ABOUT SOME SKELETAL PARTTCULARITIES OF TfIE FIRST
VERTEBRAE RELATED TO TAE MODE OF PREY CAETURF, LN
URANOSCOPUS SCABER (URANOSCOPIDAE)
Laweme HUFT,Vhnique GDQSSE, Eric PARMENTIER & pierre vANDEWALLE* (1)
-
m C T . Fetdlng ie Urunmgcops~ C o b c irs- G
by beading of thm body just beb'md tbt
M.
&dmg la dated ur the o~ganiwipad the Rrst fme vembrae; vertebral Cenm of 1
w Wght
~ ' n om
g into the uexf: short, leas ljtted m e d &ties, p e n c e vf many intmatebd bgmeak
B e n d i p 8 o f r t t e r e ~ ~ o l u ~ c ~ L h e ~ ~ r o a amtd~t ~l lpt ~marr6dq m j ~ b e m a t h
tbt m;
it also kings the pharyngeal jaw, shifted with m p c t to a& other at m, t
6 PaFt a c h
o*.
R&Il'&-
- ~ c u M t 4 squelutiqua
s
des prerrdkm es&m en relation a
w k mode de pPisc de
nomime c f m UMIMSM~UB
scabsr {Yrana:smpidac>.
La paise dtnourriaw Ehez U m m w p u sc&r
~t caractErisBe par awe p t i w du % si~ B l ' d & d e t a t W . ~ p I i u r c e s t c a ~ a L'mgmisalion&EiRgpmmi&s
p~8~
u&&w
mps m&nwpcu &lev& st mbW& Its mls d#s I= sum, lreppcpiacs comes ct red#w&,
pdwm de n m l m m Iigatmrus inferuerrEbraux. C m pIium entrapme une rpWm &e la &t qui
amkne la bwehe B h'wvtir v m le hauc immtWment sow la proie u place leo m o i r e s
~ & w d,h d & ~~I
au,
I
les uneg en face & sum les r e n h t apt&- ii saisir la pmk.
-
1Cey-words. Lhoscopid*,
U ~ I ~ O S$caber,
EIIW
~ ing, Vertcbd cohtm,
The stargazer, LFrmow~pusseaber Linne, 1758. is a Mediterranean fish that feeds
by lying in wait for its prey. Its head is flat and wide, companding with a benthic life.
Buried in the sand almost to its eyes, it a m s its prey by m m s of a protractile appendix w d e d to the mandible and waved like a lure {Patchot and has, 19m.Pietsch,
19g9). At the tight mornmt, It lunges qui~kIyout of the substrate md catchm the prey. or
tries to. The lunge is a m d by bending between the head and trunk by BOP and morc
(Gwse 4t al., 1995). The dm of the pt.~sentpaper is to exmine whether there are specid
adaptations of h e mtwior vertebral eolumn that make this bending possible, d to
assess changes in the disposition d cephdic $keIet&lmctures as W
n
i g occurs. The
cephalic skleron bas been described by Hemh (19889) and will thus not be described
*rl
here.
(I) Uniwsit6 de Lice. MtPt de ZmIagie, h b a t o i r e t M~~pholagic
fomti~~aelk
et mlutive. 22
Quai Van Ben&% B-4020Lib& Belgique. ~.Yandtwdle@rlg,ac.bel]
* AurhPr for cormpondanm.
MATERIAL A m METHODS
Twelve dead Urrmascapw seaber specimens Istandud length W e e n 16 and
S . 5 cm) were s t a d frozen or in alcohol. One was cleared with ttypsin and stsrPed with
alizarin red for observation of the h a y skeleton, the others were d i s d and examined
with a Wild MlO s ~ b i n o c u l a rmicroscope equipped with a e am era lucida and a photographic tube.
Three live spbcimcnri (standard Imgth: 17.5. 19 and B c m ) w m &&mated to living and f e e d i i on live prey in an aquarium. They were filmed at 430 gs with a Photoso&s IF% camera (Eastman Kwbk nigh Speed film, 400 ASA. 3aoOK0).
AU s@mens snrdid were from CaIvi Bay (STARESO statlan) and Lion Gulf {GFau
du Roy aquarium). Franm.
Abbreviations nsed in the figures
NA: neural arch
BOC: basioccipital
B: eye
NS: neural spine
HY: hyobrmchial apparatus OP: 0pe~~b
LI 1,2,3,4,5: ligament I to 5 PF. pectoral fine
MAX: maxilla
MD: mandible
PJ: pharyngeal jaw
PAP: paragoph ysis
POE postzygapophysis
P2: ptezygapophysis
SPNl? spinal m foman
VC: v m b d aloentrum
V1,2.3,4.5,6: vertebra 1 to 6
RESULTS
Movements
Ending of the vertebral column in Ummscopm s d e r occurs when a live prey
passes above its head (Fig. 1), Bending causes a s l i t elevation of the trunk and a major
lifting of the mrmmiurn. It always takes less than 3110D s, after which the fish mumes its initial position at a quite variable speed (32/1# s to 551100 s).
Vertebrae
l l w first five akdominal vertebrae dispIg several original featma. They bar broader neural spines than the fallowing vm&me. The fifst neural spine is sh~rtert h the
amrocraniurn heigth. The leagth of the mural spines increases from the first to h e sixth
vertebm and these fmt neural spines are not tilted w far backward as the following ones.
Viewed from the side (Pig. 3), the fmt four vertebral centra are lower than those of the
following vertebrae; they display no prominent parapophysm (Fig. 2).
The first two vertebrae bear no rib.The first vertebra i s longer than the folIowing
ones and is attached to the o~cipitalregion by short fibres, h m the top of the $hart
neural: spine to the W e ofthe vertebral cenmtn; this malses it dmst completely immobile. The next three vertebrrre are short and their vertebral centra are widw than high. The
anterior end of each one is narrower lhaYI the posterior end of the preceding one, so that
the first four vertebrae interlock. The second. third, and fourth neural arches are situated
quite forward on the vertebral centra. The from part of each vertebral centrum is narrower
than the rear part of the weding one. They Bear prezygapophyses with extended,
ouhvard-armed articulation sudaees. Each of these surfaces i s coapred to that of tbe inward-turned pos9zygqophysis of the preceding vertebra (Fig. 3).
Skelml particdaritim related to prey eaptue in Urqwscopw sc&r
I63
-
Omnoscupus scaber. S c h t i c lateral views sllowing &ow, the fish lying in wait for its prey,
and below. the fish with r a i d head. w k n the mouth is wide open and bending is m i m a l . The prey
has already been sucked into tlw b u c d cavity. The drawings were made Prom frames of a film made
at 400 frames per second.
Fa 1.
Fig.2. - Uruiw.~r.opu~
sruber. A: Yewd view of the first webrae: the interrupted lines show h e limits
of the L1.5 ligaments. B: L a t e d view of the second vertebra: the intempted Ihes situare the mne
where the postzygaphophyds ~ i c u l a t e swith the prezygapophysis of the next vertebra.
The third vertebra bears a pair of ribs at the upper extremity of the neural arch. The
fourth is flanked by ribs, articulated on the lateral walls of he neural arch. Not until the
Fig. 3. - Urannscopus scuber. A: Lateral view of the first vertebrae and associated ligaments; B:Lateral
view of the positions PC these venebrne when bending exceeds 45". Asterisks indicate where the ribs
articulate with the vertebne.
fifth vertebra do the ribs appear as usual on the parapophyses. The fifth vertebra Iooks
partially "normal". Although the front of its vertebral centturn is stilI narrow and flattened, its pasterior surface has the same shape as the following vertebra. The parapophyses
protrude ventro-laterally a1 the front of the vertebral centrum. The neural arch i s located
almost completely above the vertebral centrum and is extended by a more tapered neural
spine.
All of the vertebrae are attached to each other by ligaments. A large dorsal septum
(LI.1) encloses the neural spines from the rear to the fifth vertebra; then it thickens and
shortens as the height of the neural spines decreases. It attaches to the rear of the n w cranium where i t spreads out. A part of the epaxial musculature (wide and voluminous i n
the back of the head) inserts onto this septum.
Thick ligaments (LI.2)link each neural arch with the dorsal side of the prezygapophysis of the next vertebra. The first four ligaments are a little more tilted than the following ones. which are wider and thinner. In between the first five vertebrae there is a ligament tI.3. almost horizontal and partly masked by L1.2 (completely masked between the
next vertebrae). Another thick ligament (L1.4)
links the inner surface of a prezygapophysis with the postzygapophysis and the vertebral centrum of the preceding vertebra.
Lastly, each vertebra1 centrum is linked to the next by a ligament LI.5 consisting of short
fibres. T h e LI.5 fibres connecting the fust four vwtebrae appear longer than those of the
foIlowing ligaments.
Skeletal particularities relrded to prey Gaptltre l a Umostopur sraber
165
Buccal parts and pharyngeal jaws
One original feature of the buccal and pharyngeal jaws is their position. While the
fish is lying in wait. the two buccal jaws are almost vertical (Fig. 1A). Upon bending and
prey capture. the neurocranial elevation raises the buccal jaws but the mandible retains
practically the same vertical position whereas the rnaxillaries and premaxillaries become
almost horizontal (Fig. 1 B). The expansion of the buccal cavity is confirmed by the
hyoid depression in comparison with the neurocraniurn top, but not with the bottom
(elevation).
Observed on dead animals. the tower pharyngeal jaws are located Forward the upper
(Fig.IA). In curved position, the upper and tower pharyngeal
jaws appear opposite (Fig. 1Bl.
jaws in extended position
Teleosts have different systems fw opening their mouths. Elevation of the n e w m i u r n is one possible system; it is always caused by contractian of the epaial m~sculature (Vatrclewalle, 1878; Liem, 1979; Sibbing, 1982; Wesmear md Wainwright, 15189),
Elevation of the m u m i u r n by about loo during feeding has k e n d%scriWin many
fish (Alexander, 1967; Lim. 1978: budex. 1973, 1980. 1981; b u c k rmd Liem. 198 1;
Sibbing, 1982; Muller, 1987; Westneat, 1994: Vandewalle el a/., 1995). This Iifting
d m not saem to require special matomica1 features. Some teleosts are capable of a greater
elevarim of the cephalic regiorr: 35" for kcrochirichhys macmhirrrs {Valenciennes)
( H a m . 3 9793. 40° for L ~ i o c q h a l # puicker (Gray)
and Liem 1 98 f 1. 50' For
Symceia verrutosa BIoeh 4 Schneider (Grobecker. 1983). 409 for Synpathidae (Bergen
and Wainwright, 1997). U u k ad Lindsey (197%). H
o
w (197% arad h w k r arad Liem
(1981) have evidenced the ~peialisedmorphological f e r n s of certain tdeosts capabIe
of e
n mwked1y W n g of the front of the vertebral columa hall c a m the anterior
venebrae are modified. but in different manners. M4cmhiridthys m~cmAlrwraises its
head simply by rotating mound the first, reduced vertebra. fitting into the second vettebra
(Howes, 1979). In the charaeoid Raphidon vfilpinw (Agassix). bending can teach 45"
and orcurs posterior to the first four vmebrae, probably bcause of the p m c e of the
Weberim apparatus. The fifth vembra i s wide. not vtgy high. and bears a shorter neural
spine than the fallowing onw (Miuk and Lindsey. 19781. In Urmoscopw sc&r, the
c h m p in the vertebral column concern the first five vertebrae, which expl&s why the
bending angle can be exceptionally great in this species (Go- ei oL, 1995). When the
spaxial musculature, fixed on a small occipital crest and a wide occipital region (Piestch,
1989) contracts, vertebrae IWO to five, being not high, are lifted. This rotation is made
possible by h e interlocking of the first vertebral cmtra, the incline af the p r e and
postzygapnphyses. and the difference in width between the fmnt and rear of the first
neutat arches, enabling them to cbver each other to a certain degree. The structures limiting this rotation are probably the LI.5 ligaments and the neural spines. The s u ~ u e n ~
vertebrae, M u s e of their stai~dardmwphology. should not enable the vertebral column
to curve differently f k n what js usually observed in tefeosts (Lauder. 1979: Sibbing.
1982; Vandewalle &r a!., 19951, b~wnwmdbending of the anterior region of the vertebral
column should he minimal sIighr to. impossible in Uranusmpw scahr, due to the pre
sea@ of ligaments L1.1, L1.2,L1.3,and LI.4.
In acanthopterygians, during feeding, the mouth. pointed towards the prey, opens
first, after which the buccal cavity, then the opercular cavity dilate, causing the prey to be
sucked in. Finally the pharyngeal jaws, facing each other, separate to grasp the prey
ILauder, 1980, 1981; Westneat and Wainwright, 1989; Vandewdle el al., 1992, 1995). In
Umnoscopus scaber, the mouth i s turned upward. Opening of the mouth without rotation
of the neurocranium would protrude the mouth opening, whereas the prey i s located above
the predator. Rotation of the neurocraniurn makes it possible to open the mouth upward,
(practically) without modifying the orientation of the mandible. The distance between the
mandibular and the premaxillaries increases. nevertheless, as upon any opening of the
mouth (Alexander, 1967; Lauder, 1980, 1981; VandewalIe., 1980). This requires participation of the ventral muscuIature of the head (protractor hyoideus and sternohyoideus muscles) to maintain the mandible at its position. Contraction of this musculature is attested
by depression of the buccaI cavity bottom (ventral part of the hyobranchial system) with
respect to the skull. If this did not occur, the mandible would follow at least partially, like
the rest of the head. the rotatory motion of the neurocmnium. The originality of mouth
opening in U,scaber thus does not reside in any special motion of the buccal parts with
respect to one another. but solely in the possibility o f bending the vertebra[ column to a
larger degree than other teleosts. In the stonefish Synanceia verrucoso, which also Iies in
wait like U. scaber, bending causes only raising of the head without motion of the body.
In the stonefish the mandible is also practically vertical at rest and remains so during
opening of the mouth (Grobecker, t 983).
Bending of the vertebral column most probably has a second beneficial consequence. At rest, the toothed plates of the pharyngeal jaws of Umnoscops scaber do not
face each other as in most teleosts (Liem, 1970: Liem and Osse, 1975; Aerts +I a[., 1986;
Gobalet, 1989; Vandewalle el al., 1992); the lower ones are markedly in front of the upper
ones. In this position, the pharyngeal jaws wwId be unable to grasp a prey. Majw bending of the front of the vertebral column, causing rotation of the neurocraniurn, may cause
an upward rotation of the upper pharyngeal jaws while the lower ones are retained by the
depression of the mouth bottom: this would place the toothed plates one above the other.
position enabling them to grasp a prey.
Acknowledgemenb. - W ethank Dr D.Bay (Stpresa.Cplvi, France) for providing us with specimens of
Uranmcop~csscabcr, and Mn K. Broman for translating the text in English.
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Skeletal particularities related to prey capture in Umoscopus scaber
..
I67
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R e p le 16-12.1998.
AcceptPpour publication le 14.04.1999.