3

CBR2

CBR1

H.B

COP.A

EBR4CBR5

COP.P PBR3,4PBR3,4

HHHBR1HBR2HBR3

HBR4PAL.Q

PCRB

SPSETH.PL O

MAX

PMAX

DENTBR.R

E.B

T.M

L.C

OT.CAP

BCP

PL.O

0·5 mm

TC.P

FBCA

BCA

AC

TR

ETHM.P

H.B

IHCBR

EBR 5?

EBR

PBR3,4

OT.CAP

(a) (b)

(c) (d)


splanchnocranium, (c) dorsal view of the chondroneurocramium and (d) lateral view of the

osteocranium at 45 h post-hatch. AC, acrochordal cartilage; BCA, commissura basicapsularis

anterior; BCP, commissura basicapsularis posterior; BH, basihyal; BR.R, branchiostegal ray;

CBR, ceratobranchial; COP.A, copula anterior; COP.P, copula posterior; DENT, dentary; E.B,

epiphyseal bridge; EBR, epibranchial; ETHM.P, ethmoid plate; FBCA, fenestra basicapsularis;

H.B, hyoid bar; HBR, hypobranchial; HH, hypohyal; HSY, hyosymplectic; IH, interhyal; L.C,

commissura lateralis; MAX, maxilla; M.CA, Meckel’s cartilage; O, operculum; OT.CAP, otic

capsule; PAL.Q, palato-quadrate; PBR, pharyngobranchial; PCRB, lamina precerebralis; PL.O,

pila occipitalis; PMAX, premaxilla; PT.PR, pterygoid process; SPSE, commissura sphenoseptalis;

TC.P, tectum posterius; TH.PL, teeth plate; T.M, taenia marginalis; TR, trabecula.



Meckel’s cartilages have regressed, isolating anteriorly two small cartilaginousislets. The copula posterior (fourth basibranchial) has appeared, as have thefirst infrapharyngobranchials.Osteocranium [Fig. 5(d)]: the dentaries have thickened. The maxillae have

appeared in the form of thin stems situated above the premaxillae, the lattereach having anteriorly a small processus ascendens. The operculae are beginningto appear, along with three pairs of branchiostegal rays. The pharyngeal teethare supported by a thin bony plate.A large proportion of the oral teeth are visualized with the scanning electron

microscope; most of them have pierced the epithelial layer, and they now appearsharp and slender [Fig. 3(b)].

Sixty three hoursChondrocranium [Fig. 6(a)]: resorption zones have appeared in the hyosym-

plectic, palato-quadrate, and hyoid bar (divided into widely separated parts).The pterygoid fenestra is open ventrally. The posterior infrapharyngobranchialshave regressed.Osteocranium [Fig. 6(b)]: the parasphenoid, though very slender, and the

basioccipital are present at this age. The angulo-articulars are distinguishablefrom the dentaries, and the posterior extremities of the maxillae have broad-ened. The operculae are further developed. The number of pharyngeal teethhas increased and their supporting plates have thickened.

Ninety five hoursChondrocranium [Fig. 7(a)]: the laminae orbitonasales are present but the

trabecular bars have practically disappeared, although they were still continu-ous at 87 h. Several regressions can be seen in the splanchnocranium: Meckel’scartilages are reduced; regression of the lower part of the palato-quadrates hasisolated a small cartilaginous part at the level of the articulation with Meckel’scartilages. Similarly, the hyosymplectic is divided into isolated cartilages.Osteocranium: the parasphenoid has widened and a fourth pair of branchiostegal

rays is present.

One hundred and thirty one hoursChondrocranium: in the neurocranium and splanchnocranium, few changes

have taken place.Osteocranium [Fig. 7(b), (c)]: the parasphenoid and basioccipital have

increased in size. The bony splanchnocranium shows major changes. Thewidened rear part of the maxilla bears some teeth. The retro-articulars haveappeared posterior to the angulo-articulars, and the quadrates are well calcified.The two entopterygoids have appeared with, just ventrally, the two ectoptery-goids. Where the cartilaginous hyosymplectics have regressed, hyomandibularsare present dorsally and symplectics ventrally. The operculae have furtherincreased in size; the suboperculae and interoperculae have appeared. Theceratohyals are visible, although their ossification is still incomplete; to therear, two bony primordia have appeared, corresponding to the posteriorceratohyals. The urohyal is present in the ventral midline, anterior to theceratohyals.



One hundred and ninety nine hoursChondrocranium [Fig. 8(a)]: many resorptions have appeared throughout the

chondrocranium. The taeniae marginales, still complete at 175 h, are nowdivided, separating the ethmoid region from the otic region and isolating theepiphyseal bridge, which remains conspicuous. The hyosymplectic is reduced toa structure with three distinct regions: (1) a cartilaginous band articulating withthe neurocranium and extending to the articular process of the opercula; (2) awider central part bearing the articular process of the interhyal; and (3) a smalllower cartilaginous part. Meckelian cartilages are reduced to cartilaginous

TC.POT.CAP

(a)

HSY

EBREBR 5?

CBR

IH

H.B HSY

PAL.Q

BOC(b)

PASPHMAX

PMAX

DENTANBR.R

O

TH.PL

0·5 mm

M.CAHBR2

HBR1H.BCOP.A

HHBH

M.CA

PCRB

SPSE

T.ME.B

PT.PRTRHBR3

FIG. 6. Brycon moorei. Lateral views of (a) the chondrocranium and (b) osteocranium at 63 h post-hatch.

AN, anguloarticular; BH, basihyal; BOC, basioccipital; BR.R, branchiostegal ray; CBR, cerato-

branchial; COP.A, copula anterior; DENT, dentary; E.B, epiphyseal bridge; EBR, epibranchial;

H.B, hyoid bar; HBR, hypobranchial; HH, hypohyal; HSY, hyosymplectic; IH, interhyal; MAX,

maxilla; M.CA, Meckel’s cartilage; O, operculum; OT.CAP, otic capsule; PAL.Q, palato-quadrate;

PASPH, parasphenoid; PCRB, lamina precerebralis; PMAX, premaxilla; PT.PR, pterygoid process;

SPSE, commissura sphenoseptalis; TC.P, tectum posterius; TH.PL, teeth plate; T.M, taenia margin-

alis; TR, trabecula.



bands, that are thin except at their posterior ends. The cartilaginous cerato-branchials are also thinner than in younger specimens.Osteocranium [Fig. 8(b), (c)]: the frontals and exoccipitals have appeared. The

prootics are stained in a fragmented manner. A pair of lateral wings hasappeared in the middle of the parasphenoid, oriented towards the prootics.The maxillae are still broadening and they increasingly support the upper lip,whereas the premaxillae are becoming proportionately smaller. The teeth on themaxillae are more numerous. The scanning electron microscope shows that the

OT.CAP TC.PHBR3PT.PRE.BT.M

ONSPSE

PCRB

M.CAHH

H.BHBR1M.CAHBR2PAL.QHSYH.B

HM SYPASPH

QENTP

MAX

PMAXPMAX

DENTDENT UH

AN

MAXMAX

CHACHAPASPHRARA

QQ

SYSYHMHM

IOIO

OOSOSO

CHPTH.PL

BOCBR.R

CHP

PMAX

DENT

1 mm

ANECTPCHARA

BR.R

IO

SO

O

BOC

IH

CBR

EBR

PBR

HSY

(a)

(b)(c)

FIG. 7. Brycon moorei. (a) Lateral view of the chondrocranium at 95 h post-hatch, and (b) lateral and

(c) ventral views of the osteocranium at 131 h. AN, anguloarticular; BOC, basioccipital; BR.R,

branchiostegal ray; CBR, ceratobranchial; CHA, anterior ceratohyal; CHP, posterior ceratohyal;

DENT, dentary; E.B, epiphyseal bridge; EBR, epibranchial; ECTP, ectopterygoid; ; ENTP, ento-

pterygoid; H.B, hyoid bar; HBR, hypobranchial; HH, hypohyal; HM, hyomandibula; HSY,

hyosymplectic; IH, interhyal; IO, interopercula; MAX, maxilla; M.CA, Meckel’s cartilage;

O, operculum; ON, lamina orbitonasalis; OT.CAP, otic capsule; PAL.Q, palato-quadrate;

PASPH, parasphenoid; PBR, pharyngobranchial; PCRB, lamina precerebralis; PMAX, premaxilla;

PT.PR, pterygoid process; Q, quadrate; RA, retroarticular; SPSE, commissura sphenoseptalis; SO,

suboperculum; SY, symplectic; TC.P, tectum posterius; TH.PL, teeth plate; T.M, taenia marginalis;

UH, urohyal.



PBR3,4 TC.P PBR2HSYPBR1

COP.AT.M

HBR1

E.BPT.PR

ON

SPSE

PCRB

M.CA

BHHH

HHHH

H.BHBR2HBR3HSY

H.B

BOC EXOC HM

HMHMCHPCHP

PROTENTP

FPASPH

MAX MAXMAX

PMAX

PMAX PMAX

DENT

DENTDENTUH

ECTPCHA

CHACHA

1 mm

AN

ANAN

Q

Q

Q

RA

RA

RA

SYBR.R

IO

IOIO

SO

SOSOTH.PL

BR.R

PO

O

OO

IHCBR

EBR

M.CAPAL.Q

(a)

(b) (c)

FIG. 8. Brycon moorei. (a) Lateral view of the chondrocranium, (b) lateral view of the osteocranium and

(c) ventral view of the osteosplanchnocranium at 199 h post-hatch. AN, anguloarticular; BH,

basihyal; BOC, basioccipital; BR.R, branchiostegal ray; CBR, ceratobranchial; CHA, anterior

ceratohyal; CHP, posterior ceratohyal; COP.A, copula anterior; DENT, dentary; E.B, epiphyseal

bridge; EBR, epibranchial; ECTP, ectopterygoid; ENTP, entopterygoid; EXOC, exoccipital; F,

frontal; H.B, hyoid bar; HBR, hypobranchial; HH, hypohyal; HM, hyomandibula; HSY, hyosym-

plectic; IH, interhyal; IO, interoperculum; MAX, maxilla; M.CA, Meckel’s cartilage; O, operculum;

ON, lamina orbitonasalis; PAL.Q, palato-quadrate; PASPH, parasphenoid; PBR, pharyngobran-

chial; PCRB, lamina precerebralis; PMAX, premaxilla; PO, preoperculum; PROT, prootic; PT.PR,

pterygoid process; Q, quadrate; RA, retroarticular; SO, suboperculum; SPSE, commissura spheno-

septalis; SY, symplectic; TC.P, tectum posterius; TH.PL, toothed plate; T.M, taenia marginalis;

UH, urohyal.



teeth borne by the dentaries and premaxillae are arranged in rows; they are stillsharp and slender whereas the maxillary teeth are short and curve backward[Fig. 3(c)]. Preoperculae have appeared anterior to the operculars. Branchialspines are visible on the cartilaginous first, second, and third ceratobranchialsand epibranchials.

Two hundred and seventy one hoursChondrocranium [Fig. 9(a)]: the chondrocranium is totally fragmented mak-

ing it difficult to distinguish different structures, which are often reduced totheir articular surfaces. Only the ethmoid area remains complete. The taeniaemarginales are reduced to thin cartilaginous bands, and the epiphyseal bridge toa cartilaginous islet at the top of the skull. Reduction is also apparent at thelevel of the tectum synoticum and at several places on the otic capsule.Meckelian cartilages are each separated into three parts: a small one ante-

riorly, followed by a long, thin band, and a posterior part with which thequadrate articulates. Each palato-quadrate is reduced to a small ventral articu-lar element, a posterior part, and an anterior part extended by the pterygoidprocess. The latter has become thin and slightly curved, and still bears ante-riorly a widened pars palatina. Of the hyosymplectics only four islets remain: (1)a ventral part, (2) a larger central part with which the interhyal articulates, (3)the posterior articular process for the opercular and (4) a dorsal band ofcartilage corresponding to the zone articulating with the ossified prootics. Thehypohyals are partially reduced. Only the posterior and anterior parts of theceratobranchials remain. The central portion of the epibranchials is alsoreduced, but the ‘fifth epibranchials’ remain small and conspicuous close tothe fourth epibranchials. The hypobranchials are still present, but infrapharyn-gobranchials 1, 2 and 3 show signs of reduction. The first basibranchial isdivided in two.Osteocranium [Fig. 9(b), (c), (d)]: The neurocranium has increased in ossifica-

tion. In addition to the development of many existing elements, new ones haveappeared. The single praevomer is present as a fine band posterior to theascending processes of the premaxillae. The mesethmoid is present in the formof two latero-dermethmoids arranged almost longitudinally anterior to thefrontals and as a fine medial dermethmoid, dorsal to the praevomer. Theparietals are visible behind the frontals. Posterior to the parietals are traces ofcalcification corresponding to the supraoccipital. The pterosphenoids are pre-sent ventral to the frontals, and two small sphenotics form the posterior limit ofthe orbits.The bones of the suspensorium and the hyoid bars have developed. The

metapterygoids have appeared dorsal to the quadrates and form the dorsalpart of the pterygoid fenestrae. The central parts of the ceratobranchials areconspicuous, as are the pharyngobranchials. Branchiospines are also present onthe fourth ceratobranchials.

Three hundred and nineteen hoursChondrocranium: The central part of the epiphyseal bridge is still present.Osteocranium [Fig. 10(a), (b)]: in the splanchnocranium, the four pairs of

epibranchials are ossified. Many changes have occurred in the neurocranium.



OT.CAP HSYT.M

PT.PRE.B

ONSPSE

PCRB

DETHM VO

LDETHM

F

F

PLSPHPLSPH

PASPH

PROT

PROTSPOT

PAPA

SOC

EXOC EXOC

LDETHM

M.CA

M.CA

BHHH

1 mm

HHHSY

CBR

EBR5

EBR4

EBR2

PBR1HBR1H

BR2PBR2BBR1

EBR1

EBR3PB

R3 HSY

H.BH.B

AN

MAX MAXUH

RAAN

BR.RQ

QCBR1CBR2

CHP CHP

CBR3

HM

IO

SO

OLW.J UP.J

SO

O

IO

PO

CHA

HM

HM

CBR4

PMAX

DENT

PMAX PROTSOCHM

BOC

O

SO

PO

IOCBR

BR.RSY Q RA

CHAAN

ECTP

DENT

PMAX

METHMMAX

PASPHENTPPTSPHFSPOTPA

MPT

EX

OCHH

METHM HH

COP.APAL.Q

PAL.

Q

HSY

HBR

3

(a)

(c) (d)

(b)

FIG. 9. Brycon moorei. (a) Lateral view of the chondrocranium, (b) ventral view of the osteos-

planchocranium, (c) dorsal view of the osteoneurocranium and (d) lateral view of the osteocranium

at 271 h post-hatch. AN, angular; BBR, basibranchial; BH, basihyal; BOC, basioccipital; BR.R,

branchiostegal ray; CBR, ceratobranchial; CHA, anterior ceratohyal; CHP, posterior ceratohyal;

COP.A, copula anterior; DENT, dentary; DETHM, dermethmoid; E.B, epiphyseal bridge;

EBR, epibranchial; ECTP, ectopterygoid; ENTP, entopterygoid; EXOC, exoccipital; F, frontal;

H.B, hyoid bar; HBR, hypobranchial; HH, hypohyal; HM, hyomandibula; HSY, hyosymplectic;

IH, interhyal; IO, interoperculum; LDETHM, latero-dermethmoid; LW.J, lower pharyngeal jaw;

MAX, maxilla; M.CA, Meckel’s cartilage; METHM, mesethmoid; MPT, metapterygoid; O, oper-

culum; ON, lamina orbitonasalis; OT.CAP, otic capsule; PA, parietal; PAL.Q, palato-quadrate;

PASPH, parasphenoid; PBR, pharyngobranchial; PCRB, lamina precerebralis; PTSPH, pteros-

phenoid; PMAX, premaxilla; PO, preoperculum; PROT, prootic; PT.BR, pterygoid process; Q,

quadrate; RA, retroarticular; SO, suboperculum; SOC, supraoccipital, SPOT, sphenotic; SPSE,

commissura sphenoseptalis; SY, symplectic; T.M, taenia marginalis; UH, urohyal; UP.J, upper

pharyngeal jaw; VO, praevomer.



The praevomer has developed and now reaches the anterior end of the para-sphenoid. The calcified parts of the mesethmoid are joined and form two horns(latero-dermethmoids) extending posteriorly to contact the frontals. They arebounded laterally by the nasals and lateral ethmoids. The orbitosphenoids arevisible anterior to the pterosphenoids. The frontals have developed, but thebony epiphyseal bridge, or epiphyseal bar, is not yet complete and thus does notyet separate the anterior (prepineal) fontanel from the posterior (postpineal)

SOCPA SPOT

F

NA VOPMAX

DENTINOR1

MAXECTP

ANCHA

BR.RQ

MPTSYIO

PASPH

METHMVOVO

NA NA

LETHM LETHM

ORSP

H ORSPH

PTOTSOC

EPOC

SPOT

PROT

HMINOR 4,5

O

CBR

SOPO

IOMPT SY

Q RAANECTP INOR2

MAXDENT

1 mm

INOR1

PMAX

MAX

F

OR

SPH

EN

TP

PT

SPH

PASP

H

PA

NAAN

TO

R

ME

TH

M

SUP

OR

LET

HM

F

SPOT

F

SPOT

PROT

PTOT

PROT

PTOTPAPA

EXOC EXOC

SOC

POCBR

1 mm

SO

O

HM

BOC

PROT

EXOC

PTOT(a)

(b) (c)RA

ENTP

ORSPH

PASPH

LETHM

METHM

PTSPH

FIG. 10. Brycon moorei. (a) Lateral view of the osteocranium and (b) dorsal view of the osteoneurocra-

nium at 319 h post-hatch, and (c) lateral view of the osteocranium at 572 h. AN, angular;

ANTOR, antorbital; BH, basihyal; BOC, basioccipital; BR.R, branchiostegal ray; CBR, cerato-

branchial; CH, ceratohyal; DENT, dentary; ECTP, ectopterygoid; ENTP, entopterygoid; EPOC,

epioccipital; EXOC, exoccipital; F, frontal; HM, hyomandibula; INOR, infra-orbital; IO, inter-

operculum; LETHM, lateral ethmoid; MAX, maxilla; METHM, mesethmoid; MPT, metaptery-

goid; NA, nasal; O, operculum; ORSPH, orbitosphenoid; PA, parietal; PASPH, parasphenoid;

PTSPH, pterosphenoid; PMAX, premaxilla; PO, preoperculum; PROT, prootic; PT.BR, pterygoid

process; PTOT, pterotic; Q, quadrate; RA, retroarticular; SO, subopercula; SOC, supraoccipital,

SPOT, sphenotic; SUPOR, supra-orbital; SY, symplectic; VO, praevomer.



fontanel. The parietals and supraoccipital have also developed. Several calcifiedzones of the pterotics have appeared between the parietals and prootics. Thefirst infraorbitals, or lacrimals, are the only circumorbital bones present.

Five hundred and seventy two hoursChondrocranium: resorption is almost complete. The fifth epibranchials are

still distinguishable.Osteocranium [Fig. 10(c)]: the neurocranium is increasingly ossified. The

lateral ethmoids have developed medially. The epiphyseal bar is complete: thepre- and postpineal fontanels are now separated by bone. The frontals andparietals completely cover the top of the skull, apart from the large postpinealfontanel. The pterotics are well calcified and the epioccipitals have appearedposterior to them. The prootics and the wings of the parasphenoid have joined.The sphenotics have extended medially and posteriorly. Each of the circumor-bitals series comprises five elements plus a supraorbital and antorbital.The premaxillae are enlarged but proportionately much shorter than

the maxillae; at this stage they bear few tricuspid teeth. The same is true ofthe teeth on the dentaries. Scanning electron micrographs show that some of theteeth on the inner, anterior part of the premaxillae possess five cusps [Fig. 3(d)].The maxillae bear many small teeth. The palatines remain unossified. Theoperculae have extended in depth.

MOUTH ALLOMETRIES

Mouth-part allometries and how they relate to cannibalistic behaviours areexamined in detail elsewhere (unpubl. data). A very brief account of theserelationships is given here for the sake of completeness and clarity. At hatching,the length of the jaws is <4% of the fish LT, but it increases rapidly [Fig. 11(a)–(c)] so as to be >13% LT by the start of exogenous feeding (Fig. 12). Yet thedepth of the buccal cavity is still a limiting factor at this age, so B. moorei larvaedo not ingest their prey whole. Instead, they catch them tail first and ‘suck’them in up to the head, which is finally discarded. During the larval stage, themouth parts alternate periods of negative allometric and isometric growth thatparallels shifts between different types of predation. In fact, the mouth stopsgrowing during short developmental intervals, and shifts between differentcannibalistic behaviours take place precisely during these intervals. Duringthis period, jaw length decreases to c. 7% LT in the early juvenile stage[Figs. 11(d)–(f) and 12]; this prevents young B. moorei from consuming largeprey and accounts for the shift to complete (type II) cannibalism (Baras et al.,2000b).

MOVEMENTS OF MOUTH PARTS AND BUCCAL CAVITY

Low-amplitude movements of the mouth are occasionally observed at 7 hpost-hatch. The amplitude and frequency of these movements increase over thenext 4 h. At 15 h post-hatching, synchronous or asynchronous movements of theMeckelian cartilages and hyoid bars can be seen, i.e. there is no regularity orcoupling in the movement sequence. At 21 h post-hatch, in contrast, thesemovements are co-ordinated and appear systematically in the same sequence:



first opening of the mouth, then depression of the hyoid bars. At this stage,abduction and adduction of the suspensoria are also obvious.At 25 h post-hatch, at the onset of piscivory, larvae may exhibit a wide mouth

opening (c. 150 degrees at the mouth corner, giving a gape size >25% LT),accounted for by three components: 1) neurocranial elevation (c. 32 degrees)mediated by contraction of the epaxial muscles, which are well developed at thisstage (Fig. 13); 2) rotation (c. 10 degrees) of the premaxilla around its anteriorjoint with the neurocranium; 3) rotation of the mandible (c. 85 degrees) aroundthe quadrato-mandibular joint. The sum of these three components (127degrees) is <150 degrees, because larvae of B. moorei never fully close theirmouth, the minimum aperture being 23–25 degrees. Depression of the hyoid

(a)

(b)

(c)

(d)

(e)

(f)

FIG. 11. Brycon moorei. Pictures from videographic films of the head at (a) 1, (b) 14, (c) 24, (d) 78, (e) 130

and (f) 270 h post-hatch, showing allometric growth of the buccal jaws.



bars begins after the mouth has started opening; it extends over c. 113 degrees(Fig. 13). No movement of the opercular membrane is seen during opening ofthe mouth. During closure of the mouth, all parts return to their originalpositions. The hyoid bars begin their elevation after the mouth has startedclosing. The opercular membrane is detached from the body during closure ofthe mouth.

DISCUSSION

Several factors make it difficult to draw straightforward comparisons betweendevelopmental patterns in different teleost species. Developmental patterns aregenerally described in reference to the condition at the moment of hatching,which may vary between progenies and environmental conditions. Additionally,not all species hatch at the same developmental stage, so comparisons todetermine whether structures appear or ossify late or early may be biased ifthe incubation periods of the species under comparison vary substantially. Thedevelopmental rate also depends on environmental conditions, in particulartemperature and food availability or quality. Finally, authors disagree as tothe meaning and definition of stages and very few studies cover all events fromhatching onward. Nevertheless, this study provides evidence that the formationof the head skeleton in B. moorei is more precocious and rapid in many respectsthan in other teleosts.

CHONDROCRANIUM

In some teleosts such as Salmo trutta L. (Salmonidae) chondrocranial devel-opment begins well before hatching (De Beer, 1937) and, according to Tilney &Hecht (1993), the osteocranium of Galeichthys feliceps (Valencienne) (Ariidae) iswell developed at hatching. In other species, such as Heteropneustes fossilis

0

2

4

6

8

10

12

14

Jaw

len

gth

(% L

T)

0 100 200 300 400 500 600

Age (h post-hatch)

FIG. 12. Brycon moorei. Variations of jaw length, as a proportion of total body length, during ontogeny.



(Bloch) (Heteropneustidae) and Barbus barbus (L.) (Cyprinidae), the chondro-cranium is partially present at hatching (Srinivasachar, 1959; Vandewalle et al.,1992). In most species, however, the first signs of skeletal development appearlater (Hubendick, 1942; Elman & Balon, 1980; Surlemont & Vandewalle, 1991;Adriaens & Verraes, 1997; Vandewalle et al., 1997; Wagemans et al., 1998;Gluckmann et al., 1999). This is the case for B. moorei, in which the firststructures appear 7 h after hatching. Nevertheless, the formation of skeletalstructures in B. moorei is extremely rapid by reference to the moment offertilization, since the incubation period is short (15 h) in this species, and

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

FIG. 13. Brycon moorei. Eight successive pictures (a)–(h) from a videographic film of the head at 28 h,

showing the mouth opening. H, hyoid bar; MD, mandible; PM, premaxillary.



many structures of the chondrocranium are present at 7 h post-hatch (22 h post-fertilization). This is to be compared with the development of Chrysichthysauratus (Geoffroy Saint-Hilaire) (Claroteidae) reared at the same temperatureas here (27� C): in this fish, the first structures appear 12 h post-hatch, but thiscorresponds to 36 h post-fertilization (Vandewalle et al., 1999).

NeurocraniumAt 7 h, the trabecular bars are present, directly fused with the parachordal

cartilages delimiting a wide hypophyseal space. The left and right trabeculae aredistinct and will remain so. This type of broad skull is known as platybasic(Daget, 1964). It is encountered notably in Clupeiformes such as Clupea harengusL. (Clupeidae), Cypriniformes such as B. barbus and Siluriformes such as Clariasgariepinus (Burchell) (Clariidae) (Wells, 1923; Vandewalle et al., 1992; Adriaens &Verraes, 1997). Skulls where the trabecular bars are fused into a trabeculacommunis are said to be tropibasic (Daget, 1964). They characterize specieswith a laterally compressed head such as Rutilus rutilus (L.) (Cyprinidae), Angu-illa anguilla (L.) (Anguillidae), Psetta maxima (L.) (Scophthalmidae), and Soleasolea (L.) (Soleidae) (Norman, 1926; Hubendick, 1942; Wagemans et al., 1998;Wagemans & Vandewalle, 1999). According to Bertmar (1959), the skull of thecharaciform Hepsetus odoe (Bloch) (Hepsetidae) displays a trabecula communisand is thus tropibasic. These examples show that different types of skull can befound among phylogenetically closely related species.

At 21 h, the trabeculae fuse with the ethmoid plate forming the anteriorboundary of the hypophyseal fenestra. The parachordal cartilages, initiallyseparate, appear joined by a narrow acrochordal cartilage at 31 h; the hypo-physeal fenestra is thus closed posteriorly. Then the parachordals join to formthe basal plate or braincase floor. In other teleosts, the basal plate may formquite late (Kindred, 1919; De Beer, 1937; Badenhorst, 1989a; Vandewalle et al.,1992) or not at all (Wagemans et al., 1998; Gluckmann et al., 1999).As early as 11 h and before the appearance of the ethmoid plate, the lateral

walls of the otic capsules are present. They are independent of any otherstructure, as in S. trutta (De Beer, 1937), but this situation is not widepsreadin teleosts (Wagemans et al., 1998; Gluckmann et al., 1999; Vandewalle et al.,1999). At 21 h, the commissurae basicapsulares anteriores form the first linkbetween the otic capsules and the parachordals, as in other teleosts (Vandewalleet al., 1992; Adriaens & Verraes, 1997). Between 21 h and 25 h, developmentappears to accelerate: the taeniae marginales, commissurae sphenoseptales andepiphyseal bridge appear, forming with the trabecular bars the link between thebraincase and the ethmoid region. In other teleosts, the taeniae may progresstowards the rear (Daget & d’Aubenton, 1957; Elman & Balon, 1980;Gluckmann et al., 1999) or towards the front (Srinivasachar, 1959; Adriaens& Verraes, 1997; Vandewalle et al., 1997; Wagemans & Vandewalle, 1999) orthey may appear first above the orbits and extend both anteriorly and poster-iorly thereafter (Wagemans et al., 1998).The tectum posterius links dorsally the left and right capsules at 45 h, which is

extremely rapid in comparison to other teleosts. For example, in P. maxima,this link does not appear before day 15 (Wagemans et al., 1998). At 45 h, several



new connections between the skull floor and the otic capsules are present. Theneurocranium is complete, except for the laminae orbitonasales, which will notbe present until 95 h. Such a pattern of construction of the neurocranium seemsexceptional, but the quasi-simultaneity of events is probably related to therapidity of development. In other species, development is slower and thesequence of appearance of the skeletal parts is more obvious (De Beer, 1937;Kadam, 1961; Elman & Balon, 1980; Badenhorst, 1989a; Watson & Walker,1992; Adriaens & Verraes, 1997; Wagemans & Vandewalle, 1999).

SplanchnocraniumFrom 7h onward, the Meckel’s cartilage is present as are the first four

ceratobranchials. By 11 h, the palato-quadrate is present and finally, at 15 h,the hyoid bar and hyosymplectic appear. This is an unusual sequence. Generallyin other teleosts, the Meckel’s cartilage appears first, alone or with hyoidelements, but this is followed by the appearance of the hyoid bar and hyosym-plectic; the palato-quadrates and first four pairs of ceratobranchials appear later(Potthoff et al., 1988; Watson & Walker, 1992; Potthoff & Tellock, 1993;Wagemans et al., 1998; Gluckmann et al., 1999). The fifth ceratobranchialsappear last as is often the case in teleosts (De Beer, 1937; Vandewalle et al.,1992, 1999; Adriaens & Verraes, 1997). The ceratobranchials constitute thesupport on which the lower pharyngeal jaws rest. The posterior infrapharyngo-branchials appear at almost the same time, supporting the main elements of theupper pharyngeal jaws. The epibranchials are almost always present at the sametime as or just after the appearance of the fifth ceratobranchials. Formation ofa small ‘fifth epibranchial’ has been described previously in only two species:H. odoe and B. barbus (Bertmar, 1959; Vandewalle et al., 1992).From the 21st to the 31st h, the ventral and dorsal parts of the palato-

quadrate first grow forward, then curve towards each other to surround aspace called the pterygoid fenestra, and finally are extended by a pterygoidprocess as in other fishes. The pterygoid process terminates with the parsquadrata. This type of formation of the palato-quadrate is found also inH. odoe (Bertmar, 1959), but has not been observed in other teleosts (Potthoffet al., 1988; Potthoff & Tellock, 1993; Voskoboinikova & Kellermann, 1997;Wagemans et al., 1998; Gluckmann et al., 1999). At 25 h, the joints between thehyosymplectic and the neurocranium, and between the palato-quadrate and theMeckel’s cartilage seem well formed.

ResorptionUsually in teleosts, cartilage resorption begins at the time of, or shortly after,

the first ossified elements appear. Yet resorption varies from species to species,showing that development of the deep bony skeleton is variable (Wells, 1923;De Beer, 1937). In some species, it starts when the chondrocranium is complete(Vandewalle et al., 1997, 1999), but in other cases, it begins when the chondro-cranium is still incomplete (Wagemans et al., 1998; Gluckmann et al., 1999).The first parts to regress are often the trabecular bars (Badenhorst, 1989b;Vandewalle et al., 1992, 1999). In Heterobranchus longifilis Valenciennes (Clar-iidae), the hyoid bars and ceratobranchials are the first to regress (Vandewalleet al., 1997). In B. moorei, resorption begins with the Meckel’s cartilages as in



P. maxima (Wagemans et al., 1998). In these two species, as well as inH. longifilis and Dicentrarchus labrax (L.) (Moronidae) (Vandewalle et al.,1997; Gluckmann et al., 1999), this reduction leads to isolation of a pair ofsmall cartilaginous elements of the mandibular symphysis. Fragmentation of theMeckel’s cartilage happens very early in B. moorei (45 h). By 63 h, the palato-quadrate, hyosymplectic and hyoid bar are regressing: these regressions do notseem to be linked to the presence of calcified structures, which do not appearuntil 131 h. It is possible that, at 63 h, the osteoblasts are present but notobservable in the regressing cartilaginous structures.Resorption of the trabecular bars is very rapid and spectacular: at 87 h, they

are complete and by 95 h, they have almost disappeared. Their reduction isusually slow and progressive in other teleosts (Vandewalle et al., 1992, 1999;Gluckmann et al., 1999; Wagemans & Vandewalle, 1999). In all known cases,reduction of the trabecular bars begins only once the parasphenoid is welldeveloped. From 95 to 199 h, no further reduction is observed, possibly becausefurther reductions would make the head excessively fragile and compromise itsfunctions. At 199 h, the taeniae marginales are regressing as the frontals appear,which is a frequent pattern in teleosts (Langille & Hall, 1987; Vandewalle et al.,1992, 1995, 1999; Voskoboinikova et al., 1994; Adriaens & Verraes, 1998;Wagemans et al., 1998). From 199 h onward, the cartilaginous braincaseregresses gradually as the elements of the bony skeleton appear. The tectumposterius does not disappear until the supraoccipital is well formed, at 271 h.

OSTEOCRANIUM

At 3 h, the first teeth of the upper and lower oral jaws are visible, but asshown by electron microscopy, they are covered with epithelium (until c. 21 h).By contrast, no skeletal part is present. This situation seems exceptional forteleosts, as the teeth usually appear later then the Meckelian cartilages, at thesame time as or after the premaxillae and dentaries (Langille & Hall, 1987;Potthoff et al., 1988; Potthoff & Tellock, 1993; Vandewalle et al., 1995, 1999;Mabee & Trendler, 1996; Voskoboinikova & Kellermann, 1997; Wagemanset al., 1998). At 15 h, the dentaries and premaxillae are present but the teethare not connected to them until 21 h. The premaxilla appearance before themaxillae seems rare in teleost development (Potthoff et al., 1988; Vandewalleet al., 1992, 1995; Potthoff & Tellock, 1993; Kohno et al., 1996, 1997; Mabee &Trendler, 1996; Wagemans et al., 1998; Gluckmann et al., 1999; Wagemans &Vandewalle, 2001). In some cases, the two bones appear together (Weisel, 1967;Vandewalle et al., 1997). The situation for B. moorei is perhaps related tothe appearance of the first buccal teeth, which is always associated with thedevelopment of the premaxillae in teleosts. At this age the first pharyngeal teethappear. As in other species, these teeth do not appear connected to visible skeletalstructures (Potthoff & Tellock, 1993; Wagemans et al., 1998). Not until 45 h arethe primordia of dermal plates apparent. This is also the time of appearance ofthe opercula and maxilla. The maxilla is located just ventral to the premaxilla anddoes not contribute to framing the mouth, whereas in 12�6mm H. odoe and adultcharaciforms, it is situated posterior to the premaxilla and forms the boundary ofthe mouth (Bertmar, 1959; Weitzman, 1962; Gijsen & Chardon, 1976). A maxilla



superposed on a premaxilla is the situation encountered notably in acantho-pterygians and cypriniforms (Vandewalle et al., 1992; Potthoff & Tellock, 1993;Mabee & Trendler, 1996; Gluckmann et al., 1999). Also at 45 h, the premaxillashows a dorsal anterior protuberance, forming an emerging anchorage site onthe ethmoid region. By 45h, the teeth have pierced the epithelium that coveredthem.At 63 h, the maxilla extends further to the rear than the premaxilla, and the

angular is distinct from the dentary. The first (unpaired) elements of theneurocranium have appeared: the parasphenoid, occupying part of the hypo-physeal fenestra and the basioccipital. This is the situation encountered innearly all teleosts whose development is known (Weisel, 1967; Langille &Hall, 1987; Vandewalle et al., 1995; Mabee & Trendler, 1996; Voskoboinikova& Kellermann, 1997; Adriaens & Verraes, 1998; Gluckmann et al., 1999). Onthe other hand, no calcified structure appears to replace the regressing parts ofthe cartilaginous hyosymplectic, palato-quadrate and hyoid bar. These struc-tures (namely, the hyomandibular, symplectic, quadrate and ceratohyal) beginto ossify at 131 h. A 3 day lag between the regression of cartilage and theappearance of calcified replacement structures is exceptional, especially inview of the rapidity of the development of the head in B. moorei. In mostknown developmental patterns, the bones appear as the cartilages regress or arevisible when the cartilages are still present (Potthoff et al., 1988; Vandewalleet al., 1997; Voskoboinikova & Kellermann, 1997; Adriaens & Verraes, 1998;Wagemans et al., 1998). It is possible, however, that non-calcified bony struc-tures, which are not revealed by the methods used here, are present at this age.At 131 h, many new dermal elements of the splanchnocranium are present: a

suboperculum and an interoperculum have been added to the operculum, andthe entopterygoid and ectopterygoid have appeared. The dermal pharyngealjaws are becoming large. The maxilla has widened, particularly posterior tothe premaxilla, where its first teeth have appeared. The retroarticular, a peri-chondral bone, is also visible posterior to the mandible.At 199 h, the neurocranium possesses paired exoccipitals, prootics and fron-

tals. This is a late ossification, but this is frequently the case for the skeleton ofthe braincase (Langille & Hall, 1987; Vandewalle et al., 1992; Gluckmann et al.,1999), although in some cases the frontals appear early (Voskoboinikova &Kellermann, 1997; Wagemans et al., 1998). At this stage in B. moorei, theenchondral ossification of the pharyngeal jaws has not begun. Only the tootheddermal ossification is present. Ossification of the fifth ceratobranchials appearsvery late as compared to other species, in which they are among the firststructures to become ossified, notably for functional reasons linked to exogen-ous feeding (Langille & Hall, 1987; Vandewalle et al., 1992). Type Ib cannibal-ism (Baras et al., 2000b) seemingly does not require their presence.Between 271 h and 572 h, the neurocranium progresses toward completion.

The fontanels are well separated. The latero-dermethmoids and the dermeth-moid are fused in a mesethmoid (Adriaens et al., 1997). Only the branchialelements appear much later than observed in other species. (Vandewalle et al.,1992; Potthoff & Tellock, 1993; Gluckmann et al., 1999). At 572h, only thepalatines are missing; these bones are very small in adult Brycon meeki Eigenmann& Hildebrand (Characidae) (Weitzman, 1962).



FUNCTIONAL CONSIDERATIONS

From a functional viewpoint, the development of the head skeleton in teleostsmust, in all cases, meet essential constraints related to fry survival, namely,respiration and feeding. At hatching, the yolk sac provides endogenous foodreserves and its highly vascularized wall permits cutaneous respiration, so noskeletal structure is needed, a priori, to ensure these two essential functions ofthe head. As the yolk sac diminishes the branchial system develops, with thesuccessive appearance of the cartilaginous first four ceratobranchials followedby the epibranchials, which support the respiratory surfaces in the adult. Thefifth ceratobranchials, having no respiratory function, often develop much laterand take part in exogenous feeding. When the yolk sac is completely absorbed,cutaneous respiration is probably considerably reduced, but the branchialstructures have developed. Breathing in water imposes creation of a current ofwater from front to rear (Hughes & Shelton, 1958; Ballintijn, 1969; Osse, 1969;Vandewalle & Chardon, 1981). This flow can be created as soon as threestructures are present: a suspensorium articulating with the neurocranium, ahyoid bar suspended from the hyosymplectic, and the beginnings of an oper-culum. The ossification of the whole branchial basket is generally gradual,thereby suggesting that respiration can be effective if the gills are supportedby cartilaginous structures.The absorption of the yolk sac forces the fish to shift from an endogenous to

an exogenous food supply. Implicit in this transition is that the mouth cavityshould have a reasonably rigid periphery, otherwise the other parts of the head,and particularly the brain, might be damaged. The cartilaginous braincase isgenerally not closed ventrally, but the parasphenoid and, indirectly, the basiocci-pital complement and give rigidity to its structure, thereby limiting the mouthcavity dorsally and reducing the risk that the brain be mechanically damaged.This is a prevailing constraint in development, and the parasphenoid, basioccipi-tal and the first dermal ossification of the splanchnocranium appear generally justbefore or at the same time as the disappearance of the yolk sac (Wagemans &Vandewalle, 2001). In species with very large yolk sacs as in G. feliceps (Tilney &Hecht, 1993), however, ossifications start before the onset of exogenous feeding.Food processing requires functional mouth parts and robust, dentate phar-

yngeal jaws (Vandewalle et al., 1992; Adriaens et al., 2001). The suction-feedingmechanism, which is characteristic of teleost species, (Muller & Osse, 1984;Lauder, 1985) can be ensured when a suspensorium (even cartilaginous), ahyoid bar and an operculum are present, although with a much lower efficacythan with a more sophisticated apparatus in adults. Exogenous feeding mightconsist of attempts to seize the prey, and efficient suction might only appeargradually as the endochondral parts ossify and all the dermal elements of thesuspensorium and operculum are formed. Other functional imperatives inter-vene in the development of the head skeleton. Late closure of the cranial vaultmay be related to constraints linked to brain growth. On the other hand,development of the ethmoid region might not be subject to such crucial orobvious constraints, so that its late appearance does not jeopardise fry survival.This general pattern varies between teleosts. Yet, some general rules seem-

ingly prevail, since all species must solve the same problem linked to the



switch to exogenous feeding. This study revealed, however, that B. mooreiviolates at least two of these reputedly functional rules, but without penalty:1) mouth parts poorly developed for feeding. At 21 h, the head skeleton ofB. moorei meets the minimal requirements for aquatic breathing, but not thoseof exogenous feeding, since the only bony structures are the dentaries, premax-illae and a few pharyngeal teeth. In spite of this, larvae of B. moorei have beenfound to ingest nauplii of A. salina as early as 18–20 h, and fish prey no laterthan 21 h (Baras et al., 2000b). Henceforth, these few skeletal elements areobviously sufficient to enable exogenous feeding in B. moorei, in contrast tothe more elaborate construction of the head skeleton observed in other speciesat the start of exogenous feeding (Vandewalle et al., 1992; Adriaens & Verraes,1998; Gluckmann et al., 1999); 2) periphery of buccopharyngeal cavity not wellformed. When B. moorei starts feeding exogenously, its skull is still incompleteand the floor of the neurocranium is very rudimentary. It consists only ofcartilaginous trabeculae and parachordals, with no parasphenoid and no basioc-cipital, thereby providing very little isolation of the bucco-pharyngeal cavity.This suggests that the hypothesis stating isolation of the mouth cavity from theneurocranium is a priority requirement (Vandewalle et al., 1992; Adriaens &Verraes, 1998; Gluckmann et al., 1999), might not be valid in all cases. Otherrequirements might take precedence in some species. In particular, food intakeand growth may be a more important survival factor than isolation of themouth cavity in species that are subjected to intense competition and predationat a very early age.Muscles were not studied here, but information on their ontogeny and

operation can be retrieved from the video sequences of mouth opening. WhenB. moorei starts feeding exogenously, the epaxial musculature is conspicuousand its contraction can account for the elevation of the neurocranium. Themovements of the mandible and hyoid bars suggest that the sternohyoideus andprotractor hyoidei muscles, and the mandibulo-hyoid ligament are also presentand functional. The urohyal does not appear until 131 h, so it is likely that thesternohyoideus inserts directly or by means of tendons on the hyoid bars. Fastmouth closure, as seen on the video sequences, suggests that the adductor of themandible is also present and functional at this age. Abduction and adduction ofthe cheeks are probably related to movements of the mandible and hyoid bars.Lowering of the hyoid bars probably enables the cheeks to move laterally andthus to be supported by the suspensorium by means of the interhyal, asproposed by Elshoud-Oldenhave & Osse (1976) and Vandewalle (1978). Underthese conditions, the elevator and adductor of the suspensorium do not seemindispensable.As the first trace of the opercular does not appear until 45 h, the gill chamber

can only be opened and shut by a purely membranous structure acting passivelylike the branchiostegal membrane of adults (Liem, 1978; Vandewalle, 1978).The slowness of the movements causing the mouth cavity to enlarge suggeststhat the prey is captured by seizing and that suction plays only a minor role.This contrasts with the situation in adults, where suction is generally primordial(Lauder & Liem, 1980; Osse & Muller, 1980; Lauder, 1983, 1985). Duringingestion of large prey at the early larval stage, these prey enter the mouthcavity step by step, as a result of successive openings and closures. In this



context, the pharyngeal teeth supported by their dermal plates might retain theprey during mouth movements. Pharyngeal teeth are also likely to play a majorrole during type-Ib cannibalism, in which the prey is ingested whole, then itshead is regurgitated from the stomach into the mouth cavity, cut progressivelyand ejected (Baras et al., 2000b). At this age, the only structures capable ofcutting are the toothed pharyngeal jaws. The predator’s head rotates around theprey in one direction, then the other, causing the pharyngeal jaws to move withit (E. Baras, unpubl. data). These movements probably enable the pharyngealjaws to decapitate the prey progressively.At 45 h, the parasphenoid and basioccipital are present; they complete and

reinforce the floor of the neurocranium. From this time onward, B. mooreipossesses a head skeleton as developed as that of any other teleost at the onsetof exogenous feeding. Later B. moorei becomes a type-II cannibal (Baras et al.,2000b) and possesses skeletal structures allowing this practice. The negativeallometric growth of the jaws during the larval stage causes B. moorei to displaypiscivory on proportionally smaller prey than at a younger age.This study provides evidence that B. moorei undergoes much earlier and

faster development of the head structures specialized in feeding than mostother teleosts. This fast development is accompanied by the appearance ofjaws and teeth whose size, relative to body length during the larval stage, areconsiderable in comparison with other teleosts (Shirota, 1970; Baras & Jobling,2002). These traits contribute to making B. moorei an efficient piscivorouspredator during the larval stage, and they account for the intense, early canni-balistic behaviour of this species under culture conditions (Baras et al., 2000b).Interestingly, piscivory starts at a developmental stage when the roof of thebuccal cavity is not well delimited by hard structures, so early piscivory can beviewed as a risky strategy. From an evolutionary standpoint, this ontogeneticpattern can be interpreted as a trade-off. The risk of retaliation or injury duringingestion of large prey is likely to be offset by the advantage of rapid growthassociated with piscivory or cannibalism which will reduce the high predationpressure in the natural environment. This might have been a sufficient pressurebehind the selection of a high-risk high-return strategy against a low-risk low-return strategy. The ontogeny of other Brycon species has not been documentedin fine detail. There are, however, reports of early and intense cannibalismamong cultured specimens (e.g. Brycon cephalus Gunther; Gomes et al., 2000),and of larvae and young juveniles of Brycon spp. being 100% piscivorous in thewild. These findings support the idea that the developmental pattern ofB. moorei is shared by several Brycon species.

The authors thank K. Broman for the linguistic assistance and the referees for theirpositive suggestions and remarks. Breeders of Brycon moorei were obtained through E.U.contract CI1*-CT94-0032 (DG XII HSMU). The work was funded by grant n� 2�4558�03of the Fonds de la Recherche collective (Belgium). At the time of the study E. Baras wasa Research Associate of the Fonds national de la Recherche scientifique (Belgium).

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Electronic Reference

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Early development of the head skeleton in Brycon moorei(Pisces, Ostariophysi, Characidae)