FACULTY OF SCIENCES
UNIVERSITEIT
GENT
D e p a r tm e n t o f Biology
E volutionary M orphology o f V e rte b ra te s
Structural diversity in the cranial
musculoskeletal system in Anguilliformes:
an evolutionary-m orphological study
P a rt 1 - T e x t
Soheil Eagderi
Th esis s u b m itte d to o b ta in th e d e g re e
o f D o c to r in S ciences (B io lo g y )
A ca d em ic y e a r 2 0 0 9 - 2 0 1 0
R ector: P rof. D r. Paul v a n C a u w e n b e rg e
D ean : P rof. D r. H e rw ig D e jo n g h e
P ro m o te r: P rof. D r. D o m in iq u e A d ria e n s
miii
UNIVERSITEIT
GENT
FACULTY OF SCIENCES
DEPARTMENT OF BIOLOGY
EVOLUTIONARY MORPHOLOGY OF VERTEBRATES
S tru ctu ral d iv ers ity in th e cranial m usculoskeletal system
in A nguilliform es: an e v o lu tio n a ry m orphological study
Part 1 - Text
Soheil Eagderi
Thesis submitted to obtain the degree
of Doctor in Sciences (Biology)
Academic year 2009-2010
Rector: Prof. Dr. Paul van Cauwenberge
Dean: Prof. Dr. Herwig Dejonghe
Promoter: Prof. Dr. Dominique Adriaens
C o ver im a g e : CT scan im a g e o f th e s k u ll o f S im enchelys pa rasiticu s
M em bers of th e Exam ination C om m ittee
Prof. Koen Sabbe, Chairman
(Ghent University)
Prof. Dr. Dominique Adriaens, Promoter
(Ghent University)
Dr. Eric Parmentier
(University of Liège)
Dr. Natalie De Schepper
Dr. Sam Van Wassenbergh
(University of Antwerp)
Prof. Dr. Ann Huysseune
(Ghent University)
Dr. Tom Geerinckx
(Ghent University)
Dr. Emmanuel Vreven
(Royal Museum for Central Africa)
Prof. Dr. Luc Lens
(Ghent University)
Reading com m ittee
Dr. Eric Parmentier
(University of Liège)
Dr. Natalie De Schepper
Dr. Sam Van Wassenbergh
(University of Antwerp)
T a b le o f c o n t e n t s
C hapter 1 - In tro d u c tio n
1.1. General c o n te x t.......................................................................................................................... 1
1.1.1. Adaptation and d iv e rs ity .......................................................................... 1
1.1.2. Taxonomical history of Anguilliform es.....................................................4
1.1.3. Introduction of studied ta x a ......................................................................5
1.1.3.1. A nguillidae............................................................................................ 5
1.1.3.2. Nettastom atidae....................................................................................7
1.1.3.3. Heterenchelyidae.................................................................................. 7
1.1.3.4. Synaphobranchidae.............................................................................. 7
1.1.3.5. M uraenidae............................................................................................ 8
1.1.3.6. Congridae............................................................................................... 9
1.1.3.7. Eurypharyngidae.................................................................................. 9
1.2. Aims and thesis o u tlin e s............................................................................................................9
1.2.1. General aim of this s tu d y ..........................................................................9
1.2.2. Outline of th e s is ...................................................................................... 11
C hapter 2 - Aim s and S tru ctu re of th e thesis
2.1. Material exam ined............................................................................................................. 15
2.2. Methodsl9
2.2.1. Preparation of specim ens....................................................................... 17
2.2.1.1. Anaesthesia, sacifice and fix a tio n ................................................. 17
2.2.2. M orphology.............................................................................................. 17
2.2.2.1. In toto clearingand s ta in in g ............................................................ 17
2.2.2.2. Dissections...................................................................................... 18
2.2.2.3. Histological sections....................................................................... 19
2.2.2.4. Shape analysis.................................................................................. 22
2.2.2.5. Visualization..................................................................................... 23
2.2.3. Term inology............................................................................................. 23
C hapter 3 -H e a d M orphology of th e Duckbill Eel
i
T f t b U OF CONTENTS
3.1. A b stra ct....................................................................................................... 25
3.2. In tro d u ctio n ................................................................................................ 26
3.3. Material and m ethods.................................................................................27
3.4. Results.......................................................................................................... 27
3.4.1. Cranial Osteology of Hoplunnis p u n c ta ta ...........................................27
3.4.2. Cephalic lateral sy s te m ........................................................................ 31
3.4.3. Cranial myology of Hoplunnis p u n c ta ta ............................................ 32
3.4.4. Shape analysis.......................................................................................34
3.5. Discussion................................................................................................... 35
3.5.1. Morphological changes towards jaw elongation................................. 35
3.5.1.1. O steology......................................................................................... 35
3.5.1.2. M yology............................................................................................ 36
3.5.1.3. Jaw elongation................................................................................. 37
3.5.2. Functional consideration of snout elongation..................................... 38
C hapter 4 - Cephalic M orphology of P ythonichthys
m acruru s
4.1. A b stra ct....................................................................................................... 43
4.2. In tro d u ctio n ................................................................................................ 43
4.3. Material and m ethods................................................................................45
4.4. Results......................................................................................................... 46
4.4.1. Cranial Osteology of pythonichthys m a cruru s.................................. 46
4.4.2. Cranial myology of pythonichthys m a cruru s................................... 51
4.4.2.1. Muscles of the ch e ek.................................................................... 51
4.4.2.2. Ventral muscles of the h e a d ......................................................... 52
4.4.2.3. Body m uscles...................................................................................53
4.5. Discussion................................................................................................... 53
4.5.1. Cranial specializations related to head-first burrow ing...................53
4.5.1.1. Eye reduction.................................................................................. 54
4.5.1.2. Widened cephalic lateral line canals..............................................55
4.5.1.3. Gili o p ening..................................................................................... 55
4.5.1.4. Different orientation of the anterior section of the adductor
mandibulae muscle com plex................................................................................................... 55
T f t b U OF CONTENTS
4.5.1.5. Skull shape and large insertion sites of body muscles on the
neurocranium .............................................................................................................................. 56
4.5.2.
Variable degree of head-first burrowing specializations in
Anguilliformes
57
C hapter 5 - Cephalic Specialization in a P arasitic Eel.
S im enchelys parasiticu s
5.1. A b stra ct..................................................................................................... 61
5.2. In tro d u ctio n ................................................................................................ 61
5.3. Material and m ethods................................................................................62
5.4. Results......................................................................................................... 64
5.4.1. Cranial osteology of Simenchelys parasiticus................................. 64
5.4.2. Cranial myology of Simenchelys parasiticus....................................69
5.4.3. Cranial myology of Ilyophis b runneus..............................................72
5.4.4. Cranial myology of Synaphobranchus brevidorsalis...................... 75
5.5. Discussion................................................................................................. 77
5.5.1. Variation in cranial morphology of Synaphobranchidae................. 77
5.5.1.1. O steology...................................................................................... 78
5.5.1.2. M yology......................................................................................... 79
5.5.2. Cranial specializations in relation to parasitism ...............................80
C hapter 6 - Cephalic S pecializations in Relation to a
Second Set o f Jaws in M uraenids
6.2. A b stra ct......................................................................................................85
6.2. In tro d u ctio n ............................................................................................... 85
6.3. Material and m ethods.............................................................................. 86
6.4. Results....................................................................................................... 86
6.4.1. Cranial osteology: Arisoma gilberti ...................................................86
6.4.2. Cranial myology: Arisoma g ilb e rti...................................................... 92
6.4.3. Cranial osteology: Gymnothorax prasinus and Anarchias allardicei
(Muraeninae and Uropterygiinae: Muraenidae) ..................................................................... 95
6.4.4. Cranial Myology: Gymnothorax prasinus and Anarchias allardicei 100
6.5. Discussion............................................................................................. 104
T f t b U OF CONTENTS
C hapter 7 - Head M orphology of th e Pelican Eel,
E u ryp h aryn x o elecanoide
7.1. A b stra ct.................................................................................................... 109
7.2. In tro d u ctio n ............................................................................................... 109
7.3. Material and m ethods.............................................................................. I l l
7.4. Results....................................................................................................... 112
7.4.1. Cranial O steology............................................................................... 112
7.4.2. Cranial m yo lo g y................................................................................. 115
7.5. Discussion.................................................................................................. 115
C hanter 8 - G eneral Discussion
8.1. Evolutionary pattern of structural changes in the head musculoskeletal
S yste m ............................................................................................................................................ 121
8.2. Adaptive versus non-adaptive morphological e vo lu tio n ....................... 130
8.3. Some concluding rem arks....................................................................... 132
8.4. Insights for further research.................................................................. 133
S u m m a r y ................................................................................................................................. 135
L itra tu re c it e d .................................................................................................................... 137
Publication lis t .................................................................................................................... 157
AckNOwLEdqMENTS
A cknow ledgm ents
I wish to express m y genuine and sincere g ra titu d e to those who co n trib u te d to the
process th a t led to th is d isse rta tio n , as w ith o u t th e ir help I could not have fu lfille d
th is task.
In fin ite th a n ks go to m y su p erviso r and p ro m o te r Prof. Dr. D om inique A driaens,
w ho gave me th e o p p o rtu n ity to s ta rt and com plete m y doctoral thesis in his
research group. He not o n ly g re a tly increased m y insig h t in biology, especially in
th e w onderful w orld o f v e rte b ra te m o rph o log y, b u t he also is a tru ly inspiring
scien tist and person. His corrections and com m ents, th a t fille d all spaces between
m y d o ub le-lined m anuscripts w ith d iffe re n t colors, not o nly b ro u g h t m y w ritin g to a
h ig h e r level, but also gave m ore color to m y personal and scien tific experience. His
u nfailing enthusiasm and patience could alw ays m o tiv a te me and I tru ly find it hard
to find pro pe r w ords to express m y g ra titu d e to him .
"T h a n k you v e ry m uch, best te a ch e r I e ve r h a d."
I am deeply indebted to Prof. Dr. W a lte r Verraes fo r his help, especially when I
a rrive d in Belgium .
I wish to express m y th a n ks to
Prof.
Dr. Ann
Huysseune fo r increasing m y
know ledge o f histology.
My sincere th a n ks
go to
m y colleagues
in th e
research
group 'E v o lu tio n a ry
M orphology o f V e rte b ra te s', Dr. Tom G eerinckx, Dr. Natalie De Schepper, Dr. Frank
H uyse n tru yt, Dr. S tijn Devaere, Barbara De Kegel, Joachim C hristiaens, Marleen
B runain, Heleen Leysen, Fatemeh Tabatabaei, Paul Van Daele, Tim T k in t, Annelies
G enbrugge, Celine Id e , Emilie Deseamos and Niels De Sm et. They w ere not only
colleagues, b u t also good frie n ds o f m ine, who w ere alw ays ready to help.
Several o f these deserve an a d ditional w ord o f th a n k , as th e ir assistance had an
enorm ous and positive im pact on th is w ork:
Tom G eerinckx; th a n k you fo r y o u r assistance, co rrectin g m y w ritin g s , providing
critical co m m ents, and helping me e n th u sia stica lly and p a tie n tly to understand
m orph o log y and exp erim e nta l m ethods w he n e ve r I needed help.
Natalie
De S chepper; th a n k you fo r y o u r help in s ta rtin g
my
PhD, teaching
e xp erim e nta l m ethods and p roviding p a rt o f m y m a terial.
Frank H uyse n tru yt, S tijn Devaere and Heleen Leysen; th a n k you fo r sharing yo u r
tim e w ith me fo r answ ering m y questions.
Barbara, Joachim and M arleen; th a n k you fo r all th e practical help.
Of course, I th a n k all people o f th e th ird flo o r, especially Hilde Van W ynsberge fo r
her assistance so often d u ring m y doctorate.
I am p ro fo un d ly indebted to th e m em bers o f m y PhD ju ry : Prof. Dr. Koen Sabbe,
Dr. Eric P arm entier, Dr. Natalie De Schepper, Dr. Sam Van W assenbergh, Prof. Dr.
Ann Huysseune, Dr. Tom G eerinckx, Dr. Emm anuel V reven, and Prof. Dr. Luc Lens.
I acknow ledge th e fo llo w ing inte rn a tio n a l scientists fo r th e ir v e ry useful com m ents:
R.S. Mehta (UcDavis, USA), D.G. S m ith , (S m ith so nia n , USA), D. Johnson (N ational
Museum
o f Natural
H istory-S m ith so n ia n
In s titu tio n )
and J.G.
Nielsen
(N atural
H istory Museum o f D enm ark, Copenhagen U nive rsity).
I also acknow ledge P. Pruvost (Paris Natural H istory M useum , MNHN), R.H. Robins
and A. Lopez (Florida Museum o f Natural H isto ry), M. M cG routher (A ustralian
M useum ), D. Johnson (N ational Museum o f Natural H istory-S m ith so n ia n In s titu tio n )
and P.R. M pller (N atural H istory Museum o f D enm ark, Copenhagen U n ive rsity) fo r
m aking m useum specim ens available to me.
I appreciate th e su p p o rt o f m y colleagues a t Tehran U nive rsity d u ring m y s tu d y in
Belgium .
And o f course m y parents I ca n 't th a n k enough fo r e ve ryth in g th e y have done to
me. They did su p p o rt and m o tiv a te me th ro u g h o u t m y studies. So again m um ,
dad... THANKS!
Also I th a n k m y d a u g h te r Sania fo r understanding th a t her papa should w o rk and
not to be disturbed fro m tim e to tim e .
And, last but not least, a huge th a n ks to m y w ife, A ram , and her fa m ily . W ith o u t
A ram 's
help it w ould
have been v e ry d iffic u lt to finish
su p po rtin g me a t all tim es. Thank you again fo r e v e ryth in g .
th is w ork.
She kept
ChApTER 1
iNTROducriON
1
I n t r o c Ju c t í o n
C h ap ter one
G eneral In tro d u c tio n
1 .1 . G e n e ra l C o n te x t
1 .1 .1 . A d a p ta tio n an d d iv e rs ity
A va st body o f scien tific e ffo rt is concerned w ith cla rifyin g th e evo lu tio n in various
groups
o f organism s, w ith natural selection
behind
it (D arw in,
1859).
being th e fu n d a m e n ta l
S u rvivo rsh ip is related to
d rivin g force
a d ap tatio n s th a t can be
m easured as th e perform ance o f fu n ctio n s in th e c o n te x t o f th e in te ractio n between
an organism
and
its e n v iro n m e n t, such th a t s u rvivo rsh ip
is m aintained
o ver
g enerations (B rock, 2000). In th is process, aspects o f fo rm and fu n ctio n o f organ
(o r organ syste m ) can change. System s th a t display a co n sta n t fu n ctio n m ay re flect
re la tiv e ly little change in its com posing s tru ctu re s o r m ay ju s t change fu n ctio n w ith
a new a d aptation arising (R idley, 2004). As such, m any stru ctu re s m ay arise th a t
can
be described as e v o lu tio n a ry
novelties.
S om ething th a t we
recognize as
novelties can arise even th ro u g h th e m o dification o f e xistin g s tru ctu re s (R idley,
2004).
Hence, th e e v o lu tio n a ry origin
o f a d ap tatio n s consists o f th e gradual
accum ulation o f new o r m odified anatom ical s tru ctu re s,
physiological processes o r
behavioral tra its (Solom on e t a l., 2005).
The head m usculoskeletal system and its in te g ra tio n in th e fu n ctio n in g o f th e skull
can be considered as a h ig h ly im p o rta n t p a tte rn fo r giving rise to e vo lu tio n a ry
specializations by m eans o f natural selection. The head o f fishes is q u ite com plex,
w ith o ve r 30 individual bony elem ents th a t can be m oved by th e ir associated
muscles. T h ro u g h o u t evo lu tio n
q u ite
som e va ria tio n
o rig in ate d
in th e
cranial
m usculoskeletal system o f fishes. Judging fro m th a t, it can be expected th a t m any
com binations o f m uscles and bones are possible to perform a certain fu n c tio n , such
as those fo r m outh opening and closing. The head bones and re le va n t m uscles are
im p o rta n t elem ents com posing th e feeding and respiration apparatus.
In co n tra st, som e ch a racteristics o f an organism are not necessarily th e re su lt of
a d a p tative evo lu tio n b u t ra th e r represent e v o lu tio n a ry c o n stra in ts, phylogenetic
predispositions
o r ju s t
random
phenotypic
1
va ria tio n
th a t
has
no
e ffe ct
on
1
I n t r o c Ju c t í o n
perform ance. E volutionary co n stra in ts can be defined as lim its to th e d ire ctio n ,
n a tu re, rate o r a m o u n t o f change th a t is possible (C arroll, 1997a). A phylogenetic
predisposition can be defined as a retained ancestral cha racter th a t is shared by all
m em bers o f th a t p hylogenetic group (M ishler, 2 0 03 ). For instance, body elongation
o f A n g uillifo rm e s can be expected to be th e re su lt o f adaptive e vo lu tio n , w hereas
th is
fe a tu re
is
to
be
considered
a
p hylogenetic
predisposition
w ith in
the
A n g uillifo rm e s fam ilies.
Body
elongation
has
evolved
m any
tim e s
ind e p e nd e n tly
and
in
d iffe re n t
e n viro n m e n ta l and ecological circum stances (W ard and B rainerd, 2 0 0 7 ), which is
considered a daptive fo r a large range o f life styles (De Schepper, 2007). The
elongated body in all m em bers o f th e eel fa m ilie s is th e basic A n g uillifo rm e s body
plan, but va ria tio n exists. In som e eels, fo r exam ple body elongation is quite
e xtre m e , e .g ., th e tro p ical m o ray S tro p h id o n s a th e te (M uraenidae) (C astle, 1968).
The A n g uillifo rm e s is an o rd e r th a t still needs to be fu lly explored. Many new
species o f A n g u illifo rm e s are described each y e a r (S m ith and Kanazawa, 1977;
Castle and McCosker, 1999; Chen and Mok, 2001; Sm ith and K arm ovskaya, 2003;
S m ith , 2 0 0 4 ), and m ore are expected to be recognized as va rio u s h a bitats are
exam ined m ore closely, especially those o f th e deep sea.
There are a n u m b e r o f a d ap tatio n s which m ay have evolved fro m eels w ith a
re la tive ly
sed en tary
N em ichthyidae,
life
style
S e rrivo m e rid a e
(C astle,
and
1968).
Mesopelagic
N e tta sto m a tid ae , w hich
eels,
such
in h a b it th e
as
ocean
depths betw een surface and b o tto m , have th e ir own set o f a d ap tatio n s (such as
elongated ja w s and increased dentig e ro us areas by th e fo rw a rd prolongation o f th e
sn o ut and associated to o th -b e a rin g bones (Böhlke, 1 989a)).
As an exam ple o f tro p h ic a d ap tatio n s in eels, a few have becom e plankton feeders,
w here a p re d a to ry lifestyle represents th e p rim itiv e condition o f A n g uillifo rm e s
(G osline, 1971; S m ith , 1989a). The so-called garden eels, o f th e congrid su b fa m ily
H eterocongrinae, live in colonies in fine coral sand, usually in re e f areas w here
th e re is a re la tiv e ly strong cu rre n t. A tu b e is excavated in th e se d im e n t by th e tail
so th a t th e anim al m ay sink o u t o f sigh t in its b u rro w , o r hold a portion o f its body
out
into
th e
fo o d -be a ring
c u rre n t
(C astle,
2
1968)
(Fig.
1.1).
The
ja w s
of
1
I n t r o c Ju c t í o n
heterocongrines are much shortened and th e large eyes are placed on th e tip o f the
sn o ut (Castle and Randall, 1999; De Schepper e t a l., 2005).
A lthough th e e e l-like body fo rm
allow s sustained sw im m in g (A a re stru p e t al.,
2 0 0 9 ), it is not e ffic ie n t fo r sustained m o ve m e n t a t high sw im m in g speeds. This
body shape allow s eels w edging its e lf into crevices o r into b ottom se dim ents, th e ir
fa v o rite h a bitats (C astle, 1968). In
burrow ing species, like M oringua edw ardsi
(M oringuidae) a n u m be r o f a d ap tatio n s o f cranial s tru ctu re s have appeared in
relation to th is m ode o f life (De Schepper e t a l., 2 0 05 ). For exam ple, sm all gili
openings
positioned
m ore
v e n tra lly
m ay
assist
in
p re venting
se d im e n t fro m
e n te rin g into th e gili ca v ity (De Schepper e t a l., 2005).
Most eels are rapacious feeders and m any display a considerable e n la rg e m e n t o f
th e te e th and ja w s (C astle, 1968). For exam ple, m o ray eels th a t are found living in
holes, under rocks and crevices, possess large pointed te e th on th e ir oral jaw s. In
a d d itio n , th e y use a second set o f dentig e ro us ja w s, i.e. th e pharyngeal ja w s to
grab and pull th e prey down to w a rds th e ir esophagus (M ehta and W a in w rig h t,
2007a).
Also,
som e
eels
display
peculiar
and
unique
te e th ,
like
those
of
Sim enchelys p a rasiticu s (S ynaphobranchidae). In th is deep w a te r species, w hich is
claim ed to spend som e o f its life feeding p a rasitica lly on th e tissues o f o th e r fishes,
th e m outh gape is reduced and is considered to be m odified into an effective
sucking m echanism , w ith ch ise l-like te e th on th e ja w s (N elson, 2 0 06 ; Robins and
Robins, 1989).
A n o th e r
deep
w a te r
species,
th e
g u ip e r
eel
(E u ryp h a ryn x
pelecanoides:
E u ryp haryngidae), is probably one o f th e m ost bizarre looking cre atures w ith in th e
A n g uillifo rm e s th a t bears e x tre m e ly enlarged gapes a t the tip o f its e e l-like body
(F ig .1.1).
The
d iv e rs ity
o f eels
is astounding
and
s tru c tu ra l
d iv e rs ity
in
th e ir
cranial
m usculoskeletal system is th u s to be expected. The stu d y o f such a d iv e rs ity w ill
provide in fo rm a tio n on how th e ir s tru c tu re s have changed th ro u g h a daptive (o r
n o n -a d a p tive ) e vo lu tio n and th is m ay c o n trib u te to a b e tte r understanding o f
A n g uillifo rm e s classification and e vo lution.
3
1
I n t r o c Ju c t í o n
1 .1 .2 . T a x o n o m ic a l h is to ry o f A n g u illifo rm e s
The
A n g uillifo rm e s,
an
o rd e r o f teleosts,
belongs
to
th e
su p ero rd e r o f the
Elopom orpha (N elson, 2 0 06 ). The m em bers o f th e Elopom orpha live in a highly
diverse range o f h a bita ts, going fro m fre s h w a te r to s a ltw a te r and a t depths ranging
fro m th e shallow co n tine n ta l sh e lf to th e deep sea. The com m on fe a tu re o f th is
group is th e d is tin c t pelagic larval stage, te rm e d leptocephalus (H elfm an e t al.,
1997; Wang e t a l., 2003).
Regan (1 9 0 9 ) recognized th e A nguilloides (Apoda) as d is tin c t fro m o th e r e e l-like
fishes because o f separate
p re m a xilla ries being absent and th e v o m e r being
sutured to th e e th m o id . Regan (1 9 1 2 ) and Nelson (1 9 6 6 ) provided m ore fe a tu re s to
ju s tify
th e
hyopalatine
m o n op h yly
bones
o f th e
A n g uillifo rm e s,
(h yo m a n d ib u la ,
q u ad ra te ,
including
and
a reduced
p a la to p te ryg o id
num ber of
re m a in in g ),
elongate branchiostegals, a single p a ir o f upper dentig e ro us pharyngeal to o th
plates, and absence o f an o rb itosp h e no id , p o sttem poral and m esocoracoid. L a tte r
o th e r characters such as th e bone-enclosed eth m o id a l com m issure (G osline, 1961),
th e initial fusion o f th e a n gu la r and re tro a tric u la r bones in th e low er ja w (Forey,
1973) and crescentic nucleus in th e sperm atozoa (Jam ieson, 1991) w ere presented
to su p p o rt m on op h yly o f th e Elopom orpha.
Greenwood e t al. (1 9 6 6 ) recognized a re la tionship betw een A n g uillifo rm e s and
o th e r m em bers o f E lopom orpha, based on th e leptocephalus larval stage. These
included
th re e
A n g uillifo rm e s
orders:
Elopiform es
(A nguilloidei
(w ith
and
Elopidei
and
Saccopharyngoidei
A lbuloidei
su b orders),
suborders)
and
N otacanthiform es (Fig. 1.2). A lthough leptocephalus larvae have a fo rke d caudal fin
(resem bling w h ite b a it-lik e larvae) in M egalops and Elops, T su kam oto and O kiyam a
(1 9 9 7 ) opposed considering them as being derived fro m w h ite b a it larvae (as occurs
co m m on ly
in
clupeom orphs).
H ulet and
Robins
(1 9 8 9 )
pointed
o u t th a t the
leptocephalus larval stage should be considered as an im p o rta n t e v o lu tio n a ry step
in delaying o r avoiding osm otic problem s by fish undergoing m etam orphosis in the
course o f th e ir upstream m ig ra tio n . H owever, a lte rn a tiv e hypotheses have been
suggested (P fe ile ra n d luna, 1986; Pfeiler, 1986; Pfeiler, 1997; Pfeiler, 1999).
Nelson (1 9 7 3 ), Forey (1 9 7 3 ), Patterson and Rosen (1 9 7 7 ) and Forey e t al. (1 9 9 6 )
proposed d iffe re n t h ypothetical in te rre la tio n sh ip s am ong elopom orph fishes (Fig.
4
1
I n t r o c Ju c t í o n
1.3).
Also,
re ce ntly
published
p h ylogenetic
studies
exam ined
the
e lo p o m o rp h /a n g u illifo rm relationships and using m o le cu lar evidence, confirm ed the
m o n op h yly o f th e Elopom orph fishes. They also represented th e Elopom orpha to
include th e orders Elopiform es (M egalopidae + Elopidae), A lb ulifo rm es (A lbulidae +
N otacanthidae), and A n g u illifo rm e s (A nguilloidei + S accopharyngoidei) (O b e rm ille r
and Pfeiler, 2003; Wang e t a l., 2003; Inoue e t a l., 2004; Lopez e t a l., 2 0 07 ; Inoue
e t a l., 2010) (Figs, 1.4, 1.5, 1. and 1.7).
Inoue e t al (2 0 0 4 ) pointed o u t th a t m ito g en o m ic data s tro n g ly supported the
m o n op h yly o f E lopom orpha, indicating th e v a lid ity o f th e leptocephalus as an
elopom orph
syn a pom orphy. They also m entioned th a t th e fo rk -ta ile d
ty p e
of
leptocephalus had o rig in ate d as th e com m on ancestor o f th e Elopom orpha w hereas
fila m e n t-ta ile d and ro u n d -ta ile d typ e s have diversified se parately in tw o m ore
derived m a jo r clades.
The c u rre n t classification
o f th e a n g u illifo rm
fa m ilie s is m o stly based on th e
superficial (e x te rn a l) characters. There are few co m p ara tive studies o f eels (m o s tly
based on osteological fe a tu re s ), such as Nelson (1 9 6 6 ), Böhlke (1 9 8 9 a ), Belouze
(2 0 0 1 ) and De S chepper (2 0 0 7 ) th a t provide m any m usculoskeletal fe a tu re s o f
A n g uillifo rm e s,
b u t th e y are
rare dealing w ith
th is specious order. Also, the
Saccopharyngoidei th a t include th e deep sea g u ip e r eels, are p o orly known and
little detailed
osteological
in fo rm a tio n
is available.
Bertin
(1 9 3 4 ), Tchernavian
(1 9 4 7 ), Bertelsen and Nielsen (1 9 8 7 ) and Bertelsen e t al. (1 9 8 9 ) provided good
accounts o f th e external m o rph o log y o f th e S accopharyngoidei.
1 .1 .3 . In tro d u c tio n o f s tu d ie d ta x a
The su p ero rd e r Elopom orpha is th e m ost d ive rsifie d group o f basal teleosts and
com prises
856
species
placed
in
th re e
orders
(E lopiform es,
A lb ulifo rm es,
A n g u illifo rm e s ), 24 fa m ilie s, and 156 genera (N elson, 2 0 06 ; Inoue e t al., 2004)
(Table 1.1). As an intro du ctio n and background to th e studied species, a b rie f
o ve rvie w is given here o f th e fa m ilie s to which th e y belong.
1 .1 .3 .1 . A n g u illid a e
The fa m ily A nguillidae o r fre s h w a te r eels com prises 15 species w ith in one genus
A n g uilla (N elson, 2006). R epresentatives are found in tro p ical and te m p o ral seas,
except in th e eastern Pacific and southern A tla n tic (N elson, 2006). This fa m ily is5
1
I n t r o c Ju c t í o n
Table 1.1. S ystem atic o ve rvie w o f th e su p ero rd e r Elopom orpha (N elson, 2006;
Inoue e t a l., 2010)
Order Elopiformes (8 species):
1- Elopidae (Lady Fishes)
2- Megalopidae (Tarpons)
Order Albuliform es (2 9 species):
1- Albulidae (Bone Fishes)
2- Halosauridae (Freshwater Eels)
3- Notacanthidae (Spiny Eels)
Order Anguilliform es
-Suborder Anguilloidei (7 3 8 species):
1- Anguillidae (Freshwater Eels)
2- Heterenchelyidae (Mud Eels)
3- Moringuidae (Spaghetti Eels)
4- Chlopsidae (False Morays)
5- Myrocongridae (Thin Eels)
6- Muraenidae (Morays)
- Uropterygiinae (Morays)
-Muraeninae (Morays)
7- Synaphobranchidae
- Ilyophinae (Arrowtooth Eels)
- Synaphobranchinae (Cutthroat Eels)
- Simenchelyinae (Pugnóse Eels)
8- Ophichthidae (Snake eels and Worm Eels)
-Myrophinae
-Ophichthinae
9- Colocongridae (Colocongers)
10- Congridae (Conger Eels)
- Congrinae
- Bathymyrinae
- Heterocongrinae (Garden Eels)
11- Muraenesocidae (Pike conger Eels)
12- Derichthyidae (Longneck Eels)
13- Nemichthyidae (Snipe Eels)
14- Serrivomeridae (Sawtooth Eels)
15- Nettastomatidae (Duckbill Eels)
-Suborder Saccopharyngoidei (2 6 species):
1- Cyematidae (Bobtail Snipe Eels)
2- Saccopharyngidae (Swallowers or Whiptail Gulpers)
3- Eurypharyngidae (Pelican or Umbrella-mouth Gulpers)
4- Monognathidae (Monognathids)
6
1
I n t r o c Ju c t í o n
considered
m o rph o log ica lly
to
com prise
th e
m ost
generalized
eels
of
all
A n g uillifo rm e s (S m ith , 1989a), despite th e fa c t th a t th e phylogeny suggests th a t
th e y are a group derived fro m d e ep w a te r eels (In o u e e t al., 2010). Based on the
fo llo w ing characters, fre s h w a te r eels can be distinguished (N elson, 2 0 0 6 ): m inu te
scales pre sen t; gili opening crescentic, la te ra l; lateral line com plete on body and
head;
pectoral
fins
well
developed.
A d u lt a nguillids
live
in fre s h w a te r o r
in
estuaries. They stop feeding a t m a tu rity , when th e y m ove fro m fre s h w a te r o u t to
sea. The leptocephali m ove back to coastal areas, undergo m e tam orphosis, and
e n te r fre s h w a te r as elvers.
1 .1 .3 .2 . N e tta s to m a tid a e
The fa m ily
N etta sto m a tid ae o r duckbill eels com prises six genera, Facciolella,
H oplunnis, N etta sto m a , N ettenchelys, S aurenchelys, and Venefica, w ith a b ou t 38
species (S m ith , 1989b; Nelson, 2006). The N etta sto m a tid ae is a fa m ily o f long­
snouted, eels found m a in ly on th e o u te r co n tine n ta l sh e lf and co n tine n ta l slope o f
th e w orld 's tro p ical and w a rm -te m p e ra te
seas (S m ith ,
1989b). The fo llow ing
characters are used to define N ettastom atidae rep re se n ta tive s (N elson, 2 0 06 ):
head and sn o ut elongate and n a rro w ; m outh e n larged; ta il g re a tly a tte n u a te d ;
pectoral fin usually absent in a d u lts ; v e rte b ra e usually 1 9 0 -2 8 0 ;
m a xim u m length
a b ou t 1 m. This fa m ily is p o orly known.
1 .1 .3 .3 . H e te re n c h e ly id a e
The fa m ily H eterenchelyidae o r m ud eels com prises e ig h t species w ith in tw o genus
( P a n tu rich thys and P yth o n ich th ys ) (N elson, 2006). These eels are found in tropical
areas o f th e A tla n tic and eastern Pacific (N elson, 2006). Based on th e fo llo w ing
characters, m ud eels can be distinguished (N elson, 2 0 0 6 ): pectoral fin absent;
m outh large; scales absent; gili openings low on body; dorsal fin origin o ve r gili
o p ening; lateral line obsolete. M em bers o f th is fa m ily appear to b urrow (h e a d -firs t).
1 .1 .3 .4 . S y n a p h o b ra n c h id a e
The S ynaphobranchidae o r c u tth ro a t eels are found in A tla n tic, In dian and Pacific
oceans. This fa m ily com prises
10 genera and about 32 species w ith in
th re e
subfam ilies (Ily o p h in a e , S ynaphobranchinae and S im enchelyinae). A b rie f o verview
o f th e m orphological fe a tu re s o f th is fa m ily is given below (N elson, 2 0 0 6 ): gili
openings low on body, a t o r below insertion o f pectoral fin (th is fin is absent in a
7
1
I n t r o c Ju c t í o n
few
species);
v e rte b ra e
1 1 0 -2 0 5 ;
th ird
hypobranchial
directed
fo rw a rd
from
m idline , m eets th ird ceratobranchia! a t a sharp angle.
Ily o p h in a e :
Lower ja w
s h o rte r than
upper;
body scaleless (e xce pt in som e
Ily o p h is ); pectoral fin absent in som e species o f D ysom m a and th e m o notypic
Thermobiotes-, head shape depressed and re la tiv e ly rounded; som e te e th re la tive ly
long.
S y n a p h o b ra n c h in a e : Lower ja w longer than upper; body scaled (u su ally naked in
H aptenchelys te x is ); head shape com pressed and re la tiv e ly p o in te d ; te e th small
and n e ed le -like ; branchial aperture s co n flu e n t o r o n ly s lig h tly separated in m ost;
tw o genera, H aptenchelys and Synaphobranchus.
S im e n c h e ly in a e : Body especially slim y, w ith scales em bedded in s kin ; snout b lu n t
and
rounded
w ith
te rm in a l
s lit-lik e
m o u th ;
pectoral
fin
m oderate
in
size;
p a la to p te ryg o id arch (arcade) co m p le te ; one species, S im enchelys p a rasiticus. I t is
e sse ntia lly w orld w id e fro m tro p ical to te m p e ra te latitu de s. Little is known o f its
feeding habits and food.
1 .1 .3 .5 . M u ra e n id a e
The Fam ily M uraenidae o r m oray eels are found in tropical and te m p e ra te seas but
some species occasionally e n te r fre sh w ater. The M uraenidae com prises a b ou t 185
species classified
genera
in tw o subfam ilies (U ro p te ryg iin a e and
(N elson, 2 0 06 ).
Based on th e fo llo w ing
M uraeninae) and
15
characters, m ud eels can
be
distinguished (N elson, 2 0 0 6 ): gili openings re stricte d to sm all roundish lateral
openings; lateral line pores on head b u t not on body; tw o branchial pores; gili
arches reduced; fo u rth branchial arch stre n g th e ne d and su p po rtin g pharyngeal
ja w s ; pectorals ab sen t; p o ste rio r nostril high in head; m ost w ith long fa n g like
te e th ; ve rte b ra e usually 1 1 0 -2 0 0 .
U ro p te ry g iin a e : Ossified hypobranchials in firs t and second arches; ve rtical fins
reduced; rays confined to tip o f ta il; fo u r genera, A narchias, C hannom uraena,
S cuticaria, and U ropterygius.
M u ra e n in a e : No ossified hypobranchials; ve rtica l fins not confined to tip o f tail
(u su ally th e dorsal fin origin is above th e gili opening o r fo rw a rd ); about 11 genera,
Echidna,
Enchelycore,
Enchelynassa,
G ym nom uraena,
G ym n o th o ra x,
M onopenchelys, M uraena, R hinom uraena, S iderea, S tro p h id o n , and Thyrsoidea.
1
I n t r o c Ju c t í o n
1 .1 .3 .6 . C o n g rid a e
The Congridae are one o f th e largest and m ost d ivers a n g u illifo rm fa m ily (S m ith ,
1989c). This fa m ily com prises th re e subfam ilies (H eterocongrinae, B a thym yrinae
and C ongrinae) w ith 32 genera and ro u gh ly 160 species (N elson, 2 0 06 ). The
Congridae are found w orldw ide in tro p ical and subtropical latitu de s and occur in the
A tla n tic, Pacific and In dian Oceans. The fo llo w ing characters can be used to define
th e Congridae (N elson, 2 0 0 6 ): body shape v a ria b le ; m o d era te ly s to u t to e longate;
lateral
line co m p le te ;
pectoral fin
usually p re sen t;
branchiostega!
rays 8 -2 2 ;
ve rte b ra e 1 0 5 -2 2 5 .
H e tro c o n g rin a e : Dorsal and anal fin rays unsegm ented; pectoral fin m inu te o r
absent; body v e ry elongate and slender; m outh s h o rt and low er ja w p ro je ctin g
beyond upper; tw o genera, Gorgasia and H eteroconger, w ith 25 species.
B a th y m y rin a e : Dorsal and anal fin rays u nsegm ented; pectoral fin well developed;
p o ste rio r
nostril
below
m id-e ye
level;
five
genera,
A riosom a,
B a th ym yru s,
C hiloconger, P a rabathym yrus, and Paraconger.
C o n g rin a e :
Dorsal and anal fin rays segm ented; pectoral fin well developed;
p o ste rio r nostril a t o r above m id-e ye level; about 25 genera, e .g ., A c ro m ycte r,
Conger, Gavialiceps, G nathophis, H ildebrandia, Lum iconger, M acrocephenchelys,
Rhechias, R hynchoconger, U roconger, and X enom ystax.
1 .1 .3 .7 . E u ry p h a ry n g id a e
The m o n otypic Eurypharyngidae o r pelican eel is found in th e bathyal zone o f the
tro p ical and te m p e ra te areas o f all oceans (B öhlke, 1966; Nelson, 2006). The
fo llo w ing characters can be used to define th e Eurypharyngidae (N elson, 2006;
Bertelsen, 1989): skin black; gili openings sm all, closer to anus than to end o f
sn o ut; only te le o s t w ith five gili arches and six visceral c le fts; m outh enorm ous;
ja w s w ith num erous m inu te te e th ; pectoral fins m in u te ; caudal fin absent; caudal
p a rt com presses and less deep than tru n k ; v e rte b ra e 1 0 0 -1 2 5 .
1 .2 . A im s and th e s is o u tlin e
1 .2 .1 . G e n e ra l a im o f th is s tu d y
The general aim o f th is w o rk is to provide a co m p ara tive anatom ical stu d y on th e
stru ctu ra l d iv e rs ity in th e cranial m usculoskeletal system o f several re presentatives
9
1
I n t r o c Ju c t í o n
o f th e o rd e r A n g uillifo rm e s. Hence, th e goal is to do cum e n t th e s tru c tu ra l pa tte rn s
and e v o lu tio n a ry changes in th e ir head m usculoskeletal system , especially those
reflecting specializations to w a rds feeding. Regarding th e com m on elongated body
plan o f these fishes, it is expected th a t m ost a daptive changes w ith in th is o rd e r
m ay be concentrated a t th e level o f th e ir head m usculoskeletal system .
An e e l-like body fo rm is seen in a p p ro x im a te ly 45 o th e r fish fa m ilie s w here it is
considered
a co n verg e n t fe a tu re
(Gans,
1975;
U ndell,
1994;
C arroll,
1997b;
Renous e t a l., 1998; Cohn and Tickle, 1999; C aldwell, 2 0 03 ; A driaens e t al., 2002,
Ward
and
B rainerd,
2007).
An
elongated
body
can
be
considered
highly
advantageous fo r w edging th ro u g h sm all openings, o r fo r bu rro w ing . The stu d y o f
De Schepper (2 0 0 7 ) proposed th a t it is not body elongation but ra th e r o th e r
m orphological m o d ifications (i.e. a t the level o f th e cra n iu m , sensory system e tc.)
th a t re fle ct th e d iv e rs ity o f a d aptation to th e e n v iro n m e n t w here A n g u illifo rm e s can
be found.
Hence, th e
o rd e r A n g uillifo rm e s
provides an o p p o rtu n ity to
b e tte r
understand th e e v o lu tio n a ry changes in th e cranial m usculoskeletal system , o f
which som e are th e a d ap tations to d iffe re n t m odes o f life, w ith in a ta xo n w ith a
single e v o lu tio n a ry o rig in o f an e e l-like body.
One o f th e th e m e s o f th is co m p ara tive stu d y is a consideration o f th e fu n ctional
significance o f s tru c tu re s in relation to d iffe re n t life styles. D em onstrating th a t tra its
o f organism s are th e re su lt o f a daptive evo lu tio n has been one o f th e m a jo r focuses
in e vo lu tio n a ry biology since th e tim e o f Darwin (M ayr, 1983). For th is purpose, we
firs t need to d e te rm in e w h a t th e fu n ctio n o f a specific tr a it is and then it is
necessary to show th a t individuals possessing those tra its ta ke advantage o f having
th e m . In a co m p ara tive m ethod, it can be hypothesized th a t th e presence o f a
d iffe re n t fo rm o f a fe a tu re fro m th a t o f a closely related species m ay be th e re su lt
o f a d aptive evo lu tio n (B rock, 2000). Also, a given m orphological ch a racter th a t is
advantageous fo r one species in a specific e n v iro n m e n t m ay not be an adaptive
fe a tu re in a n o th e r species, but ra th e r a retained ancestral one. In a d ditio n , m any
organs o r organ system s are able to perform m ore than one fu n ctio n (D u lle m e ije r,
1 9 91 ); w here one o f these fu n ctio n s m ay arise as a new a d a p ta tio n , w ith o u t a
m arked stru ctu ra l change.
10
1
I n t r o c Ju c t í o n
As m any biologists advocated th e e x p lic it use o f a p hylogenetic fra m e w o rk in all
co m p ara tive studies (Lauder, 1981, 1982, 1990; Felsenstein, 1985; Rieppel, 1988),
also in th is stu d y th e observations are discussed w ith in a p h ylogenetic fra m e w o rk
w here
e v o lu tio n a ry
tra n s fo rm a tio n s
of
hom ologous
s tru c tu re s
can
be
traced
(B öhlke, 1989b; Belouze, 2001; O b e rm ille r and Pfeiler, 2003; Wang e t a l., 2003;
Lopez e t a l., 2007).
In th is stu d y, those a n g u illifo rm clades considered as case studies are those th a t
have undergone substantial changes in th e ir head m o rph o log y, as well as those o f
which h a rdly a n yth in g was known concerning th e ir m usculoskeletal m orphology.
Such
a p pa re n t
pronounced
m orphological
specializations
can
be expected
to
im prove th e potential to becom e adapted to a specific e n v iro n m e n t (Fisher, 1930).
Also, th is in fo rm a tio n can help to understand a t w h a t stru ctu ra l level, changes m ay
have occurred in relation to a specific life style.
Therefore taxa w ere selected e xh ib itin g m arked levels o f cranial specializations o r
specialized b e havior in which th e head is stro n g ly involved. These include ja w
elongation in th e duckbill eel, H oplunnis p u n c ta ta (N e tta s to m a tid a e ), h e a d -first
b u rro w ing
in
P yth o n ich thys
m a cruru s
(H ete re n ch e lyid a e),
parasitic
feeding
in
Sim enchelys p a rasiticu s (S im enchelyinae: S ynaphobranchidae), pharyngeal system
fo r m echanical tra n s p o rt o f captured prey in m uraenids, and th e e x tra o rd in a rily
m odified cephalic system in E u ryp h a ryn x pelecanoides (E u ryp ha ryn g id a e ).
1 .2 .2 . O u tlin e o f th e s is
The body te x t o f th is thesis is divided into e ig h t chapters.
CHAPTER 1\ A general in tro d u ctio n is provided, follow ed by th e goals o f th e stu d y
itse lf, in w hich th e general aim and o u tlin e (including research questions) o f th is
research are fo rm u la te d .
CHAPTER 2: The second ch a p te r presents an o ve rvie w o f th e m aterial and applied
m ethods. More details o f th e m ethods and m aterial fo r each o f th e specific topics
studied are then listed w ith in th e corresponding chapters.
11
1
I n t r o c Ju c t í o n
CHAPTER 3\ The th ird ch a pte r is th e firs t ch a pte r in which results are presented.
The skull m o rph o log y o f th e poorly studied H oplunnis p u n c ta ta (N e tta s to m a tid a e ) is
described
and
changes
in
th e
cranial
m usculoskeletal
associated
w ith
ja w
elongation w ere exam ined. P articularly th e im plication fo r th e fu n ctio n in g o f the
feeding apparatus is discussed. The central question o f th is p a rt was:
-
W hat im plicatio n s m ay ja w elongation in H. p u n c ta ta have had on th e overall
head m usculoskeletal system , p a rtic u la rly th e feeding apparatus?
CHAPTER
4\
The
fo u rth
ch a p te r
focuses
on
th e
cephalic
m orph o log y
of
P yth onichthys m a cruru s (H eterenchelyidae).
The cranial m o rph o log y o f th is h ig h ly specialized fossorial eel was exam ined.
Specializations in relation to h e a d -firs t burrow ing w ere characterised. The results
are discussed in a c o n te x t o f ad ap tatio n s to h e a d -firs t bu rro w ing in d iffe re n t lineage
o f A n g u illifo rm e s, by com paring w ith M oringuidae and O phichthidae. Therefore th is
stu d y trie s to deal w ith th e fo llo w ing questions:
-
W hat kind o f cranial specializations are related to th e fossorial life style in P.
m a c ru ru s ?
-
Is h e a d -firs t burrow ing in eels associate w ith a converging m orph o log y o r are
th e re d iffe re n t ways to be a h e a d -firs t burrow er?
CHAPTER 5: In ch a p te r five , th e head m usculoskeletal m orph o log y o f an alleged
parasitic eel, S im enchelys p a ra siticu s (S yn aphobranchidae), was exam ined.
The cephalic fe a tu re s o f th is species show m arked differences fro m o th e r m em bers
o f th e fa m ily Synaphobranchidae, to which it is com pared. These differences are
described in o rd e r to evaluate to w h a t degree th e cranial m o rph o log y re flect
a d ap tations to parasitism . Hence, th is case stu d y a tte m p ts to answ er:
-
W hat kinds o f specializations define th e head o f th e parasitic pugnóse eel,
S. p a ra s itic u s ?
-
And can these specializations be related to th e ir parasitic lifestyle?
CHAPTER 6: In ch a pte r s ix th , th e cephalic m orphological changes in relation to the
h ighly specialized pharyngeal ja w s in m uraenids is explored. The m uraenids bear an
12
1
I n t r o c Ju c t í o n
inn o va tive feeding m echanism s th a t allow them to tra n s p o rt large prey item s from
th e oral ja w all th e w ay back to w a rds th e esophagus, using th e pharyngeal ja w s
(M ehta and W a in w rig h t, 2007a).
Hence, com paring th e ir head m usculoskeletal
fe a tu re s w ith a close ly-re la te d o u tg ro u p m ay help to reveal to w h a t degree tra d e ­
offs m ay have arisen in th e oral feeding apparatus, in relation to th is pharyngeal
tra n s p o rt system . As such, we w ould like to know:
How m ay a highly specialized pharyngeal m echanical tra n s p o rt system in
m orays have affected th e e v o lu tio n a ry changes in th e head m usculoskeletal
system ?
CHAPTER
7:
The
ch a pte r
seven
focuses
on
th e
osteology
and
m yo lo g y
of
E u ryp h a ryn x pelecanoides (E u ryp ha ryn g id a e ). This pelican eel is a e n ig m a tic deepsea fish th a t occurs a t b a thypelagic depths th ro u g h o u t th e w o rld 's oceans. It's
bizarre appearance results fro m e x tre m e ly enlarged ja w s, e xh ib itin g an enorm ous
gape. The cranial osteology and m yo lo g y o f E. pelecanoides presents a splendid
exam ple
o f th e
e xtre m e
level
of
changes
th a t
m ay
have
occured
in
the
m usculoskeletal system in A n g uillifo rm e s. Hence, o u r central questions in th is case
stu d y are:
How have th e cranial m usculoskeletal elem ents becom e m odified during
e vo lution in o rd e r to fo rm th a t o f E. pelecanoides?
How can th e cephalic fe a tu re s fu n ctio n in relation to its feeding behavior?
CHAPTER 8: The final ch a pte r fo rm s th e general discussion. In th is ch a pte r, the
results obtained fro m th is thesis are inte gra te d w ith data fro m lite ra tu re , w here it is
a tte m p te d to explore th e s tru c tu ra l p a tte rn s o f th e e v o lu tio n a ry changes in the
head m usculoskeletal system
in relation to d iffe re n t specializations, as well as
showing th e stru ctu ra l d iv e rs ity
in th e cranial
m usculoskeletal system
o f th e
A n g uillifo rm e s. I t is also discussed how th e results o f th is co m p ara tive stu d y m ay
help to b e tte r understand e v o lu tio n a ry tra n s fo rm a tio n s as th e re su lt o f adaptive
and no n-a d a ptive changes o f head ch aracteristics in A n g uillifo rm e s. Finally, based
on th is stu d y, som e insights fo r fu rth e r research are discussed.
13
14
C liA p T E R 2
M ATERÍ aL ANd M E T h o d s
2 IM a t e r í a L ANd IV fE ïh o d s
C hapter tw o
M aterial and Methods
2 .1 . M a te ria l e x a m in e d
A to ta l o f 68 specim ens, representing
exam ined
10 species and 7 fa m ilie s, have been
in th is d isse rtatio n study. In a d ditio n , 8 specim ens and th e ir data,
representing 4 species; C onger co n g e r (Congrinae: Congridae), H ete roco n g er hassi
(Heterocongrinae: Congridae), M oringua e d w ardsi (M o rin g u id a e ), and Pisodonophis
b oro (O p h ichthid a e), w ere obtained fro m th e thesis p ro je c t o f De Schepper (2 0 0 7 )
(Table 2 .1 ). Museum specim ens was exam ined as well as co m m ercia lly obtained
specim ens.
The specim ens used fo r th e anatom ical descriptions in chapters II I- V II are listed in
Table 2.1. A dditional in fo rm a tio n , such as to ta l len g th , m ethod (and s ta in in g ) used
to stu d y th e specim ens are presented in th e m aterial and m ethods section o f th e
chapters III- V II.
Five specim ens o f A n g uilla a n guilla (A n g uillid a e) w ere co m m ercia lly obtained fro m
w ild catch. The m useum m a te ria ls w ere obtained fro m th e fo llo w ing collections:
USNM : Sm ithsonian National Museum o f Natural H istory.
UF: Florida Museum o f Natural H istory.
ANS: Australian Museum.
M N H N : Musée National d 'H istoire Naturel o f Paris.
MCZ: H arvard U nive rsity, Museum o f C om parative Zoology.
UGM D: Zoological Museum o f th e G hent U niversity.
N H M D : N atural H istory Museum o f D enm ark.
15
2 IM a t e r í a L ANd M E T h o d s
Table 2.1: Specim ens used in chapters II I- V II (CS: Cleared and sta in ed ; Ds:
Dissected).
species
Source
_______________________________________________
Hoplunnis punctata
(Nettastomatidae)
Hoplunnis punctata
(Nettastomatidae)
collection nr
N um ber
of
M ethods
ch ap ter
species
MNHN
MNHN 1965-0649
3
CS:hp2, h p l
Ds:hp3
III
UF
UF 216386
2
Ds:hp4, hp5
III
Conger conger
(Congrinae)
UGMD
(De Schepper, 2007)
UGMD 53065
l
Dry skeleton
III
Conger conger
(Congrinae)
commercial trade
(De Schepper, 2007)
1
DS
III
Heteroconger hassi
(Heterocongrinae)
UGMD
(De Schepper, 2007)
UGMD 175374
2
C S :h h l
Ds:hh2
III
MNHN
MNHN 1965-0640
5
CS:pm2, pm4
Ds:rest
IV
5
C S :aal
Ds:rest
IV
2
m e l and 2:
Cleared
IV
2
b p l : cleared
Ds:bp2
IV
5
CS:sp3
Ds:rest
V
7
C S :ib l
Ds:rest
V
Pythonichthys macrurus
(Heterenchelyidae)
Anguilla anguilla
(Anguillidae)
commercial trade
Moringua edwardsi
(Moringuidae)
MCZ
(De Schepper, 2007)
Pisodonophis boro
(Ophichthidae)
Simenchelys parasiticus
(Simenchelyinae)
commercial trade
(De Schepper, 2007)
Ilyophis brunneus
(Ilyophinae)
Synaphobranchus
brevidorsalis
(Synaphobranchinae)
Gymnothorax prasinus
(Muraeninae)
Anarchias allardicei
(Uropterygiinae)
Anarchias allardicei
(Uropterygiinae)
Ariosoma gilberti
(Bathymyrinae)
Eurypharynx
pelecanoides
(Eurypharyngidae)
Eurypharynx
pelecanoides
(Eurypharyngidae)
MCZ 44686
1.28736-024
1.20095-031
UF 222355
UF 230514
UF 130897
AMS
UF
USNM
USNM 273427-115
3
CS:sb2
Ds:rest
V
AMS
1.28736-024
1.20095-031
4
CS:gp2
D s :g p l, gp3
VI
AMS
1.17102-063
5
C S :aal
Ds:rest
VI
UF
UF 318044
3
Ds: aa6, aa7
VI
UF
UF 230612
UF 10803
16
CS:ag2
D s :a g l,a g l2
VI
MNHN
MNHN 1980-1354
3
CS:ep2,
D s :e p l, ep3
VII
NHMD
P2340411
P2340414
P2340415
P2340416
P2340418
5
CS:ep6
Ds:rest
VII
16
______
2 IM a t e r í a L ANd IV fE ïh o d s
2 .2 . M e th o d s
2 .2 .1 . P re p a ra tio n o f s p e c im e n s
2 .2 .1 .1 . A n a e s th e s ia , s a c rific e and fix a tio n
Specim ens o f A n g uilla a nguilla w ere anaesthetized in a 0 .0 0 1 % w a te r solution MS
222 (e th yl 3-am inobenzoic acid m e thanesulfonate sa lt - Sigma Chem ical Co) and
subsequently killed w ith an overdose o f M S-222 (Procedure occurred in accordance
w ith th e Belgian law in th e p ro te ction o f la b o ra to ry anim als (KB d.d. N ovem ber 14th,
1 9 93 )). Then, specim ens w ere fixed using a 4% buffered fo rm a lin solution (a t
neutral pH). This w id e ly used fix a tiv e was a d d itio n a lly injected in th e specim ens to
im prove and allow steady fix a tio n o f deeper tissue. Using th is fix a tiv e allow ed us to
apply clearing and staining m ethod, as explained below.
2 .2 .2 . M o rp h o lo g y
In o rd e r to exam ine th e detailed m o rph o log y o f so ft and hard tissue s tru ctu re s,
d iffe re n t procedures w ere applied. For stu d ying th e osteology, in to to cleared and
stained m a te ria l and data fro m CT-scanning w ere exam ined. M yological as well as
osteological fe a tu re s w ere studied based on dissections. A dditional in fo rm a tio n and
d etails on hard and so ft tissues w ere gathered using histological sections.
2 .2 .2 .1 . I n t o t o c le a rin g and s ta in in g
The specim ens w ere cleared and stained according to th e protocol o f Hanken and
W assersug (1 9 8 1 ) and T a ylo r and Van Dyke (1 9 8 5 ) fo r stu d ying th e osteology
(Table 2.2 and 2 .3 ). The protocol o f Hanken and W assersug (1 9 8 1 ) was s lig h tly
m odified
as th e slow ly active try p s in e was replaced
by th e
m ore aggressive
potassium hydroxide (KOH), leading to e q ua lly good results (Table 2 .2 ). In general,
co n centrations
ranging
betw een
0 .5 %
and
3%
w ere
used
th o u g h
in
large
specim ens con cen tra tio n s up to 5% w ere applied. A lizarine red S (S igm a) and
alcian
blue 8GX (S igm a )
allow ed
d iffe re n tia l
sta in in g
o f bones and
cartilage
respectively. As th e alcian blue 8GX had to be dissolved in ethanol and glacial acetic
acid, décalcification o f th e bone was induced. O ssifications m ay be m asked by this
17
2 IM a t e r í a L ANd M E T h o d s
Table 2.2. Clearing and staining procedure adapted fro m Hanken and W assersug
(1 9 8 1 ).
S o lu tio n /A c tio n
S te p
D u ra tio n
W ashing
ta p w a te r
24h
C artilage
S taining
alcian Blue (8GX, S ig m a ): 10mg in 70m l alcohol
(9 6 % ) + 30 ml acetic acid
6 -8h
D ehydratation
9 6 -1 0 0 % (tw o tim e s alcohol renew al)
75% alcohol
50% alcohol
25% alcohol
aqua dest (tw o tim e s w a te r renew al)
3 -1 0 % H20 2 in 0 .5 % KOH
ta p w a te r
try p s in e so lu tio n : 1 -4 % K O H /trypsine (0 .6 g in
400m 130% NaBOs)
OR KOH so lu tio n : 0 .5 % -4 %
M aceration
Bleaching
W ashing
Clearing
24h
2h
2h
2h
4h
l- 2 h
24h
24h
24h
Bone staining
alizarine red (S ig m a ): 0 .5 % KOH in (0 .1 %
alizarine red S in aqua dest)
12h
Preservation
25% glycerin + 75% 0 .5 % KOH
24h
50% glycerin + 50% 0 .5 % KOH
24h
75% glycerin + 25% 0 .5 % KOH
24h
100% glycerin
storage
décalcification process as alizarine red S a ctu a lly binds o nto th e calcified m a trix o f
bone (Vandew alle e t al., 1998). For th a t reason som e specim ens w ere stained w ith
alizarine red S alone. The protocol o f T a ylo r and Van Dyke (1 9 8 5 ) avoids extensive
dam age fro m th e acid ca rtila g e stain on th e bony stru ctu re s by th e alcohol series
and th e use o f borax, and by using KOH instead o f try p s in fo r th e clearing (Table
2 .3 ).
2 .2 .2 .2 . D issectio ns
The head o f specim ens w ere dissected fo r th e stu d y o f both hard and so ft tissue
stru ctu re s. V isualization o f m uscle fib e r a rra n g e m e n t, insertion sites and o rig in was
enhanced by th e use o f a ¡odium solution (Bock and Shear, 1972). For th e s tu d y o f
ca rtila g ino u s and bony ele m e n ts, dissections w ere also perform ed on cleared and
stained specim ens. This allow ed th e stu d y o f th e separate elem ents and o f those
regions th a t w ere invisible in an overall dorsal, ve n tra l and lateral view . The
18
2 IM a t e r í a L ANd M E T h o d s
specim ens w ere exam ined using an O lym pus SZX7 stereom icroscope, equipped
w ith
a cam era
lucida.
D igital
im ages
w ere
taken
using
an
O lym pus
SZX9
stereom icroscope, equipped w ith a ColorView 8 d ig ita l cam era driven by A n a ly s is
5.0 so ftw a re (O lym pus).
2 .2 .2 .3 . H is to lo g ic a l se ctio n s
In o rd e r to s tu d y th e detailed a n a to m y o f th e head o f S im enchelys p a rasiticu s
(S im en ch e lyin a e), serial histological cross sections w ere prepared according to
T a ylo r and Van Dyke (1 9 8 5 ) (Table 2 .4 ). Five pm th ic k sections w ere made using a
Reichert-Jung Polycut m icrotom e. A fte r th is , these sections w ere m ounted o nto
glass slides, stained w ith to lu id in blue (Table 2 .5 ) and covered using DPX.
Table 2.3. Clearing and staining procedure adapted fro m T a ylo r and Van Dyke
(1 9 8 5 ).
S o lu tio n /A c tio n
S te p
Dehydratation
C artilage
staining
D u ra tio n
50% alcohol
I2h
75% alcohol
I2h
9 6 -1 0 0 % alcohol
I2h
9 6 -1 0 0 % alcohol
9-3 0 mg Alcian Blue 8GX in 100 ml o f a so lution o f
4 0% glacial acetic acid and 60% absolute ethyl
alcohol
I2h
8-24h
N eutralisation
sa tu ra te d borax solution (Na 2B4O7. 1 0 H2O)
48h
Bleaching
10% H20 2 in 0 .5 % KOH
0.5h-...
Clearing
Bone staining
enzym e b u ffe r solution (0 .4 5 g in 400 ml o f 30%
sa tu ra te d borax so lu tio n )
alizarin red (S ig m a ): 0 .5 % KOH in 0 .1 % alizarin
red, until color sw itches fro m deep red to purple
(s tir)
12h-...
24h
Further clearing
0 .5 -3 % KOH
12h...
Preservation
25% glycerin + 75% 0 .5 % KOH
12h
50% glycerin + 50% 0 .5 % KOH
12h
75% glycerin + 25% 0 .5 % KOH
12h
100% glycerin
storage
19
2 IM a t e r í a L ANd M E T h o d s
Exam ination and digital im aging o f these sections was done on a Reichert-Jung
Polyvar lig h t m icroscope, also m ounted w ith a ColorView 8 cam era driven
by
A n a ly s is 5.0 so ftw a re (O lym pus). This procedure m ay induce som e im pe rfe ctio n s
as re su lt o f sh rin kin g o f e xte rn al tissue (skin ) d u ring preparation o r em b ed d ing ;
also m in o r d isto rtio n can occur in th e w hole section by im p e rfe ct stre tch in g .
Table 2.4. T echnovit 7100 em bedding procedure.
S o lu tio n /A c tio n
D u ra tio n
S te p
Vacuum
fixa tio n
W ashing
4% buffered fo rm a lin
days to weeks
ta p w a te r
8h
Décalcification
decalc (H istolab)
36h
W ashing
ta p w a te r
5h
D ehydration
30% alcohol
12h
50% alcohol
12h
70% alcohol
12h
96% alcohol (tw o tim e s alcohol renew al)
12h
te c h n o v it 7100 solution A
m in. 24h
te c h n o v it 7100 su lution A renewal
m in. 48h
add T e ch n ovit 7100 H arder II
12h
place in deepfreeze
12h
place a t room te m p e ra tu re (check progress)
approx. 2h
Place in oven
lh
Embedding
Polym erization
Table 2.5. Toluidin blue staining protocol
S o lu tio n /A c tio n
2g borax in 100 ml Aqua dest, 100 ml Aqua dest
and lg to lu id in blue pow der (pH = 9)
D u ra tio n
Rinsing
running ta p w a te r
3 min
Dring
on heating plate
3 min
M ounting
covering slide w ith m o u ntin g m edium
D rying
a t room te m p e ra tu re
S te p
S taining
30 Sec
2 h
20
2 IM a t e r í a L ANd M E T h o d s
Table 2.6. Im p ro ve d tric h o m e staining protocol
S o lu tio n /A c tio n
Parasolve 37°C
Parasolve room te m p
Alcohol 96%
Alcohol 96%
Alcohol 70%
Alcohol 70%
Aqua dest
Aqua dest
Aqua dest
H aem atoxyline
D u ra tio n
10 min
2 min
2 min
2 min
2 min
2 min
2 min
2 min
2 min
3 min
2g Haem atoxylin, 100ml ethanol 96, 100ml Glycerin, 4g Potasium -alum inium sulfate
(K al(S 04)212H 20), 0.3 g Na-iodide (Boiling together, cooling down and adding 10 ml acetic acid)
Running ta p w a te r
Acid fuchsine - ponceau de x y lid in e - orange G
10 min
10 sec. (M ove)
(a) acid fuchsin: 0.5g acid fuchsin, 1ml acetic acid and 100ml Aqua dest
(b) ponceau de xylidine: 0.5g ponceau de xyl, 1ml picric acid and 100ml Aqua dest
(c) orange G: 0.5g orange G, 1ml acetic acid and 100ml Aqua dest
Mixing 1 part (a), 2 pats (b) and 1 part (c) and making a 50% solution with Aqua dest
Aqua dest
Aqua dest
Aqua dest
T ungstophosphoric acid hydrate
T ungstophosphoric acid hydrate
Aqua dest
Aqua dest
A nilineblauw - orange G - acetic acid
1 min
1 min
1 min
few seconds
few seconds
1 min
1 min
1 min
100 ml Aqua dest, 2.2 g Orange G, 0.5 g Aniline blue and 8 ml Acetic acid
Using 1 part staining solution and 3 parts Aqua dest
Aqua dest
Aqua dest
Acetic acid 1%
Alcohol 80%
Alcohol 96%
Alcohol 96%
Xylene
1 min
1 min
2 min
even
even
even
To exam ine th e histological nature o f tw o orobranchial to n g u e -lik e appendages o f
P yth onichthys m a cruru s, these s tru ctu re s were
em bedded in paraffin. A series o f histological sections (5 pm ) was cut, stained w ith
an im proved tric h ro m e staining protocol and m ounted w ith DPX (Table 2 .6 ). Im ages
o f th e sections w ere captured using a d ig ita l cam era (C olorview 8, S oft Im a g ing
S ystem , M unster, G erm any). Also, to s tu d y th e s tru c tu re o f th e Suspensorium bone
2 IM a t e r í a L ANd M E T h o d s
and skin around th e m outh o f E u ryp h a ryn x pelecanoides, sm all pieces fro m the
hyo m andibula, and buccal ca vity's skin w ere em bedded in paraffin and cu t into 6
pm sections. The sections w ere stained w ith h e m atoxylin -e o sin based on Carson
and H ladik (2 0 0 9 ).
2 .2 .2 .4 . S h a p e a n a ly s is
For visualization purpose, th e overall shape differences betw een th e th re e species;
H oplunnis p u n c ta ta , C onger co n ge r and H ete roco n g er hassi, was presented as
d e fo rm a tio n grids using tpsS pline (version 1.16; Rohlf, 2004a). The purpose o f
tpsS pline is to fa c ilita te th e com parisons o f pairs o f 2D co n fig u ra tio n s o f landm arks.
For th is , 11 landm arks (Table 2.7) w ere digitized on one specim en o f each species
using tpsD ig (version 2 .0 8 ; Rohlf, 2005). The package tp sU til (version 1 .26; Rohlf,
2004b) was used to generate th e required tp s file.
Table 2.7: D efinition o f landm arks used fo r th e shape analysis on th e skull
N um ber
D e fin itio n o f la n d m a rk
1
The a n te rio rm o s t end o f th e rostral region
2
The a n te rio r end o f th e m a x illa ry
3
The a n te rio rm o s t end o f th e in te ro rb ita l space
4
5
6
The anterodorsal end o f th e basisphenoid which
contacts th e fro n ta l in th e p o ste rio r wall o f the
The a n te rio r end o f th e p te ro tic bone
The co n ta ct p o in t o f th e fro n ta l to th e a n te rio r
end o f th e co n ta ct line o f tw o parietals
7
The posterodorsal end o f th e neurocranium
8
The a n te rio r suspensorial a rticu la tio n
9
O p e rcu lo -h yo m a n d ibular a rticu la tio n
10
Q u a d ra to -m a n d ib u la r jo in t
11
The p o ste rio r end o f th e m a xilla ry
22
2 IM a t e r í a L ANd M E T h o d s
2 .2 .2 .5 . V is u a liz a tio n
C a m e ra
lu cida:
Draw ings
o f th e
osteology,
based
on
cleared
and
stained
specim ens, and m yology, based on dissected specim ens, w ere m ade using a
stereoscopic m icroscope (O lym pus SZX7), equipped w ith a cam era lucida.
C T -s ca n n in g : To visualize th e osteological s tru ctu re s o f th e head o f S im enchelys
pa ra siticu s and E u ryp ha ryn x pelecanoides, th e specim ens w ere scanned a t th e
m o d ula r
m icro-C T
setup
of
G hent U nive rsity
(M asschaele
et
al.
2007;
h ttp ://w w w .u a c t.u Q e n t.b e 1) using th e d irectional tu b e head, a t 80 kV tube voltage.
2 .2 .3 . T e rm in o lo g y
In
o rd e r to avoid
disse rtatio n
is
m is in te rp re ta tio n s , th e te rm in o lo g y applied th ro u g h o u t this
defined
below.
The
chosen
te rm in o lo g ie s
are
based
on
the
experiences o f De Schepper (2 0 0 7 ) and com m ents o f D.G. S m ith , (S m ith so nia n ,
USA: A n g u illifo rm S pecialist) (personal co m m un ica tion ).
T e rm ino lo gy o f cranial skeletal elem ents follow s th a t o f Böhlke (1 9 8 9 c ), Rojo
(1 9 9 1 ), De Schepper e t al. (2 0 0 5 ) and De Schepper (2 0 0 7 ).
-
T e rm ino lo gy used to define sutures and a rticu la tio n s follow s
Hildebrand
(1 9 9 5 ).
-
The te rm in o lo g y fo r th e a n te rio r and p o s te rio r ceratohyal bones follow s De
Schepper e t al. (2 0 0 5 ). The fre q u e n tly used te rm in o lo g y ceratohyal bone and
epihyal
bone,
respectively,
is
not
used
because
it
suggests
incorrect
hom ologies (De Schepper e t a l., 2005).
-
The epiotic o f teleosts is considered to be an ossification o f th e occipital arch
th a t has invaded th e o tic region and so th is bone is te rm e d "e p io c c ip ita l"
(P atterson, 1975).
-
The a n gu la r com plex is th e re su lt o f a fusion o f th e a rtic u la r w ith th e re tro a rtic u lo -a n g u la r com plex (Robins, 1989). In a d u lt eels n e ith e r a separate
a n gu la r nor a re tro a rtic u la r is discernable. They ge ne ra lly fuse to fo rm a
single bony e lem ent. The a n gu la r w ith th e re tro a rtic u la r are observed to fuse
firs t and la te r d u ring o n to g en y th is com plex fuses w ith th e a rtic u la r (Tesch,
2003).
23
2 IM a t e r í a L ANd M E T h o d s
-
The H yom andibula is considered as com posed o f a fused hyom andibula and
m e ta p te ryg o id (Belouze, 2 0 0 1 ), s tro n g ly connected o r even fused w ith the
quadrate. As th e hom ology o f suspensorial elem ents in A n g u illifo rm e s is still
am biguous, th e te rm in o lo g y o f Belouze (2 0 0 1 ) is fo llo w e d, in w hich the
p a la to p te ryg o id
bone
according
to
Belouze
(2 0 0 1 ),
m ay
represent the
e cto p te ryg oid o f teleosts (Tesch, 2003).
-
T e rm ino lo gy o f th e circu m o rb ita l bones o f th e cephalic lateral line system
follow s Böhlke (1 9 8 9 c ), Rojo (1 9 9 1 ) and A driaens e t al. (1 9 9 7 ).
-
T e rm ino lo gy o f th e cephalic lateral line system follow s o f Böhlke (1 9 8 9 c).
-
T e rm ino lo gy o f th e chondrocranial d e ve lo p m e n t follow s A driaens and Verraes
(1 9 9 7 ) and G eerinckx e t al. (2 0 0 5 ).
Muscle te rm in o lo g y follow ed W interbottom i (1 9 7 4 ) and De Schepper e t al. (2 0 0 5 ).
The branchial m uscles te rm in o lo g y follow ed Nelson (1 9 6 7 ), W interbottom i (1 9 7 4 )
and Mehta and W a in w rig h t (2 0 0 7 ).
24
ChApTER 7
H eAd M o R p h o lo q y o f
t Ne
D u c k b ill E e I,
HopluNNIS PUNCTATA
5 H eAd MoRpholoqy of
t Fi e
D u c k b ill EeI
C hapter th re e
H ead M o rp h o lo g y o f th e D u c k b ill Eel, H o p lu n n is p u n c t a ta (R e g a n , 1 9 1 5 ;
N e tta s to m a tid a e : A n g u illifo rm e s ) in R e la tio n to J a w E lo n g a tio n
Modified fro m :
S o h eil E a g d e ri, Natalie D e S c h e p p e r and D o m in iq u e A d ria e n s (2 0 0 7 ).
Head m o rph o log y o f a duckbill eel, H oplunnis p u n c ta ta (N e tta s to m a tid a e :
A n g u illifo rm e s).
Journal o f M orphology 2 6 8 (1 2 ): 1069-1070.
S o h eil E a g d e ri and D o m in iq u e A d ria e n s (2 0 10 ).
Head m o rph o log y o f th e duckbill eel, H oplunnis p u n c ta ta (Regan, 1915;
N e tta sto m a tid ae : A n g u illifo rm e s) in relation to ja w elongation.
Zoology 1 1 3 (3 ): 148-157.
3 .1 . A b s tra c t
Hoplunnis punctata, a member of the anguilliformes, is a long-snouted eel that lives in
benthic habitats of the continental shelf of tropical waters of world. The purpose of this
study was to examine the skull morphology of this little known nettastomatid and to
understand the changes associated with jaw elongation as well as the implications of jaw
elongation on the feeding apparatus. We present a detailed description of the cranial
osteology and myology of H. punctata and how these characters differ from Conger conger
(Congrinae: Congridae), a representative with moderate jaw length; and Heteroconger hassi
(Heterocongrinae: Congridae), a representative with a short jaw. Shape comparison shows
a caudal displacement of the hyomandibula bone, quadrate-mandibular articulation and
opercle-hyomandibular jo in t; decrease in the depth of the neurocranium and increase in the
distance between the anterior suspensorial facet and the posterior end of orbit in H.
punctata as a result of the elongation of the preorbital region. These characteristics along
with its immobile, long maxilla and well-developed adductor mandibulae complex, suggest
that food may be obtained by powerful biting. Jaw elongation potentially affects the
functioning of the feeding apparatus in H. punctata by providing more space for the
olfactory rosette; increasing bite speed and reducing drag during prey capture.
25
5 H eAd MoRpholoqy of tFie D uckbill EeI
3 .2 . In tro d u c tio n
The evo lu tio n o f th e feeding system
in fishes has been th e s u b je ct o f m any
fu n ctio n al m orph o log y studies (Lauder, 1982; Ferry-G raham and Lauder, 2001a;
W ilga, 2005; W estneat, 2 0 04 ; W a in w rig h t, e ta /, 2007). D ifference in feeding mode
m ay be reflected in d iffe re n t m orphological specializations o f th e head, in relation to
d iffe re n t fu n ctio n a l dem ands (W a in w rig h t and Bellwood, 2002). A m orphological
co m p ara tive analysis o f th e cephalic region in its p ro pe r phylogenetic c o n te x t, can
then
allow
extensive
a b e tte r understanding
m orphological
o f th e
specialization.
m orphological
This
m ay
then
changes,
also
allow
leading
a
to
b e tte r
understanding o f th e im plicatio n on th e perform ance as changes occur. One aspect
related to th is is th e elongation o f th e
rostral region and ja w
length, which
o rig in ate d as th e re su lt o f a co n verg e n t evo lu tio n am ong m any te le o s t lineages
(W estneat, 2004). The a n g u illifo rm fishes have adapted to diverse life styles, which
m ay be linked to th e w ide range o f cranial m orphologies. This cranial v a ria tio n , w ith
associated m uscles, can be expected to largely re fle ct e v o lu tio n a ry p a tte rn s o f
feeding specialization in th e A n g uillifo rm e s. We use an e v o lu tio n a ry perspective to
com pare th e feeding a pparatus o f th re e species o f the anguilliform is to b e tte r
understand th e changes involved w ith elongating th e jaw s.
The N etta sto m a tid ae o r duckbill eels are a group o f long-snouted eels, m a in ly found
on th e o u te r co n tine n ta l shelf and co n tine n ta l slope o f th e tropics. Little is known
a b ou t th e ir biology, except fo r th e ir benthic habits. They are n o n -b u rro w in g o r
cre vice -d w ellin g eels, feeding on a v a rie ty o f sm all fishes and in ve rte b ra te s (S m ith ,
1989b).
This stu d y was conducted to understand th e m orphological peculiarities o f th e skull
associated w ith ja w
elongation
and th e
re sulting
im plications fo r th e feeding
apparatus in th e duckbill eel, H oplunnis p u n cta ta . We provide a detailed description
o f th e cranial osteology and m yo lo g y o f H. p u n c ta ta and its differences w ith th a t o f
rep re se n ta tive s o f tw o closely related
(C ongrinae:
a n g u illifo rm
C ongridae), w ith a m oderate ja w
(H eterocongrinae:
C ongridae),
w ith
su b fam ilies:
C onger co n ge r
le n g th ; and H ete roco n g er hassi
a sh o rt ja w
length.
The
N ettastom atidae
to g e th e r w ith th e C ongrinae, M uraenesocidae, H eterocongrinae and D erichthyidae
26
5 H eAd MoRpholoqy of tFie D uckbill EeI
fo rm a m o n op h yletic group and th e N otacanthiform es, a close ly-re la te d elopom orph
taxon w ith a sh o rt ja w , is considered as o u tg ro u p (W ang e t a l., 2003; Fig. 3 .1 ).
3 .3 . M a te ria l and m e th o d s
For
anatom ical
descriptions,
five
alcohol-preserved
specim ens
of
H oplunnis
p u n cta ta obtained fro m th e Musée National d 'H istoire Naturel o f Paris and Florida
Museum o f Natural H istory (MNHN 1965 -0 6 49 and UF 216386) w ere exam ined. The
specim ens w ere o f th e fo llo w ing size range (S tandard Length (SL), distance fro m
th e tip o f th e snout to th e end o f th e caudal peduncle) HP1: SL= 365 m m ; HP2:
SL= 314 m m ; HP3: SL= 311 m m ; HP4: SL= 598 mm and HP5: SL= 531 m m . Two
specim ens w ere cleared and stained according to th e protocol o f Hanken and
W assersug (1 9 8 1 ) fo r stu d ying th e osteology. For th e dissections, m uscle fib e rs
w ere stained according to Bock and Shear (1 9 7 2 ). Specim ens w ere studied using a
stereoscopic m icroscope (O lym pus SZX -7) equipped w ith a cam era lucida. S tric tly ,
fo r visualization purpose, th e overall shape differences observed betw een th e th re e
species is presented as d e fo rm a tio n grids using tpsS pline (version 1 .16; Rohlf,
2004a) (see c h a p te r 2: Table 2 .7 ). The specim ens used w ere fro m th e Zoological
Museum o f th e G hent U nive rsity (C on g e r conger-, UGMD 5 3 065) and 3D Pictures of
H ete roco n g er hassi provided by De S chepper (2 0 0 7 ).
The te rm in o lo g y o f cranial bones follow s Böhlke (1 9 89 c). The te rm in o lo g y fo r th e
a n te rio r and p o ste rio r ceratohyal bones follow s De Schepper e t al. (2 0 0 5 ). The
fre q u e n tly used te rm in o lo g y ceratohyal bone and epihyal bone, respectively, is not
used because it suggests inco rre ct hom ologies. M usculature te rm in o lo g y follow s
W interbottom i (1 9 7 4 ) and De Schepper e t al. (2 0 0 5 ). The cranial osteology and
m yology o f H ete roco n g er hassi and C onger co n ge r have already been described by
De Schepper, e t al. (2 0 0 7 ) and De Schepper (2 0 0 7 ), respectively.
3 .4 . RESULTS
3 .4 .1 . C ra n ia l O s te o lo g y o f H o p lu n n is p u n c t a ta
The neurocranium
e th m o vom e ra l
is elongated w ith a fo rw a rd prolongation o f th e p re m a xillo -
com plex,
which
consists
o f th e
p re m a xilla ,
eth m o id
and
pars
vo m e ra lis (Fig. 3.2a, b). The o lfa c to ry organ o f H. p u n c ta ta fills th e long o lfa cto ry
27
5 H eAd MoRpholoqy of tFie D uckbill EeI
fossa, which is spread a lm o st o ve r th e e n tire p re orb ita l region. The pars vo m e ra lis
o f th e p re m a xillo -e th m o vo m e ra l com plex la te ra lly fo rm s a crest to which the
anterodorsal edge o f th e p a la to p te ryg o id is connected. The pars vo m e ra lis o f the
p re m a xillo -e th m o vo m e ra l com plex bears one row o f enlarged, s tro n g ly pointed
piercing te e th (Figs. 3.2b and 3.3a).
The o rb ital region is com prised o f th e fro n ta ls , basisphenoid, pterosphenoids and
parasphenoid. The fro n ta ls expand la te ra lly creating shelves o v e r th e o rbits. The
a n te ro la te ra l corners o f these shelves are pointed fo rw a rd and each bear tw o pores
fo r th e su p rao rb ita l canal (Fig. 3.2a). The fro n ta ls enclose th e opening o f the
su p rao rb ita l canal a t th e level o f th e anterodorsal m argin o f th e o rb its (Fig. 3.2a).
The fro n ta ls have fused and bear a ridge a t th e m idline (Fig. 3.2a). The unpaired
basisphenoid has a process th a t barely extends into th e o rb it (Fig. 3.3a). The w elldeveloped o p tic foram en is present between th e basisphenoid and fro n ta l bones
(Fig. 3 .2 b ). The pterosphenoids fo rm th e la te ro p o s te rio r p a rt o f th e p o storbital
region.
The
pterosphenoid
is
attached
to
th e
basisphenoid,
sphenotic, p te ro tic and fro n ta l. The o lfa c to ry foram en
parasphenoid,
is present betw een the
pterosphenoid and basisphenoid (Fig. 3 .2 b ). The parasphenoid, w hich is connected
to th e basisphenoid, is a long sh a ft o f bone th a t extends fro m th e to o th e d pars
vo m e ra lis bone o f th e p re m a xillo -e th m o vo m e ra l com plex up to th e basioccipital. I t
fo rm s th e ve n tra l surface o f th e neurocranium and is narrow under th e o rbits.
The o tic region com prises o f th e p te ro tics, sphenotics, parietals, prootics and
epiotics. The p te ro tics fo rm th e m a jo r lateral longitudal brace o f the skull and
com prises
o f tw o
parts.
The superficial
portion
is tu b u la r,
and
is a n te rio rly
connected to th e opening o f th e su p rao rb ita l canal th a t is form ed by th e fro n ta l.
The tu b u la r portion o f th e p te ro tic fo rm s a canal enclosing th e cephalic lateral line
system . The deeper p a rt, fo rm in g th e basis fo r th e tu b u la r p o rtio n , s lig h tly overlaps
w ith th e surrou n d in g bones. Posteriorly th e p te ro tic bears th e p o ste rio r suspensorial
a rtic u la to ry facet. The p o ste rio r bo rde r o f th e p te ro tic passes s lig h tly th e p o ste rio r
m argin o f th e supraoccipital. The sphenotic is directed v e n tro a n te rio rly and bears
an e xtensive sphenotic process (Fig. 3.2a, b). M edially th e sphenotic process bears
th e lateral p a rt o f th e a n te rio r suspensorial a rtic u la to ry facet. The large parietal
bones are fused and are situated p o ste rio rly against th e fro n ta ls. The fro n ta l ridge
28
5 H eAd MoRpholoqy of tFie D uckbill EeI
is continuous w ith a parietal ridge in th e m idline. This ridge is th e origin fo r th e
A2ßp and A2ßa subsections o f th e a d d u cto r m andibulae m uscle com plex, which
pass la te ra lly o ve r th e parietal and hyom andibula. The p ro otic fo rm s th e a n te rio r
p a rt o f th e
o tic
bulla. The
p o ste rio r end
o f th e
p ro otic
is attached
to
the
basioccipital and la te ra lly attaches to th e p te ro tic (Fig. 3 .2 b ). The p o s te rio r rim o f
th e pterophenoid is covered by th e a n te rio r rim s o f tw o p rootic bones and these
tw o bones m eet each o th e r in th e m idline above th e parasphenoid bone (Fig. 3.2b).
The su tu re betw een th e basioccipital and p rootic is in te rd ig ita tin g (Fig. 3 .2 b ). The
ju g u la r foram en is present on th e a n te rio r p a rt o f th e p rootic (Fig. 3 .2 b ). The
trig e m in o -fa c ia l foram en
epiotics fo rm
is p o ste rio r to th e ju g u la r foram en
th e posterodorsal face o f th e cranium
(Fig.
3 .2 b ). The
and m e d ia lly co n ta ct the
supraoccipital (Fig. 3.2a).
The occipital region is com prised o f th e supraoccipital, exoccipitals and basioccipital.
These th re e bones fo rm th e p o ste rio r wall o f th e neurocranium . The supraoccipital
is surrounded by th e epiotics, parietals and exoccipitals and bears a sm all m edian
crest (Fig. 3 .2 a ). C audally, th e exoccipitals are dom ed and do rsally b o rde r the
foram en m agnum . Also, th e exoccipitals v e n tra lly connects to th e basioccipital. The
big
occipital
neurocranium .
condyle
It
of
fo rm s
th e
th e
basioccipital
ve n tra l
fo rm s
m argin
of
th e
th e
p o ste rio r
foram en
end
of
m agnum .
the
The
basioccipital bone extends a n te rio rly to th e p o ste rio r b o rde r o f th e prootics and
fo rm s th e p o ste rio r p a rt o f th e o tic bullae.
The nasal, a long bone, possesses a broad w ing a t th e rear o f its tip (Fig. 3.4a). It
encloses th e a n te rio r p a rt o f th e su p rao rb ita l canal. The single in fra o rb ita l is a long,
tube-shaped bone. The in fra o rb ito -p re m a x illo -e th m o v o m e ra l lig a m e n t connects th e
a n te rio r end o f th e in fra o rb ita l bone to th e p re m a xillo -e th m o vo m e ra l com plex.
F urtherm ore th e
m a x illo -p re m a x illo -e th m o v o m e ro -in fra o rb ita l
lig a m e n t connects
th e p o ste rio r end o f th e in fra o rb ita l to th e posterodorsal side o f th e m a xilla ry. The
in fra o rb ita l encloses th e body o f th e in fra o rb ita l canal and its p o ste rio r p a rt curves
d orsally (Fig. 3.4b).
The m a xilla ry is ankylosed a n te ro m e d ia ly to th e p re m a xillo -e th m o vo m e ra l com plex
(Fig. 3.3a). The p rim o rd ia l lig a m e n t connects th e p o s te rio r edge o f th e m a x illa ry to
th e
posterolateral face o f th e m a n d ib u la r (Fig.
29
3.5a). The m a x illo -p re m a xillo -
5 H eAd MoRpholoqy of tFie D uckbill EeI
e th m o v o m e ro -in fra o rb ita l lig a m e n t connects th e posterodorsal face o f th e m a xilla ry
to th e p o ste rio r p a rt o f th e in fra o rb ita l and th e p o ste rio r p a rt o f th e ve n tra l crest o f
th e p re m a xillo -e th m o vo m e ra l bony com plex (Fig. 3.5a). The m a x illa ry bears a row
o f sm all, pointed te e th on its a n te rio r h a lf and a double row o f s m a lle r te e th on its
p o ste rio r h a lf (Fig. 3.6a). The low er ja w is s lig h tly s h o rte r than th e upper ja w (Fig.
3.3a). The d e n ta ry com plex is elongated and its coronoid process is connected to
th e a n g u la r com plex. The m a n d ib u la r te e th are arranged in tw o rows, w ith the
medial row com prising ca niniform te e th th a t are larg e r than th e ones in th e lateral
row (Fig. 3 .6 b ). The a n g u la r com plex consists o f th e fused a n gu la r and a rticu la r,
bearing a sm all re tro a rtic u la r process. The a n gu la r com plex possesses a p o ste rio r
process behind th e
m eckelian fossa
(Fig.
3 .6 b ). The re tro a rtic u la r process is
directed caudom edially.
The Suspensorium is com prised o f five elem ents: th e h yo m andibula, q u adrate,
p a la to p te ryg o id , preopercle and a ca rtila g ino u s e le m e n t w here th e sym p le ctic bone
w ould be found (Fig. 3 .3 b ). The preopercle is described as p a rt o f th e o percular
series (see below ). The ca rtila g ino u s e le m e n t o f th e Suspensorium
ve n tra l to th e hyom andibula
is situated
(Fig. 3 .3 b ). The hyom andibula and qu ad ra te are
closely connected and fo rm a solid stru c tu re . The hyom andibula a rticu la te s d orsally
w ith th e neurocranium via tw o a rtic u la r condyles. The a n te rio r one fits into a socket
form ed by th e sphenotic and p te ro tic, w hereas th e p o ste rio r one fits into a facet on
th e pte ro tic. The lateral face o f th e Suspensorium has an elevated ridge fo r the
origin o f th e A 2av and A3 subsections o f th e a d d u cto r m andibulae m uscle com plex
and insertion o f th e le v a to r arcus palatine m uscle. The opercle a rticu la te s w ith a
condyle on th e p o ste rio r edge o f th e hyom andibula (Fig. 3 .3 b ). The pala to p te ryg o id
is attached to th e a n te rio r edge o f the quadrate by connective tissue, and it is
firm ly connected to th e lateral face o f th e p re m a xillo -e th m o vo m e ra l com plex, a t the
caudal face o f th e m a xillo -e th m o vo m e ra l a rticu la tio n facet. The p a la to p te ryg o id
lig a m e n t also connects th e Suspensorium to th e p a la to p te ryg o id (Fig. 3 .3 b ).
The o p ercu la r series is com prised o f fo u r bones: th e preopercle, interopercle,
subopercle and opercle (F ig .3 .7a). The distal m argins o f th e o p ercu la r bones w ere
lig h tly stained in th e specim ens studied. The m edial face o f th e a n te rio r process o f
th e preopercle is connected to th e low er ja w th ro u g h th e a n g u lo -p re o p e rcu la r
30
5 H e Ad
M o R p h o lo q y
of
t Fi e
D uckbill
E eI
ligam ent. The tw o p reopercular pores are present on th e dorsal rim and a n te rio r
process o f th e preopercle, respectively. The interopercle is tria n g u la r in shape and
is covered la te ra lly by th e p o s te rio r p o rtion o f th e preopercle. The interopercle is
connected to th e a n g u la r com plex via th e a n g u lo -in te ro p e rc u la r ligam ent. The
subopercle abuts against th e caudal edge o f th e interopercle and curves along the
e n tire p o s te rio r m argin o f th e opercle. The subopercle is attached to th e opercle by
connective tissue. The fan-shaped opercle a rticu la te s w ith th e o p ercu la r condyle o f
th e
hyom andibula
th ro u g h
its
a n te rio r
process
(Fig.
3 .3 b ).
The
operculo-
in te ro p e rcu la r lig a m e n t connects the m edial face o f th e a n te rio r process o f the
opercle to th e dorsom edial face o f th e interopercle (Fig. 3.3b).
The hyoid com plex consists o f th e unpaired, long cylindrical basihyal, spatulate
urohyal, paired a n te rio r ceratohyals and paired p o ste rio r ceratohyals (Fig. 3.7b, c).
The p o ste rio r p a rt o f th e urohyal expands v e rtic a lly and is blade-like in its lateral
aspect. The a n te rio r ceratohyals are th e largest elem ents o f th e hyoid arch, which
a rticu la te w ith th e urohyal. The a n te rio r ceratohyal is in te rd ig ita te d p o ste rio rly w ith
th e p o ste rio r ceratohyal. Two o f seven branchiostega! rays are connected to th e
a n te rio r ceratohyal and th e others to th e p o ste rio r ceratohyal. The branchiostega!
rays curve d orsally along th e ve n tra l b o rde r o f interopercle. They reach up to the
caudal border o f th e subopercle. The p o ste rio r ceratohyals are connected to the
Suspensorium
and
a n g u la r
com plex
by
tw o
c e ra to h y a lo -h y o m a n d ib u la r
and
ce ra to h ya lo -a n g u la r ligam ents, re spectively (Fig. 3.7c).
3 .4 .2 . C ep h alic la te ra l lin e sy ste m
The cephalic lateral line system is com prised o f th e su p rao rb ita l canal, adnasal
canal,
in fra o rb ita l
canal,
te m p o ral
canal,
p re o p e rcu lo -m a n d ib u la r
canal
and
su p ratem p o ra l com m issure. The su p rao rb ita l canal extends fro m th e tip o f the
sn o ut to th e in te ro rb ita l region, and bears fo u rte e n pores. The adnasal canal, a
sh o rt ascending branch o f th e in fra o rb ita l canal, s ta rts a t th e rear o f th e a n te rio r
n ostril. The in fra o rb ita l canal curves d o rsally into th e p o sto rbita l region. This canal
bears fo u r pores e xitin g fro m in fra o rb ita l and five pores on th e p o sto rbita l region.
The p re o p e rcu lo -m a n d ib u la r canal s ta rts a lm o st fro m th e rostral tip o f th e d e n ta ry
and its a n te rio r p a rt runs in an in fe rio r crest o f th e d e n ta ry com plex. This canal
31
5 H e Ad
of
M o R p h o lo q y
t Fi e
D uckbill
E eI
curves d o rsally into th e p o storbital region and en te rs into th e p o ste rio r end o f the
te m p o ral canal (F ig .3. 4b). The supratem poral com m issure connects th e rig h t and
le ft cephalic lateral line system . The e th m o id canals w ere not observed.
3 .4 .3 . C ra n ia l m y o lo g y o f H o p lu n n is p u n c ta ta
The large a d d u cto r m andibulae m uscle com plex is com prised o f th e sections A2 and
A3. Despite a sm all and in d ire ct connection betw een tendon A2av and th e m a xilla ry
via th e
prim o rd ia l
lig a m e n t (w hich
could suggest a hom ology w ith
A Í ) , th is
subsection was te rm e d A2av based on th e te rm in o lo g y o f W interbottom i (1 9 7 4 ) and
due to its m ain insertion being onto th e posterom edial face o f th e low er ja w (Fig.
3 .5a). The section A2 can be subdivided into fo u r subsections: A2ß a n te rio r, A2ß
p o ste rio r, A2a dorsalis and A2a v e n tra lis (Fig. 3 .5 a ). The subsection A2ßp is th e
largest
p o rtion
m usculously
of
fro m
th e a d d u cto r
th e
m andibulae
su praoccipital,
epiotic,
m uscle
com plex
parietal
and
and o riginates
fro n ta l.
It
inserts
te n d in o u sly onto th e dorsom edial edge o f th e coronoid process and th e a n te rio r
portion o f th e m eckelian fossa. The subsection A2ßa o rig in ate s m usculously from
th e fro n ta l and pa rie ta l, and inserts te n d in o u sly o nto th e m edial face o f the
coronoid process. The p o ste rio r portion o f th e subsection A2ßa lies m edial to the
a n te rio r portion o f
attached
th e subsection A2ßp. The subsections A2ßa and A2ßp are
la te ra lly to a
m usculously
fro m
single tendon o f A2ß. The subsection A2ad o riginates
th e p o sterolateral
face
of
th e
hyom andibula
and
the
poste rove ntra I face o f th e p te ro tic. I t inserts te n d in o u sly o nto th e dorsom edial edge
o f th e a n g u la r com plex. The superficial portion o f th e subsection A 2av o riginates
m usculously fro m th e a n te ro la te ra l face o f th e preopercle, w ith its m edial fibers
a tta ch in g m usculously to th e hyom andibula and quadrate. The subsection A2av
inserts th ro u g h a tendon o nto th e posterom edial face o f th e a n g u la r process and
m usculously on th e m edial face o f th is process. A section Aco was not observed.
The section A3 is situated m edial to th e subsection A2ß and covers th e dorsolateral
face o f th e le v a to r arcus palatini m uscle and th e p o s te rio r p ortion o f th e a d d u cto r
arcus palatini m uscle (Fig. 3 .5 b ). This section o rig in ate s m usculously fro m the
lateral
ridge
of
th e
h yo m andibula,
th e
ve n tra l
face
of
th e
sphenotic,
the
a n te ro ve n tra l face o f th e p te ro tic , th e dorsolateral side o f th e pterosphenoid and
32
5 H e Ad
of
M o R p h o lo q y
t Fi e
D uckbill
E eI
th e p o ste roventral face o f th e fro n ta l's lateral expansion. I t inserts te n d in o u sly into
th e m eckelian fossa. The section A3 s lig h tly bulges la te ra lly a t th e level o f its
ve rtica l m idline.
The le v a to r arcus palatini m uscle o rig in ate s m usculously and te n d in o u sly fro m the
ve n tra l face o f th e sphenotic process and th e dorsolateral faces o f th e p ro otic (Fig.
3 .5c). This m uscle bulges s lig h tly in th e m idline. I t inserts m usculously on the
a n te rio r face o f th e lateral ridge and th e v e n tro la te ra l face o f th e hyom andibula.
The a d d u cto r arcus palatini m uscle o rig in ate s fro m th e v e n tro la te ra l face o f the
parasphenoid, th e
v e n tro la te ra l face o f th e
basisphenoid, th e ve n tra l face o f
pterosphenoid and th e a n te ro la te ra l face o f th e p rootic (Fig. 3.5c). I t fills the
p o ste rio r
p a rt
caudom edial
of
th e
surface
of
fissura
in fra o rb ita lis
th e
p a la to p te ryg o id
and
and
inserts
th e
m usculously on
m edial
face o f
the
the
hyom andibula. A th ic k p o ste rio r p o rtion o f th e a d d u cto r arcus palatini m uscle could
be d iscrim ina ted based on a discrete change in thickness fro m an a n te rio r th in p a rt,
but tw o parts still fo rm in g a continuous m uscle sheet. The th ic k e r p o rtion o f th e
a d d u cto r arcus palatini m uscle runs up to th e m edial face o f th e hyom andibula. The
fib e rs o f th e p o s te rio r p a rt o f th e a d d u cto r arcus palatini m uscle ta ke up the
position w here th e a d d u cto r hyom andibulae m uscle w ould be found.
The le va to r operculi m uscle o rig in ate s te n d in o u sly fro m th e caudal m argin o f the
p te ro tic. Its fibers are directed ca u d o ve n tra lly and dive rg e , inserting m usculously
on th e dorsal p a rt o f th e lateral face o f th e opercle (Fig. 3.5a, b).
The a d d u cto r operculi m uscle o rig in ate s m usculously fro m both th e p o ste rio r p a rt o f
th e p te ro tic and th e exoccipital. P roxim ally, its fib e rs run co n tinu o u sly w ith th e
fib e rs o f th e le v a to r operculi b u t in se rt on th e dorsom edial surface o f th e opercle
(Fig. 3.5c).
The d ila ta to r operculi m uscle is situated p o ste rio r to th e le v a to r arcus palatine
m uscle and th e section A3. The d ila to r operculi m uscle is a tria n g u la r m uscle, w ith
th e apex p o inting ca u d o ve n tra ly (Fig. 3 .5 b ). This m uscle o rig in ate s m usculously
fro m th e p o ste rove n tra l face o f th e sphenotic and th e p o sterolateral face o f the
p te ro tic. The d ila ta to r operculi m uscle inserts te n d in o u sly on th e sm all process,
which is situated on th e dorsal side o f th e a n te rio r process o f th e opercle (Figs. 3.5c
and 3.7a).
33
5 H e Ad
M o R p h o lo q y
of
t Fi e
D uckbill
E eI
Two separate halves (rig h t and le ft) o f th e p ro tra c to r hyoidei m uscle connect the
low er ja w to th e hyoid arch. Each o f these portions o rig in ate s te n d in o u sly fro m the
m edial face o f th e d e n ta ry a t th e re a r o f th e d e n ta ry sym physis and inserts by
m eans o f a tendon on th e dorsal surface o f th e p o s te rio r ceratohyal (Fig. 3.5d).
The sternohyoideus m uscle o rig in ate s m usculously fro m th e lateral surface and
te n d in o u sly fro m th e a n tro v e n tra l face o f th e cle ith ru m bone, w ith som e o f its fibers
m erging w ith those o f th e hypaxial m uscle. The ste rnohyoideus is a bipinnate
m uscle and th e p o ste rio r fibers o f th e le ft and rig h t halves attach via a central
tendon on th e p o ste rio r end and ve n tra l face o f th e urohyal. The a n te rio r fib e rs o f
le ft and rig h t halves o f th e sternohyoideus m uscle attach m usculously on th e lateral
sides o f th e p o s te rio r p a rt o f th e urohyal (Fig. 3 .5 d ).
The hyohyoideus m uscle com plex in te leosts ge ne ra lly includes th re e com ponents:
th e
hyohyoideus
in te rio ris,
hyohyoideus
a b d u cto r
and
hyohyoidei
adductors.
How ever, in H. p u n c ta ta these m uscles are u n d iffe re n tia te d and m erged as a th in
sac-like m uscle sheet m eeting its co u n te rp a rts a t th e ve n tra l m idline. The ve n tra l
fib e rs
o f th e
hyohyoideus
m uscle com plex attach
to
th e
dorsal face
o f the
branchiostega! rays. This sac-like m uscle connects to th e m edial face o f th e opercle
and reaches d o rsally up to th e horizontal septum .
The epaxial m usculature attaches to th e exoccipitals, p terotics and supraoccipital.
The hypaxial m u sculature attaches to th e basioccipital.
3 .4 .4 . S h a p e a n a ly s is
The d e fo rm a tio n grids in Figure 3.8 clea rly show a d is tin c t elongation o f the
p reorbital region, including th e snout, low er ja w and m a x illa ry bone going fro m
C onger co n g e r and H ete roco n g er hassi to H oplunnis p u n c ta ta
(Fig. 3 .8 ). This
elongation then results in th e q u a d ra te -m a n d ib u la r a rtic u la tio n being positioned
well to th e back in H. p u n c ta ta and C. conger, up to th e p o ste rio r region o f the
o rb it, w hereas th is jo in t is situated a t th e m id p o in t o f th e o rb it in H. hassi. The
d e fo rm a tio n grids also indicate a m ore dorsal position o f th is a rtic u la tio n , reflecting
a re la tive decrease in depth o f th e Suspensorium in H. p u n c ta ta com pared to the
o th e r tw o. The sam e decrease in depth is also observed in neurocranium .
34
5 H e Ad
M o R p h o lo q y
of
t Fi e
D uckbill
E eI
The distance betw een th e a n te rio r suspensorial fa ce t and th e p o ste rio r end o f the
o rb it is larg e r in H. p u n c ta ta , th is in relation to a reduction o f th e o rb it size and a
backward d isplacem ent o f th e hyom andibula.
The a n te rio r end o f th e p te ro tic is extended s u b s ta n tia lly in C. co n ge r and fo rm s a
sm all sh e lf o ve r th e p o ste rio r p a rt o f th e o rb it, but in H. p u n c ta ta and H. hassi it is
situated in th e p o sto rbita l region. Such a sh e lf is absent in H. hassi and is form ed
ra th e r by th e
lateral
hyo m a n d ib u la r jo in t
expansion
is also
o f th e
fro n ta l
positioned
caudal
in H. p u n cta ta .
to
th e
The opercle-
p o s te rio r edge
o f the
n eurocranium in H. p u n c ta ta (Fig. 3.8).
3 .5 . D iscussion
3 .5 .1 . M o rp h o lo g ic a l ch a n g e s to w a rd s ja w e lo n g a tio n :
H oplunnis p u n c ta ta and C onger c o n g e r are active p redators, w hereas H ete roco n g er
hassi lives in burrow s and p ro je cts th e fro n t portion o f th e body fro m th e b urrow to
feed on Zooplankton (C asim ir and Fricke, 1971; S m ith 1989a). C onger co n g e r is a
nocturnal p re d a to r feeding on fishes, crustaceans and cephalopods (B auchot and
Saldanha, 1986). H ete roco n g er hassi feeds on th e plan kto n -loa d e d cu rren ts by
snapping and picking sm all zo o planktonic particles (S m ith , 1989a; V igliola e t al.,
1996; Castle and Randall, 1999; De Schepper e t al., 2 0 0 7 ), w hereas H oplunnis
p u n cta ta is a benthic fish and feeds on sm all fishes and in ve rte b ra te s (S m ith ,
1989b).
Com parison o f m orphological s tru ctu re s w ith d iffe re n t co n fig u ra tio n s, p a rtic u la rly in
a p h ylogenetic
c o n te x t
m ay
help th e
p ro pe r u nderstanding
o f m orphological
e v o lu tio n a ry changes w ith in fu n ctio n al units. Hence, th e m orphological differences
on th e head o f th e re p re se n ta tive s w ith long (/-/. p u n c ta ta ), m oderate (C. co nger)
and
sh o rt
{H.
hassi) ja w
lengths,
used
in
th is
stu d y,
m ay
allow
a
b e tte r
understanding o f th e m orphological changes to w a rd th e elongation o f th e rostral
region and jaw s.
3 .5 .1 .1 . O s te o lo g y : The long p reorbital region o f H. p u n c ta ta and m oderate one in
C. co n ge r d iffe rs in shape fro m th a t in H. hassi, which possess a p a rtic u la rly sh o rt
one (Fig. 3 .8 ). The fro n ta ls o f H. p u n c ta ta , C. co n g e r and H. hassi are fused into a
35
5 H e Ad
M o R p h o lo q y
of
t Fi e
D uckbill
E eI
single u n it, ju s t as in th e D erichthyidae (Robins, 1989) and M uraenesocidae (S m ith ,
1989c), w hich is considered a derived cha racter in A n g uillifo rm e s (Belouze, 2001).
There is no fro n ta l sh e lf o ve r th e eyes and fro n ta l ridge in H. hassi and C. conger,
unlike in H. p u n cta ta . The parietals have not fused in C. co n g e r and H. hassi, b u t a
fusion is observed in H. p u n cta ta . The fusion o f parietals is a unique ch a racter state
in A n g uillifo rm e s (Belouze, 2 0 01 ). The conical m a n d ib u la r and vom eral te e th o f H.
p u n cta ta are large and sharp, w hereas those o f H. hassi are sm all. The te e th o f
upper and low er ja w s in C. co n ge r are arranged in a double row , w ith big incisiform
o u te r te e th and sm all inner ones. The p o ste rio r edge o f th e supraoccipital crest
does not reach th e p o ste rio r edge o f th e skull in H. p u n c ta ta w hile th a t o f C. conger
reaches beyond th e p o ste rio r edge o f th e skull. This crest is absent in H. hassi.
Absence o f th e supraoccipital crest is a plesiom orphic condition which is seen in
fossil A n g uillifo rm e s (Belouze, 2001).
The qu ad ra te
and
hyom andibula
o f H. p u n cta ta
and
C. co n ge r are stro n g ly
connected and fo rm a solid s tru c tu re . These tw o bones seem s lig h tly m obile in H.
hassi w ith respect to each o th e r, since th e y m ove so m ew hat when are pressed by
forceps. There is no sym p le ctic in C. conger, but a ca rtila g ino u s e le m e n t is present
p o ste rio r to th e quadrate in H. hassi and ve n tra l to th e hyom andibula
in H.
p u n cta ta . A posterocaudal process o f th e subopercle is connected to th e caudal
bo rde r o f th e opercle in H. p u n c ta ta and C. conger, w hile in H. hassi th is process is
lacking.
3 .5 .1 .2 . M y o lo g y : The a d d u cto r m andibulae m uscle com plex o f H. p u n c ta ta and C.
co n ge r is g re a tly enlarged com pared to th a t o f H. hassi. De S chepper e t al. (2 0 0 7 )
m entioned th a t th e expansion o f th e a d d u cto r m andibulae m uscle o f H. hassi m ay
have been re stricte d by its large eyes. The a d d u cto r m andibulae m uscle com plex
com prises sections A2 (w ith one subsection), A3 and Aco in H. hassi. In C. conger, a
m edial subsection A2ß and lateral subsection A2a are fo u n d , as well as tw o
subsections o f A3 th a t inse rt on th e m edial face o f th e m a n d ib u la r by a single
tendon (Fig. 3 .9 ). The Aco section o f th e a d d u cto r m andibulae m uscle, which is
found in m ost m a jo r o steichthyan groups (D iogo e t al., 2 0 0 8 ), is not present in
some
species in all groups w ith in th e Teleostei (Nakae and Sasaki, 2004; H ertw ig,
36
5 H e Ad
M o R p h o lo q y
of
2008).
Hence, th e
presence
t Fi e
D uckbill
E eI
o f section
Aco in H.
hassi m ay
be a retained
plesiom orphic ch aracter, b u t in th e c u rre n t absence o f additional m yological data o f
o th e r
a n g u illifo rm
ta x a ,
th is
needs
to
be
confirm ed.
The
presence
of
an
in te rm a n d ib u la ris m uscle and d iffe re n tia te d hyohyoideus inte rio ris m uscle are tw o
fe a tu re s in H. hassi th a t are not found in H. p u n c ta ta and C. conger. The shape
com parison o f the skull o f th e th re e species studied shows a re la tiv e ly longitudinal
and la titu d in a l stre tch in g o f th e Suspensorium and p o sto rbita l region in H. hassi. In
relation to th is e lo n g a tion , th e a d d u cto r arcus palatini m uscle in H. hassi is
prolonged ro s tra lly up to th e a n te rio r p o rtion o f th e o rb it.
The a d d u cto r hyom andibulae m uscle is present as a separate m uscle in H. hassi.
This m uscle has been reported in C. co n ge r by De Schepper (2 0 0 7 ), lying m edial to
th e
a d d u cto r
arcus
palatine
m uscle.
It
has
been
described
as "d iffic u lt
to
d is tin g u is h " (De Schepper, 2007). I t seems th a t th is m uscle has a co n figu ra tio n
s im ila r to th e one described here fo r H. p u n cta ta . I t is, th e re fo re , m o rphologically
an a d d u cto r hyom andibulae. In generalized, low er te leosts th e a d d u cto r arcus
palatini m uscle connects th e p rootic to th e dorsom edial face o f th e hyom andibula
(W interbottom i, 1974). Based on W interbottom i (1 9 7 4 ), th e te rm a d d u cto r arcus
palatini is applied to a m uscle th a t has expanded a n te rio rly along th e flo o r o f the
o rb it, as is seen in H. p u n c ta ta and C. co n ge r and an a d d u cto r hyom andibulae
muscle is o n ly distinguished by th e presence o f separate a n te rio r a d d u cto r arcus
palatine muscle.
3 .5 .1 .3 . J a w e lo n g a tio n : S ubstantial differences in th e length o f th e rostral region
and ja w length can be observed betw een re p re se n ta tive s o f th e m o n op h yletic group
com prising th e H ete roco n g rin a e -D e richth yid a e clade (clade A) and th e C ongrinaeM uraenesocidae-N ettastom atidae clade (clade B) (Fig. 3 .1 ). The m em bers o f clade
A possess a s h o rt to m oderate p re orb ita l region and those o f clade B a m oderate to
long one, as seen in H. p u n cta ta . In clade B, especially M uraenesocidae and
N etta sto m a tid ae
possess
a
su b s ta n tia lly
elongated
p reorbital
region
(S m ith ,
1989c).
Regarding the plesiom orphic condition o f A n g uillifo rm e s fo r having a s h o rt rostral
region (Belouze, 2 0 01 ), as is seen in m any A n g uillifo rm e s, and considering the
37
5 H e Ad
M o R p h o lo q y
of
D uckbill
t Fi e
E eI
p h ylogenetic re la tio n sh ip o f th e C ongrinae, M uraenesocidae and N ettastom atidae
(Robins, 1989; S m ith , 1989b; Wang e t al., 2003; O b e rm ille r and Pfeiler, 2003;
Lopez e t a l., 2 0 0 7 ), th e elongation o f ja w s in th e clade B should be considered as a
derived character.
Presence o f a separate
(D e rich th yid a e ),
a
p re m a x illa ry
m e m be r
of
(m edian
clade
A,
is
u n it)
a
in D erich th ys se rp en tin u s
unique
a ttrib u te
am ong
the
A n g uillifo rm e s (Robins, 1989). Robins (1 9 8 9 ) m entioned th e tre n d in D erichthyidae
to w a rds a fusion o f th e p re m a xilla ries w ith th e e th m o id to fo rm th e p re m a xillo e th m o vom e ra l
com plex.
Some
d e rich th yid
species
such
as
N essorham phus
ing o lfian u s bear a m oderate sn o ut w ith th e p re m a xilla ries fused to th e ethm oid
(Robins, 1989). F u rth e rm o re, H. hassi possesses a v e ry s h o rt rostral region, which
does include a p re m a xillo -e th m o vo m e ra l com plex. D ifferences in th e p reorbital
elem ents
of
clade
A
and
B
indicate
th a t
th e
fo rm a tio n
of
a
p re m a xillo -
e th m o vom e ra l com plex in clade A should not be considered as reflecting the
ancestral condition leading to w a rds sn o ut elongation in clade B. Hence, based on
parsim ony c rite rio n , it w ould be easy to conceive an e v o lu tio n a ry tre n d to w a rd a
separation o f th e p re m a x illa ry fro m
a p re m a xillo -e th m o vo m e ra l com plex in D.
serpentinus.
3 .5 .2 . F u n c tio n a l c o n s id e ra tio n s o f s n o u t e lo n g a tio n
The observed differences in th e feeding a pparatus o f these anguilliform is, especially
those related to ja w e lo n g a tion , can be considered having a p o tential influence on
th e fu n c tio n a lity o f th is apparatus. However, th is w ould require perform ance te stin g
to e m p irica lly su p p o rt th is hypothesis (A rn o ld , 1983).
The
m a xilla ry
in
H oplunnis p u n cta ta
is connected
firm ly
to
th e
p re m a xillo -
e th m o vom e ra l com plex along m ost o f its length, w hile in H ete roco n g er hassi only
th e
a n te rio r portion
o f th e
m a x illa ry
is resting
on th is
bony com plex.
This
co n figu ra tio n o f th e m a x illa ry in H. hassi, com bined w ith th e fo rw a rd position o f th e
q u ad ra te -m a n d ib u la jo in t, re su lt in a sm all and m ore oblique m outh border, which
has been regarded as a specialization fo r snapping pla n kto n ic prey (R osenblatt,
1967). This specialization in H. hassi m ay then com pensate fo r th e lacking o f upper
38
5 H e Ad
ja w
M o R p h o lo q y
of
t Fi e
D uckbill
E eI
pro tru sio n due to th e im m o b ility o f th e p re m a xilla ry (being fused to the
eth m o id and vo m e r).
The p o ste rio r position o f th e q u a d ra te -m a n d ib u la r jo in t in H. p u n c ta ta results in a
large m outh w ith a longer low e r ja w th a t m ay allow a rapid m outh closing (see
below ). The re la tiv e ly n arrow and low skull in H. p u n cta ta
im plies a shallow
orobranchial cham ber, which along w ith its im m ob ile , long m a x illa r is suggests th a t
food m ay be obtained by biting ra th e r than by filte rin g o r en gu lfin g th ro u g h suction
feeding (S chaeffer and Rosen, 1961). Fishes th a t re ly on h ig h -v e lo c ity lunges
follow ed by b itin g , ra th e r than suction, e x h ib it longer s trike tim e s (P o rte r and
M otta, 2004; Mehta and W a inw righ t, 2 0 0 7 b ), and th e kinem atics o f benthic biters
appear to be ty p ic a lly slow er than fo r suction feeding (A lfaro e t a l., 2 0 01 ; Rice and
W estneat, 2 0 05 ; Konow and Bellwood, 2005). Biting m ay re present an im p o rta n t
behavioural
a d aptation
enabling
predators to
subdue
large
prey
(M ehta
and
W a inw righ t, 2 007b). I t is th u s n o t su rprising to find a wide range o f m o rph o log ica lly
diverse biters (W estneat 2 0 04 ; De Schepper e t a l., 2 0 08 ; Grubich e t a l., 2008;
Mehta, 2009).
The stro n g ly developed a d d u cto r m andibulae m uscle com plex o f H. p u n c ta ta and C.
conger, com pared to a ra th e r sm all one in H. hassi, also suggests th e ir prey
ca p tu rin g m ode occurs using b iting. Enlarged a d d u cto r m andibulae m uscles m ay
allow a pow erful bite force by increasing th e m echanical load on skeletal elem ents
such as d e n ta ry com plex, Suspensorium and neurocranium (H errei e t a l., 2002; Van
W assenbergh e t a l., 2004). A p re d a to ry life style is considered th e plesiom orphic
condition fo r th e A n g uillifo rm e s (G osline, 1971; S m ith , 1989a), w ith hyp ertrop h ied
ja w muscles being com m on (B öhlke e t a l., 1989).
The m a x illa r is o f th e A n g uillifo rm e s are tig h tly jo in e d to th e cranium and are
im m obile o r can m ove v e ry little (Eaton, 1935). Hence, th e low er ja w is considered
as th e sole c o n trib u tio n o f ja w ro ta tio n , w ith th e q u a d ra te -m a n d ib u la r jo in t w orking
as a fu lcru m (A lexander, 1967; W estneat, 2004). Based on th e v e lo c ity advantage
(sm all in p u t/o u tp u t lever ra tio ), a long low er ja w m ay re su lt in a fa s te r m outh
closing (b itin g speed), which w ould be an advantage fo r a p re d a to r feeding on
elusive
prey.
S im ulta n e o usly, th is
low
ra tio also
im plies a low er m echanical
advantage. Hence, having a high in p u t force generated by h yp ertrop h ied a d du ctor
39
5 H e Ad
M o R p h o lo q y
of
t Fi e
D uckbill
E eI
m andibulae m uscles, as seen in H. p u n c ta ta and C. conger, can com pensate th is
deficiency
and
produce
s u ffic ie n tly
high
biting
forces
d u ring
snapping
bite
m ovem ents.
Elongation o f th e rostral region th a t com prise a deep lateral fossa as o lfa cto ry
cham bers, provide m ore space fo r th e o lfa c to ry rosette in benthic H. p u n cta ta ,
which is also su b s ta n tia lly long and large. Related to th is , an im proved olfaction
w ould b e ne fit th e ir p re d a to ry life style to d e te ct prey. The size o f th e ro sette is
p ro po rtio n al to th e fish 's a b ility to sm ell, and th e broadly spaced nares provide a
s ig n ifica n tly g re a te r separation betw een th e o lfa c to ry rosettes, which could lead to
an enhanced a b ility to resolve o d or gra die n ts (K a jiu ra e t a l., 2005).
Elongation
o f th e
ja w s
along
w ith
th e
reduction
o f th e
Suspensorium
and
n eurocranium depths i.e . re d u c tio n o f th e head d ia m e te r such as in H. p u n cta ta
m ay also provide a h yd rod yn a m ic advantage fo r drag reduction during feeding
strike s and sw im m in g. Fish (1 9 9 8 ) pointed o u t th a t d e p a rtu re fro m a sm o o th ly
rounded head in a n u m be r o f aquatic anim als th a t have a n te rio r p ro je ctin g beaks,
bills, and ro stru m s, m ay be related to a b e tte r fu n ctio n o f th e ir feeding m orphology
re q uiring grasping jaw s. The a lte rn a tin g concave and convex profile o f th e a n te rio r
p a rt o f th e
body, which
is seen
in aquatic anim als w ith
p ro je ctin g
a n te rio r
stru ctu re s, m ay induce a stepw ise, gradual drag pressure change th a t can reduce
skin fric tio n in anim als du rin g sw im m in g (B andyopadhyay, 1989; Bannasch, 1995;
B andyopadhyay and A hm ed, 1993). The re la tiv e ly sm all surface area o f th e a n te rio r
p ro je ctio n can also decrease drag in co n junction w ith a reduced pressure g ra die n t
d u ring sw im m in g (K ra m er, 1960; V ideler, 1995).
The cranial a n a to m y o f H. p u n c ta ta shows a n u m b e r o f d iffe re n t fe a tu re s com pared
to th e studied sh o rt snouted species, w hich m ay be related to th e observed
elongation
o f th e snout. Also, som e fe a tu re s
m ay re fle ct differences in prey
ca p tu rin g behavior, such as large and sharp piercing te e th on th e pars vo m eralis
and
m a n d ib u la r
bones,
depth
and
a n te rio rly
reduction
o f th e
Suspensorium ,
enlarged a d d u cto r m andibulae m uscle com plex, reduction o f neurocranial depth and
p o ste rio r
position
o f th e
q u a d ra te -m a n d ib u la r jo in t.
The ja w
elongation
can
assem ble som e advantages such as p roviding m ore space fo r th e o lfa c to ry rosette,
40
5 H e Ad
M o R p h o lo q y
of
t Fi e
D uckbill
E eI
increasing v e lo c ity advantage (b itin g speed) and drag reduction to prom ote the
prey capture kinem atics as a benthic b ite r predator.
A c k n o w le d g m e n ts :
We th a n k D.G. S m ith , (S m ith so nia n , USA) and R Mehta (UcDavis, USA) fo r th e ir
valuable com m ents. We th a n k P. Pruvost (Paris Natural H istory Museum , MNHN), R.
H. Robins and A. Lopez (Florida Museum o f N atural H istory) fo r m aking m useum
specim ens available and N. De Schepper (U G ent, B elgium ) fo r providing 3D pictures
o f H ete roco n g er hassi.
41
5 H e Ad
M o R p h o lo q y
of
t Fi e
D uckbill
E eI
42
ChApTER 4
CepM i'c MoRpholoqy of PyrhoNichrhys m acrurus
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
C hapter fo u r
C ep h alic M o rp h o lo g y o f P y th o n ic h th y s m a c r u r u s (H e te re n c h e ly id a e :
A n g u illifo rm e s ): S p e c ia liz a tio n s fo r H e a d -F irs t B u rro w in g
Modified fro m :
S o h eil E ag d eri and D o m in iq u e A d ria e n s ( 2 0 1 0 ) .
Cephalic m o rph o log y o f P yth onichthys m a cruru s (H eterenchelyidae:
A n g u illifo rm e s ): specializations fo r h e a d -firs t burrow ing.
Journal o f M orphology 2 7 1 (9 ): 1053-1065.
4 .1 . A b s tra c t
The Heterenchelyidae, a family of Anguilliformes, are highly specialized fossorial eels. This
study was conducted to evaluate the cranial specialization in relation to head-first burrowing
behavior in the heterenchelyid Pythonichthys macrurus. Detailed descriptions are provided
of the cranial myology and osteology of P. macrurus and its differences with those of
representatives of three families: the Moringuidae (Moringua edwardsi), a head-first
burrower; the Anguillidae (Anguilla anguilla), a non-burrowing representative, and the
Ophichthidae (Pisodonophis boro), a head and tail-first burrower. This comparison may help
to get a better understanding of the cranial specialization of head-first burrowers in
heterenchelyids and moringuids. We recognize as morphological adaptations to burrowing:
reduced eye size, a caudoventral orientation of the anteromedial section of the adductor
mandibulae muscle complex, the posterior position of the quadrate-mandibular jo in t, a solid
conical skull, large insertion sites of epaxial and hypaxial muscles on the neurocranium,
widened cephalic lateral line canals extending into the dermal cavities, and a ventral
position of the gili openings.
4 .2 . In tro d u c tio n
A n g u illifo rm fishes, a large group o f elongated, cosm opolitan te leosts (N elson,
2 0 0 6 ), are adapted fo r w edging th ro u g h sm all openings o r crevices (G osline, 1971;
S m ith , 1989c). They have evolved to a range o f d iffe re n t life styles fro m pelagic to
b u rro w in g , th e la tte r fro m h e a d -firs t (H eterenchelyidae, M oringuidae) to ta il-firs t
(O p h ichthidae). The h e a d -firs t burrow ers have been shown to have specific cephalic
43
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
fe a tu re s (M cCosker e t a l., 1989; S m ith 1989a, d, e; De Schepper e t a l., 2005,
2 0 0 7 b ), but an in te restin g question is w h e th e r h e a d -firs t burrow ing eels converge
on a sim ila r m orph o log y o r w h e th e r th e re are d iffe re n t ways to be a h e ad first
burrow er. De Schepper e t al. (2 0 0 5 , 2007b) considered som e fe a tu re s such as eye
re d uctio n ,
m o d ifications
of
th e
cranial
lateral
line
system ,
ja w
a d du ctor
h yp e rtro p h y , hyp ero ssifica tion , and ta p e rin g o f th e skull as cephalic ad ap tatio n s fo r
h e a d first burrow ing b ehavior in O phichthidae and M oringuidae.
The mud eels o r heterenchelyids, one o f th e 15 fa m ilie s o f th e A n g uillifo rm e s, are a
h ighly
specialized
fa m ily
of
b u rro w e r
eels.
They
com prise
tw o
genera
( P yth onichthys and P a n tu rich th ys) w ith e ig h t species and are considered well
adapted to th e ir bu rro w ing habits (S m ith , 1989a). The m em bers o f th is fa m ily are
found in th e tro p ical zone o f th e A tla n tic, M editerranean, and eastern Pacific and
v irtu a lly nothing is known a b ou t th e ir behavior, e xcept fo r th e ir burrow ing habits
(S m ith , 1989a). Blache (1 9 6 8 ) described th a t th e y live on sandy o r s ilty bo tto m s
and feed on sm all w orm s, crustaceans, and m olluscs. In co n tra s t to ta il-firs t
b u rro w ing ta xa , such as O phichthidae, th e heterenchelyids are h e a d first burrow ers,
th e re b y resem bling th e h a bit o f th e M oringuidae (S m ith and Castle, 1972; S m ith ,
1989e).
The aim o f th is s tu d y was to describe th e cranial m o rph o log y and recognize possible
specializations fo r h e a d -firs t burrow ing
m e m be r
of
th e
H eterenchelyidae.
b ehavior in P yth onichthys m a cruru s, a
Hence,
a
com parison
of
th e
cephalic
ch aracteristics o f th is h e te re n c h e ly s species w ith those o f a n o th e r group o f head­
firs t burrow ing eels, th e M oringuidae, is conducted. Also, a com parison o f the
cranial m orph o log y o f h e a d -firs t b u rro w e r eels w ith th a t o f a n o n -b u rro w in g , closely
related a n g u illifo rm
fa m ily w ill allow to
recognize s tru c tu ra l changes th a t are
a daptive fo r a h e a d -firs t bu rro w ing lifestyle. Hence, P. m a cruru s w ill be com pared
w ith re p re se n ta tive s o f th re e fa m ilie s: th e M oringuidae (M oringua e d w a rd si), a
h e a d -first
b u rro w e r;
th e
A nguillidae
(A nguilla
a n g u illa ),
a
n o n -b u rro w in g
re p re se n ta tive ; and th e O phichthidae (Pisodonophis b o ro ), a head- and ta il-firs t
burrow er.
Böhlke (1 9 8 9 b ) considered th e H eterenchelyidae, A nguillidae, and M oringuidae to
fo rm a m o n op h yletic clade based on m orphological data (see Fig. 4 .1 ). However,
44
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
S m ith
(1 9 8 9 e )
m entioned
th a t th e
m acrurus
re la tio n sh ip
o f th e
H eterenchelyidae
and
M oringuidae is a m a tte r o f co n je ctu re and resem blances betw een th e m are based
on plesiom orphic characters o r characters related to th e ir fossorial habits. Sm ith
(1 9 89 e ) also pointed o u t th a t it is d iffic u lt to fin d synapom orphies th a t are not
based on reduction o r losses o f characters in H eterenchelyidae and M oringuidae.
Because e a rlie r studies
have
based th e
re la tio n sh ip
o f H eterenchelyidae
and
M oringuidae on th e analysis o f e xte rn al m orph o log y and osteological data, we hope
to add valuable data to th e cladistic analysis by stu d ying th e ir cranial m yology. I t
seems th a t these h e a d -firs t burrow ers have undergone a stro n g selection fo r
p ro te cting th e head during bu rro w ing . By analyzing ch a racter sta te tra n s fo rm a tio n s
o f th e m yological com ponents involved, th e evo lu tio n o f these a d ap tatio n s fo r
h e a d -first burrow ing m ay becom e e v id e n t in an e x p lic it phylogenetic co n te xt. In
p a rticu la r,
th e
stu d y
H eterenchelyidae
and
of
Belouze
(2 0 0 1 )
M oringuidae.
Also,
did
th e
not
su p p o rt th e
p hylogenetic
m o n op h yly
tre e
based
of
on
m ito ch on d ria l ribosom al DNA sequences did not su p p o rt th e m o n op h yly o f the
A nguillidae and M oringuidae (O b e rm ille r and Pfeiler, 2 0 03 ). A lthough A nguillidae
and M oringuidae are m ore closely related to each o th e r than to heterenchelyids, we
p redict th a t th e
h e te re n c h e ly s ,
P. m a cru ru s w ill
e x h ib it m ore
m orphological
fe a tu re s in com m on w ith M. edw arsi, but w ith d iffe re n t p a tte rn being related to
synapom orphies o f th e M oringuidae and A nguillidae. Also, th e presence o f the
co n verg e n t fe a tu re s observed in s tric tly h e a d -firs t burrow ers is predicted in the
n o n -s tric tly h e a d -firs t b u rro w e r, P. b oro, b u t to a lesser degree.
4 .3 . M a te ria ls and m e th o d s
Five alcohol-preserved specim ens o f P yth onichthys m a cruru s, obtained fro m the
Musée National d 'H istoire Naturel o f Paris (MNHN 1 9 6 5 -0 6 4 0 ), w ere exam ined. The
specim ens w ere th e fo llo w ing sizes in S tandard Length (SL): P M I: SL = 288.9 m m ,
PM2: SL = 229.6 m m , PM3: SL = 44 2.5 m m , PM4: SL = 2 4 5m m , and PM5: SL =
189.3 m m ). Five co m m ercia lly obtained specim ens o f A n g uilla a n guilla (AA1: SL =
503 m m , AA2: SL = 484 m m , AA3: SL = 548 m m , AA4: SL = 518 m m , and AA5:
SL = 491 m m ) w ere exam ined. Two specim ens (PM2 and PM4) o f P. m a cruru s were
cleared and stained w ith alizarin red S and alcian blue according to th e protocol o f
45
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
Hanken and W assersug (1 9 8 1 ). Muscle fib e rs o f th e dissected specim ens were
stained according to Bock and Shear (1 9 7 2 ). The specim ens w ere studied using a
stereoscopic m icroscope (O lym pus S ZX -7), equipped w ith a cam era lucida. To
exam ine th e histological nature o f tw o orobranchial to n g u e -lik e appendages o f P.
m a cruru s, a series o f histological sections
(5
pm ) was cu t, stained w ith
im proved tric h ro m e staining protocol and m ounted w ith
an
DPX (based on PM1).
Im ages o f th e sections w ere captured using a d ig ita l cam era (C olorview 8, Soft
Im a g ing S ystem , M unster, G erm any).
Muscle te rm in o lo g y follow s W interbottom i (1 9 7 4 ) and De Schepper e t al. (2 0 0 5 ).
T e rm ino lo gy o f cranial skeletal elem ents follow s Böhlke (1 9 8 9 c) and Rojo (1 9 9 1 ).
The epiotic o f te leosts is considered to be an ossification o f th e occipital arch th a t
has invaded th e o tic region and so th is bone is te rm e d "e p io c c ip ita l" (P atterson,
1975). The cranial osteology o f M oringua edw ardsi, Pisodonophis b o ro, and A nguila
anguilla has been described in detail by De Schepper e t al. (2 0 0 5 ), Ti lak and Kanji
(1 9 6 9 ), and Tesch (2 0 0 3 ), respectively. The head m yo lo g y o f M. edw ardsi, P. boro,
and A. anguilla have alre a d y been described in detail by De Schepper e t al. (2 0 0 5 ),
De Schepper e t al. (2 0 0 7 b ), and De S chepper (2 0 0 7 ), respectively.
4 .4 . R esu lts
4 .4 .1 . C ra n ia l o s te o lo g y o f P y th o n ic h th y s m a c r u r u s
The neurocranium o f P yth onichthys m a cruru s fo rm s one solid u n it and ta p e rs fro m
th e o tic region to w a rd th e tip o f th e snout (see Fig. 4 .2 ). The e th m o id region is
com prised o f th e p re m a x illo -e th m o id com plex, vom eral bone and nasal bones. The
la tte r are described w ith respect to th e lateral line system (see below ). The vom eral
bone
fo rm s
th e
a n te rio r
base
o f th e
skull
and
is situ a te d
ve n tra l
to
th e
parasphenoid (Figs. 4 .2 b and 4 .3 a ). The vo m e rin e te e th are arranged in one to tw o
rows w ith te e th o f va rio u s lengths. The o lfa c to ry fossa is re la tiv e ly sm all and lies
betw een th e pars eth m o id o f th e p re m a x illo -e th m o id com plex and th e a n te rio r
bo rde r o f th e lateral expansion o f th e fro n ta l bone (Fig. 4 .3 a ). A pore is present on
th e o lfa cto ry fossa (Fig. 4 .3 a ).
A n te rio rly , a sm all m edian ridge is present w here th e tw o fro n ta l bones m eet. Each
fro n ta l bone bears tw o arches on its dorsal surface, which su p p o rt th e p o ste rio r p a rt
46
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
o f th e su p rao rb ita l canal and th e fro n ta l com m issure (Figs. 4.3a and 4 .4 a ). These
tw o fro n ta l arches are in a p e rpendicular position to each o th e r, w ith th e lateral
expansions o f th e fro n ta l bones fo rm in g th e base o f these arches (Fig. 4 .2 a ). The
sm all eye o f P. m a cruru s is situated under th e lateral expansion o f th e fro n ta l bone.
A n te rio rly , th e fro n ta l bones b o rde r th e p re m a x illo -e th m o id com plex. The e n tire
fro n ta l arches and th e a rch -like in fra o rb ita l bones are covered w ith th ic k connective
tissue. The basisphenoid fo rm s th e p o ste rio r b o rde r o f a sm all o rb it and is situated
dorsal to th e parasphenoid. I t bears tw o dorsal w ings th a t are surrounded by the
fro n ta l bones, pterosphenoids, and parasphenoids (Fig. 4 .2 b ). The foram en opticum
is present betw een th e tw o w ings o f th e basisphenoid th a t bears a tu b e -like
s tru ctu re on its a n te ro ve n tra l portion. The parasphenoid runs fro m
th e o rbits
p o ste rio rly, w ith its m iddle ridge co n tinu in g below th e p rootic and basioccipital
bones (Fig. 4 .2 b ). The parasphenoid is bifurcated a t its p o ste rio r end w ith a
basioccipital process wedged in-betw een (Fig. 4 .2 b ). T o g e th e r w ith th e prootic
bone, th e
pterosphenoid
borders th e
foram en
fo r th e
trig e m in o -fa c ia l
nerve
com plex (Fig. 4 .2 b ). The lacrim al and in fra o rb ita l bones are described w ith respect
to th e cranial lateral line system (see below ).
The o tic region com prises the sphenotic, p te ro tic, p rootic, e pioccipital, and parietal
bones. The sphenotic bone bears a ro s tro v e n tra lly directed process and fo rm s the
a n te rio r wall o f th e a n te rio r a rtic u la to ry fa ce t o f th e hyom andibula (Fig. 4 .2 b ). The
process bears a sm all pore on its ve n tra l face, w hereas th e rest o f th e ve n tra l
surface is p itte d . The p te ro tic bone overlaps w ith th e fro n ta l, p a rie ta l, and prootic
bones. The p te ro tic bone a n te rio rly bears a tu b u la r s tru c tu re in w hich th e te m poral
canal en te rs and w hich opens a t its p o s te rio r end. The p o ste rio r fa ce t o f the
hyom andibula
and th e
p o ste rio r p ortion
o f th e a n te rio r a rtic u la to ry fa ce t are
enclosed by th e p te ro tic bone. The p rootic bones fo rm th e a n te rio r p o rtion o f the
large o tic bullae, w hich are also enclosed by th e exoccipital bones and basioccipital
bone. The epioccipital bones fo rm th e m edial m argin o f th e p o ste rio r opening o f the
p te ro tic tu b u la r stru c tu re . The parietal bones show a serrated su tu re a t th e m idline
(Fig. 4 .2 a ). They bear an a n te ro la te ra l process th a t overlaps w ith th e fro n ta l bones.
The occipital
region
com prises th e
exoccipital
bones,
basioccipital
bone, and
supraoccipital bone. The supraoccipital bone is surrounded by th e epioccipital and
47
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
parietal bones and bears a sm all crest a t th e m idline (Fig. 4 .2 a ). The exoccipital
bones are dom ed and bear p itte d borders w ith th e foram en m agnum . Two rin g -like
e xtra sca p u la r bones are present p o ste rio r to th e occipital region. They are covered
w ith
a th ic k
layer o f connective
tissue
and
also su p p o rt th e
su pratem poral
com m issure.
The m a xilla ry bone is ankylosed a n te ro m e d ia ly to th e neurocranium . A n te rio rly , it
bears a dorsal ascending process th a t m e d ia lly possesses a m a x illa ry condyle (Fig.
4 .3 a ). The p o ste rio r end o f th e m a x illa ry bone is connected to th e dorsolateral face
o f th e low er ja w via th e p rim o rd ia l ligam ent. The conical m a xilla ry te e th lie in tw o
rows (Fig. 4 .5 a , b). The a n te rio r tip o f th e low er ja w is positioned s lig h tly a n te rio r
to th e upper ja w and its te e th run up to the coronoid process (Fig. 4 .5 c). The
coronom eckelian is a sm all e le m e n t on th e a n te ro ve n tra l side o f th e Meckelian
fossa, enclosed by th e d e n ta ry bone (Fig. 4 .5 c). The d e n ta ry bone fo rm s the
coronoid process th a t is connected to th e a n gu la r bony com plex. The m a n dib u la r
te e th are arranged in tw o rows w ith a m edial row and a longer lateral row (Fig.
4 .5 c). The a n gu la r bony com plex consists o f th e fused re tro a rtic u la r, angular, and
a rtic u la r bones. The m a n d ib u la r a rticu la tio n fa ce t is dorsal to th e a n g u la r bony
com plex (Fig. 4 .5 c). The re tro a rtic u la r process is directed caudally. The preoperclea n gu la r and in te ro p e rcle -a n g u la r ligam ents connect th e re tro a rtic u la r to th e medial
faces o f th e preopercle and interopercle bones, respectively.
The
Suspensorium
p a la to p te ryg o id ,
consists
and
o f fo u r
preopercle.
The
bones,
i.e .,
preopercle
th e
hyom andibula,
is described
as
q u adrate,
p a rt o f the
o p ercu la r series (see below ). The sym p le ctic bone is fused to th e p o ste rio r portion
o f th e quadrate. The hyom andibula bears a d is tin c t ridge on its lateral surface. The
hyom andibula a rticu la te s d orsally w ith th e neurocranium via tw o a rtic u la r condyles,
th e a n te rio r one situated on its anterodorsal co rn er (Fig. 4 .3 b ). The long, p o ste rio r
suspensorial a rtic u la r condyle is form ed
by a caudally extended
posterodorsal
process o f th e hyom andibula (Fig. 4 .3 b ). The o p ercu la r bone a rticu la te s w ith a
ve n tro ca u d a lly directed condyle, a t th e p o s te rio r edge o f th e hyom andibula. The
h yo m a n d ib u la -q u a d ra te axis is directed v e rtic a lly , th u s positioning th e q u ad ra te m a n d ib u la r a rticu la tio n p o ste rio r to th e o rb it. The p a la to p te ryg o id is a broad bone
and only its p o s te rio r end is connected to th e q u adrate by connective tissue (Fig.
48
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
4 .3 b ). The h yo m a n d ib u la r-p a la to p te ryg o id lig a m e nt connects th e dorsal m argin o f
th e p a la to p te ryg o id to th e h yo m a n d ib u la r ridge.
The o p ercu la r series com prises five e lem ents (opercle, preopercle, inte rop e rcle ,
subopercle,
and
su p ra-p re o pe rcle ).
The
preopercle
bears a tu b u la r,
a rch -like
s tru ctu re w ith an anterodorsal pro je ctio n on its a n te ro la te ra l face (Fig. 4 .3 b ). This
a rch -like s tru c tu re , w hich is covered by th ic k connective tissue, encloses a p a rt o f
th e p re o p e rcu lo -m a n d ib u la r canal (Figs. 4 .3 b and 4 .4 a ). The p o s te rio r portion o f
th e preopercle overlaps and is connected to th e a n te rio rh a lf o f th e interopercle. The
preopercleangular lig a m e n t connects th e a n terom edial rim o f th e preopercle to the
a n gu la r bony com plex. The interopercle is a re la tiv e ly large re cta n g u la r bone. The
in te ro p e rcle -a n g u la r
interopercle
and
lig a m e n t
continues
is
attached
p o ste rio rly
to
to
th e
th e
a n terom edial
p o ste rio r end
face
o f th e
of
the
p o ste rio r
ceratohyal bone. The subopercle is situated ve n tra l to th e opercle, to w hich it is
firm ly attached. C onnective tissue also attaches it to th e interopercle. A small
ve n tra l process is present on th e ro stro ve n tra l end o f th e opercle and acts as th e
a tta c h m e n t p o in t fo r th e d ila ta to r operculi m uscle. The s u p ra -p re o p e rcu la r bone,
which encloses p a rt o f th e p re o p e rcu lo -m a n d ib u la r canal, lies above th e a n te rio r
portion o f th e opercle (Fig. 4 .3 b ).
The hyoid com plex consists o f th e unpaired m edian basihyal and urohyal bones and
paired
a n te rio r and
p o ste rio r ceratohyal
bones (see
Fig. 4 .6 ).This expansion,
com prising th e urohyal a rtic u la r facets, lies v e n tra lly against th e a n te rio r end o f the
ceratohyal bones, and th e basihyo-ceratohyal ligam ents connects th e late rove n tra l
faces o f th e basihyal bone to th e ve n tra l face o f th e a n te rio r ceratohyal bones (Fig.
4 .7 a ). The urohyal bone is expanded a n te rio rly and is connected to th e a n te rio r end
o f th e a n te rio r ceratohyal bones via sm all u ro hyo -ce ra to hya l ligam ents (Fig. 4 .7 a ).
The basihyal bone is a cylindrical bone, which is expanded p o ste rio rly (Fig. 4 .6 a ).
No separate hypohyal bone could be distinguished. The a n te rio r ceratohyal bone is
connected to th e Suspensorium by m eans o f th e c e ra to h y o -h y o m a n d ib u la r lig a m e n t
(Fig. 4 .7 a ). A to ta l o f nine branchiostega! rays are supported by the a n te rio r and
p o ste rio r ceratohyal bone (Fig. 4 .6 b ). All o f them a rtic u la te w ith th e p o ste rio r
ceratohyal bone, w ith th e exception o f one. The branchiostega! rays curve dorsally
49
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
along the ve n tra l border o f th e inte rop e rcle and reach up to th e caudal b o rde r o f
th e opercle.
The cranial lateral line system com prises th e s u p ra o rb ita l, in fra o rb ita l, te m p o ral and
p re o p e rcu lo -m a n d ib u la r canals, and th e fro n ta l and su p ratem p o ra l com m issures.
The eth m o id and adnasal canals are absent. The cranial lateral line canals are
w idened due to th e arched bony elem ents th a t enclose th e m . The nasal bone lies
on th e anterodorsal face o f th e o lfa c to ry organ and supports th e a n te rio r portion o f
th e su p rao rb ita l canal. The m ain body o f th e nasal bone is tu b e -lik e , bearing a
v e n tro la te ra lly positioned w ing (Fig. 4 .4 b ). The fro n ta l- nasal lig a m e n t connects the
nasal bone to th e a n te ro ve n tra l co rn er o f th e lateral expansion o f th e fro n ta l bone
(Fig. 4 .7 b ). The p o ste rio r p a rt o f th e su p rao rb ita l canal is supported by th e a n te rio r
fro n ta l arch, which is expanded la te ra lly (Fig. 4 .4 a ). The fro n ta l com m issure is
enclosed by th e p o ste rio r fro n ta l arches (Fig. 4 .4 a ). Four in fra o rb ita l bones seem
m erely to
be lying
in an arched
position
(Fig. 4 .4 b ). The lacrim al and fo u r
in fra o rb ita l bones su p p o rt th e in fra o rb ita l canal. The a n te rio r p a rt o f th e in fra o rb ita l
canal
is enclosed
by th e
lacrim al
bone. The tu b u la r lacrim al
bone
bears an
a n te rio rly fla tte n e d p a rt superim posing th e m a x illa ry dorsal process. D orsally, th is
fla tte n e d p a rt o f th e lacrim al bone bears a m ore narrow tu b u la r s tru c tu re (Fig.
4 .4 b ). The prim o rd ia l lig a m e n t continues a n te rio rly and connects to th e p o ste rio r
p a rt o f th e lacrim al bone. The supra- and in fra o rb ita l in fra o rb ita l canal anastom ose
in th e fro n t o f th e p te ro tic opening and continue into th e te m p o ral canal. The
p re o p e rcu lo -m a n d ib u la r canal begins in th e v e n tro a n te rio r tip o f th e d e n ta ry bone.
I t runs inside th e m andíbula, w hich bears six pores (Fig. 4 .4 b ). The preoperculom a n d ib u la r canal
is curved
enclosed
a rch -like
by th e
caudodorsally a fte r e xitin g
s tru c tu re
o f th e
preopercle
th e
(Fig.
m andíbula and
4 .4 b ).
is
A supra-
p reopercular bone encloses th e p o ste rio r p ortion o f th e p re o p e rcu lo -m a n d ib u la r
canal before anastom osing w ith th e te m p o ra l canal. The su p ratem p o ra l com m issure
is enclosed by tw o rin g -lik e e xtra sca p u la r bones (Fig. 4 .7 b ). Despite e xistin g pores
on some bony elem ents th a t enclose th e lateral line system , such as those o f the
low er ja w , th e cephalic lateral line system bears few tin y pores on th e preoperculom a n d ib u la r canal. These are visib le under high m a g nifica tio n , im plying reduced
head pores.
50
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
4 .4 .2 . C ra n ia l m y o lo g y o f P y th o n ic h th y s m a c r u r u s
4 .4 .2 .1 . M uscles o f th e c h e e k
The a d d u cto r m andibulae com plex, th e m ost conspicuous m uscle o f th e cheek, is
subdivided into th e sections A2, A3, and Aco. The section A2 is subdivided into tw o
subsections:
A2a and A2b. The A2a
is th e ve n tra l e le m e n t o f th e
a d du ctor
m andibulae m uscle com plex and has a fleshy origin a t th e lateral face o f the
h yo m andibula, q u ad ra te , and th e a n te rio r rim o f th e preopercle; it has an additional
origin as a tendon fro m th e p o sterolateral face o f th e hyom andibula. This tendon is
also connected to th e th ic k connective tissue, w hich covers th e a rch -like stru ctu re
o f th e preopercle. The A2a inserts as a tendon on th e m edial face o f th e coronoid
process and as a m uscle on th e posterom edial face o f th e a n g u la r bony com plex.
The lateral face o f th e A 2 -tendon connects to th e p o ste rio r edge o f th e p rim o rd ia l
lig a m e n t and inserts on th e posterom edial face o f th e m andíbula (Fig. 4 .7 b ). The
subsection A2b is th e largest and m ost posterodorsal e le m e n t o f th e a d du ctor
m andibulae m uscle com plex. I t has a m uscular origin on th e fro n ta l, parietal and
supraoccipital bones and inserts as a m uscle and w ith tendons on th e dorsom edial
face o f th e Meckelian fossa. A p o ste rio r portion o f th e subsection A2b th a t is
situated lateral to th e le v a to r arcus palatini m uscle, bulges p o ste rio rly. The A3section o f th e a d d u cto r m andibulae m uscle com plex has a fle sh y origin fro m the
ve n tra l face o f th e lateral expansion o f th e fro n ta l bone, th e a n te ro la te ra l face o f
th e sphenotic process and th e pterosphenoid bone, and inserts as a tendon onto
th e Meckelian fossa. The p o ste rio r fib e rs o f th e section A3 are directed v e n tra lly
w hereas its a n te rio r fib e rs are directed m ore ca u d o ve n tra lly (Fig. 4 .7 c). The section
Ax arises as a tendon fro m th e a n te ro ve n tra l fib e rs o f th e subsection A2b. I t inserts
into the Meckelian fossa along w ith th e ve n tra l fib e rs o f th e subsection A2b.
The le v a to r arcus palatini m uscle o rig in ate s as a tendon fro m th e dorsal p ortion o f
th e h yo m a n d ib u la r ridge. Its fib e rs are spread ra d ia lly and in se rt on th e parietal
bone, th e supraoccipital bone, th e p o s te rio r region o f th e p te ro tic bone, and the
posterodorsal process o f th e h yo m a n d ib u la r bone (Fig. 4 .7 c).
The a d d u cto r arcus palatini is a re cta n g u la r m uscle w ith its fibers o rig in a tin g fro m
th e p o ste rove n tra l side o f th e pterosphenoid and th e v e n tro la te ra l face o f the
51
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
sphenotic bone. I t inserts w ith fib e rs on both th e lateral and m edial face o f the
anterodorsal
p a rt o f th e
h yo m a n d ib u la r
bone.
There
is no
insertion
on
the
p a la to p te ryg o id . Its dorsal fib e rs are covered by th e a n te rio r portion o f th e d ila ta to r
operculi m uscle (Fig. 4 .7 d ).
The a d d u cto r hyom andibulae m uscle connects w ith fib e rs to th e basioccipital,
p rootic,
and
parasphenoid
bones
and
runs
to
th e
dorsom edial
face
o f the
h yo m an d ibu la r bone. Its a n te rio r m argin is situated a t th e level o f th e a n te rio r
m argin o f th e h yo m a n d ib u la r bone.
The u n d iffe re n tia te d le v a to r operculi and a d d u cto r operculi m uscles, w hich can be
considered as a single le v a to r/a d d u c to r opercula m uscle, d ire c t ca u d o ve n tra lly (Fig.
4 .7 b ). Based on d iffe re n t origins o f m uscle parts, th e le v a to r/a d d u c to r operculi
m uscle can be divided into an a n te rio r, m esial, and p o ste rio r bundle. The a n te rio r
bundle has a fle sh y origin fro m th e ve n tra l edge o f th e posterodorsal process o f the
h yo m a n d ib u la r bone. Its lateral fib e rs in se rt on th e dorsolateral face o f th e opercle,
w hereas th e m edial fib e rs inse rt on th e dorsom edial face o f th e opercle. The mesial
bundle o rig in ate s as a tendon fro m th e p o ste rio r end o f th e posterodorsal process
o f th e h yo m a n d ib u la r bone and inserts w ith fib e rs on th e d orsolateral face o f the
opercle (Fig. 4 .7 b ). The p o ste rio r bundle o rig in ate s as a tendon fro m th e p o ste rio r
process o f th e
p te ro tic bone and
its lateral and
m edial fib e rs
in se rt on th e
dorsolateral and dorsom edial faces o f th e opercle, re spectively (Fig. 4 .7 d ).
The d ila ta to r operculi is tria n g u la r in shape (Fig. 4 .7 d ). I t o rig in ate s w ith m uscle
fib e rs fro m th e posterolateral face o f th e sphenotic bone and v e n tro la te ra l face o f
th e p te ro tic bone. I t inserts as a tendon on th e ro stro ve n tra l process o f th e opercle.
4 .4 .2 .2 . V e n tra l m uscles o f th e head
Left and rig h t halves o f th e p ro tra c to r hyoidei m uscle m erge a t th e m idline o f th e ir
length, b u t rem ain separated a t th e ir ends. Each halves o f th is m uscle o rig in a te as
a tendon fro m th e m edial face o f th e d e n ta ry bone, ju s t a t th e re a r o f th e dental
sym physis. They inse rt w ith m uscle fibers on th e ve n tra l faces o f th e a n te rio r and
po ste rio r ceratohyal bones (Fig. 4 .7 a ).
Left and rig h t bundles o f th e sternohyoideus m uscle m erge in th e m idline a fte r
o rig in a tin g w ith fib e rs fro m the e n tire a n te rio r and th e a n te ro la te ra l m argin o f left
52
4 CepIiaLíc MoRphoLoqy o f PyrhoN ichrhys
m acrurus
and rig h t cleith ra . They in se rt on th e p o ste rio r end o f th e urohyal bone via the
sternohyoideus tendon (Fig. 4 .7 a ).
The hyohyoideus m uscle com plex in teleosts ge ne ra lly includes th re e com ponents
(th e hyohyoideus in te rio ris, hyohyoideus a b du ctor, and hyohyoidei adductores).
How ever, in P. m a cruru s th e y are u n d iffe re n tia te d , m erging a n te rio rly as a th in
saclike m uscle sheet m eeting th e ir co u n te rp a rts a t th e ve n tra l m idline. Posteriorly,
both m uscle halves rem ain separate a t th e end o f th e orobranchial ca vity. This sac­
like m uscle interconnects th e m edial faces o f th e branchiostega! rays, opercle, and
subopercle and reaches d orsally up to th e horizontal septum betw een th e epaxial
and hypaxial muscles.
4 .4 .2 .3 . B ody m uscles
The epaxial m uscles inse rt d ire c tly on th e epioccipital bones, dorsal rim o f the
exoccipital bone, and as an aponeurosis on th e supraoccipital bone. The dorsal
fib e rs o f th e epaxial m uscles connect to th e fascia o f th e a d d u cto r m andibulae
muscle
com plex
and
th ic k
e xtra sca p u la r bones. The
connective
hypaxial
tissue,
m uscles
w hich
inse rt as an
covers
th e
aponeurosis
rin g -like
on the
ventrocaudal bo rde r o f th e basioccipital and exoccipital bones.
Two to n g u e -lik e appendages are present in th e ro o f o f th e orobranchial mucosa
(see Fig. 4 .8 ). Each appendage contains a ca v ity w ith few , sh o rt m uscle fibers
inserting on its internal base. This m ay resem ble a m o rph o log y s im ila r to th a t o f
th e palatal organ o f c y p rin ifo rm fishes, and hence a s im ila r fu n ctio n in assisting the
tra n s p o rt o f food could be speculated (S ibbing e t a l., 1986, Hernandez e t al.,
2007). How ever, fu rth e r research is required to elucidate th e tru e nature o f th is
organ.
4 .5 . D iscussion
4 .5 .1 . C ra n ia l s p e c ia liz a tio n s re la te d to h e a d -fir s t b u rro w in g
B urrow ing b ehavior is considered useful to use th e su b stra tu m
fo r p ro te ctio n ,
crypsis,
2 0 03 ),
and
feeding
purposes
(S u bram anian,
1984;
Bozzano,
and
is
observed to occur in va rio u s degrees in a n g u illifo rm fishes. P yth onichthys m a cruru s
appears to rem ain buried in th e su b stra tu m except, perhaps, fo r b rie f excursions in
53
4 CepIiaLíc MoRphoLoqy o f PyrkoN ichrkys
m acrurus
search o f food (S m ith , 1989a). M oringua ed w a rd si spends all its tim e burrow ed in
th e sand when it is im m a tu re (G ordon, 1954; Gosline, 1965), w hereas a dults o f th is
species lim it th e ir fossorial behavior to when th e y leave th e ir burrow s d u ring the
n ig h t (S m ith , 1989b). Pisodonophis boro penetrates th e su b stra te ta il-firs t b u t it is
able to b u rro w h e a d -firs t as well (T ilak and Kanji, 1969; S ubram anian, 1984;
A tkinson and T a ylo r, 1991). I t is known to b u rro w fo r sh e lte r and to find food
(S u bram anian, 1984). Anguilla anguilla is a n o n -b u rro w in g species (Tesch, 2003).
4 .5 .1 .1 . Eye re d u c tio n : P yth onichthys m a cruru s shares several cranial fe a tu re s
w ith tw o n o n-h e te re n che lyid burrow ing anguilliform is. One o f these characters is
eye reduction. Eye reduction in o p hichthids and m o ringuids are considered to be
a d ap tations to
h e a d -firs t bu rro w ing
(De Schepper e t a l.,
2005,
2 007b).
Eye
reduction is observed in m any o th e r fossorial elongated fishes such as Clariidae
(D evaere e t a l., 2001, 2 0 0 4 ), M astacem belidae (Poll, 1973), and A n g u illifo rm e s (De
Schepper e t a l., 2004, 2005, 2 007b; Aoyam a e t a l., 2005). The reduced eye o f the
O phichthidae and M oringuidae has been reported to be a d ap tatio n s fo r h e a d -first
b u rro w ing (M cCosker e t a l., 1989; S m ith 1989a, d ; De Schepper e t al., 2005,
2 007b). The s m a lle r eye size,
p a rtic u la rly
in
relation
to th e
m a crop h th a lm ic
ancestral state o f A n g u illifo rm e s (B öhlke, 1989a), can have a substantial e ffe ct on
th e spatial design o f head (Boel, 1985).
Eye reduction allow s a caudoventral
o rie n ta tio n o f th e a n terom edial section o f th e a d d u cto r m andibulae m uscle com plex
in P. boro and M. ed w a rd si (De Schepper e t a l., 2005, 2 0 0 7 b ), and th e reduction o f
th e
circu m o rb ita l
bones to
sm all tu b u la r bones
in M.
edw ardsi, clariids and
o p hichthids (T ilak and K anji, 1969; McCosker e t a l., 1989; Bozzano, 2 0 03 ; Devaere
e t al., 2 0 04 ; De Schepper e t a l., 2 007b). Eye reduction also has been linked to the
h yp e rtro p h y o f th e ja w m uscle in a n g u illifo rm
clariids (D evaere e t a l., 2001).
Hence, th e reduction o f th e eye in P. m a cruru s m ay be linked to th e caudoventral
o rie n ta tio n
o f th e
a n terom edial
section
o f th e
a d d u cto r
m andibulae
muscles
com plex (th e section A3) and tu b u la r circu m o rb ita l bones. F u rth e rm o re, th e opaque
skin o f th e eye in P. m a cruru s m ay also be a daptive to bu rro w ing . This fe a tu re has
been reported in O phichthus ru fu s (O p h ichthidae) as an a d aptation to p ro te ct from
m echanical in ju ry when th is eel ro u tin e ly enters and leaves a b urrow (Bozzano,
2003).
54
4 CepIiaLíc MoRphoLoqy o f PyrkoN ichrkys
4 .5 .1 .2 .
W id e n e d
c e p h a lic
la te ra l
m acrurus
lin e canals:
Because o f th e
associated
reduced visio n , o th e r sensory system s (such as o lfa cto ry, som atosensory, lateral
line and a u d ito ry system s) m ay becom e m ore im p o rta n t to provide e n viro n m en tal
in fo rm a tio n
p re do m ina te
(G ordon,
in
1954;
burrow ing
M ontgom ery,
organism s
1989).
th a t
th e ir
Chemical sensory cues m ay
vision
is
considered
poorly
developed (P ankurst and Lythgoe, 1983). Klages e t al. (2 0 0 2 ) has pointed o u t th a t
fin d in g prey fo r organism s th a t usually w a it fo r food by resting on th e sea flo o r o r
inside burrow s is based on th e detection o f th e noise (th e residual low -level sound)
produced by elastic w aves a t th e w ater-sea flo o r interface. Unlike M. edw ardsi,
which has its cephalic lateral line canals w idened into derm al cavities, P. m a cruru s
has w idened canals enclosed in th e arched bony elem ents o f th e skull under the
skin. This w idened cephalic lateral line canals m ay fu n ctio n as a kind o f sensory
pads, w hich are stim u la te d m echanically during bu rro w ing when in co n ta ct w ith
prey (De Schepper e t a l., 2 0 05 ). Most o f th e w idened canals o f th e cephalic lateral
line system o f P. m a cru ru s lack e xte rn al pores, except fo r th e tin y pores o f the
p re o p e rcu lo -m a n d ib u la r canal. M oringua ed w a rd si lacks any e xte rn al pores o f th e
cephalic lateral line system , w hereas ta il-firs t b u rro w e r, P. b o ro, retains pores in all
th e canals o f th e cephalic lateral line system . The lack o f head pores has the
advantage o f avoiding th e e n te rin g o f se d im e n t into th e canals d u ring h e a d -first
bu rro w ing (De Schepper e t al., 2005).
4 .5 .1 .3 . Gili o p en in g : The opercle is o rie n ta te d p o s te ro v e n tra lly in P. m a cruru s,
M. edw ardsi, and P. boro whereas th a t one o f A. a n guilla is directed caudally. As a
re su lt o f th is c o n fig u ra tio n , th e gili opening is positioned m ore v e n tra lly in the
bu rro w ing species. This m ay p re ve n t e n te rin g o f se d im e n t into gili c a v ity (G osline,
1971; S m ith , 1989c).
4 .5 .1 .4 .
D iffe re n t
o r ie n ta tio n
o f th e
a n te r io r
s e ctio n
o f th e
a d d u c to r
m a n d ib u la e m u s c le c o m p le x : The h yo m an d ibu lo -qu a d rate axis o f P. m a cruru s,
M. edw ardsi, and P. boro is directed d o rs o v e n tra lly , in co n tra s t to th e fo rw a rd ly
inclined one in A. anguilla. As a re su lt, th e q u a d ra te -m a n d ib u la r a rtic u la tio n is
positioned p o s te rio r to th e o rb it. In addition to th e sm all size o f eye, th e p o ste rio r
position o f th e q u a d ra te -m a n d ib u la r jo in t in these species also creates space
allow ing
a caudoventral
o rie n ta tio n
o f th e
55
a n te rio r
section
o f th e
a d d u cto r
4 CepIiaLíc MoRphoLoqy o f PyrkoN ichrkys
m acrurus
m andibulae m uscle com plex. The a n te rio r fib e rs o f th e section A3 in P. m a cruru s
are directed c a u d o ve n tra lly, w hereas its p o ste rio r fib e rs are directed v e rtic a lly. An
opposite o rie n ta tio n o f th e d iffe re n t section o f th e a d d u cto r m andibulae m uscle
com plex (ca u d o ve n tra lly versus ro s tro v e n tra lly ) can th e re b y help in p re venting the
dislocation o f th e m a n d ib u la r jo in t, even when large forces are exerted th a t induce
to rq u e forces (De Schepper e t a l., 2 007b). This sta b iliza tion o f th e m a n d ib u la r jo in t
m ay especially p re ve n t th e dislocation o f th e low e r ja w during initial h e a d -first
p e ne tra tio n considered as firs t stage o f b u rro w co n struction (James e t a l., 1995).
Despite o f a sh o rt and sharp snout, w hich is considered to be an a d aptation to
h e a d -first burrow ing
(M cCosker e t a l.,
1989;
S m ith ,
1989b, c), th e
p o ste rio r
position o f th e q u a d ra te -m a n d ib u la r jo in t also results in a large m outh gap and a
longer low er ja w . A large gape and longer low er ja w com bined w ith large te e th on
th e upper and low er ja w s in P. m a cruru s suggest a potential fo r rapid m outh closing
and dealing w ith large prey item s. Many bentic, lie -in -w a it o r c ry p tic predators have
p a rticu la rly large m ouths th a t can be opened and closed ra p id ly to grasp prey
(H elfm an e t al., 1997; Mehta and W a in w rig h t, 2007; M ehta, 2 0 09 ; Eagderi and
Adriaens, 2010a).
4 .5 .1 .5 . S kull s h a p e and
la rg e in s e rtio n s ite s o f body m uscles on th e
n e u ro c ra n iu m : The m o dification o f th e skull into a solid conical s tru c tu re w ith
sharp sn out, as seen in P. m a cruru s and tw o o th e r fossorial species, M. edw ardsi
and P. b oro, m ay fa c ilita te b u rro w in g , w here pow er is provided by th e cylindrical
body (C astle, 1968; S m ith , 1989d). S m ith (1 9 8 9 d ) m entions rapid m ovem ents o f
th e body, ju s t beneath th e surface, fo r subterranean
hunting and feeding
in
b u rro w ing A n g uillifo rm e s. The large insertion sites o f th e epaxial and hypaxial
m uscles on th e neurocranium (com prising exoccipital, e pioccipital, basioccipital, and
supraoccipital bones), which are also connected to th e a d d u cto r m andibulae m uscle
com plex, in P. m a cruru s can be considered an advantage fo r tra n s fe rrin g forces
fro m th e body o nto th e head. The physical coupling betw een th e ja w m uscles and
th e epaxial m uscles has been observed in M. ed w a rd si and P. boro (De Schepper e t
a l., 2005, 2 0 07b). B urrow ing fishes appear to use tw o m ain stra te g ies: m outh
excavation o r com pression and displacem ent o f se d im e n t by body m o ve m e n t
56
4 CepIiaLíc MoRphoLoqy o f PyrkoN ichrkys
m acrurus
(A tkinson and T a ylor, 1991). The head m orph o log y o f P. m a cru ru s suggests th a t
th e second s tra te g y is th e bu rro w ing m ethod applied.
4 .4 .2 .
V a ria b le
d e g re e
of
h e a d -firs t
b u rro w in g
s p e c ia liz a tio n s
in
A n g u illifo rm e s
Com pared
w ith
A n g uilla
a n gu illa ,
M oringua
edw arsi,
and
Pisodonophis
boro,
P yth onichthys m a cruru s exh ib its several unique characters such as presence o f the
fro n ta l arches, th e preopercle w ith its a rch -like s tru ctu re s, th e tu b u la r and a rch -like
circum o rb ita l
bones,
th e
a rc h -lik e
su p rap re o pe rcu lar
bone,
and
tw o
rin g -like
e xtra sca p u la r bones, which su p p o rt portions o f th e cephalic lateral line canals.
These characters are all considered synapom orphies fo r heterenchelyids (Belouze,
2 00 1 ).
Only M. e d w arsi lacks a basisphenoid, and P. m a cruru s was th e o nly anguillid in th is
stu d y to e x h ib it a separate vom eral bone. Fusion o f p re m a xilla ry, e th m o id , and
vom eral bones, fo rm in g th e p re m a x illo -e th m o v o m e rin e com plex in M. edw ardsi, A.
an gu illa , and P. b o ro, is considered synapom orphic fo r A n g uillifo rm e s (E aton, 1935;
Gosline, 1980; S m ith , 1989c). The p a la to p te ryg o id o f A. a nguilla is connected a t
both ends to th e q u adrate bone and th e p re m a x illo -e th m o v o m e rin e com plex,
respectively, w hereas th e p a la to p te ryg o id o f M. edw ardsi, P. m a cruru s, and P. boro
attaches only to th e Suspensorium . The pectoral fins are present in both A. anguilla
and P. boro but are w eakly developed in M. edw ardsi. According to Böhlke (1 9 8 9 b ),
all heterenchelyids lack pectoral fin s, w hereas m o ringuids have w eakly developed
pectoral fins.
Body elongation
com bined
w ith
lim blessness
allow s
unhindered
m o ve m e n t below th e su b stra te surface (Gans, 1975; Pough e t a l., 1998).
The a d d u cto r m andibulae m uscle com plex o f P. m a cru ru s shows s im ila r com ponents
bu t a d iffe re n t co n figu ra tio n w ith th a t o f th e o th e r fossorial species stu d ied , except
fo r th e lack o f th e section A l in M. ed w a rd si and P. boro. In basal a ctin op teryg ian
fishes, th e section A Í is defined by its dorsal position in th e a d d u cto r m andibulae
muscle com plex and its insertion on th e m a x illa ry bone th ro u g h a long tendon o r on
th e m a xilla ry bone its e lf (E aton, 1935; W interbottom i, 1974). The presence o f such
a section A Í has been reported in M. ed w a rd si and P. boro (De Schepper e t al.,
2005, 2 007b). In A. anguilla and P. m a cruru s, a sm all te n dinous connection was
57
4 CepIiaLíc MoRphoLoqy o f PyrkoN ichrkys
m acrurus
found betw een th e ve n tra l subsection o f th e section A2 and th e m a x illa ry bone via
th e p rim o rd ia l ligam ent. Based on th e te rm in o lo g y o f W interbottom i (1 9 7 4 ) and
regarding its main insertion on th e low er ja w , th is section in A. anguilla and P.
m a cruru s was considered as a subsection o f A2. Hence, th e section A2 o f the
a d d u cto r m andibulae m uscle com plex o f A. a nguilla consists o f fo u r subsections
(A2a, A2d, A2v, and A 2 m ; Fig. 4.9a, b, d). The hom ology o f each m uscle o f the
a d d u cto r m andibulae com plex (va rio u s ly d e te rm in e d as a subdivision, section, o r
subsection) is accepted on th e basis o f sharing an identical insertion p a tte rn onto
th e ja w s , fo llo w ing th e tra d itio n a l n om enclature used fo r th e a d d u cto r m andibulae
m uscles (V e tte r, 1878; W interbottom i, 1974; Nakae and Sasaki, 2004). M igrations
o f th e
m uscle
insertions
have
like ly
occurred
in e v o lu tio n a ry
h is to ry o f the
elopom orphs, resulting in th e lum ping o f non-hom ologous m uscles under a single
nam e. Hence, th e insertion o f th e ve n tra l subsection o f th e A2 in A. a nguilla and P.
m a cruru s m ay have m igrated fro m th e m a x illa ry bone to th e low er ja w as a nonhom ologous subsection o f th e A2.
Despite e xte rn a l, osteological and m usculature s im ila ritie s am ong th e fossorial
species stu d ied , th e co n figu ra tio n o f th e ir head m usculature e xh ib its m ore d ive rsity.
The a n te rio r p a rt o f th e section A2 and e n tire section A3 is directed ca u d o ve n tra lly
in M. edw ardsi, w hereas only th e section A3 in P. boro and a n te rio r fib e rs o f the
section A3 in P. m a cruru s are directed ca u do ve n tra lly. The le v a to r arcus palatini
m uscle is positioned caudally in P. m a cru ru s com pared w ith th e one in th e o th e r
species studied. Also, th e le v a to r arcus palatini m uscle connects th e p o ste rio r
elem ents o f th e ne uro cra n iu m , such as the p a rie ta l, su p raoccipital, and p te ro tic
bones to th e posterodorsal face o f th e h yo m a n d ib u la r bone. In th e th re e others,
how ever, th is m uscle connects th e v e n tro la te ra l face o f th e o rb ito te m p ra l elem ents
o f th e ne uro cra n iu m , such as th e sphenotic and parasphenoid bones, to th e lateral
face o f th e Suspensorium . Merging le ft and rig h t bundles o f th e ste rnohyoideus and
p ro tra c to r hyoidei
muscles
in P. m a cruru s is a n o th e r difference
in th e
head
m usculature o f th e species studied. The cephalic fe a tu re s th a t are considered
specializations fo r a burrow ing m ode o f life, such as a reduced eye, d o rsove n tra l
positioning o f th e h yo m an d ibu la -qu a d rate axis, caudoventral o rie n ta tio n o f the
a n terom edial section o f th e a d d u cto r m andibulae m uscle com plex, a widened
58
4 CepIiaLíc MoRphoLoqy o f PyrkoN ichrkys
cephalic
lateral
line
system
th a t
m acrurus
extends
into
th e
derm al
cavities,
ve n tra l
p ositioning o f th e gili opening, and large insertion sites o f epaxial and hypaxial
m uscles on th e neurocranium are absent in n o n -b u rro w e r a nguillids ( A a n gu illa ).
C haracteristics th a t are shared exclu sive ly by M. e d w ardsi and A. a n gu illa , such as
th e p re m a x illo -e th m o v o m e rin e com plex, th e pectoral fin and separate p ro tra c to r
hyoidei m uscle are considered as synapom orphies fo r th e m o n op h yletic group th a t
com prised th e A nguillidae and M oringuidae. The presence o f fe a tu re s th a t are
associated w ith h e a d -firs t burrow ing in P. boro suggest convergence w ith th e
studied fossorial fishes.
D iffe re n t p a tte rn s o f h e a d -firs t bu rro w ing fe a tu re s fo r th e H eterenchelyidae and
M oringuidae reveal th a t th e re is m ore than one w ay to re stru ctu re th e skull fo r
h e a d -first bu rro w ing . A lte rn a tiv e ly , s im ila r m orphological ch a racteristics, resulting
fro m sim ila r e n viro n m e n ta l pressures related to fossorial habit, m ay also explain
th e clustering o f heterenchelyids and m o ringuids in th e p hylogenetic tre e presented
by Böhlke (1 9 89 c). In clu din g data o f th e head m usculature o f th e th re e studied
fossorial eels, m ay provide additional in fo rm a tio n which we can use to resolve the
ph ylogenetic re la tio n sh ip o f a n g u illifo rm fishes (D iogo, 2004).
A CK N O W LE DG M ENTS
The a u th o rs w ould like to th a n k P. Pruvost (Paris Natural H istory M useum , MNHN)
fo r providing m useum specim ens, N. De Schepper (G hent U n ive rsity) fo r o ffe rin g
her exam ined m a te ria l, B. De Kegel (G hent U n ive rsity) fo r her technical assistance,
and D.G. S m ith (S m ith so nia n , USA) fo r his valuable com m ents.
59
4 CepIiaLíc MoRphoLoqy o f PyrkoN ichrkys
60
m acrurus
ChApTER 5
C e p h A lic SpECÍAlizATÍON
ín a
P a r a s ít íc E e L,
SÎMENckelys pARAsmcus
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
C hapter fiv e
C ep h alic S p e c ia liz a tio n in an a lle g e d P a ra s itic E el, S im e n c h e ly s p a r a s itic u s
(S im e n c h e ly in a e : S y n a p h o b ra n c h id a e )
S o h eil E a g d e ri, J o ach im C h ris tia e n s , M a tth ie u B oone, P a trie Jacobs and
D o m in iq u e A d ria e n s
Cephalic S pecialization in a Parasitic Eel, S im enchelys p a ra siticu s (S im enchelyinae:
S ynaphobranchidae).
To be su b m ite d : Copeia
5 .1 . A b s tra c t
The pugnóse eel, Simenchelys parasiticus, is the only member of the Simenchelyinae,
occurring worldwide from tropical to temperate latitudes. This deep-water eel has been
described as being parasitic. This study, based on head musculoskeletal morphology, tries
to provide a characterisation of the specializations of the pugnóse eel in relation to this
alleged parasitism. Its cranial myology and osteology are compared with the ancestral
morphology
of
non-parasitic
representatives
of
two
other
subfamilies
of
the
Synaphobranchidae, i.e. Ilyophis brunneus (Ilyophinae) and Synaphobranchus brevidorsalis
(Synaphobranchidae). The cephalic musculoskeletal elements of S. parasiticus, compared to
the situation in I. brunneus, and S. brevidorsalis show some morphological modifications,
such as the stretchable skin around the small terminal mouth opening, cutting-edge teeth, a
stout mouth closing apparatus with large associated muscles, a large tongue-like secretory
structure and branchial arches with the capacity to transport food items in the buccal cavity.
These may represent modifications in relation to its specialized way of feeding, however not
allowing to falsify or support the hypothesis of parasitism (versus scavenging).
5 .2 . In tro d u c tio n
Pugnóse eel, S im enchelys p a ra siticu s is a specialized d e e p -w a te r eel, occurring
w orldw ide
fro m
tro p ical
to
te m p e ra te
la titu d e s
(N elson,
2006).
S im enchelys
p a rasiticu s has been described as being parasitic, burrow ing into th e bodies o f
ha lib u t and o th e r large fish (Goode and Bean, 1896; Bigelow and S chroeder, 1953),
w hereas, Castel (1 9 6 1 ) concluded th a t th is eel is probably m ore o f a scavenger
61
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
than a predator. Robins and Robins (1 9 8 9 ) also pointed o u t th a t th e presum ed
m ode o f feeding is to rasp and rem ove th e flesh o f dead o r dying fishes by tw istin g
m o ve m e n ts, g ra d u a lly excavating a path into a carcass. Two pugnóse eels have
been found nestled into th e h e art o f a s h o rtfin m ako sh a rk displaying its potential
to e n te r into a n o th e r living organism to which th e y caused som e degree o f harm
(Caira e t a l., 1997).
Little is known a b ou t th e feeding behavior o f S. p a rasiticu s, except fo r th e abovem entioned observations. I f S. p a ra siticu s w ould be parasitic, then th e cephalic
specialization
in
S ynaphobranchidae,
w hich
m ay
it
d iffe rs
re flect
fro m
s tru c tu ra l
o th e r
m em bers
a d ap tatio n s
to
of
th e
parasitism .
fa m ily
These
m orphological specialisations, especially s tru c tu re s o f th e feeding apparatus, m ay
help to b e tte r understand th e actual feeding behaviour o f th is species. The pugnóse
eel belonging to th e m o n otypic S im enchelyinae, represents th e only known parasitic
species w ith in th e th re e subfam ilies o f S ynaphobranchidae (N elson, 2006). W ithin
syn a p h o b ra n ch u s, th e m axim um p a rsim ony tre e based on m ito ch on d ria l ribosom al
DNA sequences su pports th e m o n op h yly o f th e S im enchelyinae, Ilyo p hin a e and
S ynaphobranchinae (Lopez e t a l., 2 0 07 ). As such, a com parison w ith th e ancestral
m orph o log y o f th e n o n -p a ra sitic condition is p e rfo rm ed , w here th e cephalic fe a tu re s
o f rep re se n ta tive s o f tw o o th e r subfam ilies o f th e Synaphobranchidae, i.e. Ily o p h is
brunneus (Ily o p h in a e ) and Synaphobranchus b re vid o rsalis (S ynaphobranchidae),
are studied.
5 .3 . M a te ria l and m e th o d s
For th e anatom ical d e scription, five alcohol-preserved specim ens o f S im enchelys
p a ra siticu s (1.28736-024 and 1 .2 0 0 95 -0 3 1), seven specim ens o f Ily o p h is b runneus
(UF 222355, UF 230514 and UF 130897) and th re e specim ens o f S ynaphobranchus
b re vid o rsalis (USNM 2 7 3 4 2 7 -1 1 5 ) obtained fro m th e A ustralian Museum ( I) , Florida
Museum o f Natural H istory (UF) and S m ithsonian
National Museum o f Natural
H istory (USNM) w ere exam ined. The specim ens w ere o f fo llo w ing size in Total
Length, (TL) S. parasiticus', S P I: TL: 192 m m ; SP2: TL: 218.5 m m ; SP3: TL: 199
m m ; SP4: TL: 203; SP5: TL: 279 m m ; SP6: TL: 353 m m ; I. brunneus', IB 1: TL:
503 m m ; IB 2: TL: 348 m m ; IB 3: TL: 273 m m ; IB 4: TL: 573 m m ; IB 5: TL: 491
62
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
m m ; IB 6: TL: 496 m m ; IB 7: TL: 497 m m ; S. brevidorsalis', SB1: TL: 472 m m ;
SB2: TL: 357 m m ; SB3: TL: 397 m m .
One specim en o f each species (SP3, SB2 and I B l ) was cleared and stained w ith
alizarin red S and alcian blue according to th e protocol o f T a ylo r and Van Dyke
(1 9 8 5 )
fo r
osteological
exa m in a tio ns.
Dissections
w ith
m uscle
fib e r
staining
according to Bock and Shear (1 9 7 2 ) w ere p erform ed. To stu d y th e detailed internal
m orph o log y o f th e head, serial histological cross sections w ere generated. One
specim en
(S P I;
1.34900-002)
was decalcified
using
Decalc 2 5 % ,
dehydrated
th ro u g h an alcohol series, and em bedded in T ech n ovit7 1 0 0 . Series o f sections (5
pm ) w ere cu t using a Leica Polycut SM 2500, stained w ith Toluidin blue, and
m ounted w ith dpx. A n o th e r specim en (SP4) was scanned a t th e m o d ula r m icro-C T
setup o f G hent U nive rsity (Masschaele e t al. 2007; h ttp ://w w w .u g c t.u g e n t.b e ). The
specim en was scanned using th e d irectional tube head, a t 80 kV tube vo lta ge . The
d e te cto r was an a:Si fla t panel (Varian Paxscan 2520) w ith Csl s c in tilla to r. The
d e te cto r was used in binning m ode, enlarging th e d e te c to r pixels to 2 5 4 2 p m 2. The
g e o m e tric m a g nification o f 7.94 resulted in an e ffe ctive voxel size o f 3 2 3 p m 3. In
to ta l 1001 pro je ctio n s w ere m ade covering th e fu ll 360 degrees. The raw data was
processed and reconstructed using th e in-house developed CT softw are Octopus
(Vlassenbroeck e t al. 2007) and rendered w ith VG Studio Max (V olum e Graphics
GmbH
H eidelberg,
System s GmbH
G erm any)
M érignac,
and
A m ira
4 .1 .0
France). The lateral
softw are
line system
(M ercury
C om puter
was visualised
by
m a n ua lly draw ing it in Rhino 3D (M cNeel).
Muscle te rm in o lo g y follow s Nelson (1 9 6 7 ), W interbottom i (1 9 7 4 ) and De Schepper
e t al. (2 0 0 5 ). T e rm ino lo gy o f cranial skeletal elem ents follow s Böhlke (1 9 8 9 a ) and
Rojo (1 9 9 1 ). The e p io tic o f teleosts is te rm e d "ep io ccip ita l", th e re b y fo llow ing
Patterson (1 9 7 5 ). The external m o rph o log y o f S. p a rasiticu s has been described by
Regan (1 9 1 2 ), Jaquet (1 9 2 0 ), S olom on-R aju and R osenblatt (1 9 7 1 ), and Robins
and Robins (1 9 8 9 ). Also, b rie f osteological fe a tu re s o f S. p a ra siticu s w ere described
by Jaquet (1 9 2 0 ) and Robins and Robins (1 9 8 9 ). The cranial osteology o f Ily o p h is
b runneus and S ynaphobranchus species has been described in detail by Robins
(1 9 7 1 ).
63
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
5 .4 . R esu lts
5 .4 .1 . C ra n ia l o s te o lo g y o f S im e n c h e ly s p a r a s itic u s
The neurocranium ta pers fro m th e o tic region to w a rds th e sn o ut (Fig. 5 .1 a ). The
eth m o id region is com prised o f fused p re m a xilla ries and eth m o id bones, fo rm in g
th e p re m a xillo -e th m o id a l com plex, and th e vo m e r. The nasal bones cover the
o lfa cto ry rosettes th a t locate above th e sn o ut (Fig. 5.2c). A n te rio rly , th e fused
p re m a xilla ries spread la te ra lly and fo rm a m a x illa ry a rtic u la r fa ce t on th e ir p o ste rio r
face. The a n te ro ve n tra l p a rt o f th e p re m a xillo -e th m o id a l com plex bears tw o rows o f
te e th : an a n te rio r one w ith large te e th w ith a cu ttin g edge, and a p o s te rio r one w ith
tw o sm all, b la de-like te e th (Fig. 5 .1 b ). The d e n titio n o f th e v o m e r is discontinuous
w ith th a t o f th e p re m a xillo -e th m o id a l com plex and bears five ch ise l-like te e th on its
a n te ro ve n tra l face (Fig. 5 .1 b ). Posteriorly, th e v o m e r wedges into th e a n te ro ve n tra l
p a rt o f th e parasphenoid.
The o rb ital region com prises th e nasals, p re orb ita ls, s u p ra o rb ita l, in fra o rb ita ls,
p o sto rbita ls, fro n ta l, basisphenoid, pterosphenoids and parasphenoid. The nasals,
p re orb ita ls, su p ra o rb ita l, in fra o rb ita ls and p o sto rbita ls are described in relation to
th e cephalic lateral line system (see below ). A single fro n ta elem entl is form ed by
th e fused fro n ta l bones and bears tw o sm all pores on th e lateral face o f its
m idsection (Fig. 5 .1 a ). The foram en olfa cto riu s is present on th e a n te ro la te ra l face
o f th e fro n ta l (Fig. 5.1a). The fro n ta l bears a groove th a t lies in th e extension o f the
p te ro tic process and supports th e p o s te rio r end o f th e su p rao rb ita l canal before it
anastom oses w ith th e in fra o rb ita l canal (Figs. 5.2a and 5.3a). The fo ra m e n opticum
is present betw een th e tw o a n te ro ve n tra l parts o f th e fro n ta l and dorsal w ings of
th e basisphenoid (Fig. 5.2a). The basisphenoid fo rm s th e p o ste rove n tra l wall o f the
o rb it and its ve n tra l rim is enclosed by th e parasphenoid. The basisphenoid bears
tw o
w ings
th a t
fo rm
th e
ve n tra l
p a rt
o f th e
large
foram en
o p ticum .
The
pterosphenoid is situ a te d p o ste rio r to th e basisphenoid and bears a hole a t its
m argin w ith th e p rootic (Fig. 5 .1 b ). A n te rio rly , th e parasphenoid runs dorsal to the
v o m e r and fo rm s th e flo o r o f th e o rb it. I t spreads a t its m idsection and fo rm s tw o
lateral a la r processes th a t overlie th e posterom edial face o f th e pterosphenoids
(Fig. 5 .1 b ). Posteriorly, th e parasphenoid is bifurcated and bears a sm all keel on its
ve n tra l surface (Fig. lb ) .
64
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
The
o tic
region
com prises
th e
p te ro tics,
sphenotics,
parietals,
prootics
and
epioccipitals. The p te ro tic fo rm s th e lateral brace o f th e neurocranium and its
a n te rio r p a rt fo rm s a tu b u la r-lik e s tru c tu re th a t encloses the a n te rio r p a rt o f th e
te m p o ral canal. P osteriorly, th is canal opens a t th e caudal b o rde r o f th e p te ro tic
(Fig. 5.3a). The a n te rio r suspensorial a rtic u la to ry fa ce t is bordered m e d ia lly by the
p te ro tic, and la te ra lly by th e sphenotic (Fig. 5 .1 b ). The p o ste rio r suspensorial
a rtic u la to ry fa ce t com prises a caudodorsally directed groove in th e p te ro tic, w ith its
lateral wall fo rm e d by th e p o sterolateral crest o f th e p te ro tic (Fig. 5 .1 b ). The
ve n tra l surface o f th e sphenotic is connected to th e dorsolateral p a rt o f th e prootic.
The sphenotic process is directed a n te ro v e n tra lly . The parietals p o ste rio rly surround
th e lateral sides o f th e supraoccipital and overlie its a n te rio r part. The parietal
connects to th e p o ste rio r rim o f th e epioccipital th a t fo rm s th e dorsal rim o f the
p o ste rio r wall o f th e neurocranim , along w ith th e supraoccipital. The epioccipital
also fo rm s th e posterodorsal face o f th e neurocranium . The prootics fo rm the
v e n tro la te ra l
m idsection
o f th e
neurocranial flo o r and
la te ra lly bear L-shaped
depressions w here th e le v a to r interni and e xte rn i m uscles o f th e branchial arches
o rig in ate . The trig e m in o -fa c ia l foram en is present a n te rio r to th e p o s te rio r m argin
o f th e o tic bulla on th e p rootic (Fig. 5.1b).
The occipital region com prises th e su p raoccipital, exoccipitals and basioccipital.
These
bones,
to g e th e r
w ith
epioccipitals,
fo rm
th e
p o ste rio r
wall
of
the
neurocranium . A n te rio rly , th e supraoccipital bears a process th a t wedges into the
in te rp a rie ta l su ture (Fig. 5 .1 a ). Posteriorly, it bears a p o ste rio r w in g -lik e process
directed caudally w ith a crest on its ve n tra l face. In addition to th e foram en
m agnum , a re la tiv e ly large opening is present ve n tra l to th e supraoccipital on the
p o ste rio r wall o f th e neurocranium th a t is bordered by su p ra-, exo and epioccipitals.
The foram en m agnum is bordered d o rsally and la te ra lly by th e exoccipitals, and
v e n tra lly by th e basioccipital. The exoccipitals are dom ed to w a rd s th e foram en
m agnum fro m
its epioccipital m argin. The exoccipital is extended v e n tra lly to
c o n trib u te to th e ve n tra l surface o f th e neurocranium and is situated betw een the
basioccipital and p o ste rio r p a rt o f th e p te ro tic (Fig. 5 .1 b ). The a n te ro la te ra l faces o f
th e
basioccipital, to g e th e r w ith th e anterom edial
p a rt o f th e exoccipitals and
p o ste rio r p a rt o f th e prootics fo rm tw o re la tiv e ly sm all o tic bullae (Fig. 5 .1 b ). The
65
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
p o ste rio r end o f th e parasphenoid covers th e a n te rio r m idline o f th e basioccipital
th a t wedges into the p o ste rio r incisure o f th e parasphenoid (Fig. 5.1b).
The low er ja w is deep and sto u t. The d e nto -sp le n o -m e n to m e cke lia n com plex i.e.
th e d e n ta ry com plex bears one row o f the te e th w ith cu ttin g edges th a t reaches up
to th e coronoid process on th e p o s te rio r p a rt o f th e d e n ta ry (Fig. 5.4a). Also, th re e
sm all, b la de-like te e th could be observed m edial to th is row (Fig. 5 .4 a ). V e n tra lly,
th e d e n ta ry bone bears five large pores o f th e p re o p e rcu lo -m a n d ib u la r canal, which
is extended into th e la te ro ve n tra l groove o f th e a n gu la r com plex (Fig. 5 .3 b ). In
a d ditio n , th e d e n ta ry com plex bears five sm all nerve pores on its laterodorsal face
(Fig. 5.2a). The coronom eckelian bone is situ a te d a t th e re a r o f th e posterom edial
m argin o f th e d e n ta ry com plex inside th e Meckelian fossa. The a n gu la r com plex
consists o f th e fused a n gu la r, a rtic u la r and re tro a rtic u la r bones. The a n gu la r
com plex bears the m a n d ib u la r a rtic u la r facet im m e d ia te ly above th e re tro a rtic u la r,
and is directed caudodorsally. W ith th e low er ja w , tw o ligam ents are associated:
in te ro p e rc u lo -a n g u la r
and
ce ra to h ya lo -a n g u la r
ligam ents
th a t
attach
on
the
p o ste rio r face o f th e re tro a rtic u la r (Fig. 5.4a). The prim o rd ia l lig a m e n t connects th e
laterodorsal face o f th e a n g u la r com plex to th e
posterodorsal
m argin
o f the
m a xilla ry (F ig .5 .2a). The low er ja w is s lig h tly p ro tru d in g .
The m a xilla ry is a s to u t bone, w ith its ascending process m e d ia lly possessing a
p re m a xillo -e th m o id a l a rtic u la r condyle. The m a x illa ry bears a depression on the
lateral face o f its a n te rio r ascending process in w hich th e a n te rio r p a rt o f the
o lfa cto ry ro sette is fitte d (Fig. 5.2a). The m a xillo -p re m a x illo -e th m o id a l lig a m e nt
connects th e a n te rio r m argin o f th e m a x illa ry to th e lateral expansion o f the
a n te rio r tip o f th e p re m a xillo -e th m o id a l com plex. Thick fle sh y lips surround the
ja w s (Fig. 5.2c). Also, th e e n tire o lfa c to ry capsule and th e p o s te rio r th re e fo u rth
along th e length o f th e ja w s are covered by th ic k connective tissue o f th e derm is
(Fig. 5 .5 b ). The m a x illa ry also bears a laterodorsal depression on its m idsection in
which th e p o ste rio r p a rt o f th e in fra o rb ita l bone fits. The m a x illa ry bears a single
row o f tw e lve te e th w ith cu ttin g edges (Fig. 5.4b).
The
Suspensorium
com prises
fo u r
elem ents:
th e
hyom andibula,
q u adrate,
p a la to p te ryg o id and preopercle (Fig. 5 .2 b ). The preopercle is described as p a rt o f
th e o p ercu la r series (see below ). The h yo m andibula, q u adrate and pala to p te ryg o id
66
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
are tig h tly connected. The hyom andibula d orsally a rticu la te s w ith th e neurocranium
th ro u g h th e a n te rio r and p o ste rio r condyles (Fig. 5 .2 b ). The hyom andibula bears a
posterodorsal process th a t th e p o ste rio r condyle is situ a te d a n te rio r to th is process
on th e dorsal edge o f th e hyom andibula (Fig. 5 .2 b ). The suspensorial fossa is
form ed by th e a n te rio r parts o f th e hyom andibula and q u ad ra te , and a p o sterior,
broadened p a rt o f th e p a la to p te ryg o id and a ridge is present p o s te rio r to th is fossa.
The hyom andibula also bears a pore on th e m idsection o f its ridge and a lateral
process on th e dorsal end o f th is ridge (Fig. 5 .2 b ). The h yo m a n d ib u la -q u a d ra te axis
is inclined a n te rio rly , th u s positioning th e q u a d ra te -m a n d ib u la r jo in t a t th e level o f
th e
p o ste rio r
p a rt
of
th e
o rb it
(Fig.
5.2a).
The
o p ercu la r
condyle
of
the
hyom andibula is situated on th e posterom edial face and is directed ca u d o ve n tra lly
(Fig. 5 .2 b ). The p a la to p te ryg o id is connected p o ste rio rly to th e anterodorsal edge o f
th e hyom andibula and a n te rio rly to th e la te ro ve n tra l face o f th e m idsection o f the
v o m e r (Fig. 5.2a).
The o p ercu la r series is com prised o f fo u r bones: th e preopercle, interopercle,
subopercle and opercle (Fig. 5.6a). The preopercle fo rm s a groove to enclose the
p re o p e rcu lo -m a n d ib u la r canal. A n te rio rly , it bears a w ing th a t connects to the
poste rove ntra I edge and m edial face o f th e hyom andibula by connective tissue (Fig.
5 .6a). The interopercle is connected to both th e opercle and m andíbula by a
lig a m e nt:
th e in te ro p e rc u lo -a n g u la r and o p e rc u lo -in te ro p e rc u la r ligam ents (Fig.
5 .6a). The interopercle covers th e ve n tra l p a rt o f th e preopercle. The subopercle
connects to th e p o ste rio r edge o f th e opercle by connective tissue. The subopercle
a n te rio rly bears tw o p o s te rio r processes fo rm in g its a n te rio r incisure (Fig. 5.6a).
The opercle is a brace-like bone th a t curves p o ste rio rly. The o p ercu la r series are
also covered by a th ic k layer o f connective tissue. The sm all gili slits are positioned
well p o ste rio r to th e caudal b o rde r o f th e gili co ve r and are even located on the
ve n tra l side o f th e body, a t th e level o f th e p o ste rio r edge o f th e cleithra.
The hyoid com plex consists o f a m edian, sh o rt basihyal and urohyal, dorsal and
ve n tra l hypohyals, and a n te rio r and p o ste rio r ceratohyals (Fig. 5 .6 b ). The basihyal
is a cylindrical bone w ith expanded p o ste rio r condyle th a t a rticu la te s w ith the
hypohyals (Fig. 5 .6 b ). A th ic k layer o f g la n d u la r tissue covers th e basihyal. The
to n g u e -like stru c tu re contains m any se cre to ry unites w ith large se cre to ry cells th a t
67
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
opens on its dorsal surface th ro u g h th e ducts (Fig. 5.5b, c). The urohyal is sm all
and bears tw o dorsal hypohyal condyles and a p o s te rio r process to w hich attaches
th e
sternohyoideus
m uscle.
The
ve n tra l
and
dorsal
hypohyals
p o ste rio rly
in te rd ig ita te s w ith th e a n te rio r ceratohyal. The ve n tra l hypohyal bears a socket on
its ve n tra l face in which th e urohyal condyle a rticu la te s.
D orsally, th e dorsal
hypohyal bears th e basihyal facet. The a n te rio r ceratohyal is tig h tly connected to
th e
p o ste rio r ceratohyal.
The
nine
branchiostega!
rays are connected to
the
p o ste rio r ceratohyal and are curved caudally along th e ve n tra l and caudal border o f
th e inte rop e rcle , reaching up to th e p o ste rio r and dorsal region o f th e opercle. The
ce ra to h ya lo -a n g u la r
lig a m e n t
connects
th e
dorsolateral
face
o f th e
p o ste rio r
ceratohyal to th e a n gu la r com plex (Fig. 5.6b).
The cephalic lateral line system com prises th e su p ra o rb ita l, in fra o rb ita l, te m p o ra l,
and
p re o p e rcu lo -m a n d ib u la r
canals,
and
th e
fro n ta l
and
su pratem poral
com m issures (Fig. 5.3a). The su p rao rb ita l canal s ta rts a t th e a n te rio r end o f the
nasal bone and is extended to w a rds th e a n te rio r groove o f th e fro n ta l (Fig. 5.3a).
The nasal bone is a p la te -like bone w ith an irre g u la r m argin and d o rsally fo rm s a
tu b u la r s tru c tu re th a t supports th e a n te rio r p a rt o f th e su p rao rb ita l canal (Fig.
5 .3 b ). The largest p a rt o f th e nasal was o n ly lig h tly stained in th e specim en
studied. The su p rao rb ita l bone is a sm all ossicle th a t surrounds th e su p rao rb ita l
canal, ju s t a n te rio r to th e anastom osis w ith th e in fra o rb ita l canal. The infra orb ita l
canal sta rts a t th e a n te rio r end o f th e sm all p reorbital bone th a t is situated a t the
level o f th e a n te rio r m argin o f th e o lfa c to ry ro sette (Fig. 5 .3 ). Then, the tu b u la r
in fra o rb ita l bone, which is located on th e dorsal face o f th e m a x illa ry , encloses the
in fra o rb ita l canal (Fig. 5 .3 ). There are fo u r sm all, tu b e -lik e p o storbital elem ents
th a t enclose th e in fra o rb ita l canal a t th e p o storbital region
(o n ly th e ve n tra l
e le m e n t o f these bones was stained in specim ens stu d ied ) (Fig. 5 .3 b ). The te m poral
canal runs inside th e a n te rio r groove o f th e fro n ta l and th e bony canal o f the
p te ro tic. The p re o p e rcu lo -m a n d ib u la r canal s ta rts a t th e rostral tip o f th e d e n ta ry
bone and runs p o ste rio rly inside th e m a n d ib u la r canal. Then it continues into the
sensory groove o f th e preopercle before anastom osing w ith th e p o ste rio r end o f the
te m p o ral canal, as th e la tte r exits th e skull (Fig. 5 .3 a ). The p re o p e rcu lo -m a n d ib u la r
canal bears six sm all, e xte rn al pores. The fro n ta l com m issure lies on th e p o ste rio r
68
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
p a rt o f th e p re m a xillo -e th m o id a l com plex. The su p ratem p o ra l com m issure runs
u nder th e p o s te rio r p a rt o f th e a d d u cto r m andibulae m uscle com plex a t th e level o f
th e second v e rte b ra (Fig. 5.3a).
The gili arches are com prised o f th e fo llo w ing bones: tw o basibranchia! bones (Bb I
and I I )
(and tw o unossified basibranchials;
Bb I I I and Bb IV ), th re e pairs o f
hypobranchials (Hb I - I I I ) , five pairs o f ceratobranchials (Cb I-V ), one p a ir o f upper
pharyngeal to o th plates (UP), fo u r pairs o f epibranchials (Eb I-IV ), th re e pairs of
infra ph a ryn go b ra n chia ls (Ib II- IV ) and one p a ir o f low er pharyngeal to o th plates
(LP) (Fig. 5.7a).
5 .4 .2 . C ra n ia l m y o lo g y o f S im e n c h e ly s p a r a s itic u s
The large a d d u cto r m andibulae m uscle com plex com prises th e sections A2 and A3.
The section A2 is subdivided into a dorsal A2ß and a ve n tra l A2a (Fig. 5.8a). The
subsection A2ß is th e largest e le m e n t o f th e a d d u cto r m andibulae m uscle com plex
(Fig. 5.8a). Its a n te rio r p a rt bulges and has th e sam e d irection as th e p o ste rio r
part. The bulged p a rt o f th e A2ß is attached to th e posterodorsal p a rt o f th e tendon
A2ß, w hich inserts on th e m edial face o f th e d e n ta ry (a n te rio r to th e Meckelian
fossa) and its coronoid process. The tendon A2ß also fo rm s a te n dinous sheet
betw een th e lateral and m edial fib e rs A2ß (Fig. 5.5a). The p o s te rio r fib e rs o f A2ß
are also attached to th e ve n tra l p a rt o f th is tendon. The p o s te rio r p a rt o f th e large
A2ß covers th e a n te rio r p a rt o f th e epaxial m uscles and connects tig h tly to th e ir
dorsal faces by connective tissue (Fig. 5.8a). The subsection A2ß is also connected
to its co u n te rp a rt and d o rsally o rig in ate s m usculously fro m
th e supraoccipital,
e pioccipital, p a rie ta l, fro n ta l and p te ro tic bones.
The subsection A2a is th e ve n tra l e le m e n t o f th e a d d u cto r m andibulae m uscle
com plex th a t o rig in ate s m usculously fro m th e a n te rio r face o f th e preopercle,
posterodorsal process o f th e h yo m andibula, p o ste rio r parts o f th e hyom andibula
and q u ad ra te , a n te rio r face o f th e suspensorial fossa and ve n tra l face o f th e lateral
process o f th e hyom andibula (Fig. 5.8a). Its lateral fib e rs inse rt te n d in o u sly on the
d o rso p o ste rio r edges o f th e d e n ta ry and a n g u la r bones. The m edial fib e rs o f A2a
inse rt m usculously o nto th e p o s te rio r p a rt o f th e Meckelian fossa. There is also a
tendon A2a, w hich runs ve n tra l to th e lateral fibers o f th e A2a and inserts o nto the
69
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
poste rove ntra I p a rt o f th e Meckelian fossa. The dorsom edial fib e rs o f th e subsection
A2a are m erged w ith th e ve n tro m ed ia l ones o f A2ß. The section A3 o riginates
m usculously fro m th e ve n tra l p a rt o f th e fro n ta l, a n te rio r p a rt o f th e p te ro tic , dorsal
face o f th e pterosphenoid and anterodorsal face o f th e sphenotic process (Fig.
5 .8 b ). This m uscle inserts m usculously o nto th e ve n tra l p a rt o f th e Meckelian fossa.
The large le v a to r arcus palatini com prises tw o subsections (Fig. 5 .8 b ). The a n te rio r
subsection has its lateral fib e rs o rig in a tin g m usculously fro m th e la te ro ve n tra l face
o f th e sphenotic process, w hereas its m edial fib e rs o rig in a te te n d in o u sly ve n tra l to
th a t (Fig. 5 .8b, c). This subsection diverges v e n tra lly and inserts m usculously on
th e a n te rio r p a rt o f th e q u adrate and hyom andibula a t th e level o f th e suspensorial
fossa. The p o ste rio r subsection o f th e le v a to r arcus palatini o rig in ate s m usculously
fro m th e p te ro tic, p a rie ta l, a n te rio r p a rt o f th e epioccipital and p o ste rio r p a rt o f the
fro n ta l. Its lateral fib e rs inse rt te n d in o u sly on th e lateral m argin o f th e lateral
process o f th e hyom andibula and th e m edial fib e rs inse rt m usculously on th e medial
face o f th e lateral process o f th e hyom andibula (Fig. 5.8b).
The large a d d u cto r arcus palatini s ta rts a t th e level o f th e p o s te rio r p a rt o f th e o rb it
and o rig in ate s m usculously fro m th e a n te ro ve n tra l face o f th e parasphenoid, p rootic
and pterosphenoid (Fig. 5.8c). This m uscle is extended caudally to th e m edial face
o f th e p o s te rio r process o f th e hyom andibula and inserts m usculously on th e
dorsolateral m argin o f th e p a la to p te ryg o id , a n terom edial face and m edial face o f
th e m idsection o f th e h yo m andibula, and m edial face o f th e quadrate.
The a d d u cto r hyom andibula is a sm all m uscle th a t lies lateral to th e a d d u cto r arcus
palatini. I t o rig in ate s m usculously fro m th e v e n tro la te ra l depression o f th e prootic
and inserts on th e m edial face o f th e h yo m andibula, dorsal to its o p ercu la r condyle.
The d ila ta to r operculi o rig in ate s m usculously fro m the po ste rove n tra l face o f th e
sphenotic and p te ro tic and, inserts te n d in o u sly on th e a n te ro la te ra l face o f the
opercle (Fig. 5.8c).
The le va to r operculi o rig in a te s m usculously fro m th e posterom edial face o f the
p o ste rio r process o f th e h yo m andibula, b u t its p o s te rio r fib e rs are connected tig h tly
to th e la te ro ve n tra l face o f th e epaxials by connective tissue. This m uscle inserts
m usculously on th e dorsal edge and lateral face o f th e opercle (Fig. 5.8b).
70
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
The a d d u cto r operculi o rig in ate s m usculously fro m th e v e n tro la te ra l p a rt o f the
p te ro tic. I t is directed ca u d o ve n tra lly and inserts m usculously on th e dorsom edial
m argin th e opercle (Fig. 5.8c).
The th ic k p ro tra c to r hyoidei o rig in ate s m usculously fro m th e m edial face o f the
d e n ta ry a t th e rear o f the dental sym physis (Fig.
5 .8 d ). This m uscle inserts
m usculously on th e lateral face o f th e p o ste rio r ce ra to hya l, below the origin o f the
hyohyoideus inte rio ris m uscle.
The sternohyoideus m uscle inserts m usculously on th e lateral sides o f th e urohyal,
and th ro u g h a te n dinous sheet th a t separates th e le ft and rig h t halves. The m uscle
o rig in ate s m usculously fro m th e v e n tro la te ra l face o f th e cle ith ru m (Fig. 5.8d).
The hyohyoideus inte rio ris m uscle o rig in ate s m usculously fro m th e dorsal face o f
th e p o ste rio r ceratohyal. Both m uscle halves continue v e n tra lly to connect to a
m edian raphe, lying a t th e a n te rio r to th e hyohyoideus su p erio r m uscle com plex
(Fig. 5 .8 d ).
The
hyohyoideus
s u p e rio r
m uscle
com plex
fo rm s
a
sheet
of
fibers
th a t
interconnects th e successive branchiostega! rays, w here a n te ro d o rsa lly its fibers
attach to th e m edial faces o f th e opercle and subopercle, ve n tro m ed ia l face o f the
h yo m a n d ib u la r p o ste rio r process and th e m edial face o f th e a d d u cto r operculi
m uscle (Fig. 5.8a).
Both m uscle halves m eet th e ir co u n te rp a rt v e n tra lly a t a
hyohyoidal fascia but rem ain separate a t th e end o f th e orobranchial ca vity. This
m uscle attaches d orsally to th e horizontal septum betw een th e epaxial and hypaxial
muscles.
The le va to r e xte rn i m uscles o rig in a te m usculously fro m th e prootic, p o ste rio r to th e
a n te rio r suspensorial a rtic u la to ry facet. Posteriorly, these m uscles are subdivided
into th re e bundles inserting on th e posterodorsal faces o f th e epibranchials I - I I I
(Fig. 5 .7 b ).
The le va to r interni m uscles o rig in a te s im ila r to th e le v a to r e xte rn i m uscles and are
subdivided
into
tw o
bundles
inserting
on
th e
dorsal
faces
of
the
infra ph a ryn go b ra n chia ls II- IV and th e anterodorsal face o f th e upper pharyngeal
to o th plate (Fig. 5 .7 b ).
The large subpharyngealis has lon g itu d in a l fib e rs running on th e dorsal sides o f the
ve n tra l parts o f th e gili arches, including th e basibranchials I - I I I , hypobranchials I71
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
II and a n te rio r p a rt o f th e ceratobranchials I-IV . This m uscle o rig in ate s m usculously
fro m th e anterodorsal face o f th e a n te rio r ceratohyals, w ith co u n te rp a rts being
m erged caudally. T h e ir m edial fib e rs in se rt on th e a n te rio r face o f th e ve n tra l parts
o f th e gili arches and p o ste rio rly are m erged w ith fib e rs th a t o rig in ate fro m the
dorsal and p o ste rio r faces o f th e ve n tra l parts o f th e gili arches. I t m usculously
inserts
on
th e
a n te ro la te ra l
face
of
th e
fo u rth
ceratobranchials
above
the
tra n sve rsus v e n tra lis m uscle (Fig. 5.7b).
The tra n sve rsus v e n tra lis m uscle spans th e m idline betw een th e a n te ro ve n tra l faces
o f th e fo u rth p a ir o f ceratobranchials (Fig. 5.7b).
The p h aryn g o cle ith ra lis m uscle o rig in ate s m usculously fro m th e late ro ve n tra l face
o f th e cleith ru m and inserts m usculously on th e p o ste rove n tra l and posterom edial
faces o f th e fo u rth ceratobranchia! and th e m edial faces o f th e fifth ceratobranchia!
(Fig. 5 .8 d ).
The pharyngeal to o th plate a d d u cto r m uscle connects th e posterodorsal face o f the
fo u rth ceratobranchia! bone to th e ve n tra l face o f th e hypobranchial bone o f the
same
arch.
connected
The
to
th e
fo u rth
ceratobranchia!
low er and
upper
and
fo u rth
pharyngeal
hypobranchial
to o th
plates,
are
tig h tly
re spectively
by
connective tissue. C ontraction o f th is m uscle can bring upper and low er pharyngeal
to o th plates to g e th e r (Fig. 5 .7 b ). O ther branchial m uscles w ere not observed.
The
epaxial
m uscles
in se rt
m usculously
on
th e
su praoccipital,
epioccipitals,
p te ro tics, exoccipitals and basioccipital. The hypaxial m uscles inse rt te n d in o u sly on
th e p o ste rio r p a rt o f th e o tic bullae th a t are form ed
by th e exoccipitals and
basioccipital.
5 .4 .3 . C ra n ia l m y o lo g y o f I ly o p h is b r u n n e u s
The a d d u cto r m andibulae m uscle com plex is also com prised o f th e sections A2 and
A3. The section A2 is subdivided into a dorsal subsection A2ß and a ve n tra l
subsection A2a (Fig. 5.9a). The subsection A2ß, th e largest e le m e n t o f th e a d d u cto r
m andibulae m uscle com plex, inserts th ro u g h a tendon on th e m edial face o f th e
coronoid process. The a n te rio r fibers o f A2ß o rig in a te fro m a com m on fascia w ith its
co u n te rp a rt and its p o ste rio r fib e rs o rig in a te m usculously fro m th e supraoccipital,
e pioccipital, parietal and posterolateral m argin o f th e p te ro tic (Fig. 5.9a). The
72
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
subsection
A2a
h yo m andibula,
o rig in ate s
m usculously
anterodorsal
face
of
fro m
th e
th e
p o sterolateral
preopercle,
p o s te rio r
face
of
the
edge
of
the
suspensorial fossa and dorsal face o f th e quadrate. The lateral fib e rs o f th is
subsection inse rt te n d in o u sly on th e dorsal edge o f th e a n gu la r bone, p o ste rio r
edge o f th e coronoid process and its m edial fib e rs in se rt m usculously o nto the
Meckelian fossa. The m a x illa ry bone is connected to th e dorsolateral face o f the
a n gu la r com plex by th e p rim o rd ia l lig a m e n t th a t is located ve n tra l to A2a (Fig.
5 .9a). The section A3 o rig in ate s m usculously fro m th e a n te ro ve n tra l face o f the
p te ro tic, dorsal face o f th e pterosphenoid, dorsal face o f th e basisphenoid and
a n te ro la te ra l
face
o f th e
sphenotic.
This
m uscle
inserts
m usculously on
the
posterom edial face o f th e low er ja w fro m th e a n te rio r level o f th e coronoid process
to th e a n te rio r edge o f th e m a n d ib u la r a rtic u la tio n facet. Both th e inte rop e rcu lo a n gu la r and ce ra to h ya lo -a n g u la r ligam ents are present (Fig. 5.9b).
The a d d u cto r arcus palatini m uscle o rig in ate s m usculously fro m th e lateral face o f a
sm all ve n tra l keel on th e parasphenoid and inserts on th e m edial face o f the
q u adrate and posterom edial face o f th e hyom andibula. This m uscle s ta rts a t the
p o ste rio r level o f th e basisphenoid and runs caudally up to th e p o ste rio r level o f the
sphenotic. A th in , slen d e r-like pte ryg oid bone, w hich is situ a te d under th e a d d u cto r
arcus palatini
m uscle, connects to th e
p re m a xillo -e th m o id a l com plex and the
anterodorsal co rn e r o f th e q u adrate by th e p te ry g id e o -p re m a x illo -e th m o id a l and
p te ryg o id e o -q u a d ra te ligam ents, respectively.
The le va to r arcus palatini m uscle o rig in ate s m usculously fro m th e ve n tra l face o f
th e sphenotic process w ith
its fib e rs directed ca u d o ve n tra lly (Fig.
5 .9 b ). This
m uscle inserts m usculously on th e posterolateral face o f th e suspensorial fossa th a t
is form ed by th e a n te rio r parts o f th e hyom andibula and quadrate.
The d ila ta to r operculi m uscle o rig in ate s m usculously fro m th e p o ste rove n tra l face o f
th e sphenotic and late ro ve n tra l face o f th e p te ro tic and inserts m usculously on the
a n te ro la te ra l face o f th e opercle (Fig. 5 .9 b ).
The u n d iffe re n tia te d
le v a to r and a d d u cto r operculi m uscle com plex is directed
ca u d o ve n tra lly (Fig. 5 .9 a ), and o rig in ate s fro m
th e posterodorsal edge o f the
hyom andibula and v e n tro la te ra l face o f th e exoccipital. The lateral and m edial fib e rs
73
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
o f th e le v a to r/a d d u c to r operculi m uscle inse rt m usculously on th e dorsolateral and
dorsom edial faces o f th e opercle, re spectively (Fig. 5.9a, b).
The p ro tra c to r hyoidei o rig in ate s te n d in o u sly fro m th e m edial face o f th e d e nta ry,
p o ste rio r to th e dental sym physis (Fig. 5.9c). The lateral fib e rs o f th is m uscle inse rt
m usculously on th e anterodorsal face o f th e a n te rio r ceratohyal and its few medial
fib e rs connect to a p o ste rio r p ro tra c to r hyoidei tendon th a t is attached to the
u rohyalo-basihyal lig a m e n t and a n terom edial face o f th e interopercle (Fig. 5.9c).
The ste rnohyoideus m uscle o rig in ate s m uscoulously fro m th e ve n tro m e d ia l face o f
th e cle ith ru m , w ith le ft and rig h t halves m erging before inserting te n d in o u sly on the
p o ste rio r end o f th e urohyal (Fig. 5.9c).
The hyohyoideus m uscle com plex o f I. b runneus fo rm s a sheet o f fib e rs th a t
interconnects th e m edial faces o f th e branchiostega! rays, opercle and subopercle
and reaches d o rsally up to th e horizontal septum betw een th e epaxial and hypaxial
muscles. Both m uscle halves extend v e n tra lly to m eet th e ir a n tim ere s to fo rm s a
sac-like m uscle th a t covers th e branchial cham ber (Fig. 5.9a).
The le va to r e xte rn i m uscles o rig in a te m usculously fro m
a depression situated
p o ste rio r to th e a n te rio r suspensorial a rtic u la to ry fa ce t on th e prootic. Posteriorly
these m uscles are subdivided into th re e bundles inserting on th e posterodorsal
faces o f th e epibranchials III- IV .
The le va to r interni m uscles o rig in ate s im ila r as th e le v a to r e xte rn i m uscles and are
subdivided
into
tw o
bundles
inserting
on
th e
anterodorsal
face
of
th e
infra ph a ryn go b ra n chia l and dorsal face o f th e upper pharyngeal to o th plate.
Left and rig h t halves o f th e subpharyngealis run on th e dorsal sides o f th e ve n tra l
p arts o f th e gili arches, including th e basibranchials I - I I I , hypobranchials I - I I and
anterodorsal faces o f th e ceratobranchials III- IV . Each h a lf o f th is m uscle o riginates
m usculously fro m th e a n terom edial face o f th e a n te rio r ceratohyal and inserts on
th e a n te rio r p a rt o f th e fo u rth ceratobranchia!.
The p h aryn g o cle ith ra lis m uscles o rig in a te m usculously fro m th e late ro ve n tra l face
o f th e cleith ra and inse rt m usculously on th e p o ste rove n tra l face o f th e last
basibranchials and a n te ro ve n tra l face o f th e low e r pharyngeal to o th plates.
The pharyngeal to o th plate a d d u cto r m uscle connects th e posterodorsal face o f the
fo u rth ceratobranchia! bone to th e ve n tra l face o f th e fo u rth hypobranchial bone.
74
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
The tra n sve rsus v e n tra lis m uscle spans the m idline betw een th e a n te ro ve n tra l faces
o f th e fo u rth p a ir o f ceratobranchials.
The obliquus dorsalis m uscle interconnects the posterodorsal face o f th e fo u rth
epibranchial to th e anterodorsal face o f th e infra ph a ryn go b ra n chia l I.
The
ve n tra l
re tra c to r
m uscle
connects
th e
p o ste rove n tra l
face
o f th e
low er
pharyngeal to o th plate to th e d orsolateral face o f th e cle ith ru m .
The epaxial m uscles inse rt m usculously on th e supraoccipital, exoccipitals and
p te ro tics, epioccipitals. The hypaxial m uscles in se rt m usculously and te n d in o u sly on
th e exoccipitals and basioccipital.
5 .4 .4 . C ra n ia l m y o lo g y o f S y n a p h o b r a n c h u s b r e v id o r s a lis
The a d d u cto r m andibulae m uscle com plex is also com prised o f th e sections A2 and
A3. The section A2 is subdivided into a dorsal subsection A2ß and a ve n tra l
subsection A2a (Fig. 5.1 0 a ). The subsection A2ß o riginates m usculously fro m the
su praoccipital, p a rie ta l, p o s te rio r p a rt o f th e fro n ta l and a n te rio r p a rt o f the
p te ro tic. The subsection A2ß inserts te n d in o u sly on th e dorsal edge o f th e sh o rt
coronoid process and m usculously a t th e a n te rio r level o f th e long Meckelian fossa.
The lateral fib e rs o f A2a o rig in a te m usculously fro m th e p o ste rio r p a rt o f the
hyom andibula and anterodorsal face o f th e tu b e -lik e preopercle (Fig. 5.1 0 a ). They
inse rt m usculously a t th e p o s te rio r level o f th e Meckelian fossa, w hereas th e medial
fib e rs o rig in ate m usculously fro m th e p o ste rio r face o f th e suspensorial fossa th a t is
fo rm e d by th e a n te rio r parts o f th e hyom andibula and q u adrate. The m edial fib e rs
o f A2a are inserted m usculously on th e p o ste rove n tra l m argin o f th e Meckelian
fossa and posterodorsal face o f th e coronom eckelian bone. The section A3 is a
s trip -lik e m uscle th a t o rig in ate s m usculously fro m the a n te ro ve n tra l face o f the
sphenotic
process
(Fig.
5 .1 0 b ).
It
is
directed
c a u d o ve n tra lly
and
inserts
m usculously on th e p o ste rio r face o f th e coronom eckelian bone.
The a d d u cto r arcus palatini m uscle s ta rts a t th e level o f th e lateral expansion o f the
parasphenoid
w ith
fib e rs
directed
ca u do ve n tra lly.
This
m uscle
o riginates
m usculously fro m th e lateral face o f th e m idsection o f th e parasphenoid (Fig.
5 .1 0 a ). The a n te rio r fibers o f th e a d d u cto r arcus palatini inserts on th e p o ste rio r
p a rt o f th e p terygoid th a t is connected to th e anterodorsal end o f th e quadrate
75
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
process by th e p te ryg o id e o -q u a d ra te ligam ent. The p o ste rio r fib e rs o f th is m uscle
inse rt m usculously on th e anterodorsal edges o f th e a n te rio r process o f the
quadrate.
The a d d u cto r hyom andibulae m uscle o rig in ate s m usculously fro m th e p o ste rio r p a rt
o f th e sphenotic and ve n tro m e d ia l face o f th e p ro otic and inserts m uscoulously on
th e a n terom edial face o f th e hyom andibula.
The le va to r arcus palatini m uscle o rig in ate s both te n d in o u sly and m usculously fro m
th e la te ro ve n tra l and ve n tra l faces o f th e sphenotic process (Fig. 5 .1 0 b ). I t is
directed ca u d o ve n tra lly and inserts m usculously on th e a n te ro la te ra l faces o f the
hyom andibula and qu ad ra te (Fig. 5.1 0 b ).
The d ila ta to r operculi is a s trip -lik e m uscle th a t o rig in ate s m usculously fro m the
p o ste rove n tra l face o f th e sphenotic process and runs ca u d o ve n tra lly (Fig. 5.1 0 b ).
I t is connected to th e d ila ta to r operculi tendon a fte r e n te rin g th e p o s te rio r groove
o f th e hyom andibula and inserts on a lateral process o f th e opercle situated on its
a n te ro la te ra l face (Fig. 5.1 0 b ).
The le va to r operculi m uscle o rig in ate s m usculously fro m th e m edial face o f the
posterodorsal m argin o f th e hyom andibula and ve n tra l face o f th e p o s te rio r process
o f th e
p te ro tic.
It
is directed
ca u d o ve n tra lly and
inserts m usculously on the
laterodorsal face o f th e opercle (Fig. 5.10a).
The a d d u cto r operculi m uscle o rig in ate s m usculously fro m th e v e n tro p o s te rio r face
o f th e
exoccipital
and
v e n tro m e d ia l
face
o f th e
p te ro tic.
It
inserts
on
the
dorsom edial m argin o f th e opercle (Fig. 5 .1 0 b ).
The p ro tra c to r hyoidei o rig in ate s te n d in o u sly fro m th e m edial face o f th e d e nta ry,
a t th e rear o f th e dental sym physis (Fig. 5 .10c). The m edial fib e rs o f th e p ro tra c to r
hyoidei inse rt m usculously on th e anterodorsal face o f th e a n te rio r ce ratohyal,
w hereas
a
sm all
bundle
of
its
lateral
fibers
extends
caudally
and
inserts
m usculously on th e p o sterolateral face o f th e p o s te rio r ceratohyal (Fig. 5.10c).
The sternohyoideus is s im ila r to th a t o f I. b runneus but its le ft and rig h t halves
o rig in ate fro m th e v e n tro la te ra l faces o f th e cleith ra (Fig. 5.10c).
The hyohyoideus m uscle com plex is connected to its co u n te rp a rt a t its m edian
raphe to fo rm a th in sac-like sheet o f fib e rs th a t cover th e branchial cham ber. Its
fib e rs inte rcon n e ct th e successive branchiostega! rays and d orsally attach to the
76
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
ve n tra l rim o f th e epaxial fascia and th e horizontal septum betw een th e epaxial and
hypaxial muscles.
The le va to r e xte rn i m uscles o rig in a te
m usculously fro m
a p te ro tic depression
situated p o s te rio r to th e a n te rio r suspensorial a rtic u la to ry facet. P osteriorly these
m uscles are subdivided into fo u r bundles inserting on th e posterodorsal faces o f the
epibranchials I-IV .
The le v a to r inte rnu s m uscle o rig in ate s fro m th e p te ro tic depression, m edial to the
le va to r e xte rn i m uscles. This m uscle inserts on th e dorsal face o f th e upper
pharyngeal to o th plate.
The subpharyngealis runs on th e dorsal side o f th e ve n tra l parts o f th e gili arches,
including th e basibranchials I-IV , hypobranchials I - I I and anterodorsal faces o f the
ce ra to b ra n c h ia ^ III- IV . Both halves o f th is m uscle o rig in ate te n d in o u sly fro m the
b a sibranchialo-hypohyal lig a m e n t and in se rt on th e a n te rio r p a rt o f th e fo u rth
ceratobranchia!.
O rigin and insertion o f th e p h aryn g o cle ith ra lis, to o th plates a d d u cto r and ve n tra l
re tra c to r m uscles in S. bre vid o rsalis are s im ila r w ith those o f I. brunneus.
The
epaxial
m uscles
in se rt
m usculously
on
those
parts
o f th e
epioccipitals,
p te ro tics, exoccipitals and basioccipital th a t co n trib u te to fo rm the p o ste rio r wall of
th e neurocranium . The hypaxial m uscles inse rt te n d in o u sly on th e le ft and rig h t
sides o f th e o tic bullae fo rm e d by th e a n te ro ve n tra l p a rt o f th e basioccipital.
5 .5 . D iscussion
5 .5 .1 . V a ria tio n in c ra n ia l m o rp h o lo g y o f S y n a p h o b ra n c h id a e
D ive rsity in feeding habits can be considered as being reflected in those stru ctu ra l
elem ents associated w ith
fee d in g ,
in relation
to
d iffe re n t fu n ctio n al dem ands
(W a in w rig h t and Bellwood, 2002, Konow and S anford, 2 0 08 ). Ily o p h is brunneus,
th e m uddy a rro w to o th eel, feeds on annelids and crustaceans (S m ith e t a l., 1999;
Heem stra e t a l., 2006). S ynaphobranchus b re vid o rsalis, th e shortdorsal c u tth ro a t
eel, is assum ed to feed on decapods, am phipods, cephalopods and fishes, ju s t like
o th e r S ynaphobranchus species (H ouston
and
Haedrichi,
1986;
Saldanha
and
Bauchot, 1986). In co n tra s t to th is m ore generalised w ay o f feeding, S im enchelys
p a ra siticu s has been described as being parasitic o r a scavenger, burrow ing into th e
77
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
bodies o f o th e r fishes (B igelow and S chroeder, 1953; Castel, 1961; Robins and
Robins, 1989; Goode and Bean, 1896; Caira e t al., 1997). Hence, com parison o f
th e head m usculoskeletal m o rph o log y o f I. b runneus, S. b re vid o rsalis w ith th a t o f
S. p a rasiticu s, re p re se n ta tive s o f th e th re e subfam ilies o f S ynaphobranchidae th a t
show d iffe re n t feeding habits, m ay help to b e tte r understand th e nature o f the
m orphological
specializations o f th e feeding
apparatus
in S. p a rasiticus. This
provides an ind ire ct tool to te s t th e hypothesis th a t it w ould be specialized fo r this
p arasitic w ay o f feeding.
5 .5 .1 .1 . O s te o lo g y : The characters o f S. p a ra siticu s are a co m bination o f p rim itiv e
fe a tu re s and u niquely derived characters. S im enchelys p a rasiticu s resem bles the
syn a p h o b ra n ch u s in m any fe a tu re s o f its osteology, w ith som e exceptions th a t m ay
be related to an a d aptation to its feeding behavior.
The p reorbital region o f I. bru nn e u s is re la tiv e ly long, th a t o f S. b re vid o rsalis is
m o derate, w hereas S. p a rasiticu s bears a sh o rt snout. The p a la to p te ryg o id o f S.
pa ra siticu s is firm ly connected to th e Suspensorium (hyo m a n d ib u la and q u a d ra te )
and n e urocranium , w hereas o n ly a slender pterygoid is presents in I. b runneus and
S. b re vid o rsalis. The p te ryg oid o f I. b runneus and S. bre vid o rsalis is connected to
th e Suspensorium and neurocranium via a ligam ent.
The h yo m a n d ib u la -q u a d ra te axis is s lig h tly inclined p o ste rio rly in S. bre vid o rsalis,
unlike a ve rtica l one in I. brunnensis. This axis is inclined fo rw a rd in S. p a rasiticu s
and hence th e q u a d ra te -m a n d ib u la r a rticu la tio n is positioned a t th e level o f the
p o ste rio r
p a rt o f th e
o rb it.
A
p o ste rio r
position
o f th e
q u a d ra te -m a n d ib u la r
a rtic u la tio n , caudal to th e p o ste rio r end o f th e ne uro cra n iu m , is coupled to an
elongation o f th e low e r ja w , resulting in a large, n o n -circu la r m outh gape in I.
brunneus and S. b re vid o rsalis w ith slender jaw s. A phenom enon also observed in
o th e r lon g -jaw e d A n g u illifo rm e s (Eagderi and Adriaens, 2010 a, b). In co n tra st, S.
p a ra siticu s has s h o rt, deep and sto u t upper and low er jaw s.
The hypohyal and urohyal o f S. p a rasiticu s are co m p le te ly m odified com pared to
those in I. b runnensis and S. bre vid o rsalis. The urohyal o f S. p a rasiticu s is sh o rt
and large unlike th e long, slen d e r-like one o f I. b runnensis and S. brevidorsalis. The
urohyal o f th e S. p a ra siticu s provides a large insertion area fo r th e sternohyoideus
78
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
m uscle, and has tw o dorsal condyles th a t a rtic u la te w ith th e ve n tra l hypohyals,
w hereas
it a rticu la te s w ith
brevidorsalis.
The
dorsal
th e
and
a n te rio r ceratohyals
ve n tra l
hypohyals
in I.
o f S.
b runnensis and S.
p a ra siticu s
are
firm ly
connected to th e a n te rio r ceratohyals, w hereas only a sm all s h a ft-lik e hypohyal is
p resent in I. b runnensis and S. brevidorsalis.
E xternally S. p a rasiticu s d iffe rs fro m o th e r a n g u illifo rm species in having uniserial
cu ttin g edged te e th , a sm all te rm in a l n arrow m outh opening and a v e ry large
to n g u e -like s tru c tu re (Regan, 1912). The presence o f th e sm all, sim ple te e th on th e
m a xilla ry, d e n ta ry and v o m e r (v e ry num erous in th e firs t tw o ) in I. b runnensis and
S. bre vid o rsalis is a p rim itiv e ch a ra cte ristic o f th e Synaphobranchidae (Robins and
Robins, 1989). The c u ttin g
edge te e th o f th e
m a x illa ry and low er ja w
in S.
pa ra siticu s are uniserial and aligned w ith th e ir cu ttin g edges situated late ra lly,
fo rm in g a scissor-like stru c tu re . The ch ise l-like te e th on th e p re m a xillo -e th m o id a l
com plex, v o m e r, m a x illa ry and low e r ja w o f S. p a rasiticu s can be considered
beneficial when rem oving big chunks o f flesh fro m prey.
The m outh opening o f S. p a rasiticu s is covered by a m u ltila y e r epithelial tissue
s im ila r to a tra n s itio n a l e p ithe liu m th a t is specialised fo r dealing w ith extensive
stre tch in g (S w anson, 1996; Genten e t a l., 2 0 09 ). This m u ltila ye re d e p ithe liu m o f
th e oral mucosa shows th e presence o f num erous g o ble t cells (Fig. 5 .5 ). Also, the
derm is around its m outh opening is th ic k and bears a th ic k s tra tu m com pactum ,
consisting o f a dense connective tissue g iving th e skin s tre n g th and e la sticity
(Sw anson, 1996) (Fig. 5 .5 ).
Hence, th e a n te rio r tip o f th e bony snout in S.
p a ra siticu s is positioned som e distance aw ay fro m th e a n te rio r tip o f th e fleshy
sn o ut (Fig. 5.2c). The to n g u e -lik e s tru c tu re o f S. p a ra siticu s fills th e ve n tra l p a rt o f
th e buccal c a v ity and, considering its histological nature seems to be a secretory
organ w ith large se cre to ry cells organised in m any se cre to ry units (Fig. 5.5).
5 .5 .1 .2 .
M yolo gy: The cephalic m yology o f S. pa rasiticu s shows rem arkable
differences in both size and shape o f th e m uscles, com pared to th e condition in
Ily o p h is bru nn e u s and S ynaphobranchus bre vid o rsalis, p a rtic u la rly in th e m uscles of
th e ve n tra l surface o f th e head. Also, th e a d d u cto r m andibulae m uscle com plex o f
79
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
S. p a rasiticu s
is g re a tly
enlarged
com pared
to
th a t o f I.
bru nn e u s
and
S.
brevidorsalis.
Sim enchelys p a rasiticu s bears an enlarged le v a to r arcus palatini w ith an a n te rio r
and a p o s te rio r subsection, and w ith its origin extended a lm o st to th e p o ste rio r part
o f th e neurocranium . In I. b runneus and S. b re vid o rsalis, th e m uscle o rig in ate s only
fro m th e ve n tra l p a rt o f th e sphenotic process and is not subdivided. Also, S.
p a ra siticu s bears a large a d d u cto r arcus palatini m uscle and s m a lle r a d du ctor
hyom andibulae. A d is tin c t a d d u cto r hyom andibulae is absent in I. brunneus.
The muscles o f th e ve n tra l surface o f th e head in S. p a rasiticu s are large and show
m ore specializations com pared to those o f I. bru nn e u s and S. b revidorsalis. The
hyohyoideus infé rio n s
m uscle is a d iffe re n tia te d
p a rt in th e
hyoideus m uscle
com plex in S. p a rasiticu s, b u t not in I. b runneus and S. b re vid o rsalis. In a d ditio n ,
th e p ro tra c to r hyoidei and sternohyoideus o f S. p a rasiticu s are larg e r in com parison
to th e o th e r tw o species studied.
The le v a to r e xte rn us, le v a to r inte rnu s, subpharyngealis, p h aryn g o cle ith ra lis and
pharyngeal to o th plate a d d u cto r m uscles are gili arch m uscles present in all th re e
species and seem to be syn apom orphic in th e syn a p h o b ra n ch u s b u t shared w ith
o th e r A n g u illifo rm e s such as m uraenids. How ever, th e le v a to r e xte rn us, le va to r
inte rnu s, subpharyngealis and p h aryn g o cle ith ra lis m uscles are w ell-developed in S.
p a ra siticu s com pared to th e tw o o th e r species studied.
5 .5 .2 . C ra n ia l s p e c ia liz a tio n s in re la tio n to p a ra s itis m
Parasitism by m arine fishes is not a com m on s tra te g y , but it does occur in a
n u m be r o f d iffe re n t species (H utchins e t a l., 2003). S im enchelys p a ra siticu s has
been found burrow ed into the flesh o f various b o tto m -d w e llin g fishes, but has also
been recorded fro m th e h e art o f a m ako sh ark (Caira e t a l., 1997). The m odified
cephalic m usculoskeletal elem ents o f S. p a rasiticu s, com pared to those o f Ily o p h is
brunneus and S ynaphobranchus b re vid o rsalis, m ay re fle ct th e specialized w ay o f
feeding in th is pugnóse eel.
The sm all te rm in a l m outh opening o f S. p a ra siticu s surrounded by a th ic k and
stre tch a b le skin and its gape reaches p o ste rio r to th e n o strils, halfw ay o f its sh o rt
b lu n t snout. S im enchelys p a rasiticu s m ay utilize th is specialized te rm in a l m outh in
80
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
o rd e r to attach to its host, fo rm in g a seal w ith its lips. In co n tra st, I. bru nn e u s and
S. bre vid o rsalis bear a large, no ncircu la r m outh gape due to th e p o ste rio r position
o f th e q u a d ra te -m a n d ib u la r a rtic u la tio n . An aquatic p re d a to r w ith a large, non­
circu la r m outh gape as in m uraenids is able to m ove ja w s into a bitin g position
w ith o u t pushing p o tential prey aw ay fro m th e opened m o u th , and hence consum e
large preys (P o rte r and M otta, 2 0 04 ; Mehta and W a in w rig h t, 2007b, 2008, 2009).
The cu ttin g edge and b la de-like te e th o f S. p a rasiticu s on th e p re m a xillo -e th m o id a l
com plex, upper and low er ja w s , along w ith th e enlarged a d d u cto r m andibulae
m uscle com plex can be em ployed to shear and rem ove a chunk o f flesh fro m its
prey, ju s t like scissors. The bitin g m echanism o f S. p a ra siticu s m ay show some
s im ila ritie s w ith th a t o f th e c o o k ie -c u tte r shark, Is is tiu s brasiliensis. This small
sh ark attaches to th e prey by fo rm in g a seal w ith its fle sh y lips. The upper ja w o f I.
brasiliensis is reduced in size and is com posed o f tw o pieces: an a n te rio r section
th a t can p ivo t d orsally, and a p o s te rio r section. Presum ably, its upper ja w pivots a t
th is ju n c tio n when th e sh a rk is attached to its prey w ith its upper ja w , allow ing the
sh ark to p ivo t do rsally about th is jo in t and sink its low er ja w te e th into th e prey
(Jones, 1971; LeBoeuf e t a l., 1987; Shirai and Nakaya, 1992).
The
tig h t
connection
o f th e
large
p a la to p te ryg o id
o f S.
p a ra siticu s
to
th e
Suspensorium and neurocranium m ay be linked to its a b ility fo r a pow erful bite.
Grubich e t al. (2 0 0 8 ) pointed o u t th a t a large pala to q u a dra te can fu n ctio n as a
shock absorber to p ro te ct th e eye o rb it fro m high im pact forces d u ring th e strike
and subsequent bites in the great barracuda.
The s to u t m outh closing ap pa ra tu s, as observed in th e ja w s in S. p a rasiticu s m ay
re fle ct th e presence o f large m echanical loads fro m m uscle forces du rin g biting
(D uellm an and T rueb, 1986; H ildebrand, 1995, S um m ers e t a l., 1998; Devaere et
a l., 2 0 0 1 ), which can be expected to be large considering th e h yp ertrop h ied ja w
a d d u cto r muscles. Enlarged a d d u cto r m andibulae m uscles o f S. pa rasiticu s w ith a
p e rpendicular insertion o f th e tendon A2ß and th e fib e rs o f A3 o nto th e low er ja w ,
suggest an a d aptation to pow erful bitin g due to an e ffic ie n t force tra n s fe r during
m outh closure (D evaere e t a l., 2 0 01 ; Herrei e t a l., 2 0 02 ). Also, th e insertion
surface o f th e a d d u cto r m andibulae m uscles is along tw o th ird s o f th e length o f the
low er ja w in S. p a rasiticus. This, to g e th e r w ith th e sh o rt ja w s , im plies a bigger
81
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
m echanical
advantage
(la rg e r in p u t/o u tp u t
lever ra tio ),
b u t a reduced
biting
v e lo city, all w hich are linked to a large b itin g force. In co n tra st, I. bru nn e u s and S.
b re vid o rsalis bear long ja w s w ith th e length equal o r longer than th e neurocranium ,
which
indicates th a t these
predators
re ly on a h ig h -v e lo c ity ja w
closure fo r
ca p tu rin g prey (N orton and Brainerd, 1993; Ferry-G raham e t a l., 2001b, 2001c;
Porter and M otta, 2004; K am m erer e t a l., 2005; De Schepper e t a l., 2 0 08 ; Eagderi
and Adriaens, 2010a). Also, th e a d d u cto r m andibulae m uscles o f S. p a ra siticu s are
attached to th e epaxial m uscles. The coupling betw een th e ja w m uscles and the
epaxial m uscles could be considered an advantage fo r tra n s fe rrin g forces fro m th e
body o nto th e head during feeding
(Liem and Osse, 1975; C aroli, 2004;
De
Schepper e t a l., 2005).
The large p ro tra c to r hyoidei and ste rnohyoideus o f S. pa ra siticu s suggests th e
a b ility to v e n tra lly expand th e buccal c a v ity and produce suction forces (Lauder,
1985; De Visser and Barel, 1998; C arroll, 2 0 04 ; Sanford and W a in w rig h t, 2002;
Mehta and W a in w rig h t, 2 0 07 b ; Konow and S anford, 2 0 08 ). Also, S. p a rasiticu s
bears a h e avily ossified u ro hya l-cera toh ya l system to su p p o rt these tw o large
muscles. We speculate th a t these specializations o f S. p a rasiticu s m ay be beneficial
fo r creating h ig h e r suction force to attach to its prey, th e re b y assisted using its
fle sh y lips.
The bony elem ents o f th e branchial arches in th e th re e studied syn a p h o b ra n ch u s
do not show an e xtre m e reduction like those o f m uraenids do but th e y bear m any
sim ila r corresponding m usculature a tta ch m e n ts to those o f th e m uraenids th a t
enable them to tra n s p o rt re la tiv e ly large prey into th e esophagous using th e ir
pharyngeal ja w s (M ehta and W a inw righ t, 2007a). In these species, th e le va to r
e x te rn i, le v a to r in te rn i, subpharyngealis, pharyngeal to o th
plate a d d u cto r and
p h aryn g o cle ith ra lis m uscles o f th e syn a p h o b ra n ch u s could play a role in p ro tra ctin g
and re tra ctin g th e branchial arches fo r tra n s fe rrin g food in th e buccal ca vity. The
le va to r e xte rn i and le v a to r inte rni m uscles could then lift th e dorsal parts o f the
branchial arches and s h ift them fo rw a rd a t th e sam e tim e (Vandew alle e t a l., 2000;
Mehta
and
W a in w rig h t,
2007a).
The
subpharyngealis
and
p ro tra c to r
hyoidei
m uscles can then pull th e ve n tra l parts o f th e branchial arches fo rw a rd . The
pharyngeal to o th plate a d d u cto r m uscles could then bring th e low er and upper
82
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
to o th plates to g e th e r to grasp th e food item s. The p h aryn g o cle ith ra lis m uscles and
extended stern o hyo id eu s m uscle m ay then draw th e branchial arches back and
dow nw ard to its resting position (Vandew alle e t a l., 2000; Mehta and W a in w rig h t,
2007a). I t is suggested th a t th is syn a po m o rp hic fe a tu re o f S yn a p h o b ra n ch u s i.e.
th e p otential fo r m echanical tra n s p o rt system , w ould be still advantagous fo r
specialised w ay o f feeding in S. pa ra siticu s
to tra n s p o rt chunks o f rem oved flesh
fro m a prey into th e esophagus, w hile it is attached to it. A fte r having b itte n o f a
chunk o f flesh and d u ring m a n ip u la tio n o f food in th e buccal c a vity, th e food m ay
be co n tinm a te d w ith th e secretions o f th e large to n g u e -lik e s tru c tu re , before being
tra n sfe rre d into th e esophagous.
In
a d d itio n ,
Bigelow and S chroeder (1 9 5 3 )
pointed
o u t th a t th e
body o f S.
pa ra siticu s is covered by a sheet o f m ucus when draw n o u t o f th e w ater. Such a
slim y body o f S. p a ra siticu s m ay be advantageous d u ring excavating a path into the
body o f th e prey.
The cephalic m usculoskeletal system o f th e pugnóse eel, S. p a rasiticu s, a t least
shows th a t it has th e s tru c tu ra l m o d ifications needed to rem ove chunks o f flesh
fro m a food item and excavating into it. In th is process, S. p a rasiticu s can use its
stre tch a b le skin around a sm all te rm in a l m outh opening, cu ttin g edge te e th , sh o rt
and sto u t ja w s and associated m uscles, and tra n s fe rrin g th e rem oved flesh into th e
esophagus using branchial arches, w hile being attached to its prey. H ow ever, th is
does not rule o u t any o f th e tw o stra te g ie s, w h e th e r it is a scavenger o r a tru e
p arasitic eel.
A CK N O W LE DG M ENTS
The a u th o rs w ould
like to th a n ks M. M c G ro u th e r (A ustralian
M useum ), R.H
Robins and J.A Lopez (Florida Museum o f Natural H istory) and D. Johnson
(N ational Museum o f Natural H istory-S m ith so n ia n In s titu tio n ) fo r providing m useum
specim ens, N. D e S c h e p p e r (G hent U n ive rsity) fo r her assistance and D.G. S m ith
(S m ith so nia n , USA) fo r his valuable com m ents.
83
5 C e p Iia Líc S pecía Lízatíon ¡ n a P arasítíc E eL
84
ChApTER 6
C E p lfA lic SpECÍAlizATÍONS ¡N R e U t ÍON TO
a SeconcI S e t o f Jaws ¡ n M u ra e n k Is
6
C e p ^ a I í c M o R p h o lo q y o f M u r a e n íc Is
C hapter six
C ep h alic S p e c ia liz a tio n s in R e la tio n to a Second S e t o f Ja w s in M u ra e n id s
6 .1 . A b s tra c t
The Muraenidae, one of the largest clades within the anguilliform fishes, exhibit an
innovative feeding mechanism that allows them to transport large prey items from the oral
jaw all the way back towards the esophagus using the pharyngeal jaws (Mehta and
Wainwright, 2007a). The current study was conducted to show the degree to what trade­
offs in muraenids may have arisen in the oral feeding apparatus, in relation to this
pharyngeal transport system. Hence, the head musculoskeletal features of Anarchias
allardicei
(Uropterygiinae:
Muraenidae)
and
Gymnothorax
prasinus
(Muraeninae:
Muraenidae) were compared with that of a closely-related outgroup with a hydraulic-based
prey transport, Ariosoma gilberti (Bathymyrinae: Congridae) and a detailed description of
their cranial osteology and myology is provided. The results showed that this innovative
feeding mechanism may be linked to many cephalic modifications such as, the stout and
robust neurocranial elements, an elongated lower jaw as the result of the posterior position
of the quadrato-mandibular articulation, enlarged teeth of oral jaws and premaxilloethmovomeral complex, reduction in the movable cranial bones and their muscular
connections,
hypertrophied
adductor
mandibulae
muscle
complex,
presence
of the
quadrato-maxillary and preoperculo-angular ligaments, connection of the quadrate to the
A2 tendon of the adductor mandibulae complex, caudoventral orientation of the fibers of the
large A3 section of the adductor mandibulae complex.
6 .2 . In tro d u c tio n
The eels o f th e A nguilloidei are a su b ord e r com prising fifte e n fa m ilie s, th e re b y
fo rm in g th e richest su b ord e r w ith in th e Elopom orpha. The M uraenidae, one o f the
largest clades w ith in th e anguilliform is and known as m orays, include a b ou t 200
species w ith in m ore than fifte e n genera (Böhlke e t a l., 1989; Nelson, 2006). Two
m o n op h yletic
subgroups
are
recognized,
i.e.
U ropterygiinae
and
M uraeninae
(O b e rm ille r and Pfeiler, 2003; Wang e t a l., 2003; Lopez e t a l., 2 0 07 ). Typically
m orays are s h a llo w -w a te r re e f and cre vice -d w ellin g eels. They are carnivores and
85
6
C e p ^ a I í c M o R p h o lo q y o f M u rae im íc Is
th e ir abundance and biom ass w ith in shallow w a te r reef in general is much g re a te r
than casually perceived (B öhlke e t al.,
1989; Santos and Castro, 2 0 03 ). The
m uraenids
m echanism ,
bear an
e v o lu tio n a ry success.
inn o va tive
feeding
Using th e ir pharyngeal ja w s ,
w hich
m ay
explain
th e ir
m uraenids are capable to
tra n s p o rt large captured prey item s fro m th e oral ja w all th e w ay back to w a rds th e
esophagus (M ehta and W a in w rig h t, 2007a) (Fig. 6 .1 ).
In co n tra s t to th e m orays, m ost ra y-fin n e d fishes use a suction-induced flo w o f
w a te r to m ove prey fro m th e oral ja w s to th e pharyngeal ja w s (G illis and Lauder,
1995;
Mehta and W a in w rig h t,
2007a,
2008). Therefore, th e
specialized m echanical tra n s p o rt system
presence o f th e
in m orays provides an o p p o rtu n ity to
b e tte r understand m orphological changes on th e head m usculoskeletal system in
relation
to
a
novel
feeding
behavior and
th is
w ith in
a
proper
phylogenetic
fra m e w o rk. Hence, by com paring th e cephalic m orph o log y o f rep re se n ta tive s o f
both
lineage
w ith in
m orays,
u ro p te ryg iin e s
re p re se n ta tive o f a close ly-re la te d
a n g u illifo rm
and
m uraenines,
fa m ily th a t still
as
well
as
possesses the
plesiom orphic hydraulic-based prey tra n s p o rt syste m , th e cephalic m orphological
changes in relation to th is specialization m ay be b e tte r understood.
This stu d y was aim ed to b e tte r understand th e m orphological changes o f th e head
th a t have occurred during e vo lu tio n , associated w ith th e m echanical tra n s p o rt
system in m oray eels. Hence, we provide a detailed description o f th e cranial
m yology
and
osteology
o f A narchias
a lla rd ice i
(U ro p te ryg iin a e :
M uraenidae),
G ym n o th o ra x pra sin u s (M uraeninae: M uraenidae) and re p re se n ta tive o f a closelyrelated a n g u illifo rm fa m ily w ith a hydraulic based prey tra n s p o rt, A riosom a g ilb e rti
(B a th ym yrin a e : C ongridae) and com pare th e ir head m usculoskeletal fe a tu re s to
reveal th e im plicatio n s o f th e m echanical tra n s p o rt system on th e head m orphology
o f m orays. The choice fo r th is o u tg ro u p is based on th e single m ost parsim onious
tre e o f elopom orph fishes, using th e com bined data o f m ito ch on d ria l 12S ribosom al
RNA sequences, which su pports th e m o n op h yly o f th e clade com prising M uraenidae
and B a th ym yrina e (C ongridae) (O b e rm ille r and Pfeiler, 2003).
86
6
C e p ^ a I íc M o R p h o lo q y o f M uraeimíc I s
6 .3 . M a te ria l and m e th o d s
For th e anatom ical d e scrip tio n , fo u r alcohol-preserved specim ens o f G ym n o th o ra x
pra sin u s (1 .2 8 736-024 and 1 .2 0 0 95 -0 3 1), e ig h t specim ens o f A narchias a lla rd ice i
(1.17102-063 and UF 31 80 4 4 ) and sixteen specim ens o f A riosom a g ilb e rti (UF
230612 and UF 10803) obtained fro m th e A ustralian Museum and Florida Museum
o f Natural H istory w ere exam ined. The specim ens w ere o f fo llo w ing size in Total
Length, (TL) G. pra sin u s (GP)1: TL: 437 m m ; GP2: TL: 385.5 m m ; GP3: TL:
4 9 7 m m ; GP4: TL: 4 4 7 .2 ; A. a lla rd ice i (A A )1: TL: 99 m m ; AA2: TL: 101 m m ; AA3:
TL: 108 m m ; AA4: TL: 107 m m ; AA5: TL: 110 m m ; AA6: TL: 146 m m ; AA7: TL:
129 m m ; AA8: TL: 136 m m ; A. g ilb e rti (AG )1: TL: 133 m m ; AG2: TL: 182 m m ;
AG3: TL: 134 m m ; AG4: TL: 143 m m ; AG5: TL: 162 m m ;, AG6: TL: 149 m m ; AG7:
TL: 132 m m ; AG8: TL: 152 m m ; AG9: TL: 132 m m ; TL: 145.5 m m ; AG IO : TL:
156.5 m m ; AG11: TL: 129 m m ; AG12: TL: 198 m m ; AG13: TL: 157 m m ; AG14:
TL: 151 m m ; AG15: TL: 123.5 m m ; AG16: TL: 133 m m . One specim ens o f each
species (GP2, AA1 and AG2) was cleared and stained w ith A lizarin red S and Alcian
blue according to th e protocol o f Hanken and W assersug (1 9 8 1 ) fo r osteological
e xa m inations. Dissections w ith m uscle fib e r staining according to Bock and Shear
(1 9 7 2 ) w ere p e rform ed.
Specim ens w ere studied using a stereoscopic m icroscope
(O lym pus S ZX-7) equipped w ith a cam era lucida.
The m usculature te rm in o lo g y follow s W interbottom i (1 9 7 4 ), De Schepper e t al.
(2 0 0 5 ) and Mehta and W a in w rig h t (2 0 0 7 a ). The circu m o rb ita l bones o f th e cephalic
lateral line system fo llo w A driaens e t al. (1 9 9 7 ). T e rm ino lo gy o f cranial skeletal
elem ents follow s Nelson (1 9 6 6 ), Böhlke (1 9 89 c) and Rojo (1 9 9 1 ). The e p io tic o f
teleosts
is
te rm e d
"ep io ccip ita l",
th e re b y
fo llo w ing
Patterson
(1 9 7 5 ).
The
te rm in o lo g y o f scarf jo in t follow s H ildebrand (1 9 9 5 ).
6 .4 . R esu lts
6 .4 .1 . C ra n ia l o s te o lo g y : A r io s o m a g il b e r t i (B a th y m y rin a e : C o n g rid a e )
The neurocranium
fo rm s one u n it, ta p e rin g fro m
the o tic region to w a rds th e
a n te rio r end o f th e fro n ta l bone and then co n tinu in g as a narrow bar to w a rds the
s p a tu la te -lik e sn o ut (Fig. 6 .2 a ). The eth m o id region is com prised o f th e fused
p re m a xilla ries,
eth m o id
and
vom eral
bones,
87
as th e
p re m a xillo -e th m o vo m e ra l
6
C e p ^ a I íc M o R p h o lo q y o f M uraeimíc I s
com plex, as well as th e nasals. The nasal bone is described w ith respect to the
lateral line system (see below ). The p re m a xillo -e th m o vo m e ra l com plex bears a
lateral process, which is directed a n te ro v e n tra lly w ith a sm all horizontal process a t
its end (Figs. 6.2 and 6.3a) and th e o lfa c to ry ro sette is located a n te rio r to th is
process.
The
a n te ro ve n tra l
face
o f th e
p re m a xillo -e th m o vo m e ra l
com plex
is
dentig e ro us w ith a n te rio r, longer and recurved ca niniform te e th (Fig. 6 .2 b ).
The o rb ita l region com prises th e tw o sm all lacrim al bones, fo u r in fra o rb ita l bones,
fro n ta l bones, parasphenoid, basisphenoids and pterosphenoids. Posteriorly, the
fro n ta l bones are connected w ith th e parietal bones by an e xtensive scarf jo in t (Fig.
6 .2 a ). Also, le ft and rig h t fro n ta l bones show a m in o r scarf jo in t (Fig. 6 .2 a ). The
v e n tro p o s te rio r rim o f th e fro n ta l bone encloses th e a n te rio r portion o f th e te m p o ral
canal, w hich enters th is bony canal a t th e connection betw een th e fro n ta l and
pterosphenoid (Fig. 6 .3 a ). The fro n ta l fo rm s th e posterodorsal wall o f th e large
o rb it, and th e foram en opticum lies betw een th e ve n tra l portions o f th e fro n ta l
bones. A n te rio rly , th e fro n ta l bears a sm all lateral process o ve r th e o rb it w ith a
pore on its p o s te rio r part. The basisphenoid fo rm s th e p o ste rove n tra l wall o f the
o rb it and bears a sm all fossa on its a n te ro ve n tra l face. The dorsal p a rt o f th is bone
runs into th e o p tic foram en and overlaps v e n tra lly w ith th e parasphenoid. The
pterosphenoid is surrounded by th e fro n ta l, basisphenoid, parasphenoid, sphenotic
and p rootic bones. The pterosphenoid possesses a pore on its lateral face (Fig.
6 .3 a ). The parasphenoid is bifurcated a t its tw o ends and fo rm s th e ve n tra l ele m e n t
o f th e o rb it. A t th e m id p o in t, th e parasphenoid bone bears d is tin c t a la r processes as
well as a ve n tra l keel (Fig. 6 .2 b ).
The o tic region is com prised o f th e sphenotics, p te ro tic, prootics, parietals and
epioccipitals. The sphenotic is connected to th e p rootic bone by a bony s tru t o f the
prootic. The sphenotic c o n trib u te s to fo rm th e a n te rio r suspensorial a rtic u la to ry
fa ce t, to g e th e r w ith th e p rootic bone (Figs. 6.2b and 6 .3 a ). The sphenotic bone
bears
a
lateral
process
d ire ctin g
v e rtic a lly .
The
p te ro tic
bone
braces
the
n eurocranium la te ra lly and encloses th e p o ste rio r portion o f th e te m p o ral canal,
which opens a t th e posterodorsal face o f th e p te ro tic (Figs. 6 .4 a ). P osteriorly, this
bone connects to th e exoccipital bone and c o n trib u te s to fo rm th e p o ste rio r wall o f
th e neurocranium . The p o ste rio r a rtic u la to ry fa ce t fo r th e hyom andibula is form ed
88
6
C e p ^ a I íc M o R p h o lo q y o f M uraeimíc I s
by th e p te ro tic bone (Fig. 6 .2 b ). The large p ro otic fo rm s th e a n te rio r p a rt o f th e otic
bullae, w ith th e fo ra m e n trig e m in o -fa c ia lis a t the a n te rio r edge o f th e bulla and tw o
pores a n te rio r to th is foram en (Fig. 6 .2 b ). The p ro otic possesses a long dorsal
p ro je ctio n on its anterodorsal co rn er th a t runs under th e p o s te rio r p o rtion o f the
fro n ta l. The a n te rio r p a rt o f th e parietal is covered by th e fro n ta l bone fo rm in g a
re la tive ly extended scarf jo in t.
The
occipital
region
consists
of
th e
exoccipital
and
basioccipital
bones.
A
surpraoccipital is absent. Both exoccipital bones are interconnected posterodorsally.
The exoccipital bones v e n tra lly fo rm a depression on th e poste rove ntra I face o f the
n eurocranium (Fig. 6 .2 b ). The foram en m agnum is bordered d o rsally and la te ra lly
by
th e
exoccipitals
and
v e n tra lly
by
th e
condyle
of
th e
basioccipital.
The
basioccipital fo rm s th e p o ste rio r p o rtion o f th e large o tic bullae and wedges into the
long p o ste rio r incisure o f th e parasphenoid.
The low er ja w v e n tra lly fo rm s a long groove, enclosed deep internal wall and
sh o rte r e xte rn al
w all,
which
supports
th e
a n te rio r
p a rt
o f th e
preoperculo-
m a n d ib u la r canal (Figs. 6.3a and 6 .4 a ). The a n te rio r portion o f th e low er ja w
represents th e d e nto -sp le n o -m e n to m e cke lia n com plex, here referred to as the
d e n ta ry com plex. The d e n ta ry com plex poste rod o rsa lly bears th e coronoid process
w ith a sm all coronom eckelian bone ve n tra l to th e process and bearing an apophysis
on its m edial face (Fig. 6 .5 b ). The a n te rio r portion o f th e coronom eckelian is
enclosed by th e d e n ta ry com plex. A sm all Meckelian fossa is present a t th e rear o f
th e coronom eckelian (Fig. 6 .5 b ). A n te rio rly , th e d e n ta ry te e th are arranged in th re e
rows and p o ste rio rly in tw o rows o f te e th w ith th e ir tip s p o inting m edially. The
a n gu la r com plex consists o f th e fused a n gu la r and a rtic u la r bones, bearing a sm all
re tro a rtic u la r process (Fig. 6 .5 b ). This com plex wedges into th e d e n ta ry com plex.
The re tro a rtic u la r process is directed caudally and bears a pore. The opening o f a
canal is present a n te rio r to th e re tro a rtic u la r process and a n te rio rly th is canal opens
into th e p o s te rio r p a rt o f th e Meckelian fossa (Fig. 6 .5 b ). Also, th e re is a sm all pore
on th e medial face o f th is canal. The a n gu la r com plex bears th e caudodorsally
directed m a n d ib u la r a rtic u la r facet. In th e upper ja w , th e m a xilla ry bone is attached
a n te ro m e d ia lly to th e p re m a xillo -e th m o vo m e ra l com plex via an ascending a rtic u la r
process th a t is situ a te d a t th e rear o f its a n te rio r end (Figs. 6.3a and 6.5a).
89
6
C e p ^ a I íc M o R p h o lo q y o f M uraeimíc I s
A n te rio rly , th e m a x illa ry bone bears a patch o f pointed te e th and p o ste rio rly a
double row o f curved and pointed ones w ith a few p o ste rio r te e th th a t are arranged
in a single row. The p o ste rio r end o f th e m a x illa ry bone descends v e n tra lly and is
connected to th e a n gu la r com plex via th e p rim o rd ia l ligam ent.
The Suspensorium
is com prised
o f fo u r
bones:
th e
h yo m andibula,
q u adrate,
p a la to p te ryg o id and preopercle. The preopercle is described as p a rt o f th e o p ercu la r
series (see below ). The Suspensorium is longer than deep and bears an a n te rio r
fossa th a t is form ed by th e a n te rio r portions o f th e hyom andibula and quadrate
(Fig. 6 .3 b ). The p a la to p te ryg o id a n te rio rly connects to th e a n te rio r p a rt o f the
parasphenoid (Fig. 6 .3 a ). There is a large synchondrosis a t th e connection o f the
p a la to p te ryg o id to th e Suspensorium . The hyom andibula is firm ly connected to the
quadrate w ith an in te rd ig ita te d suture. The axis o f th e h yo m an d ibu la -qu a d rate
inclines fo rw a rd ly ,
placing
th e
q u a d ra te -m a n d ib u la r jo in t a t th e
level
o f the
p o ste rio r p a rt o f th e o rb it (Fig. 6 .3 a ). The hyom andibula bears th re e a rtic u la r
condyles: an a n te rio r one a rtic u la tin g w ith th e sphenotic and p ro o tic; a p o ste rio r
one a rticu la tin g
w ith th e
p te ro tic ;
and the o percular condyle situ a te d a t th e
posterodorsal m argin o f th e h yo m a n d ib u la r bone (Fig. 6 .3 b ). A d is tin c t sym plectic
was not observed.
The o p ercu la r series consists o f fo u r bones: th e preopercle, inte rop e rcle , subopercle
and opercle (Fig. 6 .6 a ). The distal m argins o f th e o p ercu la r and subopercle bones
w ere
lig h tly
stained
in th e
specim en
studied.
The v e n tro m e d ia l
face
o f the
preopercle is connected to th e poste rove ntra I rim o f th e Suspensorium . The e n tire
a n te ro la te ra l face o f th e preopercle fo rm s a tu b u la r s tru c tu re th a t encloses th e
p o ste rio r p ortion o f th e p re o p e rcu la r-m a n d ib u la r canal (Figs. 6.4a and 6 .6 a ). The
p o ste rio r rim o f th e preopercle covers th e a n te rio r m argin o f th e interopercle. The
ve n tra l face o f th e interopercle curves m e d ia lly and its anterom edial edge is
connected to th e a n g u la r bony com plex by th e in te ro p e rc u lo -a n g u la r ligam ent. The
subopercle lies curved against th e e n tire p o ste rio r m argin o f th e opercle. The fa n ­
shaped opercle a rticu la te s th ro u g h its rostral process to th e h yo m an d ibu la r bone.
Two ridges are present on th e lateral face o f th e opercle, a n te rio rly fo rm in g an
apophysis a t the a n te ro la te ra l face o f th e o p ercu la r ro stru m .
90
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
The hyoid com plex is com prised o f th e unpaired basihyal and u ro hya l, paired
a n te rio r and p o s te rio r ceratohyals (Fig. 6 .6 b ). The ro d -like basihyal bone bears a
ve n tra l crest th a t is connected to th e lateral face o f th e a n te rio r ceratohyal bone by
th e b a sih yalo-ceratohyal lig a m e nt. A n te rio rly , th e urohyal bone bears a deep and
th ic k portion w ith a cross-like ridge on its dorsal face th a t fo rm s th e le ft and rig h t
ceatohyal a rtic u la r facets. P osteriorly, th e urohyal fo rm s a brace-like p a rt th a t bears
tw o long processes (Fig. 6 .6 b ). The a n te rio r ceratohyal is firm ly connected to the
p o ste rio r one. The a n te rio r ceratohyal v e n tro m e d ia lly bears th e urohyal a rtic u la r
condyle and d o rsom e d ia lly th e basihyal a rtic u la r condyle. The p o ste rio r p a rt o f the
po ste rio r ceratohyal curves do rsally and is connected to th e poste rove ntra I co rn er
o f th e a n gu la r com plex by th e ce ra to h ya lo -a n g u la r ligam ent. Four o f th e eleven
branchiostega! rays are connected to th e a n te rio r ce ra to hya l, th e o thers to the
p o ste rio r ceratohyal. The branchiostega! rays curve d o rsally along th e ve n tra l
bo rde r o f th e inte rop e rcle and reach up to th e caudal b o rde r o f th e subopercle.
The cephalic lateral line system
is com prised o f th e su p ra o rb ita l, in fra o rb ita l,
te m p o ral and p re o p e rcu lo -m a n d ib u la r canals, and su p ratem p o ra l com m issure.
The
eth m o id canal, adnasal canal and fro n ta l com m issure w ere not observed. The
su p rao rb ita l canal extends o ve r the o lfa c to ry rosette to th e p o sto rbita l region and
possesses a single e xte rn al pore. The a n te rio r openings o f th e le ft and rig h t
su p rao rb ita l canals a b u t (Fig. 6 .4 a ). The nasal bone is a re cta n g u la r bone w ith a
ve n tra l process a t its m id p o in t (Fig. 6 .4 b ). D orsally, it bears a tu b u la r s tru c tu re th a t
supports th e a n te rio r portion o f th e su p rao rb ita l canal (Fig. 6 .4 b ).
This bone was
also s lig h tly stained. The in fra o rb ita l canal sta rts a t th e rear o f th e sn o ut tip . This
canal extends
p o ste rio rly and curves d o rsally
into th e
p o sto rbita l
region and
anastom oses w ith th e su p rao rb ita l canal in fro n t o f th e entrance o f th e te m p o ral
canal into th e skull (Fig. 6 .4 a ). Two lacrim al bones su p p o rt th e a n te rio r p a rt o f the
in fra o rb ita l canal and its p o ste rio r p a rt is enclosed by fo u r in fra o rb ita l bones before
anastom osing w ith th e su p rao rb ita l canal (Fig.
6 .4 b ). The in fra o rb ita l canal bears
five e xte rn al pores. The te m p o ra l canal runs inside th e fro n ta l and p te ro tic bones.
The p re o p e rcu lo -m a n d ib u la r canal s ta rts fro m th e tip o f th e d e n ta ry com plex and
runs in th e ve n tra l groove o f th e m andíbula. This canal continues into th e tu b u la r
91
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
p a rt o f th e preopercle and anastom oses w ith th e p o ste rio r end o f th e te m p o ral
canal (Fig. 6 .4 a ). The p re o p e rcu lo -m a n d ib u la r canal bears nine e xte rn al pores.
A lm ost all ve n tra l elem ents o f th e branchial arches are present (Fig. 6 .7 ): Four
basibranchia! bones (Bb I- V I) , tw o pairs o f hypobranchial bones (Hb I - I I ) (th e th ird
p a ir is sm a lle r and unossified), five pairs o f ceratobranchia! bones (Cb I-V ) (fifth
p a ir is reduced, located v e n tra lly to th e p h aryn g o cle ith ra lis m uscle), and one p a ir o f
low er pharyngeal to o th plates (LP). The dorsal elem ents o f th e gili arches present
are:
Four
pairs
of
epibranchial
bones
(Eb
I- IV ) ,
tw o
pairs
of
the
infra ph a ryn go b ra n chia l bones and one p a ir o f th e upper pharyngeal to o th plates
(UP) (Fig. 6 .7 ). The upper and low er to o th
plates bear sm all te e th , pointing
caudally.
6 .4 .2 . C ra n ia l M yolo gy: A r is o m a g i l b e r t i
The a d d u cto r m andibulae m uscle com plex com prises th e sections A2 and A3. The
section A2 can be subdivided into th re e subsections: A2a, A2ß a n te rio r (A2ßa) and
A2ß p o ste rio r (A2ßp) (Fig. 6 .8 a ). The lateral fib e rs o f th e subsection A2ßa o rig in ate
m usculously fro m
th e epioccipital, p te ro tic , parietal and p o ste rio r p a rt o f the
fro n ta l, its m edial fib e rs o rig in a tin g m usculously fro m th e a n te rio r p a rt o f the
sphenotic process. This subsection inserts as a tendon o nto th e anterom edial face
o f th e coronoid process. The posterodorsal fib e rs o f A2ßp are attached to th e ir
co u n te rp a rt and fa scia lly to th e epaxial, and o rig in ate
m usculously fro m
the
e pioccipital, p te ro tic and parietal. The lateral fib e rs, to g e th e r w ith th e lateral fibers
o f th e subsection A2a, are connected to th e tendon A2 th a t inserts on the
posterom edial face o f th e coronoid process. The m edial fib e rs o f A2ßp also inse rt
m usculously on th e posterom edial edge o f th e coronoid process. The lateral fibers
o f th e A2a o rig in a te m usculously fro m th e preopercle, hyom andibula and quadrate
bones. Its m edial fib e rs o rig in a te m usculously fro m th e la te ro p o s te rio r face o f the
hyom andibula and th e v e n tro p o s te rio r edge o f th e suspensoria! fossa. They insert
m usculously on th e posterom edial face o f th e m andíbula fro m th e Meckelian fossa
to th e a n te rio r edge o f th e re tro a rtic u la r process.
The section
pterosphenoid
A3 o rig in ate s
and
a n te rio r
m usculously fro m
p a rt
of
th e
92
th e
prootic,
ve n tra l
and
p a rt o f th e fro n ta l,
te n d in o u sly
fro m
the
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
a n te ro ve n tra l face o f th e sphenotic process (Fig. 6 .8 b ). The a n te rio r fibers o f th is
m uscle inse rt te n d in o u sly on th e ve n tro m e d ia l face o f th e coronoid process, a t the
rear o f th e insertion p o in t o f th e tendon A2ß. Its p o ste rio r fib e rs in se rt o nto the
dorsal face o f th e Meckelian fossa.
The a d d u cto r arcus palatini is a th in m uscle th a t o rig in ate s m usculously fro m the
ve n tra l keel o f th e parasphenoid (Fig. 6 .8 b ). This m uscle inserts m usculously on the
laterodorsal face o f th e p a la to p te ryg o id and a n terom edial face o f th e hyom andibula.
Its
p o ste rio r
fib e rs
m erge
w ith
th e
anterom edial
fibers
of
th e
a d du ctor
hyom andibulae.
The a d d u cto r hyom andibulae is distinguished fro m th e a d d u cto r arcus palatini due
to its th ic k e r d ia m e te r. This m uscle o rig in ate s m usculously fro m th e a n te rio r p a rt o f
th e basioccipital, p te ro tic and p rootic and inserts m usculously on th e ve n tro m ed ia l
face o f th e hyom andibula and quadrate.
The le v a to r arcus palatini is situated p o ste rio r to th e section A3 o f th e a d d u cto r
m andibulae m uscle com plex (Fig. 6 .8 b ). I t o rig in ate s m usculously fro m ve n tra l face
o f th e sphenotic process, lateral face o f th e p rootic and p o ste rio r face o f th e
parasphenoid
alae
and
inserts
m usculously
on
th e
late ro ve n tra l
face
o f the
suspensorial fossa and th e laterodorsal face o f th e h yo m a n d ib u la r body.
The le va to r operculi com prises a ve n tra l and a dorsal bundle (Fig. 6 .8 a ). The
ve n tra l bundle o rig in ate s te n d in o u sly fro m th e posterodorsal depression o f the
hyom andibula th a t is situated dorsal to th e opercle a rtic u la r condyle and inserts
m usculously on th e v e n tro la te ra l face o f th e opercle. The dorsal bundle originates
te n d in o u sly fro m th e la te ro ve n tra l face o f th e exoccipital and inserts m usculously
on th e dorsolateral face o f th e opercle (Fig. 6.8a).
The a d d u cto r operculi m uscle o rig in ate s m usculously fro m a ve n tra l depression on
th e exoccipital and th e p osterolateral face o f th e basioccipital. I t inserts on the
dorsom edial rim o f th e opercle. The lateral fib e rs o f th is m uscle m erge w ith the
m edial fib e rs o f th e dorsal bundle o f th e le v a to r operculi (Fig. 6 .8 b ).
The d ila ta to r operculi is a tria n g u la r m uscle th a t is situated p o ste rio r to th e le va to r
arcus palatini (Fig. 6 .8 b ). I t o rig in ate s m usculously fro m th e lateral face o f th e
p rootic and ve n tra l face o f th e p te ro tic and inserts te n d in o u sly o nto an apophysis
on th e a n te ro la te ra l face o f th e rostral o p ercu la r process (Fig. 6 .8 b ).
93
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
The p ro tra c to r hyoidei m uscle connects th e p o ste rio r ceratohyal to th e low er ja w .
Each h a lf (rig h t and le ft) o f th is m uscle o rig in ate s te n d in o u sly fro m th e m edial face
o f th e d e n ta ry bone a t th e rear o f its sym physis and inserts te n d in o u sly on the
lateral face o f th e p o s te rio r ceratohyal (Fig. 6.8c).
The ste rnohyoideus m uscle inserts as a tendon on th e a n te rio r th ic k e r p a rt o f the
urohyal and m usculously on th e m edial faces o f tw o p o s te rio r processes o f the
urohyal (Fig. 6.8c). The ve n tra l fib e rs o f th e ste rn o hyo id eu s, which inse rt on the
a n terom edial faces o f th e p o ste rio r processes o f th e u ro hya l, m erge w ith th e
ve n tra l extended fib e rs o f th e hypaxials. The dorsal fib e rs o f th e sternohyoideus,
which inse rt on th e e n tire m edial faces o f th e p o s te rio r processes o f th e urohyal,
are divided p o ste rio rly into tw o bundles and o rig in ate fro m th e lateral face o f tw o
cleithra.
The hyohyoideus su p e rio r m uscle connects th e posterom edial edge o f th e p o ste rio r
ceratohyal to th e m edial m argin o f th e rostral o p ercu la r process (Fig. 6.8c).
The hyohyoideus m uscle com plex (p resu m a b ly an u n d iffe re n tia te d com plex o f th e
hyohyoideus
inte rio ris and
hyohyoidei a d du ctors)
is a m uscle sheet th a t lies
betw een th e m edial faces o f th e branchiostega! rays and fo rm s a th in sac-like
m uscle m eeting its co u n te rp a rt a t th e ve n tra l m idline (Fig. 6 .8 a ). The anterodorsal
fib e rs o f th is m uscle attach on th e m edial face o f th e opercle and poste rod o rsa lly on
th e horizontal septum betw een th e epaxial and hypaxial m uscles, by connective
tissue.
The m uscles serving th e ve n tra l parts o f th e branchial arches consist o f the
p h aryn g o cle ith ra lis (PHC), th re e pairs o f the obliqui ve n tra le s (O b.v I - I I I ) , rectus
com m unis (RC) and tra n sve rsus v e n tra lis o f th e low er to o th plates (T ra n s.v). The
p h aryn g o cle ith ra lis m uscle connects th e low er to o th plate to th e cle ith ru m (Fig.
6 .7 ). The obliquus v e n tra lis spans th e ce ra to bra n ch ia l-h ypo b ra nch ia l jo in t o f the
firs t th re e branchial arches. The rectus com m unis connects th e posterodorsal face
o f th e second hypobranchial to th e fo u rth ceratobranchia!. The tra n sve rsus v e n tra lis
te n d in o u sly connects th e pharyngeal low e r to o th plates to th e p o ste rio r end o f the
fo u rth basibranchia! (Fig. 6 .7 ). The rectus dorsalis I - I I (RD I: connects th e firs t and
second e p ib ra n chia l; RD II : connects th e second and th ird e p ib ra n chia l), medial
rectus
dorsalis
(R D .m ;
interconnects
firs t
94
and
second
e p ib ra n chia l),
obliquus
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
dorsalis I - I I (O b .d I: connects th e epibranchial I and infra ph a ryn go b ra n chia l I; O b.d
II : connects epibranchial II and infra ph a ryn go b ra n chia l II ) and m edial obliquus
dorsalis m uscle (O b .d .m : connects th e infra ph a ryn go b ra n chia ls) are m uscles th a t
serve th e dorsal p a rt o f th e branchial arches (Fig. 6 .7 ).
6 .4 .3 . C ra n ia l o s te o lo g y : G y m n o th o r a x p r a s in u s and A n a r c h ia s a lla r d ic e i
(M u r a e n in a e and U ro p te ry g iin a e : M u ra e n id a e )
The general co n fig u ra tio n o f th e skull o f G. pra sin u s and A. a lla rd ice i are ve ry
sim ila r. For detailed description o f th e cranial osteology o f G ym n o th o ra x p rasinus
and A narchias a llardicei, here is provided o n ly those elem ents th a t show differences
w ith respect to A riosom a g ilb e rti to avoid re p e titio n o f th e elem ents w ith same
conditions.
The neurocranium o f G. pra sin u s and A. a lla rd ice i is s to u t and ta p e rs fro m th e otic
region to w a rds th e p o ste rio r p a rt o f th e p re m a xillo -e th m o vo m e ra l com plex. T heir
eth m o id region com prises th e p re m a xillo -e th m o vo m e ra l com plex and nasals (Figs.
6.9a and 6 .1 0 a ). In both species, th e o lfa c to ry rosette is located dorsal to th e
ro stru m and is separated fro m th e o lfa c to ry rosette o f o th e r side by a ve rtica l wall
o f th e p re m a xillo -e th m o vo m e ra l com plex (Figs. 6.9a and 6 .1 0 a ). In G. pra sin u s the
tw o
le ft and
rig h t inle t tubes o f th e o lfa c to ry system
p re m a xillo -e th m o vo m e ra l
com plex canal th a t are
are connected to the
p o ste rio rly
opened
into the
o lfa cto ry rosettes. The snout o f G. pra sin u s and A. a lla rd ice i are re la tiv e ly s h o rt and
sh o ve l-like in a ve n tra l view (Figs. 6.1 1 b and 6 .1 2 b ). Posterodorsally, th e shovel­
like snout o f G. pra sin u s bears caudally directed s tru ts on its left and rig h t sides
(Fig. 6 .1 1 ), w hereas th a t o f A. a lla rd ic e i possesses th e tw o sm all processes i.e. the
m a xilla ry a rtic u la r facets (Fig. 6 .1 2 ). In both species, th e d e n titio n o f th e p o ste rio r
p a rt o f th e p re m a xillo -e th m o vo m e ra l com plex is separated by a space fro m th e
a n te rio r ones (Figs. 6.1 1 b and 6 .1 2 b ). The d e n titio n o f th e a n te rio r p a rt o f the
p re m a xillo -e th m o vo m e ra l com plex in G. pra sin u s com prises th re e rows o f large,
curved te e th w ith sm all te e th betw een th e tw o lateral rows (Fig. 6 .1 1 b ). Its te e th o f
th e p o ste rio r p a rt are arranged in one row w ith s h o rte r te e th than those o f the
a n te rio r ones. The a n te rio r p a rt o f th e p re m a xillo -e th m o vo m e ra l com plex in A.
a lla rd ice i contains o f few , pointed te e th on its ve n tra l face w ith a row o f sm a lle r
95
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
te e th on its rim (Fig. 6 .1 2 b ). In a d d itio n , som e sm all te e th are scattered am ong its
large te e th (Fig. 6 .1 2 b ). Its te e th o f th e p o ste rio r p a rt are arranged in one row
sim ila r to G. p ra sin u s but w ith th re e pointed te e th (Fig. 6 .1 2 b ).
The o rb ital region o f G. p ra sin u s consists o f th e adnasal, lacrim al, in fra o rb ita ls,
su p rao rb ita ls,
fro n ta l,
basisphenoid,
parasphenoid
and
pterosphenoid
bones,
w hereas th a t o f A.
a lla rd ice i lacks th e su p rao rb ita l and adnasal bones.
In G.
pra sin u s th e fro n ta l
bears an anterodorsal process w ith a dorsal and a
lateral
opening (Fig. 6 .9 a ).
Also, a sm all fro n ta l fo ntanel is present (Fig. 6 .1 1 a ). In A.
a lla rd ice i th e fro n ta l
a n te rio rly bears a T -like groove, a n te rio r to entrance o f the
te m p o ral canal (Fig. 6 .1 0 a ). Also, th e re is a sm all canal ve n tra l to th is fro n ta l
groove th a t p o ste rio rly is connected to th e te m p o ral canal (Fig. 6 .1 0 a ). The fro n ta ls
o f A.
a lla rd ic e i overlie
th e
a n te rio r
h a lf o f th e
parietals
(Fig.
6 .1 2 a ).
The
basisphenoid fo rm s th e p o ste rio r wall o f th e sm all o rb it in G. pra sin u s and A.
a lla rd ice i (Figs. 6.9a and 6 .1 0 a ). In both m uraenids th e basisphenoid bears the
o p tic foram en on its lateral face (Figs. 6.9a and 6 .1 0 a ). The o lfa c to ry foram en o f G.
pra sin u s is present on th e p o ste rove n tra l face o f th e basisphenoid (Fig. 6 .9 ),
w hereas th e pterosphenoid o f A. a lla rd ice i bears a canal on its ve n tra l p a rt th a t
encloses th e o lfa c to ry nerve and th is canal is opened on th e a n te rio r face o f the
pterosphenoid
as
o lfa c to ry
foram en
(Fig.
6 .1 0 ).
The
parasphenoid
of
both
m uraenids is th ic k , long bone th a t fo rm s th e flo o r o f th e o rb it (Figs. 6.9a, 6.10a,
6 .1 1 b and 6 .1 2 b ). Laterally, it expands in th e m idsection and narrow s p o ste rio rly to
a n arrow p o in t to w edge into th e basisphenoid (Figs. 6.1 1 b and 6 .1 2 b ). T heir
pterosphenoid is enlarged com pared to A. g ilb e rti.
The o tic region o f G. pra sin u s and A. a lla rd ice i com prises th e sphenotics, p te ro tics,
prootics, epioccipitals and parietals. The sphenotic o f G. pra sin u s bears a lateral
process d ire ctin g v e n tra lly , w hereas th a t o f A. a lla rd ice i is directed a n te ro v e n tra lly
(Fig. 6 .1 0 a ). In both m uraenids th e p te ro tic fo rm s th e posterolateral e le m e n t o f th e
n eurocranium and also th e long p o ste rio r suspensorial a rtic u la to ry fa ce t (Figs.
6 .1 1 b and 6 .1 2 b ). The p rootic o f G. p ra sin u s is fe n e stra te d w ith num erous fo ra m ia ,
including th e trig e m in o -fa c ia l foram en on its a n te ro la te ra l face (Fig. 6 .1 1 b ). Its
po ste rio r end also bears an apophysis to w hich attaches th e le v a to r inte rnu s m uscle
o f th e upper pharyngeal ja w (Fig. 6 .1 3 d ). The la te ro ve n tra l p a rt o f th e p rootic in A.
96
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
a lla rd ice i bears a depression w ith th re e pores th a t th e le v a to r inte rnu s m uscle
inserts on th e c e n te r o f th is depression (Fig. 6 .1 2 b ). The trig e m in o -fa c ia l foram en
o f A. a lla rd ice i present on th e a n te rio r rim o f th e p rootic bone (Fig. 6 .1 2 b ). The
parietals o f G. pra sin u s are irre g u la rly in te rd ig ita te d a n te rio rly w ith th e fro n ta l and
p o ste rio rly are bordered by th e epioccipital and supraoccipital bones, w hereas those
o f A. a lla rd ice i show overlapping w ith th e fro n ta ls and epioccipitals. A fontanel
present a t th e trip le su tu re p o in t betw een th e supraoccipital and parietals in G.
pra sin u s (Fig. 6 .1 1 a ). In both m uraenids th e p o s te rio r rim o f th e epioccipital is
curved v e n tra lly fo rm in g th e dorsal rim o f th e p o s te rio r wall o f th e neurocranium .
The occipital region o f G. pra sin u s and A. a lla rd ice i com prises th e supraoccipital,
exoccipitals and basioccipitals. T h e ir supraoccipital is situated a t th e posterodorsal
m idline o f th e neurocranium and bears a w ell-developed crest d ire ctin g caudally
(Figs. 6.9a, 6.10a, 6.11a and 6 .1 2 a ). T h e ir paired exoccipitals b o rde r th e foram en
m agnum w ith exception o f th e ve n tra l p a rt, which is bordered by th e basioccipital.
In both th e exoccipital is dom ed to w a rds th e foram en m agnum . The basioccipital o f
G. pra sin u s bears tw o apophyses on th e le ft and rig h t sides o f th e wedged p o ste rio r
end o f th e parasphenoid th a t th e le v a to r e xte rn us m uscle o f th e upper pharyngeal
ja w s inse rt on th e m . The p o ste rio r portion o f th e basioccipital in G. p rasinus
co n trib u te s to fo rm a nipple-shaped, s h o rt o tic bulla to g e th e r w ith th e exoccipital
and p rootic (Fig. 6 .1 1 b ) and p o ste rio rly, it bears fo u r pores. In A. a lla rd ice i th e
basioccipital situ a te s betw een tw o ve n tra l parts o f th e exoccipitals and co n trib u te s
to fo rm th e p o ste rio r p a rt o f th e low o tic bullae along w ith th e exoccipital and
prootic (Fig. 6 .1 2 b ).
The m a xilla ry o f G. pra sin u s is attached to th e s tru t o f th e posterodorsal process of
th e p re m a xillo -e th m o vo m e ra l com plex. I t bears tw o rows o f th e ca niniform te e th on
th e a n te rio r h a lf w ith longer lateral ones, and th e te e th on th e p o ste rio r h a lf are
arranged in a single row (Fig. 6 .1 4 a ). The m a x illa ry in A. a lla rd ice i is longer than
th a t o f G. pra sin u s and is firm ly attached to th e m a xilla ry a rtic u la r fa ce t o f th e
p re m a xillo -e th m o vo m e ra l com plex (Fig. 6 .1 0 a ). In A. a llardicei, th e a n te rio r p a rt o f
th e m a xilla ry bears an ascending process th a t m e d ia lly possesses tw o large te e th
and a single row o f pointed te e th on its a n terom edial fossa (Fig. 6 .1 5 a ). The
q u a d ra to -m a x illa ry lig a m e n t in G. pra sin u s connects th e posterolateral face o f the
97
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
a rtic u la to ry condyle o f th e q u adrate to th e posterodorsal face o f th e m a x illa ry (Fig.
6 .1 3 a ), w hereas th a t o f A. a lla rd ic e i runs m edial to th e Suspensorium and attaches
to th e m edial face o f th e a rtic u la to ry condyle o f th e quadrate. In both m uraenids
th e large coronoid process is form ed by th e d e n ta ry com plex. A n te rio rly , the
d e n ta ry com plex o f G. pra sin u s bears tw o rows o f th e ca niniform te e th w ith th re e
larg e r m edial ones th a t continue in a single row o f caudally pointed te e th running
up to th e coronoid process (Fig. 6 .1 4 b ). The d e n ta ry in A. a lla rd ice i bears tw o rows
o f ca niniform te e th w ith a longer m edian row th a t is extended to th e m id p o in t o f
th e lateral one (Fig. 6 .1 5 b ). Also, few sm all, recurved te e th are present m edial to
th e longer ones (Fig. 6 .1 5 b ). Laterally, th e d e n ta ry com plex o f G. pra sin u s bears
six pores o f th e p re o p e rcu lo -m a n d ib u la r canal and one on its a n terom edial face
(Figs. 6.9a and 6 .1 4 b ), w hereas th a t o f A. a lla rd ice i bears only five pores (Fig.
6 .1 0 a ). The coronom eckelian bone in G. pra sin u s is situated betw een th e d e n ta ry
and a n gu la r com plexes, ve n tra l to th e Meckelian fossa and a n te rio rly covered by
th e d e n ta ry (Fig. 6 .1 4 b ) and th a t o f A. a lla rd ic e i is attached to th e posterom edial
face o f th e d e n ta ry and ve n tro m ed ia l face o f th e a n g u la r com plex (Fig. 6 .1 5 b ).
In both m uraenids th e a n gu la r com plex consists o f th e fused angular, a rtic u la r and
re tro a rtic u la r
bones.
T h e ir
m a n dib u la r a rtic u la tio n
fa ce t
is
positioned
a t the
p o ste rio r end o f th e a n gu la r com plex d ire ctin g caudodorsally (Figs. 6.1 4 b and
6 .1 5 b ). The p re o p e rcu lo -m a n d ib u la r canal in both m uraenids is opened on the
p o ste rio r side o f th e sh o rt, caudally directed re tro a rtic u la r bone. In both m uraenids
th e a n te ro la te ra l portion o f th e a n gu la r com plex overlies th e p o ste rio r p a rt o f the
d e n ta ry com plex. In G. p ra sin u s and A. a lla rd ice i, a sh o rt p re op e rcu lo -a n gu la r
lig a m e n t
connects
th e
posterom edial
face
of
th e
a n gu la r
com plex
to
the
ve n tro m ed ia l face o f th e preopercle.
In both m uraenids th e Suspensorium com prises fo u r bones; th e hyom andibula,
q u ad ra te , p a la to p te ryg o id and preopercle (Figs. 6 .9b and 6 .1 0 b ). A n te rio rly , the
hyom andibula bears a fossa w ith a pore on its dorsal h a lf (Figs. 6 .9b and 6 .1 0 b ).
M edially, th e hyom andibula bears a canal th a t is opened on its dorsom edial face.
The p o ste rio r a rtic u la r condyle o f th e hyom andibula is long w ith serrated edges on
its
dorsal
m idsection.
The
hyom andibula
bears
a o p ercu la r a rtic u la r condyle
m e d io ve n tra lly dire ctin g ca u d o ve n tra lly (Figs. 6 .9b and 6 .1 0 b ). The quadrate bears
98
6
C
e p ^ a I íc
a
p o ste rio r
M o R p h o lo q y o f M
process
d ire ctin g
u r a eim íc I s
caudally
th a t
runs
under th e
peropercle.
The
h yo m a n d ib u la -q u a d ra te axis is directed v e rtic a lly , th u s positioning th e q u ad ra te m a n d ib u la r jo in t a t th e occipital level o f th e neurocranium . Hence, th e low er ja w is
a b ou t equal in length to th e neurocranium . The q u adrate bears a p o s te rio r process
on its medial face running caudally under th e preopercle. The p a la to p te ryg o id is
reduced
as a th in
slender bone atta ch in g
to th e
a n te ro ve n tra l
edge o f th e
hyom andibula by connective tissue and lig a m e nto usly on th e a n te rio r end o f the
quadrate.
In G. pra sin u s th e fo u r elem ents o f th e o p ercu la r series are reduced in size (Fig.
6 .9 b ). The preopercle is a sm all, tu b e -lik e bone and connected to th e quadrate. The
preopercle
encloses th e
m idsection
o f th e
p re o p e rcu lo -m a n d ib u la r canal. The
opercle bears an a n te ro la te ra l tu b e ro s ity on its a rtic u la to ry process (Fig. 6 .9 b ).
Also, th e re
is a sm all
process on th e
m edial
face
o f th e
o p ercu la r rostral
prom inence. The sm all re cta n g u la r subopercle and interopercle position a n te rio r to
th e
opercle
(Fig.
6 .9 b ).
The
o p ercu la r series
o f A.
a lla rd ice i shows
sim ila r
co n figu ra tio n and com ponents w ith G. pra sin u s, e xcept fo r lacking a m id p o in t pore
on th e lateral face o f th e preopercle (Fig. 6 .1 0 b ).
The hyoid com plex o f G. pra sin u s is e x tre m e ly reduced and consists o f th e paired
a n te rio r
and
p o ste rio r
ceratohyals
(Fig.
6 .13c).
The
p o ste rio r
ceratohyal
is
connected to th e m id p o in t o f th e slender a n te rio r ceratohyal by a ca rtila g ino u s s tru t
a t its a n te rio r end. Also, th e p o ste rio r ceratohyal is a slender bone th a t is connected
to all e ig h t branchiostega! rays a n te rio rly and to th e m edial face o f a p o ste rio r
process o f th e q u adrate by connective tissue. The hyoid com plex o f A. a lla rd ice i is
also e x tre m e ly reduced and like G. pra sin u s consists o f th e paired a n te rio r and
p o ste rio r ceratohyals w ith a s im ila r co n fig u ra tio n (Fig. 6 .16c).
The cephalic lateral line system o f G. pra sin u s com prises th e eth m o id and adnasal
canals in addition to those o f A. g ilb e rti (Fig. 6 .1 7 b ). The eth m o id canal is a sh o rt
descending branch o f th e su p rao rb ita l canal and sta rts a t th e a n te rio r edge o f the
o lfa cto ry ca vity. I t bears a single e xte rn al pore. The su p rao rb ita l canal is caudally
extended to th e dorsal pore o f th e a n te rola te ra l process o f th e fro n ta l. A n te rio rly, it
is enclosed by a tu b e -lik e nasal bone and p o ste rio rly by tw o su p rao rb ita l bones
(Fig. 6 .1 7 a ). The su p rao rb ita l canal bears one e xte rn al pore. The in fra o rb ita l canal
99
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
is curved do rsally into th e p o storbital region a fte r e xitin g th e firs t in fra o rb ita l bone
positioned ve n tra l to th e o rb it (Fig.
6 .1 7 a ). This canal anstom oses w ith
the
su p rao rb ita l canal inside th e a n te ro la te ra l process o f th e fro n ta l. The infra orb ita l
canal bears fo u r exteral pores. A n e rio rly, th e in fra o rb ita l canal is supported by the
lacrim al and firs t in fra o rb ita l bones and p o s te rio rly, by th e th re e in fra o rb ita l bones
(Fig. 6 .1 7 a ). The adnasal canal is an ascending branch o f th e in fra o rb ita l canal
exited fro m th e m edial face o f th e ve n tra l in fra o rb ita l bone a t its m idp o int. This
canal is supported a t its m id p o in t by th e adnasal bone. All circu m o rb ita l bones are
tu b u la r (Fig. 6 .1 7 a ). The p re o p e rcu lo -m a n d ib u la r canal runs inside th e m andíbula
(Fig. 6 .1 7 b ).
In com parison to G. pra sin u s, th e cephalic lateral line system o f A. a lla rd ice i lacks
th e eth m o id and adnasal canals and possesses a fro n ta l com m issure (Fig. 6 .1 8 b ).
The p o ste rio r p a rt o f th e su p rao rb ita l canal in A. a lla rd ice i is entered to th e a n te rio r
p a rt o f th e T -like groove o f th e fro n ta l. The nasal bone was not stained com pletely.
The su p rao rb ita l canal bears th re e e xte rn al pores. The fro n ta l com m issure runs
inside th e dorsal p a rt o f th e fro n ta l groove (Fig. 6 .1 8 b ). The in fra o rb ita l canal
anstom oses w ith th e su p rao rb ita l canal in th e fro n t o f th e T -like groove o f the
fro n ta l. This canal bears five e xte rn al pores. Two lacrim al and six in fra o rb ita l bones
su p p o rt th e in fra o rb ita l canal (Fig. 6 .1 8 a ). The p re o p e rcu lo -m a n d ib u la r canal bears
six e xte rn al pores.
In G. pra sin u s th e ve n tra l elem ents o f th e reduced gili arches are th e fo llo w ing :
fo u r pairs o f c e ra to b ra n c h ia ^ (Cb I-IV ) and one pair o f low er pharyngeal to o th
plates (LP) (Fig. 6 .1 9 b ). Its dorsal elem ents o f th e gili arches are com prised o f the
fo u r pairs o f epibranchials (Eb I-IV ) and one p a ir o f upper pharyngeal to o th plates
(UP)
(Fig.
6 .1 9 a ).
The
gili
arches
A.
a lla rd ice i
bear
tw o
pairs
of
infra ph a ryn go b ra n chia ls (Ib I I - I I I ) in addition to those o f G. pra sin u s (Fig. 6 .2 0 ).
6 .4 .4 . C ra n ia l M yolo gy: G y m n o th o r a x p r a s in u s and A n a r c h ia s a lla r d ic e i
The co n figu ra tio n o f th e h yp ertrop h ied a d d u cto r m andibulae m uscle com plex o f
G ym n o th o ra x pra sin u s and A narchias a lla rd ic e i are v e ry sim ila r. T h e ir a d d u cto r
m andibulae com plex com prises th e sections A2 and A3. The section A2 in G.
pra sin u s is subdivided into tw o subsections: a h yp e rtro p h ie d A2 lateral (A 2al) and
100
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
s trip -lik e A2 m edial (A 2y) (F ig . 6 .13a, b). The h yp ertrop h ied A2al o f G. p ra sin u s is
th e largest e le m e n t o f th e a d d u cto r m andibulae com plex and its fib e rs o rig in ate
fro m
th e fro n ta l, p a rie ta l, p te ro tic , su p raoccipital, hyom andibula and quadrate
bones. The la te ro a n te rio r fib e rs o f th e A2al in se rt as a tendon on th e m edial face of
th e d e n ta ry a t th e rear o f th e coronoid process, w hereas its la te ro p o s te rio r fibers
are attached as a tendon on th e m ediodorsal edge o f th e coronoid process and
medial m argin o f th e a n gu la r bone. Also, th e la te r tendon is connectd to th e lateral
face o f th e a rtic u la to ry condyle o f th e q u adrate by a tendon. The m edial fib e rs o f
th e A2al in G. pra sin u s inse rt m usculously into th e Meckelian fossa (Fig. 6 .1 3 c). The
A2y o f G. pra sin u s is positioned p o s te rio r to th e le v a to r arcus palatini m uscle and
runs m edial to th e d ila ta to r operculi m uscle (Fig. 6 .1 3 b ). The fib e rs o f A2y o rig in ate
fro m th e posterodorsal face o f th e hyom andibula bone and inse rt by a tendon on
th e a n g u la r com plex a t th e ve n tra l rim o f th e Meckelian fossa (Fig. 6 .1 3 b ).
The A2 section o f A. a lla rd ice i can also be subdivided into tw o subsections; A2
dorsal (A2ß) and A2 ve n tra l (A 2a) (Fig. 6 .1 6 a ). The A2ß is th e largest com ponent
and
its
fibers
o rig in a te
fro m
th e
fro n ta l,
p a rie ta l,
p te ro tic ,
epioccipital
and
supraoccipital bones. This m uscle inserts as a tendon on th e ve n tro m ed ia l face o f
th e coronoid process and m usculously on th e m edial rim o f th e d e n ta ry and
an gu la r, p o s te rio r to th e coronoid process. The tendon A2ß is connected on the
p o sterolateral face o f th e m a x illa ry by a tendon. The A2a o f A. a lla rd ice i is the
ve n tra l e le m e n t and has a m uscle origin a t th e p o ste rio r p a rt o f th e hyom andibula
and quadrate bones (Fig. 6 .1 6 a ). The m edial fib e rs o f th e A2a in se rt m usculously
into
th e
Meckelian
fossa, and
its
lateral
fib e rs
a ttach
both
te n d in o u sly and
m usculously on th e posterom edial face o f th e a n gu la r com plex. In both m uraenids
th e la te ro p o s te rio r fib e rs o f th e le ft and rig h t A2 subsection (A2al in G. p rasinus
and A2ß in A. a lla rd ice i)
m erge w ith
th e ir co u n te rp a rts fibers and are also
connected te n d in o u sly to th e epaxial m uscles and a fascia seperating th e m fro m the
le va to r operculi m uscle (Figs. 6.13a and 6.1 6 a ).
The A3 section o f th e a d d u cto r m andibulae m uscle com plex in A. a lla rd ice i and G.
pra sin u s is a large m uscle w ith its a n te rio r fib e rs dire ctin g ca u d o ve n tra lly (Figs.
6 .1 3 b and 6 .1 6 b ). In G. pra sin u s, it o rig in ate s m usculously fro m th e fro n ta l,
pterosphenoid,
p te ro tic ,
p o ste rio r p a rt o f th e
101
basisphenoid, parasphenoid and
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
a n te ro la te ra l face o f th e sphenotic bones (Fig. 6 .1 3 b ). The a n te rio r fib e rs o f A3 o f
G. p ra sin u s are connected to th e ve n tro m ed ia l face o f th e a n gu la r com plex as a
tendon and its p o s te rio r fib e rs attach m usculously to its posterom edial face. The A3
o f A. a lla rd ice i o rig in ate s m usculously fro m th e fro n ta l, pterosphenoid, p o ste rio r
p a rt o f th e basisphenoid and a n te ro la te ra l face o f th e sphenotic bones (Fig. 6 .1 6 b ).
The a n te rio r fib e rs o f th is section inse rt as a tendon into th e p o ste rio r p a rt o f the
Meckelian fossa and its p o ste rio r fib e rs attach m usculously on th e posterodorsal
m argin o f th e m edial face o f th e a n gu la r com plex.
The a d d u cto r arcus palatini o f G. pra sin u s and A. a lla rd ice i o rig in a te m usculously
fro m th e depression o f th e p rootic a t th e re a r o f th e trig e m in o -fa c ia l foram en and
inserts on th e a n terom edial face o f th e hyom andibula and dorsom edial face o f the
q u adrate (Fig. 6 .1 3 d ).
The le va to r arcus palatini in G. p ra sin u s and A. a lla rd ic e i is positioned p o ste rio r to
th e A3 section o f th e a d d u cto r m andibulae com plex th a t also covers its anterodorsal
p a rt (Figs. 6.1 3 b and 16b). Its fib e rs o rig in a te fro m th e ve n tra l and m edial faces o f
th e sphenotic process and la te ro ve n tra l face o f th e pte ro tic. This m uscle inserts on
th e p o ste rio r face o f th e suspensorial fossa, p o s te rio r face o f th e hyom andibula and
anterodorsal m argin o f th e q u adrate (Figs. 6.1 3 b and 6 .1 6 b ).
The a d d u cto r hyom andibulae m uscle connects th e p o ste rove n tra l m argin o f the
m edial face o f th e hyom andibula to a depression on th e posterolateral face o f the
exoccipital in G. pra sin u s and A. a lla rd ice i (Fig. 6 .1 3 d ).
The d ila ta to r operculi is a s trip -lik e m uscle in both G. pra sin u s and A. a llardicei,
directed c a u d o ve n tra lly (Figs. 6 .1 3 b and 6 .1 6 b ).
In A. a lla rd ice i th e d ila ta to r
operculi o rig in ate s m usculously fro m th e lateral face o f th e sphenotic process and
inserts as a tendon o nto th e a n terom edial face o f th e o p ercu la r rostral prom inence
(Fig. 6 .1 6 b ). In G. p ra sin u s it o rig in ate s m usculously fro m th e lateral face o f the
sphenotic process and v e n tro la te ra l face o f th e p te ro tic and inserts on th e process
o f th e m edial face o f th e o p ercu la r rostral prom inence (Figs. 6 .1 3 b and 6 .1 6 b ).
The le va to r operculi o f A. a lla rd ice i o rig in ate s as a tendon fro m th e posterodorsal
edge o f th e hyom andibula (Fig. 6 .1 6 b ), w hereas in G. pra sin u s th is is o nly th e case
fo r a n te rio r fibers. In th e la tte r species, th e p o s te rio r fib e rs o rig in a te fro m a tendon
th a t attaches to th e epaxial m uscles and a n te rio r p a rt o f th e horizontal septum
102
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
betw een th e epaxial and hypaxial m uscles (Fig. 6 .1 3 d ). The le v a to r operculi inserts
on th e lateral faces o f th e opercle, subopercle and interopercle in both G. pra sin u s
and A. a lla rd ice i (Figs. 6.1 3 b and 6 .1 6 b ).
The a d d u cto r operculi m uscle o riginates in both G. p ra sin u s and A. a lla rd ice i as a
tendon fro m th e dorsom edial co rn er o f th e hyom andibula and inserts on th e medial
faces o f th e opercle, subopercle and interopercle (Fig. 6 .1 3 d ). In G. pra sin u s, the
a d d u cto r operculi tendon is also connected to th e tendon o f th e epaxial muscles.
The
p ro tra c to r
hyoidei
m uscle
connects
th e
long,
th in
and
fle xib le
a n te rio r
ceratohyal bone to th e low er ja w in both G. pra sin u s and A. allardicei. I t o riginates
te n d in o u sly fro m th e m edial face o f th e d e n ta ry bone, close to th e sym physis, and
inserts m usculously on th e a n te rio r face o f th e a n te rio r ceratohyal (Figs. 6.13c and
6.16c).
The sternohyoideus in G. pra sin u s and A. a lla rd ice i o rig in ate s a n te rio rly fro m th e
a n te rio r h a lf o f th e a n te rio r ce ra to hya l, in th e extensions o f th e hypaxial muscles.
Its lateral fib e rs o rig in a te fro m th e p o ste rio r h a lf o f th e a n te rio r ce ra to hya l, fo rm s
th e rectus com m unis to p ro tra c t th e low er pharyngeal ja w (Figs. 6.13c and 6.16c).
The sm all hyohyoideus su p e rio r in G. pra sin u s connects th e p o ste rio r end o f the
po ste rio r ceratohyal to a sm all process on th e m edial face o f o p ercu la r rostral
prom inence (Fig. 6 .1 3 d ). This m uscle is absent in A. allardicei.
The hyohyoideus m uscle com plex in G. pra sin u s and A. a lla rd ic e i is a m uscle sheet
th a t lies betw een th e m edial faces o f th e branchiostega! rays and fo rm s a th in saclike m uscle m eeting its c o u n te rp a rt a t th e ve n tra l m idline (Figs. 6.13a and 6 .1 6 a ).
The dorsal fib e rs o f th is m uscle com plex attach to th e horizontal septum between
th e epaxial and hypaxial muscles.
The epaxial m uscles in G. pra sin u s and A. a lla rd ice i inse rt m usculously on th e
e pioccipital,
supraoccipital,
exoccipital
and
basioccipital
bones.
The
hypaxial
m uscles m erge w ith th e ste rn o hyo id eu s m uscle.
In
both
m uraenids
th e
rectus
com m unis
m uscle
attaches
to
th e
fo u rth
ceratobranchia! bone (Figs. 6.13c and 6 .16c). The fib e rs o f th e le v a to r e xte rn u s and
le va to r inte rnu s in G. pra sin u s inse rt on th e basioccipital and p rootic bones,
respectively. Those o f A. a lla rd ice i are attached to th e exoccipital and th e prootic,
103
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
respectively. O ther m uscles serving th e branchial arches o f G. p ra sin u s and A.
a lla rd ice i are s im ila r to those described in Mehta and W a in w rig h t (2 0 07 a ).
6 .5 . D iscussion:
A riosom a g ilb e rti (O gilby, 1898) lives in burrow s on th e fla t sandy b o tto m o f th e
co n tine n ta l sh e lf and feeds on m obile crustaceans, cephalopods and fishes. They
are
ta il-firs t
burrow ers
and
em erge
fro m
th e ir
b u rro w
at
n ig h t
to
forage
(R osenblatt, 1958; Asano, 1962; S m ith , 1989a). The im m ob ile m a x illa ry equipped
w ith
large pointed te e th , th e ca niniform
m andíbula,
th e
large,
pointed
te e th
and backw ardly curved te e th
o f th e
a n te rio r
tip
o f th e
o f the
p re m a xillo -
e th m o vom e ra l com plex and an a n te rio r m oderate m outh gape o f A. g ilb e rti suggest
grasping and im paling o f elusive prey upon capture (Lauder, 1980b; A lfaro e t al.,
2 0 01 ; Porter and M otta, 2004). Com bined w ith th e large ja w closing m uscles, th e y
w ill assist in p re venting escape du rin g subsequent tra n s p o rt. Also, th e large lateral
and ve n tra l bony elem ents o f th e skull and associated m uscles linked to th e buccal
ca vity expansion and large o p ercu la r series in w hich is provided m ore room fo r the
orobranchial c a vity, suggest th e presence o f a hydraulic, suction-based m echanism
as subsequent tra n s p o rt b ehavior in A. g ilb e rti. In th is m echanism , fishes tra n s m it
th e piece o r w hole o f th e prey into th e esophagus by hyd rau lic suction th a t is
produced by depressing th e m andible (G rubich e t a l., 2008).
Morays on th e o th e r hand, are carnivores and s h a llo w -w a te r reef, cre vice -d w ellin g
eels th a t are found in all tro p ical and subtropical oceans and seas, w ith a few
species occurring in te m p e ra te w aters (B öhlke e t al., 1989; Santos and Castro,
2 003; Young and W inn, 2 0 03 ). Morays like m any anim als such as snakes and
g u ip e r fishes, sw allow th e ir large prey as a w hole (Yukihira e t al., 1994; Santos and
Castro, 2003; W estneat, 2 0 07 ). I t is q u ite e v id e n t th a t m orays have a d iffe re n t
head a rch ite ctu re than snakes, and even th e m ore closely related g u ip e r eels, to
perform th is fu n ctio n . Morays have evolved an a lte rn a tiv e to th is hydra ul ¡es-based
prey tra n s p o rt to m ove large prey fro m th e oral ja w s to th e pharyngeal ja w s (M ehta
and W a in w rig h t, 2007a). M odification o f th e branchial arches in relation to the
pharyngeal ja w
fu n c tio n a lity
in m uraenids has been described
by Mehta and
W a in w rig h t (2 0 0 8 ). In com parison to o th e r A n g uillifo rm e s, including th e closely104
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
related A. g ilb e rti th a t still perform th e hydraulic-based
prey tra n s p o rt, some
cephalic fe a tu re s o f m uraenids can be considerd as specializations to seize and
devoure large prey in relation to th e presence o f th is second set o f jaw s.
The
neurocranial
elem ents
of
m uraenids,
such
as
p re m a xillo -e th m o vo m e ra l
com plex and parasphenoid are s to u t and robust, com pared to th a t o f A. g ilb e rti.
The re in force m e n ts o f neurocranial elem ents m ay help in resisting high im pact
forces during biting and prey grabbing.
The p o ste rio r position o f th e q u a d ra to -m a n d ib u la r a rtic u la tio n , being a p p ro xim a te ly
a t th e level o f th e p o ste rio r m argin o f th e ne uro cra n iu m , is associated w ith the
elongation o f th e low er ja w and a large, n o ncircular m outh gape in m uraenids. A
p a tte rn o f ja w elongation as in m uraenids is also found in S ynaphobanchidae th a t
also posses a s im ila r gili arch m u scu la tu re , suggesting th e capacity to tra n s p o rt
food in th e ir buccal ca vity.
How ever, syn a p h o b ra n c h u s do possess an a lm ost
com plete set o f branchial arches (see ch a p te r 5). An aquatic p re d a to r w ith a large,
n o ncircu la r m outh gape, as seen in m uraenids, can allow to m ove th e ja w s into a
b itin g position (w ith o u t pushing potential prey aw ay fro m th e opened m o u th ), as
well as consum ing large preys (C astle, 1968; Porter and M otta, 2 0 04 ; Mehta and
W a inw righ t, 2007a, 2008, 2009). F u rtherm ore, th e presence o f long low er ja w s
fa cilita te s fa s t m outh closure, e ffe ctive fo r ca p tu rin g m obile and elusive prey, is
beneficial in these predators th a t are known to re ly on h ig h -v e lo c ity ja w closure fo r
ca p tu rin g prey (Lauder, 1979; Norton and B rainerd, 1993; W estneat, 2004; Porter
and
M otta,
2004;
Eagderi
and
Adriaens,
2010a).
For
instance,
m echanical
advantage fo r opening and closing o f th e low er ja w in G ym n o th o ra x ja v a n ic u s is
low, i.e. th is fish can bite fa st (W estneat, 2004). In co n tra s t to m uraenids, in o th e r
A n g uillifo rm e s w ith elongated ja w s such as th e N em ichthyidae, N ettastom idae and
S e rrivo m e rid a e , ja w elongation is ra th e r coupled to th e elongation o f th e rostral
region (S m ith and Nielsen, 1989; Tighe, 1989; Eagderi and A driaens, 2010a).
The p o ste rio r d isplacem ent o f th e gili arches in anguilliform is is like ly related to the
reduction o f th e head d ia m e te r (N elson, 1966), w ith th e gili arches displaced fro m a
position beneath th e cranium to one behind it. Hence, a ja w elongation coupled to a
backw ards
s h ift
o f th e
q u a d ra te -m a n d ib u la r jo in t
in
m uraenids
(instead
of
elongation o f th e rostral region) m ay be beneficial fo r having a fa st bite w ith o u t
105
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
increasing th e distance betw een th e im paling p o in t o f prey on th e m andíbula and
th e pharyngeal jaw s.
Moray eels display a considerable e n la rg e m e n t o f th e te e th o f th e oral ja w s and
p re m a xillo -e th m o vo m e ra l com plex, com pared to A. g ilb e rti. A lm ost th e fu ll a n te rio r
h a lf o f th e d e n ta ry com plex o f m uraenids is de ntig e ro us w ith larg e r a n te rio r te e th ,
and
those
te e th
o f th e
m a x illa ry
and
p re m a xillo -e th m o vo m e ra l
com plex are
extended caudally up to its v e n tro p o s te rio r p o rtion . I t can be noted th a t m uraenids
like ly im pale large prey by th e a n te rio r p a rt o f th e oral ja w . The te e th in th e oral
ja w s can restrain th e prey even if o n ly in co n ta ct w ith a sm all portion o f th e prey by
sinking a few te e th into th e prey (M ehta and W a in w rig h t, 2007b).
Species w ith enlarged ja w adductors appear "a d a p te d " to grab th e prey item a t
p o ste rio r p a rt o f th e ja w s (Gans and De Vree, 1987), w hereas th is probably is not
th e case in m uraenids. Morays are well suited fo r closing th e tip s o f th e ja w s a t
high velocities but th e y have a m echanical disadvantage a t th e ir tip s in te rm s o f
force production (P o rte r and M otta, 2004).
M axim ization o f force and ve lo city
tra n s fe r in m outh closing system s, as tra d e -o ffs , have been suggested before in fish
species
(W estneat,
1994,
2004;
T uringan
e t al.,
1995;
C ollar e t a l.,
2005;
K äm m erer e t al., 2005; Van W assenbergh e t a l., 2005; De Schepper e t al., 2008).
Morays, th e re fo re , w ith th e ir h yp e rtro p h ie d ja w -c lo s in g m uscles, long low er ja w and
large, sharp te e th can be expected to generate re la tiv e ly large forces to bite and
im pale th e prey by th e ir te e th . Then, th e pharyngeal ja w s can p ro tra c t to d e live r a
second bite (M ehta and W a in w rig h t, 2007b).
Muraenids show a reduction in th e m ovable cranial e lem ents and a th in slender
p a la to p te ryg o id . Also th e o p ercu la r bones o f m uraenids are reduced in size and the
hyoid apparatus is re stricte d to tw o slender a n te rio r and p o s te rio r ceratohyal
bones. F u rth e rm o re, m uraenids show a reduction in th e n u m b e r and size o f th e
bones o f th e branchial arches such as th e basibranchia! and hypobranchial bones.
Mehta and W a in w rig h t (2 0 0 8 ) pointed o u t th a t th e reduction o r loss o f th e ve n tra l
elem ents o f th e branchial arches, hyoid apparatus and th e ir m uscular connections
in m uraenids m ay be linked to th e absence o f th e hyd rau lic tra n s p o rt system , and
hence th e need fo r a n o th e r m echanical tra n s p o rt system . In doing so, these
106
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
reductions did provide m ore room in th e orobranchial ca v ity fa c ilita tin g th e m o b ility
o f th e pharyngeal jaw s.
Speed alone is not th e sole ch a ra cte ristic o f m orays th a t is related to feeding on
large prey. The a d d u cto r m andibulae m uscle com plex in A. a lla rd ice i and G.
pra sin u s is la rg e r than th a t o f A. g ilb e rti. The pow erful bite to im pale prey is
a n o th e r re q u ire m e n t to o ve rta ke th e large prey in m uraenids. The h yp ertrop h ied
a d d u cto r m andibulae m uscle com plex o f m o ray eels, which is a lm o st re stricte d to
th e e xte rn al m ost ja w ad du ctor, suggests th is pow erful bite (D evaere e t a l., 2001;
Herrei e t a l., 2 0 02 ; Van W assenbergh e t a l., 2004). M uraenids w ith h yp ertrop h ied
ja w muscles bear a large and elevated supraoccipital crest, to increase th e insertion
site area fo r th e ja w m uscles (De Schepper, 2007). H ow ever, A. g ilb e rti w ith
sm a lle r ja w m uscle even lacks th e supraoccipital bone.
Grabbing large prey item s and dragging them into th e p h aryn x using th e second set
o f grasping ja w s can induce dislocating forces o nto th e q u a d ra te -m a n d ib u la r jo in t in
m uraenids. Some specializations o f m uraenids, including (1 ) th e presence o f the
q u a d ra to -m a x illa ry and p re op e rcu lo -a n gu la r ligam ents, (2 ) th e connection o f the
quadrate
to
th e
A2
tendon
o f a d d u cto r
m andibulae
com plex,
and
(3 )
the
caudoventral o rie n ta tio n o f th e fibers o f large A3 can help p re ven tin g a dislocation
o f th e m a n d ib u la r jo in t. The c a u d o ve n tra lly m uscle o rie n tio n can pull th e m andíbula
up- and fo rw a rd , th e re b y co u nte ra ctin g th e im pa ct force o nto th e jo in t generated
by m outh closing m uscle. The presence o f ca u d o ve n tra lly o rie n ta te d fibers o f th e A3
also is advantageous in h e a d -firs t b urrow ers in p re ven tin g such a dislocation (De
Schepper e t a l., 2 0 07b; Eagderi and Adriaens, 2 0 10b). The fib e rs o f th e large A3
section run c a u d o ve n tra lly in m uraenids, in co n tra s t to a n te ro ve n tra l dire ctio n in A.
g ilb e rti. In a d ditio n , th e reduction o f th e a n te rio r p a rt o f th e Suspensorium along
w ith th e lengthening o f th e pterosphenoid in both m orays (com pared to A. g ilb e rti),
provides additional space fo r th e large A3 section.
The p o ste rio r position o f th e a d d u cto r arcus palatini and a d d u cto r hyom andibulae
m uscles in m uraenids could be related to th e p o ste rio r position o f th e Suspensorium
and th e lengthening o f th e pterosphenoid, and hence m ay not necessarily be an
a daptive change. This is also reflected in th e fa ct th a t th e lateral m otion o f th e
Suspensorium , a key co m ponent o f buccal expansion in m ost te leosts (Lauder,
107
6
C
e p ^ a I íc
M o R p h o lo q y o f M
u r a eim íc I s
1985) and observed in m orays du rin g re sp ira tio n, appeared to be too slow to re su lt
in su fficie n t suction flo w velocities to m ove prey item s (M ehta and W a in w rig h t,
2007a).
An inn o va tive pharyngeal ja w ap pa ra tu s, as present in m orays, enabled th e use o f
a m echanical tra n s p o rt system ra th e r than a hyd rau lic one to pull prey into the
esophagus (M ehta and W a in w rig h t, 2007a). The c u rre n t s tu d y shows th a t th is
inn o va tive feeding m echanism m ay be linked to m any cephalic m o d ifications in
addition to those o f branchial arches, w hich have been described by Mehta and
W a in w rig h t (2 0 0 7 a ). These m arked m o ifications such as th e s to u t and robust
neurocranial elem ents, an elongated
low er ja w as th e re su lt o f th e p o ste rio r
position o f th e q u a d ra to -m a n d ib u la r a rtic u la tio n , enlarged te e th o f oral ja w s and
th e p re m a xillo -e th m o vo m e ra l com plex, reduction in th e m ovable cranial bones and
th e ir m uscular connections, h yp ertrop h ied a d d u cto r m andibulae m uscle com plex,
presence o f th e q u a d ra to -m a x illa ry and p re op e rcu lo -a n gu la r ligam ents, connection
o f th e qu ad ra te to th e A2 tendon o f a d d u cto r m andibulae com plex, caudoventral
o rie n ta tio n o f th e fib e rs o f th e large A3 section o f a d d u cto r m andibulae com plex,
are m ore than subtle m o d ifications in e xisting system s th a t was already proposed
by Mehta and W a in w rig h t (2 0 0 7 a ), in o rd e r to allow an o p tim al perform ance o f the
cranial m usculo-skeletal system .
A CK N O W LE DG M ENTS
The a uthors w ould like to th a n ks M. M c G ro u th e r (A ustralian M useum ), R. H
Robins and J. A Lopez (Florida Museum o f Natural H istory) fo r providing m useum
specim ens, N. D e S c h e p p e r (G hent U nive rsity) fo r her assistances, D. G. S m ith
(S m ith so nia n , USA) and R. S. M e h ta fo r th e ir valuable com m ents.
108
C liA p T E R 7
H eAd M o R pholoqy o f
t I ie
Peücan E eI,
EuRyphARyNx pclccANoidcs
7 H eAd MoRphoLoqy o f t Iie P eUcan E eL
C hapter seven
H ead M o rp h o lo g y o f th e P elican Eel, E u r y p h a r y n x p e le c a n o id e s
(S a c c o p h a ry n g o id e i: E u ry p h a ry n g id a e )
7 .1 . A b s tra c t
Eurypharynx pelecanoides, as only member of the Eurypharyngidae, is found in the bathyal
zone of the tropical and temperate areas of all oceans. It is characterized by the reduction
and loss of many structural elements of the head and by an extreme modification of many
of the remaining elements. The study was aimed to understand to what degree the
ancestral anguilliform cranial musculoskeletal system has become modified into this highly
specialized 'gulping' feeding system in E. pelecanoides. Hence, a detailed description is
added to the current knowledge, as well as the description of the cranial osteology to those
already
known
and
a complete
head
musculature.
In
relation
to
these extensive
modifications, possible implications for the functioning of the feeding apparatus were
described based on its cephalic musculoskeletal system and a broadcasted short footage
(sixty-five seconds) of a feeding pelican eel in the BBC documentary series (Blue planet:
Eposide2 - The Deep, 2001). The results revealed that many extreme modifications of head
structures of E. pelecanoides are to be seen in relation to functional shifts compared to
those of other Anguilliformes. Also, it shows two novel cephalic muscles that have no
equivalent in other fishes, as far as we know.
7 .2 . In tro d u c tio n
The Saccopharyngoidei o r g u ip e r eels are w ell-kno w n deep-sea fishes th a t occur a t
bathypelagic depths th ro u g h o u t th e w orld 's oceans (B ertelsen e t a l., 1989). The
fa m ily o f th e E urypharyngidae, to g e th e r w ith th e S accopharyngidae, M onognathidae
and C yem atidae, belong to th is suborder. The Saccopharyngoidei ge ne ra lly have
been considered to be close relatives o f th e tru e eels (su b o rd e r A n g u illo id e i),
because th e y show a s im ila r leptocephalus larval stage (G reenw ood e t al., 1966;
Inoue e t al., 2 0 01 ).
Phylogenetic analysis using th e m ito g en o m ic data o f th e
E urypharyngidae and S accopharyngidae have d e m on stra ted not o n ly these g u ip e r
eels fo rm a sis te r-g ro u p re la tio n sh ip w ith a high p ro b a b ility (1 0 0 % ), b u t also th e y
109
7 H eAd MoRphoLoqy of t Iie P e U can EeL
are deeply nested w ith in th e A n g uillifo rm e s (tru e eels), stro n g ly suggesting th a t
th e y have been derived fro m an e e l-like ancestor (In o u e e t a l., 2003; 2010) (Fig.
1.7). Wang e t al. (2 0 0 3 ), O b e rm ille r and Pfeiler (2 0 0 3 ) and Inoue e t al. (2 0 1 0 ) aiso
confirm ed th e m o n op h yly o f th e A nguilloidei and Saccopharyngoidei clade w ith in
th e a n g u illifo rm e fishes inferred fro m m ito ch on d ria l ribosom al RNA sequences.
E u ryp h a ryn x pelecanoides is th e only m e m be r o f th e fa m ily
E urypharyngidae
(M cCosker, 1998) and is found in the bathyal zone o f th e tro p ical and te m p e ra te
areas o f all oceans (B öhlke, 1966). I t is characterized by th e reduction and loss o f
m any s tru c tu ra l elem ents o f th e head and by an e xtre m e m o dification o f m any o f
th e rem aining elem ents (B e rtin , 1934; Tchernavian, 1947; Bertelsen e t a l., 1989).
Com pared to th e A n g uilloidei, E. pelecanoides shows th e
loss o f m any bony
elem ents such as pre m a xilla ries, p a la to p te ryg o id s, sym plectics, pterosphenoids,
su praoccipital, hyoid arches, o p ercu la r series, branchiostega! rays, and pectoral fin
and g ird le (B e rtin , 1934; T chernavian, 1947; Bertelsen e t al., 1989).
E u ryp h a ryn x pelecanoides, o r pelican eel, is a c tiv e ly searching fo r food during
sw im m ing by its w h ip -lik e tail (Nielsen e t al., 1989). Also, E. pelecanoides bears a
com plex organ w ith num erous te n ta cle s a t th e end o f its ta il, which is p resum ably a
lure to a ttra c t th e prey (Nielsen and Bertelsen, 1985). I t feeds on wide range o f
prey such as fishes, crustaceans, cephalopods, sargassum weeds, chaetognathans,
urochordataes, scyphozoaens and ne m ertin e s (Nielsen e t a l., 1989).
Since th e description o f E. pelecanoides by V a illa n t (1 8 8 2 ), its bizarre appearance
due to th e e x tre m e ly enlarged ja w s and Suspensorium re su ltin g in a huge gape a t
th e tip o f th e e e l-like body, has a ttra c te d much a tte n tio n fro m m any researchers
(Gili and Ryder, 1883;
N usbaum -H ilarow icz, 1923;
B ertin,
1934; Tchernavian.
1947; Bertelsen e t al., 1989; Nielsen e t a l., 1989). Its e xte rn al m o rph o log y and
anatom ical d e scrip tio n , such as osteological fe a tu re s, caudal organ, lateral line
system have been described by V a illa n t (1 8 8 2 ), Gili and Ryder (1 8 8 3 ), Nusbaum H ilarowicz (1 9 2 3 ), Bertin (1 9 3 4 ) and Tchernavian (1 9 4 7 ) and stom ach c o n te n t and
assum ed feeding s tra te g y by Nielsen e t a l., (1 9 8 9 ). Despite these w orks, it is still
p oorly known and little detailed osteological in fo rm a tio n is available. Also, the
hypothesized feeding s tra te g y o f th is g u ip e r eel, deduced fro m its head m orph o log y
by Nielsen e t al. (1 9 8 9 ) does not correspond to th e broadcasted sh o rt footage o f a
110
7 H eAd MoRphoLoqy of t Iie P e U can EeL
feeding g u ip e r eel in th e BBC d o cu m e n ta ry series (Blue planet: Eposide2 - The
Deep, 2001; h ttp ://w w w .v o u tu b e .c o m /w a tc h ? v = IN J 5 T k 7 N b i4 T
This stu d y provides a detailed description o f th e cranial osteology to those already
known and a com plete description o f th e head m usculature. This can help to
understand
to
w h a t degree th e
ancestral
a n g u illifo rm
cranial
m usculoskeletal
system has becom e m odified into th is h ig h ly specialized 'g u lp in g ' feeding system in
E. pelecanoides. In relation to these e xtensive m o d ifica tio n s, possible im plications
fo r th e fu n ctio n in g o f th e feeding apparatus are described. Because o f th e g re at
depth o f th e h a b ita t o f E. pelecanoides, aspects o f its b ehavior are largely the
su b je ct o f co n je ctu re .
bizarre
cephalic
Hence, a fu n ctio n al
characters
m orphological in te rp re ta tio n
o f E. pelecanoides
provides
an
o f the
insig h t to
b e tte r
understand its feeding behavior, since m ost m orphological characters are generally
correlated w ith fu n ctio n al dem ands (Liem , 1967).
7 .3 . M a te ria l and m e th o d s
For th e anatom ical d e scrip tio n , e ig h t alcohol-preserved specim ens o f E u ryp ha ryn x
pelecanoides
(1 9 8 0 -1 3 5 4 ,
P2340418), obtained fro m
P2340411,
th e
P2340414,
P2340415,
Musée National d 'H istoire
P2340416
and
Naturel o f Paris and
Natural H istory Museum o f D enm ark, w ere exam ined. Due to a dam aged ta il in tw o
o f th e specim ens o f E. pelecanoides (EP4 and 8 ), th e ir to ta l length was estim a te d
based on th e preanal length. The specim ens w ere o f th e fo llo w ing size range in
Total Length (TL): EP1: TL= 515 m m ; EP2: TL= 446 m m ; EP3: TL= 491 m m ; EP4:
TL= 502; EP5: TL= 506 m m ; EP6: TL= 120 m m ; EP7: TL= 376 m m ; EP8: TL= 445
m m . Two specim ens (EP2 and EP6) w ere cleared and stained w ith alizarin red S and
alcian
blue
according
to
th e
protocol
o f T a ylo r and
Van
Dyke
(1 9 8 5 ),
fo r
osteological e xa m inations. Dissections w ith m uscle fib e r staining according to Bock
and Shear (1 9 7 2 ) w ere perform ed.
To stu d y th e s tru c tu re o f th e Suspensorium bones and skin, sm all pieces fro m the
hyom andibula and buccal skin o f EP3 w ere em bedded in paraffin and cut into 6 pm
sections. The sections w ere stained w ith h e m a to xylin -e o sin , fo llo w ing Carson and
Hladik (2 0 0 9 ).
Ill
7 H eAd MoRphoLoqy of t Iie P e U can EeL
A n o th e r
specim en
(EP7)
was
scanned
at
th e
m o d ula r
m icro-C T
setup
of
G hent U nive rsity (Masschaele e t a l., 2 0 07 ; h ttp ://w w w .u g c t.u g e n t.b e ) using the
d irectional tu b e head, a t 80 kV tube voltage. The d e te c to r was an a : Si fla t panel
(Varian Paxscan 2520) w ith Csl s c in tilla to r. The specim en was im aged a t th e full
d e te cto r resolution o f 1496x1880 pixels o f 12 7 2 p m 2. Due to th e elongated shape
o f th e sam ple, a sm a lle r g e o m e tric m a g nifica tio n o f 2.2 was used, resulting in an
e ffe ctive voxel size o f 5 8 3 p m 3. In to ta l 1001 p ro je ctio n s o f 1496x1880 pixels were
m ade covering th e fu ll 360 degrees. The raw data was processed and reconstructed
using th e in-house developed CT softw are Octopus (Vlassenbroeck e t al. 2007) and
rendered w ith VG Studio Max (V olum e Graphics GmbH H eidelberg, G erm any) and
Am ira 4 .1 .0 softw are (M ercury C om puter System s GmbH M érignac, France).
Muscle te rm in o lo g y follow s W interbottom i (1 9 7 4 ). T e rm ino lo gy o f cranial skeletal
elem ents follow s Böhlke (1 9 8 9 a ) and Rojo (1 9 9 1 ). The e p io tic o f te leosts is term ed
"ep io ccip ita l",
th e re b y
fo llo w ing
Patterson
(1 9 7 5 ).
T e rm ino lo gy
of
the
chondrocranium follow s A driaens and Verraes (1 9 9 7 ) and G eerinckx e t al. (2 0 0 5 ).
7 .4 . R esu lts
7 .4 .1 . C ra n ia l o s te o lo g y
The bony neurocranium is com prised o f only perichondral bones th a t are connected
synchondrously.
The
neurocranium
is fla tte n e d
ve n tro d o rs a lly .
S trik in g ly ,
the
a n te rio r portion o f th e skull (e th m o id and o rb ital regions) is co m p le te ly unossified,
except fo r a ro d -like vom eral
bone th a t v e n tra lly su p ports th is cartilaginous
ro stru m . This ca rtila g ino u s e le m e n t seems to com prise th e e th m o id plate, trabecula
cranii and a n te rio r portion o f th e taenia m arginalis (o rb ita l ca rtilla g es). Laterally, it
fo rm s th e o rb its th a t are o n ly bordered d o rsally and caudally by bone i.e. fro n ta l
and sphenotic, re sp ective ly (Figs. 7.1a and 7 .2 ). The v o m e r is positioned a t the
m idline o f th e ve n tra l face o f th e ca rtila g ino u s ro stru m and is extended caudally
w here it is connected to th e anterodorsal face o f th e parasphenoid (Fig. 7 .2 b ).
The o rb ital region com prises th e nasals, fro n ta ls , and parasphenoid. The nasal
bones are tw o sm all bones on th e dorsal face o f th e ca rtila g ino u s snout. The
o lfa cto ry rosette is positioned on th e anterodorsal corners o f th e cartilaginous
ro stru m . The fro n ta l bones are situated p o s te rio r to th e ca rtila g ino u s ro stru m (Fig.
112
7 H eAd MoRphoLoqy of t Iie P e U can EeL
7 .2 a ).
Laterally, th e fro n ta l connects to th e sphenotic and p o ste rio rly, to the
parietal (Fig. 7 .2 a ). The parasphenoid is a s trip -lik e bone possessing a m idline ridge
on its ve n tra l face (Fig. 7 .2 b ). I t fo rm s th e p o ste rio r base o f th e neurocranium and
runs caudally, ve n tra l to th e prootics and basioccipital (Figs. 7.1a and 7 .2 b ).
The
o tic
region
com prises
th e
sphenotics,
p te ro tics,
p arietals,
prootics
and
epioccipitals. D orsally, th e sphenotic fo rm s th e a n te ro la te ra l p ortion o f th e bony
n eurocranium
v e n tra lly
bearing
tw o
tu b e -lik e
sw ellings
th a t
are
directed
v e n tro ca u d a lly (Fig. 7 .1 a ). The a n te ro ve n tra l m argin o f th e sphenotic is attached to
th e p o ste rove n tra l face o f th e ro stru m by th ic k connective tissue. The sphenotic
along w ith p rootic and p te ro tic bones b o rde r th e large suspensorial a rtic u la r facet
(Fig. 7 .2 b ). The p te ro tic fo rm s th e lateral brace o f th e neurocranium
and its
a n te rio r p a rt, i.e. th e d e rm o -p te ro tic , is fused to th e a n te ro ve n tra l edge o f its
p o ste rio r p a rt, i.e. th e a u to -p te ro tic . L a te ro ve n tra lly, it bears a v e n tra lly directed
process (Fig. 7 .2 b ).
The epioccipitals fo rm th e ro o f o f th e skull along w ith parietals (Fig. 7 .2 a ). The
p o ste rio r parts o f epioccipitals are curved v e n tra lly and c o n trib u te to fo rm the
spherically shaped p o s te rio r wall o f th e neurocanium (Figs. 7.1a and 7 .2 a ). The
posterom edial corners o f these bones are positioned betw een th e tw o exoccipitals
bones. The prootics fo rm th e ve n tra l m idsection o f th e neurocranial flo o r and
la te ra lly are connected to th e p te ro tic and sphenotic. A foram en is present on the
lateral m argin o f th e p rootic (Fig. 7 .2 b ).
The occipital region com prises th e exoccipitals and basioccipital. This region is not
excavated fo r m uscle insertion as A nguilloidei. The foram en m agnum is bordered
d o rsally and la te ra lly by th e exoccipitals and epioccipitals, and v e n tra lly by the
basioccipital (Fig. 7 .2 a ). The exoccipitals are dom ed to w a rds th e foram en m agnum .
The exoccipitals are extended v e n tra lly to c o n trib u te to th e ve n tra l surface o f the
n eurocranium and is situated betw een th e basioccipital and p o s te rio r p o rtion o f the
p te ro tics (Fig. 7 .2 b ). I t bears a large foram en on its ve n tra l face. The basioccipital
p o ste rio rly fo rm s th e occipital condyle (Fig. 7 .2 b ).
The m a xilla ry is a th in b u t e x tre m e ly elongated bone, connected p o ste rio rly to the
p o ste rio r depression o f th e m andíbula th ro u g h th e m a x illo -m a n d ib u la r lig a m e n t
(Fig. 7 .1 b ). The a n te rio r ends o f th e m a x illa r is are interconnected a t the m idline ,
113
7 H eAd MoRphoLoqy of t Iie P e U can EeL
and lie ve n tra l to th e neurocranium . They are connected to th e a n te ro ve n tra l
m argin o f th e ca rtila g ino u s rostrum by a broad ligam entous sheet th a t also la te ra lly
attaches to th e anterodorsal edges o f th e m a xillarie s and th e lateral tendon o f the
le va to r arcus palatini m uscle (Fig. 7 .3 a ). The co n figu ra tio n o f th e m a xillarie s as well
as th e ir connections to each o th e r and to th e neurocranium is unique, even fo r
A n g uillifo rm e s. The m a x illa ry bears num erous sm all te e th
on
its ve n tra l and
anterodorsal faces. The elongated m andíbula consists o f th e fused d e n ta ry , angular,
a rtic u la r and re tro a rtic u la r. I t bears a depression on its anterom edial face w ith
num erous sm all te e th on its dorsom edial rim (Fig. 7 .1 ).
The
Suspensorium
is
directed
ca u d o ve n tra lly
and
consists
of
an
e x tre m e ly
elongated hyom andibula and q u adrate bones (Fig. 7 .1 a ). The suspensorial bones
are elongated ca rtila g n o us rods covered w ith a th in layer o f perichondral bone. The
hyom andibula bears a ridge a t th e m idline o f its m edial face and a ridge on its
dorsolateral face (Fig. 7 .1 a ). A n te ro la te ra lly , it bears a depression th a t serve as the
insertion face o f th e lateral fib e rs o f th e le v a to r arcus p a latini. The hyom andibula
a rticu la te s w ith th e neurocranium via a single a rtic u la r condyle (Fig. 7 .1 a ). Its
dorsom edial face is connected to th e ve n tra l face o f th e p te ro tic by th e p te ro tich yo m a n d ib u la r lig a m e nt. The q u adrate
is a tu b e -lik e
bone, connected to the
hyom andibula by a synchondrosis. Thick connective tissue surrounds th is jo in t.
P osteriorly, it bears th e lateral and m edial condyles w hich fits into th e m a n dib u la r
fa ce t o f th e m andíbula (Fig. 7 .1 ). The lateral face o f th e lateral condyle bears a
sm all process o nto which th e lateral m a n d ib u lo -q u a d ra te lig a m e n t inserts (Fig.
7 .3 a ). A sim ila r m edial m a n d ib u lo -q u a d ra te lig a m e n t then connects th e m edial face
o f th e m edial condyle to th e p o ste rio r depression o f th e m andíbula (Fig. 7 .1 b ). The
hyom andibula
and
q u adrate
are
perichondral
ossifications
re ta inin g
a hyaline
ca rtila g ino u s core. The chondrocyte cells o f th is ca rtilage are scattered in its dense
m a trix (Fig. 7 .4 b ).
A th ick, black skin encloses th e buccal c a v ity and contains both derm al and
epiderm al m elanophores. D istrib u tio n o f th e m elanophors is dense in th e epiderm is,
w hereas derm al m elanophors are m ore scattered am ong collagen fib e rs (Fig. 7 .4 a ).
The inte rna l derm is contains a th ic k laye r o f connective tissue. The s tria te d m uscle
114
7 H eAd MoRphoLoqy of t Iie P e U can EeL
fib e rs are present betw een th e e xte rn al and internal d erm is o f skin, running
tra n s v e rs a l^ (Fig. 7.4a).
7 .4 .2 . C ra n ia l m y o lo g y:
The a d d u cto r m andibulae
m uscle com plex o f E. pelecanoides shows e xtre m e
m odifications. I t o riginates m usculously fro m th e a n te rio r face o f th e q u adrate and
inserts th ro u g h a tra n sve rse tendon on th e a n terom edial face o f th e m andíbula
(Figs.
7 .1b and
7 .3 a ). This
m uscle
is unipennate.
No subdivisions could
be
recognized.
The a d d u cto r arcus palatini o rig in ate s m usculously fro m th e ve n tro m e d ia l face o f
th e p ro otic and inserts m usculously on th e anterodorsal rim o f th e m edial face o f
th e hyom andibula (Fig. 7 .3 a ).
The
le va to r arcus
palatini
is th e
largest
m uscle
o f th e
head.
It
o riginates
te n d in o u sly and m usculously fro m th e a n te ro la te ra l m argin o f th e sphenotic, and as
lateral tendon fro m th e o rb ito -e th m o id ca rtilage (Fig. 7 .3 a ). The lateral fib e rs o f
th is
m uscle
inse rt
on
th e
dorsolateral
depression
and
lateral
ridge
o f the
h yo m andibula, and m usculously and te n d in o u sly on th e dorsolateral m argin o f th e
q u ad ra te , ve n tra l to th e a n te rio r portion o f th e a d d u cto r m andibulae m uscle (Fig.
7 .3 a ). The m edial fib e rs o f th e le v a to r arcus palatini inse rt m usculously on the
a n terom edial face o f th e hyom andibula.
The a d d u cto r hyom andibulae
connects
m usculously th e
p o ste rio r face
o f th e
p te ro tic to th e d o rso p o ste rio r edge and dorsolateral rim o f th e m edial face o f the
hyom andibula (Fig. 7 .3 b ). The laterl fib e rs fo rm a separate bundle w hich attaches
te n d in o u sly to th e dorsal tendon o f th e a n te rio r depressor m andibulae m uscle (Fig.
7.3a).
E u ryp h a ryn x pelecanoides also bears tw o novel cephalic m uscles th a t have no
e q u iva le n t in o th e r fishes, as fa r as we know. Based on th e ir insertions, th e y are
considered as an a n te rio r and p o ste rio r depressor m andibulae m uscle (Fig. 7 .3 a ).
The
a n te rio r
depressor
m andibulae
m uscle
o rig in ate s
te n d in o u sly
fro m
the
ve n tro m ed ia l face o f th e p te ro tic and inserts on th e a n te rio r edge o f th e m andíbula,
via a slender but long, sesam oid bone (Fig. 7 .3 a ). A n te rio rly , th is sesam oid bone is
connected
m usculously and te n d in o u sly to th e a n te rio r depressor m andibulae
115
7 H eAd MoRphoLoqy of t Iie P e U can EeL
m uscles and
p o ste rio rly, to
a s trip -lik e
lig a m e n t th a t d is ta lly
runs o ve r the
a rtic u la to ry head o f th e qu ad ra te before inserting on th e a n te rio rm o s t edge o f the
m andíbula. As such, th e qu ad ra te head fu n ctio n s as a pulley fo r th is a n te rio r
depressor m uscle. The p o s te rio r depressor m andibulae m uscle is a sm all and sh o rt
bundle th a t o rig in ate s te n d in o u sly fro m th e la te ro ve n tra l face o f th e sphenotic and
inserts as a tendon on th e a n te rio r portion o f th e above m entioned sesam oid bone
(Fig. 7 .3 a ). The tendon o f th e p o ste rio r depressor m andibulae m uscle runs inside
th e m uscle bundle and attaches to th e a n te rio r p a rt o f th e sesam oid bone.
Laterally, th e epaxial m uscles are covered w ith a m uscle sheet w ith its a n te rio r
fib e rs inserting te n d in o u sly on th e la te ro ve n tra l process o f th e p te ro tic (Fig. 7 .3 ).
The rest o f th e epaxial m uscles in se rt te n d in o u sly on th e p o ste rio r m argin o f th e
parietals and m usculously on th e e n tire face o f th e epioccipitals. The hypaxial
muscles inse rt te n d in o u sly on th e a n te ro ve n tra l face o f th e basioccipital (Fig. 7 .3 ).
7 .5 . D iscussion:
Nelson (2 0 0 6 ) considered th e Saccopharyngoidei as com prising "pe rh a ps th e m ost
a n ato m ica lly m odified o f all v e rte b ra te species". In co n tra s t to o th e r anguilliform is,
th e m o n otypic E urypharyngidae bear a g re a tly enlarged m outh resulting fro m an
extensive elongation o f th e Suspensorium and ja w s (B e rtin , 1934; T chernavian,
1947). The loosely-hinged
m outh
is covered
by a th ic k ,
black skin th a t can
w ith sta n d an e xtensive d istending o f th e buccal ca vity. The skull o f E. pelecanoides
reflects
som e
paedom orphis
fe a tu re s,
such
as th e
unossified
o rb ito -e th m o id
cartilage and th e su p erficia lly ossified skull ro o f bones. This condition is s im ila r to
th a t found in th e Saccopharyngidae and M onognathidae (Nielsen and Bertelsen,
1985; Bertelsen and Nielsen, 1987). The unossified ro stru m o f E. pelecanoides
possesses a unique shape resem bling th a t o f th e Early Devonian a ctin o p te ryg ia n ,
D ialipina (S chultze and Cum baa, 2001).
The hyom andibula o f E. pelecanoides a rticu la te s w ith th e neurocranium via a single
a rtic u la r condyle th a t provides its freedom fo r fo rw a rd and backward m ovem ents.
The qu ad ra te is probably fused to th e sym p le ctic because d orsally it is connected to
th e hyom andibula by a synchondrosis and not th ro u g h an in te rd ig ita tin g su tu re as
in o th e r a n g u illifo rm species. The p rim itiv e te le o st condition o f th e hyom andibula is
116
7 H eAd MoRphoLoqy of t Iie P e U can EeL
to be connected only w ith th e sym p le ctic th ro u g h a sim ple synchondrosis (Forey e t
a l., 1996).
In co n tra s t to th e general condition in A n g u illifo rm e s, th e Suspensorium and the
attached m uscles, such as th e le v a to r arcus palatini and a d d u cto r hyom andibulae
m uscles, c o n trib u te to closing and opening o f th e ja w s (ra th e r than o nly add-and
abducting o f th e Suspensorium ). Such a s itu a tio n can show th a t co n stru ction s have
th e p otential to serve purposes o th e r than th e fu n ctio n fo r w hich th e y are designed
(D u lle m e ije r, 1991; Gould and Vrba, 1982). Hence, these elem ents can be called
upon to serve a new purpose.
I t is d iffic u lt to hom ologize som e cranial elem ents o f E. pelecanoides w ith those o f
A n g uillifo rm e s. The hom ology o f th e a n te rio r and p o ste rio r depressor m andibulae
muscles is th e su b je ct o f co njecture. T h e ir co n fig u ra tio n and fu n ctio n are unique
com pared to those o f o th e r anguilliform is, hence th e y p robably are novel cephalic
muscles. On th e o th e r hand, based on th e tra d itio n a l nam ing system
a d d u cto r m andibulae
m uscles (V e tte r,
1878; W interbottom i,
1974;
o f the
Nakae and
Sasaki, 2 0 0 4 ), th e y m ay be hom ologues w ith one o f th e A2 sections o r subsections
o f th e a d d u cto r m andibulae m uscle com plex b u t w ith the insertion site having
m igrated to th e a n te ro la te ra l face o f th e m andíbula.
Because o f th e g re a t depths a t w hich E. pelecanoides lives, aspects o f its behavior
are largely th e su b je ct o f speculation. How ever, its head m usculoskeletal system
s tro n g ly suggests th e capacity to e n g u lf prey by its enorm ous m outh (Nielsen e t al.,
1989). Nielsen e t al. (1 9 8 9 ) rejected sw im ing w ith a open m outh to w a rds a prey
item in E. Pelecanoides because o f its narrow gili opening. In ste a d , Nielsen e t al.
(1 9 8 9 ) proposed th a t E. Pelecanoides w ould open its huge m outh a t a sh o rt
distance fro m th e prey, less than its ja w length, a fte r a fo rw a rd tru s t w ith the
closed jaw s. Based on Nielsen e t al. (1 9 8 9 ), E. Pelecanoides opens its m outh by
slackening th e a d d u cto r m andibulae and fu rth e r by th e pressure o f th e w a te r
caused by th e fo rw a rd m o ve m e n t o f th e head like a parachute. In th is assumed
w ay o f fe e d in g , th e ja w m uscles close th e m outh slow ly by bringing a tria n g u la r lid
form ed by th e bones o f th e low er ja w and th e elastic skin streched betw een them
(Fig, 7 .5 ).
117
7 H eAd MoRphoLoqy of t Iie P e U can EeL
Based on th e cephalic m usculoskeletal system and a broadcasted sh o rt footage o f a
feeding pelican eel in th e BBC d o cu m e n ta ry series (Blue planet: Eposide2 - The
Deep, 2 0 01 ), th e skin o f E. pelecanoides appears to be a loose flap when th e m outh
is still closed. A fte r de te ctin g th e prey, E. pelecanoides opens its m o u th , which can
be realized by th e co n tra ction o f th e a n te rio r and p o s te rio r depressor m andibulae
muscles, until th e m andíbula lies a t a horizontal level. The lateral bundle o f the
a d d u cto r hyom andibulae could also co n trib u te to depress th e m andíbula because of
its a tta ch m e n t to th e a n te rio r depressor m andibulae m uscles. A t th e sam e tim e , the
le va to r arcus palatini m ay p ro tra c t th e long Suspensorium to a lm o st fo rty five
degrees. In a d d itio n , th e co n tra ction o f th e lateral fib e rs o f th e le v a to r arcus
palatini m uscle can abduct th e Suspensorium to distend th e buccal cavity.
Then th e a n te rio r and p o s te rio r depressor m andibulae and le v a to r arcus palatini
m uscles can continue to open th e huge m outh and synchronously, th e epaxial
m uscles elevate th e head. In th is stage, th e m outh opening is re stricte d m a in ly to a
depression o f th e low er ja w , w here E. pelecanoides opens its m outh until it m akes
n early a rig h t angle w ith th e suspensorial axis. M eanwhile, all loose skin around the
m outh becomes stretched and p a rticip a te s to fo rm an expanded buccal ca vity.
A fte r th a t, E. pelecanoides th ru s ts its head to w a rds th e prey w ith th e m outh
opened. In th is w ay th e prey and th e w a te r su rrou n d in g it m aw be enclosed in the
buccal ca v ity by th e fo rw a rd m o ve m e n t o f th e head. The lateral fib e rs o f th e epaxial
m uscles th a t inse rt as a tendon on th e v e n tro la te ra l process o f th e p te ro tic m ay
play a role to fix th e position o f its sm all head a t a horizontal position during
opening o f th e large m outh o r m oving to w a rds th e prey w ith opened m outh.
A fte r en gu lfin g o f th e prey, th e a d d u cto r m andibulae m uscle m ay elevate th e low er
ja w to close th e m outh. The co n figu ra tio n o f th e a d d u cto r m andibulae m uscle,
being unipennate and w ith s h o rt fib e rs connecting to a long te n d o n , probably
provides an advantage fo r forceful closing o f an e xtre m e long low er ja w and
avoiding th e engulfed
prey fro m
escaping. A unipennate m uscle w ith a large
pennation angle and s h o rte r m uscle fib e rs has th e positive e ffe ct o f allow ing m ore
m uscle fib e rs to a ttach along th e tendon plate, th e re b y e xe rtin g g re a te r co n tra ctile
forces (N arici and M agnaris, 2006).
118
7 H eAd MoRphoLoqy of t Iie P e U can EeL
A fte r closing th e large m o u th , th e a d d u cto r hyom andibula m uscle m ay bring the
Suspensorium back to its s ta rtin g position and th e a d d u cto r arcus palatini m uscle
adducts th e Suspensorium m edially. R eturning th e long Suspensorium to its s ta rtin g
position m ay also bring th e m andíbula backw ard. Most probably, m outh closure is
slow because o f th e h ig h ly force in e fficie n t lever system o f th e elongated ja w .
D uring slow m outh closure, little engulfed w a te r w ould then be expelled. The
vo lu m e o f th e buccal ca v ity then is g ra d u a lly reduced sieving o u t th ro u g h the
narrow gili opening by closing th e long Suspensorium and ja w s and by co ntraction
o f th e elastic skin around th e m outh. The la tte r is possible when th e m uscle fibers
inside the skin around th e buccal ca v ity co n tra c t and re tu rn skin to its resting state
(Fig. 7.4a).
Nielsen e t al. (1 9 8 9 ) pointed o u t th a t food item s sta y in th e ve n tra l pouch o f the
buccal ca v ity fo r a w hile
before
en te rin g
th e
stom ach
as seen
in th e
BBC
d o cu m e n ta ry series (Blue planet: Eposid2 - The Deep, 2001) (Fig, 7 .6 ). The prey
then
probably
is covered
w ith
a secretion
o f th e
g la n d u la r (w ith
acidophilic
proteinaceous g ranules) and m ucous g o ble t cells th a t co ver a pale area on th e
ve n tra l side o f hypaxial m uscles th a t run fro m th e m outh opening to th e esophagus
(Nielsen e t a l., 1989).
The tra p p ed prey w ill be tra n sp o rte d to th e heavily folded esophagus, th a t has a
co lu m n a r e p ithe liu m on th e to p o f th e ridges and num erous u n ice llu la r glands
(Nielsen e t a l., 1989), and subsequently to an expandable stom ach (N ubaum H ilarow ics, 1923; Nielsen e t a l., 1989). The co n tra ction o f th e skin around the
m outh using th e m uscle fib e rs o f the th ic k skin a fte r m outh closure w ill help to
conduct th e prey to th e esophagus and subsequently to th e stom ach (N ubaum H ilarow ics, 1923).
This stu d y based on head m orph o log y o f E. pelecanoides and an observation o f the
live anim al revealed th a t those p reviously assum ed feeding stra te g ies based on
solely m orphological data, does not correspond w ith those we proposed except fo r
keeping food item s in th e ve n tra l pouch o f m o u th , co n tra ction process o f th e elastic
skin around th e m outh and tra n s p o rtin g food to th e heavily folded esophagus.
How ever, th is s tu d y cannot re je c t th e p o ssib ility o f th e assum ed feeding s tra te g y o f
E. pelecanoides.
119
7 H eAd MoRphoLoqy of t Iie P e U can EeL
A CK N O W LE DG M ENTS
The a u th o rs w ould like to th a n ks P. P ru v o s t (Musée National d 'H istoire Naturel o f
Paris) and
P.
U n ive rsity)
fo r
R.
M o lle r
providing
(N atural
m useum
H istory
Museum
specim ens, J.
o f D enm ark,
G.
Nielsen
Copenhagen
(N atural
H istory
Museum o f D enm ark, Copenhagen U n ive rsity) fo r p roviding valuable references, T.
G e e rin c k x (G hent U n ive rsity) fo r his valuable com m ents.
120
ChApTER 8
G
eneraI
D
ís c u s s ío n
8 G
eneraI
D
ís c u s s ío n
C h a p te r e ig h t
G e n e ra l D iscussion
The m a jo r fe a tu re o f life's h isto ry is a legacy o f perpetual change. Despite an
a p pa re n t perm anence o f th e natural w orld , change characterizes all th in g s on earth
and produces various fo rm s o f life. U nderstanding th e d iv e rs ity o f life as th e result
o f e vo lu tio n can help to understand th e historical processes th a t generate and
m aintain
species d iv e rs ity
and
a d ap tatio n s th ro u g h
e v o lu tio n a ry
h isto ry.
The
e vo lution o f th e cranial m usculoskeletal system in anim als is an exce lle nt case
stu d y o f th e w ay fo rm changes in relation to change in fu n ctio n al dem ands w ith in a
c o n te xt o f a changing
e n viro n m e n t.
It
reflects th e
p la s tic ity
o f e v o lu tio n a ry
processes, in how s tru ctu re s th a t are used in a certain w ay can be rem odeled to
m eet changing fu n ctional re q uire m en ts. The feeding apparatus in association w ith
th e hyoid arches, Suspensorium and gili arches and th e ir associated m uscles is to
be expected to be stro n g ly involved in these changes.
8 .1 . E v o lu tio n a ry p a tte rn o f s tru c tu ra l ch a n g e s in th e h ead m u s c u lo s k e le ta l
s y s te m
The
goal
o f th is
stu d y
is to
explore
th e
stru ctu ra l
d iv e rs ity
o f th e
cranial
m usculoskeletal system in A n g uillifo rm e s. By in te g ra tin g th e obtained data w ith
data
fro m
lite ra tu re
can
also
unravel
e v o lu tio n a ry
p a tte rn s th a t explain
th e
observed changes in th e head m usculoskeletal system . S tru ctu ra l changes, as an
a d aptation
to
a changing
fu n ctio n
o r e n v iro n m e n t,
could
be constrained
by
ancestral co n dition. Hence, know ing th e ancestral o r p rim itiv e condition o f th e head
m orph o log y is especially im p o rta n t to explore e v o lu tio n a ry changes fro m th e re on
w ith th e resulting d iv e rs ity in th e A n g uilliform es.
Regan (1 9 09 , 1912) recognized th e A nguilloides (A poda) as d is tin c t fro m o th e r eel­
like fishes based on th e absence o f separate pre m a xilla ries, which are united w ith
th e v o m e r and th e eth m o id into a p re m a xillo -e th m o vo m e ra l com plex. How ever, in
121
8 G
eneraI
D
ís c u s s ío n
some cases th e v o m e r is present as a separate bone (M arshall, 1962) such as in
th e
H eterenchelyidae and Synaphobranchidae.
Some researchers consider th is
separate v o m e r in som e a n g u illifo rm fa m ilie s as an autogenous vom eral to o th
plate, w hereas th e (to o th less) vom eral bone its e lf is then included w ith in th e
com plex (D. Johnson, S m ithsonian m useum : personal co m m un ica tion s). However,
th is needs fu rth e r inve stig a tio ns. This p re m a xillo -e th m o vo m e ra l com plex lim its the
m o b ility o f th e upper ja w elem ents, and in m any a n g u illifo rm lineages is associated
w ith a considerably enlarged ja w a d d u cto r m usculature. Hence, an a d aptation to a
p re d a to ry w ay o f life has been assum ed (G egory, 1933; Gosline, 1971). Fusion o f
th e eth m o id bone into a p re m a xillo -e th m o vo m e ra l com plex is also a syn apom orphy
o f recent A n g uillifo rm e s (Belouze, 2 0 01 ).
How ever, th e lateral process o f the
p re m a xillo -e th m o vo m e ra l com plex in B a thym yrinae and M uraenesocidae has been
in te rp re te d as fused lateral eth m o id s (Belouze, 2001).
Jaw e lo n g a tio n :
The sh o rt rostral (a n te ro -o rb ita l) region is th e plesiom orphic state o f A n g uillifo rm e s,
as seen in H eterocongrinae and Colocongridae (Belouze, 2 0 01 ). How ever, d iffe re n t
e v o lu tio n a ry p a tte rn s have resulted in ja w elongation in A n g uillifo rm e s. A firs t
p a tte rn involves th e elongation o f th e p re m a xillo -e th m o vo m e ra l com plex, as seen
in th e C yem atidae, N em ichthyidae, S e rrivom eridae and N ettastom atidae. These
rapacious feeders display considerable e n la rg e m e n t o f th e te e th and ja w s (C astle,
1968).
For
instance,
th e
dentig e ro us
areas
are
enlarged
by
th e
fo rw a rd
p rolongation o f th e sn o ut (p re m a x illo -e th m o v o m e ra l co m p le x), as seen in th e
n e tta sto m a tid H oplunnis p u n cta ta . This can be linked to som e advantages, such as
providing
m ore
space
fo r th e
o lfa c to ry
ro se tte ,
but also
increasing
v e lo city
advantage (b itin g speed) and reducing drag (see ch a p te r 3). These a d ap tatio n s can
im prove th e prey capture kinem atics o f th is benthopelagic, b ite r predator. Also, the
larg e r a d d u cto r m andibulae m uscle com plex o f H. p u n cta ta (N e tta s to m a tid a e ),
com pared to th a t o f S e rriv o m e r sp. (S e rrivo m e rid a e ) and N em ichthys scolopaceus
(N e m ich th yid a e ), indicates th a t forceful bitin g a t th e p o ste rio r p a rt o f th e ja w s
122
8 G
eneraI
D
ís c u s s ío n
(b itin g o f fa irly la rg e r prey) m ig h t be fa vo re d, a b e ne fit fo r H. p u n c ta ta th a t feeds
on larg e r benthic preys (S m ith , 1989b).
As a second p a tte rn o f ja w elongation in A n g u illifo rm e s, th e m outh has become
enlarged by a backward elongation o f th e m andíbula coupled to a p o s te rio r position
o f th e q u a d ra te -m a n d ib u la jo in t, tiltin g th e suspensorial axis into a backw ardlyoblique
angle
as
(M uraenidae),
seen
Ily o p h is
in
A narchias
b runneus
a lla rd ice i
and
and
G ym n o th o ra x
S ynaphobranchus
p rasinus
b re vid o rsalis
(S yn a ph o b ran ch id ae ), K aupichthys hyo pro ro id e s (C hlopsidae) and M yrophis va fe r
(O p h ichthid a e). This m o dification is associated w ith a large, no ncircu la r m outh gape
th a t enables v e ry large prey to be seized and devoured. This p a tte rn o f ja w
elongation can provides a fa s t b ite, w ith o u t increasing th e distance betw een the
pharyngeal ja w s and th e tip o f oral ja w s. The gili arch m orph o log y o f these species
w ith such a ja w elongation shows th e p otential to tra n s p o rt food item s in th e buccal
ca vity (see below ).
Hence, th is p a tte rn o f ja w elongation
in A n g uillifo rm e s is
probably linked to th e presence o f a h ig h ly specialized m echanical tra n s p o rt system
but needs fu rth e r investigations.
A
th ird
p a ttern
of
ja w
elongation
is
seen
in
E u ryp h a ryn x
pelecanoides
(E u ryp ha ryn g id a e ), resulting fro m an extensive elongation o f th e Suspensorium and
th e ja w s (B e rtin , 1934; Tchernavian, 1947). The hyom andibula o f E. pelecanoides
a rticu la te s w ith th e neurocranium via a single a rtic u la r condyle th a t provides its
freedom fo r fo rw a rd and backward m ovem ents, w hereas th e hyom andibula o f o th e r
A n g uillifo rm e s d o rsally bears tw o a rtic u la r condyles, as in m ost teleosts. As a
re sult, th e m o ve m e n t o f th e Suspensorium is re stricte d to m e d io -la te ra l ro ta tio n s
only. S till, even in those cases, som e s tru c tu ra l v a ria tio n exists a t th e level o f these
a rticu la tio n s , as fo r exam ple th e p o ste rio r a rtic u la r condyle in A narchias a lla rd ice i
and G ym n o th o ra x pra sin u s (M uraenidae), Ily o p h is b runneus and S ynaphobranchus
b re vid o rsalis
(S yn a ph o b ran ch id ae ),
is
longer
anguilliform is (see chapters 5 and 6).
123
com pared
to
th e
one
in
o th e r
8 G
eneraI
D
ís c u s s ío n
Suspensoria! m o d ific a tio n s :
W ith respect to th e Suspensorium , th e long quadrate o f E. pelecanoides probably is
d o rsally connected to th e hyom andibula by a synchondrosis and not th ro u g h an
in te rd ig ita tin g
su tu re
as
in
o th e r
a n g u illifo rm
species.
The
p rim itiv e
te le o st
condition is fo r th e hyom andibula to be connected only w ith th e sym p le ctic th ro u g h
a sim ple synchondrosis (Forey e t al., 1996). In m ost eels th e sym p le ctic is not
p resent as a separate
bone, w hereas only a d is tin c t ca rtila g ino u s
processus
sym plecticus on th e hyom andibula can be observed in eel larvae (N orm an, 1926;
Tesch, 2003). C onsequently, it has already been suggested th a t a sym p le ctic bone
in A n g uillifo rm e s has becom e fused w ith th e hyom andibula o r th e qu ad ra te (Leiby,
1981). The sym p le ctic could be found as a fused bony p ortion a t th e p o s te rio r p a rt
o f th e
q u adrate
in P yth onichthys m a cruru s
(N e tta s to m a tid a e )
o r as a sm all
ca rtila g ino u s p a rt in H oplunnis p u n c ta ta (H ete renchelyidae). Also, a cartilaginous
sym p le ctic has been described p o s te rio r to th e quadrate in H ete roco n g er hassi
(C ongridae) (De Schepper, 2007).
W ith respect to th e suspensorial m u sculature, and in relation to th e elongated ja w s
in E. pelecanoides (E u ryp ha ryn g id a e ), th e suspensorial m uscles c o n trib u te to a
closing and opening o f th e ja w s (ra th e r than o n ly ad- and abducting o f the
S uspensorium ),
in co n tra s t to
th e
general condition
in A g u illiform e s.
Such a
situ a tion in E. pelecanoides can show th a t such a fe a tu re has th e potential to serve
purposes o th e r than th e ancestral fu n c tio n , fo r w hich it is adapted (D u lle m e ije r,
1991). These elem ents can then be called upon to serve a new purpose (Gould and
V rba, 1982). Also, in E. pelecanoides, it is d iffic u lt to hom ologize som e o th e r cranial
elem ents w ith those o f o th e r anguilliform is. The v e ry d is tin c t cranial m orph o log y o f
E. pelecanoides is already d is tin c t fro m th e leptochalus larval stage, w ith an oblique
m outh gape, a long low e r ja w , and v e ry long patch o f th in te e th e xtending fo rw a rd
fro m th e to p o f th e upper ja w (M iller, 2009) (Fig. 8 .1 ).
D e n titio n p a tte rn s :
Tooth
m orph o log y o f A n g u illifo rm e s
m ay re fle ct differences
in prey ca p tu rin g
behavior. For instance, te e th can be large, sharp and piercing like those o f H.
124
8 G
eneraI
D
ís c u s s ío n
p u n cta ta
(N e tta s to m a tid a e ),
(S im enchelyinae).
The
long
or
and
ch ise l-like
sharp
as
te e th
in
on
S im enchelys
th e
a n te rio r
p a rasiticu s
p a rt
of
the
n eurocranium in m ost a n g u illifo rm fa m ilie s m ay be used to im pale prey and are
useful fo r prey holding.
S. p a rasiticu s d iffe rs fro m o th e r a n g u illifo rm species in
having ch ise l-like te e th . The cu ttin g edge and b la de-like te e th o f S. pa ra siticu s on
th e p re m a xillo -e th m o id a l com plex, m a xilla ry and low er ja w , along w ith th e enlarged
a d d u cto r m andibulae m uscle com plex m ay be em ployed to shear and rem ove a
chunk
o f flesh
fro m
larg e r
prey,
ju s t
like
using
scissors
(see
ch a pte r
5).
E u ryp h a ryn x pelecanoides (E u ryp ha ryn g id a e ) and N. scolopaceus (N em ich th yida e )
bear num erous sm all te e th on th e ir ja w to o th bands. In species w ith long ja w s,
such as H. p u n c ta ta (N e tta s to m a tid a e ), S e rriv o m e r sp. (S e rrivo m e rid a e ) and N.
scolopaceus (N e m ich th yid a e ), th e to o th rows o f th e ja w s extend fu rth e r p o ste rio rly,
th u s increasing th e fu n ctio n al capacity o f th e ja w system fo r grabbing prey. Biting
w ith th e p o ste rio r te e th
is also advantageous because hig h e r bite forces are
produced (H errei e t a l., 2002).
S uction feeding versus b itin g :
Sim enchelys p a ra siticu s and H ete roco n g er hassi are tw o exam ples o f anguilliform is
th a t m ay rely on suction forces du rin g feeding. In these tw o species w ith sh o rt ja w ,
th e h yo m an d ibu la -qu a d rate axis is tilte d fo rw a rd ly and th e a n te rio r p a rt o f the
Suspensorium
is extended
fo rw a rd .
In
a d ditio n ,
th e y
bear a w ell-developed
p a la to p te ryg o id connected a t its ends to th e neurocranium and th e quadrate. Such
a co n figu ra tio n m ay be related to th e ir a b ility to produce suction by providing m ore
room fo r th e oral ca v ity (h o w e ve r, kine m a tic studies to su p p o rt th e hypotheses of
suction feeding still need to confirm th is ) (see c h a p te r 3 and 5). These tw o species
also bear w ell-developed ve n tra l m uscles o f th e head, which m ay confirm the
im portance o f producing suction. Large ve n tra l m uscles in S. p a rasiticu s, including
th e p ro tra c to r hyoidei and ste rn o hyo id eu s, suggest th e a b ility to v e n tra lly expand
th e buccal ca v ity m ore, hence producing suction forces (Lauder, 1985; De Visser
and
Barel,
W a in w rig h t,
1998;
C arroll,
2 007b;
2 0 04 ;
Konow
and
Sanford
and
S anford,
125
W a in w rig h t,
2008).
I
2002;
speculate
Mehta
th a t
and
these
8 G
eneraI
D
ís c u s s ío n
specializations o f S. p a ra siticu s m ay be beneficial fo r creating h ig h e r suction forces
to attach to its prey, th e re b y assisted by its fle sh y lips (see ch a pte r 5).
The a d d u cto r m andibulae m uscle com plex o f A n g uillifo rm e s shows va ria tio n in size,
com ponents and insertion sites. Some A n g uillifo rm e s possess sm all ja w muscles
(e .g ., H ete roco n g er h assi), w hereas oth e rs have s u b s ta n tia lly enlarged ones (e .g .,
H oplunnis p u n c ta ta , C onger conger, S im enchelys p a rasiticu s and G ym n o th o ra x
pra sin u s). Enlarged a d d u cto r m andibulae m uscles m ay allow a pow erful bite by
increasing
th e
m echanical
load
on
skeletal
elem ents
such
as
m andíbula,
suspensoria and neurocranium (H errei e t a l., 2 0 02 ; Van W assenbergh e t a l., 2004).
A
p re da to ry
life
style
is
considered
th e
plesiom orphic
A n g u illifo rm e s (G osline, 1971; S m ith , 1989a), w ith
condition
h yp ertrop h ied ja w
fo r
the
muscles
being com m on (Böhlke e t a l., 1989) and th is suggest a derived condition o f H.
hassi.
Jaw m u scu la tu re :
The A2 and A3 sections o f the a d d u cto r m andibulae m uscle com plex are oriented
ca u d o ve n tra lly in som e a n g u illifo rm fa m ilie s, such as m uraenids, m o ringuids and
syn a p h o b ra n ch u s. A ca u d o ve n tra lly oriented m uscle can pull th e m andíbula upward
and fo rw a rd and re d is trib u te forces, i.e. little re s u lta n t force im pacts th e jo in t. An
opposite o rie n ta tio n o f th e d iffe re n t sections o f th e a d d u cto r m andibulae m uscle
com plex (ca u d o ve n tra lly versus a n te ro v e n tra lly ) can also help in p re venting the
dislocation o f th e m a n d ib u la r jo in t, even when large forces are exerted th a t induce
to rq u e forces (De Schepper e t a l., 2007a) (Fig. 8 .2 ).
The insertion site o f th e ja w m uscles d iffe r based on th e low er ja w co n figurations.
In n e tta sto m id s w ith long ja w s , th e m uscles inse rt on th e p o ste rio r portion o f the
m andíbula, w hereas in m uraenids these m uscles' insertion sites are enorm o u sly
expanded on th e p o s te rio r h a lf o f th e m andíbula.
A narchias a lla rd ic e i and G ym n o th o ra x pra sin u s (M uraenidae) show an a d du ctor
m andibulae
m uscle
com plex
w here
m uscle
mass
is
h yp ertrop h ied .
The
hyp ertrop h ied a d d u cto r m andibulae m uscle com plex can be expected to be ve ry
e fficie n t fo r bitin g and im paling th e prey. These m uraenids also bear a large and
126
8 G
eneraI
D
ís c u s s ío n
elevated supraoccipital crest, to increase th e insertion area fo r th e ja w m uscles (De
Schepper, 2 0 07 ). How ever, A riosom a g ilb e rti (B a th y m y rin a e ), w ith s m a lle r ja w
muscles, even lacks th e supraoccipital bone. Along w ith th e h yp ertrop h ied a d du ctor
m andibulae m uscle o f m uraenids, neurocranial elem ents, such as th e p re m a xillo e th m o vom e ra l com plex and parasphenoid, are deep and robust. This m ay help in
resisting th e generated hig h e r im pact forces during prey grabbing and b itin g (see
ch a pte r 6).
Based on th e te rm in o lo g y o f W interbottom i (1 9 7 4 ) and th e tra d itio n a l nom enclature
used fo r th e a d d u cto r m andibulae m uscles (V e tte r, 1878; W interbottom i, 1974;
Nakae and Sasaki, 2 0 0 4 ), all in th is s tu d y exam ined species only have th e A2 and
A3 sections o f th e a d d u cto r m andibulae m uscle com plex. The absence o f th e A Í is
to be expected, because A n g uillifo rm e s lack a m obile upper ja w .
A section A Í has
been reported in M oringua ed w a rd si and Pisodonophis boro (De Schepper e t al.,
2005, 2007a).
Epaxia! m u scu la tu re :
The epaxial m uscles also show q u ite som e va ria tio n
in th e ir insertion to the
n e uro cra n iu m , even w ith a d ire c t a tta c h m e n t o nto th e ja w m uscles in anguilliform is.
In p rim itiv e te leosts th e epaxial m uscles inse rt la te ra lly w ith in th e roofed and
unroofed posttem poral fossa and m e d ia lly on th e rear o f th e neurocranial wall
(Forey e t al., 1996). In A n g uilifo rm e s th e y also in se rt on th e p o ste rio r w all, but in
eels w ith large ja w m uscles, such as th e M uraenidae and H eterenchelyidae, the
epaxial m uscles also attach te n d in o u sly o r fa scia lly to th e ja w muscles. The large
insertion sites o f th e epaxial muscles and its fu n ctio n al coupling to ja w m uscle
co n tra ction are considered an advantage fo r tra n s fe rrin g forces fro m th e body onto
th e head during h e a d -firs t bu rro w ing o r d u ring ro ta tio n a l feeding (H elfm an and
C lark, 1986). F u rtherm ore, th e epaxial muscles probably c o n trib u te to elevate th e
neurocranium during m outh opening in som e A n g uillifo rm e s. In E urypharyngidae
th e epaxial m uscles la te ra lly bear a m uscle sheet th a t w ith its a n te rio r fibers inserts
te n d in o u sly on th e la te ro ve n tra l process o f th e p te ro tic bone. This novel, lateral
127
8 G
eneraI
D
ís c u s s ío n
fib e rs o f th e epaxial m uscles m ay play a role in stabilizing th e position o f its small
head d u ring opening o f th e large m outh (see ch a pte r 7).
O percular series:
The o p ercu la r series is w ell-developed in som e fa m ilie s such as th e Congridae and
A nguillidae. This series also possesses va rio u s shapes and sizes in A n g uilliform es.
The o p ercu la r series is reduced in th e M uraenidae, th e sub- and interopercle are
lost in N em ichthys (N e m ich th yid a e ), w hereas E urypharyngidae lack th e o percular
series as a w hole. Like in o th e r Teleostei, th e o p ercu la r series o f studied species
also co n trib u te s to th e feeding system by th e ir connection to th e m andíbula due to
having th e in te ro p e rc u lo -a n g u la r ligam ents th a t trig g e rin g one o f th e biom echanical
system s to depress th e m andíbula (W estneat, 1990). The p reopercular bone in
m any
a n g u illifo rm
fa m ilie s
su p ports
th e
p re o p e rcu lo -m a n d ib u la r canal
o f the
cephalic lateral line system . This bone also is an insertion site o f the ja w a d ductor,
as observed in m any a n g u illifo rm fa m ilie s. The opercle and subopercle has not
increased in length as th e gili apparatus becam e elongated.
Gili arch m o rp h o lo g y :
S ynapom orphic fo r A n g u illifo rm e s are gili arches th a t are displaced p o ste rio rly so
th a t th e bony connection w ith th e neurocranium no lon g e r exists. This is likely
related to th e
reduction
o f th e
head d ia m e te r (N elson,
1966).
Losses o f an
interconnection betw een th e gili skeleton and th e cranium m ay also be related to
th e
e xp a n s ib ility
of
th e
p h aryn x,
w hich
is
obvious
in
eels.
The
p o ste rio r
displacem ent o f gili arches is s lig h t in C onger co n ge r (C ongridae) and e xtre m e in
G ym n o th o ra x
pra sin u s
(M uraenidae)
and
M oringua
edw ardsi
(M o ringuidae),
w hereas in S im enchelys p a rasiticu s (S im en ch e lyin a e), th e y are positioned beneath
th e neurocranium (see ch a p te r 5).
Respiration o f eels is carried o u t by a ve ry ch a ra cte ristic and strong p u m p-like
action o f th e
branchial cham ber, th e w a te r being forced
o ve r th e gills. The
d e velo p m en t o f a long, n arrow branchial ch am ber m ay fa c ilita te th e re sp ira to ry
process
a d d u cto r
in A n g uillifo rm e s
operculi
and
(Tesch,
d ila ta to r
2 0 03 ).
operculi
128
The w ell-developed
m uscles,
as
well
le v a to r operculi,
as
th e
sh e et-like
8 G
eneraI
D
ís c u s s ío n
hyohyoideus m uscle com plex are th e m ain m uscles th a t p robably serve to expand
and co n tra c t th is long, narrow branchial cham ber o f th e A n g uillifo rm e s. The position
o f th e gili opening
m ay d iffe r fro m
a ve n tra l one
in fossorial species (e .g .,
P yth onichthys m a c ru ru s) to a lateral one in pelagic species like S e rriv o m e r sp.
(S e rrivo m e rid a e ).
The gili arches o f th e A n g uillifo rm e s bear a series o f sm all to o th plates associated
w ith th e fifth ceratobranchials th a t are opposed to th e dorsal to o th plates. The
num erous te e th o f these plates are pointed and long in som e anguilliform is, such as
G. pra sin u s, A. a lla rd ice i (M uraenidae) and K aupichthys h yo pro ro id e s (C hlopsidae).
Nelson (1 9 6 6 ) m entioned th a t on th e basis o f th e nature o f th e te e th and the
branchial m usculature o f som e A n g uillifo rm e s, such as M uraenidae, these to o th
plates a p p a re n tly fu n ctio n in m oving food fro m th e ja w s to th e esophagus. They
have developed in relation to m echanical problem s involved in m oving re la tive ly
large food item s th ro u g h a secondarily elongate p h aryn x (N elson, 1966). Mehta and
W a in w rig h t (2 0 0 7 a ) described the pharyngeal ja w s o f m orays, w here th e y a ctu a lly
d e m on stra ted th a t these ja w s are indeed capable o f tra n s p o rtin g large prey item s
fro m th e oral ja w to w a rd th e esophagus. The presence o f th is m echanical prey
tra n s p o rt system shows th a t despite a backward displacem ent o f gili arches, th e y
still keep th e ir role in m a n ip u la tin g prey.
O ur stu d y showed th a t in Ily o p h is bru nn e u s and S ynaphobranchus bre vid o rsalis
(S yn a ph o b ran ch id ae ), m any s im ila r corresponding m uscle a tta ch m e n ts are present,
ju s t as those
found
in
m uraenids
(see
C hapter 5).
In
I.
b runneus
and
S.
bre vid o rsalis it is claim ed th a t th e capacity to tra n s p o rt food in th e buccal ca vity is
possible, despite having a com plete gili skeleton com pared to a h ig h ly reduced one
in
m uraenids
hyo pro ro id e s
(see
C hapter
(C hlopsidae)
5).
I
exam ined
and S e rriv o m e r sp.
th e
gili
arches
of
(S e rrivo m e rid a e )
K aupichthys
and
observed
stru ctu re s th a t could be associated w ith such a tra n s p o rt system . Hence, it should
be
noted th a t an
co m p ara tive
stu d y
inve stig a tio n
of
Nelson
o f th e
(1 9 6 6 ),
129
gili arches o f A n g u illifo rm e s,
but
also
including
th e
like the
m usculature
8 G
eneraI
D
ís c u s s ío n
a tta ch m e n ts, can help to b e tte r understand th e feeding b ehavior and possible
e vo lu tio n a ry changes o f th is m echanical prey tra n s p o rt system .
Cephalic la te ra l line s y ste m :
Many eels show a se d en tary life style , show ing m any m orphological ad ap tatio n s fo r
th e ir burrow ing b e havior (see C hapter 4 ). Exam ples like sm a lle r eye size, solid
conical skull, w idened cephalic lateral line canals e xtending into th e derm al cavities,
and ve n tra l position o f th e gili openings, as observed in P yth onichthys m a cruru s
(H ete renchelyidae) and M oringua ed w a rd si (M o rin g u id a e ), are considered to be
specializations fo r h e a d -firs t burrow ing (C hapter 4 ). Also, d iffe re n t p a tte rn s in
h e a d -first burrow ing fe a tu re s in H eterenchelyidae and M oringuidae reveal th a t
th e re is m ore than one w ay to re stru ctu re th e skull in relation to h e a d -first
b u rro w ing . For instance, P yth o n ich thys m a cruru s (H ete renchelyidae) bears a rch -like
stru ctu re s, w hich su p p o rt th e w idened p re o p e rcu la r-m a n d ib u la r canal, w here as
th a t o f M oringua ed w a rd si (M oringuidae) lacks these bony stru ctu re s. Also, as an
a lte rn a tive hypothesis, th e w idened cephalic lateral line canals can be used to
d e te ct hidden prey item s in th e sea bed as seen in cichlids and deep sea fishes
(W ebb, 2002).
The cephalic lateral line system o f th e exam ined A n g uillifo rm e s is g e ne ra lly w elldeveloped. I t fre q u e n tly is cavernous and porous and is supported by m any bones
o f th e skull th a t have d iffe re n t shapes w ith in anguilliform is.
For instance, the
p re o p e rcu lo -m a n d ib u la r canal in som e A n g u illifo rm e s runs inside th e m andíbula,
w ith som e pores connecting to th e e x te rio r (e .g ., P yth onichthys m a c ru ru s ) whereas
in oth e rs th e m andíbula only bears a groove on its lateral o r ve n tra l faces th a t
supports th is canal (e .g ., H oplunnis p u n c ta ta ) (see ch a p te r 3).
8 .2 . A d a p tiv e v e rs u s n o n -a d a p tiv e m o rp h o lo g ic a l e v o lu tio n
In te rn a l co n stra in ts in a v e rte b ra te skull re fle ct va rio u s stru ctu ra l and spatial
inte ractio n s
between
com ponents
(Liem ,
1980;
Lauder,
1981b;
Barel,
1985).
Changes in one co m ponent o f th e head ge ne ra lly occur in relation to changes in
o th e r com ponents th a t m ay be considered as n o n-a d a ptive m orphological change.
130
8 G
eneraI
D
ís c u s s ío n
For exam ple ja w
elongation
as a re su lt o f th e elongation o f th e
p re m a xillo -
e th m o vom e ra l com plex as seen in H oplunnis p u n c ta ta (N e tta s to m a tid a e ) can be
coupled to an increased distance betw een th e a n te rio r suspensorial fa ce t and the
p o ste rio r edge o f th e o rb it (see c h a p te r 3).
A n o th e r change in th is regard is observed in H ete roco n g er hassi (C ongridae), a
re p re se n ta tive w ith sh o rt ja w s , w here o rb it size, and hence eye size, is enlarged. In
general, eye size is an im p o rta n t p a ra m e te r fo r vision e fficiency (B arel, 1985; Barel
e t al., 1989). Hence, all fe a tu re s o f th e eye m ay be considered a d ap tatio n s to m eet
visual re q uire m en ts associated w ith a p a rtic u la r lifestyle . The sh o rt rostral region o f
H. hassi brings th e eyes to th e sn o ut tip , allow ing close up binocular vision fo r th is
plankton fe e d e r (De Schepper e t al, 2007a). On the o th e r hand as a no n-a d a ptive
m orphological change, th e expansion o f th e a d d u cto r m andibule m uscles o f H. hassi
has been re stricte d by th e large eyes (De Schepper e t a l., 2007a).
Eye
reduction
in
Pisodonophis
boro
(O p h ichthid a e),
M oringua
edw ardsi
(M oringuidae) and P yth o n ich thys m a cruru s (H eterenchelyidae) is considered to be
an ad ap tatio n
to
h e a d -firs t b u rro w in g ,
i.e. to
d a rk and
m uddy e n v o ro n m e n t
(ch a p te r 4). R elatively sm all o rb its leave m ore room fo r th e bony elem ents and the
ja w
a d d u cto r
m uscles.
C onsequently,
th e
hard
bitin g
anguilliform is,
such
as
Sim enchelys p a rasiticu s (S im enchelyinae) and P. m a cruru s (H ete re n ch e lyid a e),
which have sm all eyes, possess large ja w a d d u cto r m andibulae m uscles (C hapter
5).
The circu m o rb ita l bones have d iffe re n t shapes and sizes in A n g uillifo rm e s and
su p p o rt th e cephalic lateral line system . The arched, large circu m o rb ita l bones o f
heterenchelyids provide m ore space fo r th e w idened cephalic lateral line canals th a t
is considered as an a daptive fe a tu re fo r th is h e a d -firs t b u rro w e r (c h a p te r 4 ). On the
o th e r hand, a v a rie ty in shape and size o f circu m o rb ita l bones probably is related to
th e ir com prom ising fo r space w ith o th e r head s tru c tu re s such as ja w closing
muscles, eye, etc. The reduction o f th e bony skull elem ents m ay occur in fa v o r o f
th e sensory organs (H aken, 1983; w ake, 1986).
131
8 G
eneraI
D
ís c u s s ío n
The presence o f th e large o lfa c to ry rosette in o th e r a n g u illifo rm s m ay be related to
o th e r fa cto rs ra th e r than having p re d a to ry life style as seen in H oplunnis p u n cta ta
(N e tta sto m a tid a e ). The o lfa c to ry organs are o f g re a t biological im portance as th e y
help in detection o f food and prey (P arker, 1922) and in o th e r behaviors like
parental care, recognition o f sexes (N ordeny, 1971), o rie n ta tio n etc. In S e rriv o m e r
sp. (S e rrivo m e rid a e ) and N em ichthys scolopaceus (N e m ich th yid a e ), th e elongated
p re m a xillo -e th m o vo m e ra l
(N e tta sto m a tid a e )
to
com plex
provide
is
large
not
as
o lfa c to ry
deep
cham bers;
as
in
H.
p u n cta ta
hence th e ir o lfa cto ry
ro sette is confined to a sm a lle r space a n te rio r to th e eye. Also, th e exam ined
S e rrivom eridae and N em ichtyidae have larg e r eyes, which is like ly to be related to
being pelagic predators. Hence, size and shape o f th e o lfa c to ry organs o f some
a n g u illifo rm e s m ay re flect spatial inte ractio n s betw een head com ponents ra th e r
than representing a tru ly adaptive characteristic.
A ca u d o ve n tra lly orie n te d ja w m uscle m ay be an a d aptive m orphological change in
both h e a d -firs t burrow ers and in fishes th a t feed on large prey item s, such as
m uraenids in p re ven tin g th e dislocation o f th e m a n d ib u la r jo in t (see chapters 4 and
6 ). On th e o th e r hand, in m any a n g u illifo rm fa m ilie s, th e p a la to p te ryg o id is reduced
and has lost its connection a t one o r both ends. The reduction o f th e a n te rio r p a rt
o f th e Suspensorium , along w ith th e elongation o f th e elem ents o f th e o tic region in
some species (e .g ., A narchias a lla rd ice i and G ym n o th o ra x prasinus'. M uraenidae),
m ay
provide
m ore
space
fo r
ja w
m uscles,
p a rtic u la rly
ca u do ve n tra lly. This m ay be linked to th e observation
those
dire ctin g
o f th e w ell-developed
a d d u cto r hyom andibulae m uscle being present in a n g u illifo rm fa m ilie s such as
m uraenids (see ch a pte r 6).
8 .3 . S o m e c o n clu d in g re m a rk s
W hat th is
e v o lu tio n a ry
disse rtatio n
changes
reveals
and
a b ou t th e
d iv e rs ity
of
various
head
aspects
o f th e
m usculoskeletal
p a tte rn
system
of
in
A n g uillifo rm e s seems fra g m e n ta ry w ith in th is specious order. In a d dition to this
co m p ara tive
anatom ical
s tu d y
on
th e
132
s tru c tu ra l
d iv e rs ity
of
th e
cranial
8 G
eneraI
D
ís c u s s ío n
m usculoskeletal system , th is stu d y is in line w ith m any e v o lu tio n a ry biology studies
a tte m p te d to co n te m pla te on s tru c tu ra l va ria tio n . However, deducing fu n ctional
correlates o f such v a ria tio n has proven to be a challenging ta s k (Russell and Bauer,
2005). S till, in lack o f live specim ens fo r a biom echanical stu d y, th is approach,
which depends upon th e assum ption o f a close m atch betw een s tru c tu re and
fu n ctio n (Lauder, 1995), can still provide an insig h t into possible fu n ctio n s o f
stru ctu re s as m ost m orphological characters are g e ne ra lly correlated w ith fu n ctional
dem ands (Bock and Von W ahlert, 1965; Liem, 1967). An exam ple o f th is approach
is th e stu d y o f Nelson (1 9 6 6 ) th a t suggested a m echanical prey tra n s p o rt system in
m uraenids by th e ir pharyngeal jaw s. Forty years la te r th is suggested fu n ctio n was
confirm ed by Mehta and W a in w rig h t (2 0 07 a ) using high speed and ra diography
film in g .
A d aptations are ch aracteristics th a t enhance th e survival o r reproduction as a result
o f natural selection, and th a t have b ro u g h t into existence creatures th a t are in
m any respects m a rvelously w ell-designed. As a p a tte rn , th e ch ise l-like te e th in the
alleged parasite S im enchelys p a ra siticu s (S im en ch e lyin a e), along w ith th e fleshy
lips, sm all te rm in a l m outh opening, large ve n tra l head m uscles and ja w m uscles,
and a large to n g u e -lik e s tru c tu re , suggest a w e ll-fitte d cranial a rch ite ctu re fo r its
special m ode o f life (see ch a p te r 5). This co m p ara tive s tu d y o f th e a n a to m y, as a
m ethod o f stu d ying a d a p ta tio n , th u s revealed these fe a tu re s o f w hich th e adaptive
nature
(in
relation
to
th is
m ode
o f life)
could
be tested
against th e
basal
m orph o log y o f n o n-p a ra sitic re p re se n ta tive s o f th e Synaphobranchidae.
8 .4 . In s ig h ts fo r f u r th e r re s e a rc h
This stu d y can also provide insights fo r fu tu re inve stig a tio ns a b ou t w hich stru ctu re
should be ca re fu lly considered. For instance, m any studies in A n g u illifo rm e s have
been accom plished solely based on osteology, hence th e m yology o f those is poorly
known. Some a u th o rs explain w hich m uscular characters are p a rtic u la rly 'h ig h ly
c o rro b o ra tiv e ' i.e. non-hom oplasic and reliable characters reflecting th e tru e p a ttern
o f an e v o lu tio n a ry re la tio n sh ip (D iogo, 2005). This s tu d y shows th e im portance o f
133
8 G
th e
eneraI
D
ís c u s s ío n
m uscular fe a tu re s o f th e
head th a t clearly
re flect d iffe re n t stra te g ies
in
e v o lu tio n a ry changes in th e anguilliform is. Data on head m usculature can also be
considered as valuable data to be included in a p h ylogenetic analysis although
understanding th e hom ology o f those m ay be d iffic u lt (D iogo, 2005).
The A n g uillifo rm e s a p p a re n tly show a reductive tre n d w ith in th e skeleton. Many
fe a tu re s o f th e head o f eels are h ig h ly sim p lifie d , b u t w h e th e r th is is because of
loss, fusion, o r p rim itiv e absence still needs to be fu rth e r exam ined based on
o n to g en e tic o r m ore elaborate co m p ara tive and p hylogenetic studies.
134
Summary
SuMMARy
S um m ary
The general goal o f th is d issertation is to d o cum e n t th e stru ctu ra l p a tte rn s and
e v o lu tio n a ry changes in th e head m usculoskeletal system o f several A n g u illifo rm
taxa in relation to d iffe re n t tre n d s o f specializations, such as (1 ) ja w elongation
( H oplunnis p u n c ta ta : N e tta sto m a tid a e ), (2 ) h e a d -firs t burrow ing ( P ythonichthys
m a cru ru s:
H eterenchelyidae),
(3 )
parasitic
feeding
(S im enchelys
p a rasiticu s
:S im enchelyinae; S ynaphobranchidae), (4) a pharyngeal system fo r m echanical
tra n s p o rt o f captured prey in m uraenids, and (5 ) e x tra o rd in a ry m odified cephalic
system in E u ryp h a ryn x pelecanoides (E u ryp ha ryn g id a e ).
•
The
head
A n g uillifo rm e s
m usculoskeletal
w ith
a
system
long ja w ,
of
was
H.
p u n c ta ta ,
com pared
w ith
a
th a t
re p re se n ta tive
of
o f C onger co n ge r
(C ongridae), a re p re se n ta tive w ith m oderate ja w le n g th ; and H ete roco n g er hassi
(C ongridae), a re p re se n ta tive w ith a sh o rt ja w . A shape com parison showed th a t
some stru c tu ra l changes in th e head o f H. p u n c ta ta are as a re su lt o f th e elongation
o f th e p reorbital region. Also, th e results showed th a t ja w elongation p o te n tia lly
affects th e fu n ctio n in g o f th e feeding apparatus in H. p u n c ta ta by increasing biting
speed and reducing drag during prey capture.
• The head m usculoskeletal fe a tu re s o f P. m a cruru s w ere com pared w ith those o f
th e
M oringuidae
(A nguilla
(M oringua
a n g u illa ),
a
ed w a rd si),
a h e a d -firs t
n o n -b u rro w in g
b u rro w e r;
re p re se n ta tive
and
th e
th e
A nguillidae
O phichthidae
( Pisodonophis b o ro ), a head and ta il-firs t b u rrow er. The re su lt o f th is co m p ra tive
stu d y showed som e cranial fe a tu re s o f P. m a cruru s as m orphological adaptations
fo r its burrow ing behavior. D iffe re n t p a tte rn s o f h e a d -firs t burrow ing fe a tu re s fo r
th e H eterenchelyidae and M oringuidae revealed th a t th e re is m ore than one w ay to
re stru ctu re the skull fo r h e a d -firs t bu rro w ing .
• The cranial osteology and m yo lo g y S im enchelys p a rasiticu s, an alleged parasitic
eel
w ere
com pared
to
those
of
n o n-p a ra sitic
re p re se n ta tive s
o f tw o
o th e r
subfam ilies o f th e S ynaphobranchidae, i.e. Ily o p h is b runneus (Ily o p h in a e ) and
S ynaphobranchus b re vid o rsalis (S ynaphobranchinae). The cephalic m usculoskeletal
elem ents o f S. p a rasiticu s, com pared to th e s itu a tio n
in I. brunneus, and S.
b re vid o rsalis show som e m orphological m o d ifica tio n s, such as th e stre tch a b le skin
135
SuMMARy
around th e sm all te rm in a l m outh opening, cu ttin g -e d g e te e th , s to u t m outh closing
apparatus w ith its large associated m uscles, large to n g u e -lik e se cre to ry stru ctu re
and branchial arches w ith th e capacity to tra n s p o rt food item s in th e buccal cavity.
•
The
head
m usculoskeletal
fe a tu re s
o f A narchias
a lla rd ice i (U ro p te ryg iin a e :
M uraenidae) and G ym n o th o ra x pra sin u s (M uraeninae: M uraenidae) w ere com pared
w ith th a t o f a close ly-re la te d o u t-g ro u p w ith a hydraulic based prey tra n s p o rt,
A riosom a
g ilb e rti
(B a th y m y rin a e :
C ongridae).
The
re su lt
showed
th a t
this
inn o va tive feeding m echanism is probably linked to m any cephalic m odifications
such as, s to u t and ro b ust neurocranial elem ents, elongated low er ja w th e as re su lt
o f th e p o ste rio r position o f th e q u a d ra to -m a n d ib u la r a rtic u la tio n , enlarged te e th o f
th e oral ja w s and p re m a xillo -e th m o vo m e ra l com plex, reduction
in th e m oable
cranial bones and th e ir m uscular connections, h yp ertrop h ied a d d u cto r m andibulae
m uscle
com plex,
presence
of
th e
q u a d ra to -m a x illa ry
and
p re op e rclo -a n g ula r
ligam ents, connection o f th e qu ad ra te to th e A2 tendon o f th e a d d u cto r m andibulae
com plex, caudoventral o rie n ta tio n o f th e fibers o f large A3 section o f th e a d du ctor
m andibulae com plex.
• A detailed description o f th e cranial osteology and m yo lo g y o f E. pelecanoides
was provided. In relation to its extensive m o d ifica tio n s, possible im plications fo r the
fu n ctio n in g
of
feeding
apparatus
w ere
described
based
on
its
cephalic
m usculoskeletal system and a broadcasted sh o rt footage (s ix ty -fiv e seconds) o f this
g u ip e r eel in th e BBC d o cu m e n ta ry series (Blue planet: Eposide2 - The Deep,
2001). The re su lt revealed th a t m any e xtre m e m o d ifications o f head s tru ctu re s o f
E. pelecanoides are to be seen in relation to fu n ctio n al sh ifts com pared to those o f
o th e r A n g uilliform es.
The present disse rtatio n m ay lead to a b e tte r u nderstanding o f re lations between
m orphological m o d ifications and com ponents th a t m ay change w ith o r are coupled
to o th e r m o d ifications in th e head o f A n g uillifo rm e s. As m ain conclusion it should be
said th a t p o tential cephalic fe a tu re s are linked to each o th e r and m ay be ind ire ctly
related to o th e r m orphological o r physiological s tru c tu ra l elem ents, i.e. th e y fo rm a
close n e tw ork. In addition such a co m p ara tive a n a to m y s tu d y m ay reveal crucial
in fo rm a tio n o f spatial and fu n ctio n al inte ractio n s betw een th e specific com ponents.
136
L íterature CÍTEd
LÍTRATURE C ÍT E d
LITR A TU R E C IT E D
A a re s tru p K, O k la n d F, H an s en M M , R ig h to n D, G a rg a n P, C a s to n g u a y M,
B e rn a tc h e z L, H o w e y P, S p a rh o lt H , P e d e rse n M I, M c K in le y RS. 2 0 0 9 .
Oceanic spaw ning m igra tio n o f th e european eel CA nguilla a n g u illa ). Science
325:
1660-1660.
A d ria e n s D, V e rra e s W . 1 9 9 7 . The onto g en y o f th e chondrocranium in Clarias
gariepinus'. tre n d s in siluroids. Journal o f Fish Biology 50: 1221-1257.
A d ria e n s D, V e rra e s W , T a v e rn e L. 1 9 9 7 . The cranial la te ra l-lin e system in
Clarias g a rie p in u s
(B urchell,
1822)
(S ilu ro id e s
C lariidae):
m orph o log y and
d e velo p m en t o f canal related bones. European Journal o f M orphology. 3 5 (3 ):
181-208.
A d ria e n s
D,
D e v a e re
S,
In tra sp e c ific va ria tio n
T e u g e ls
GG,
D ekegel
B,
in lim blessness in ve rte b ra te s :
V e rra e s
W.
2002.
a unique exam ple o f
m icroe vo lutio n . Biological Journal o f th e Linnean S ociety 7 5 :3 6 7 -3 7 7 .
A le x a n d e r R M cN. 1 9 6 7 . The fu n ctio n s and m echanism s o f th e p ro tru sib le upper
ja w s o f som e aca nth op te ryg ian fish. Journal o f Zoology, London 151: 4 3 -64 .
A lfa ro ME, J a n o v e tz J, W e s tn e a t M W . 2 0 0 1 .
stra te g ies:
m uscle a c tiv ity
o f b itin g
and
M otor control across tro p h ic
suction feeding
fishes. Am erican
Zoologist 41: 1266-1279.
A rn o ld SJ. 1 9 8 3 . M orphology, perform ance and fitness. A m erican Z oologist 23:
347-361.
Aoyam a
J,
S h in o d a
A,
S asai
S,
M ille r
MJ,
T s u k a m o to
K.
2005.
First
observations o f th e burrow s o f A n g uilla ja p o n ic a . Journal o f Fish Biology 67:
1534-1543.
A san o H. 1 9 6 2 . Studies on th e congrid eels o f Japan. Bulletin o f th e Misaki Marine
Biology In s titu te o f Kyoto U nive rsity I: 1-143.
A tk in s o n RJ, T a y lo r AC. 1 9 9 1 . B urrow s and b u rro w ing beha vio ur o f fish. In :
Meadows PS, Meadows A, editors. The E nvironm ental Im p a c t o f B urrow ing
Anim als and Anim al Burrows. O xford: Clarendon Press, pp. 133-155.
B a n d y o p a d h y a y PR. 1 9 8 9 . Viscous drag reduction o f a nose body. AIAA Journal
27: 274-282.
137
LÍTRATURE C ÍT E d
B a n d y o p a d h y a y PR, A h m ed A. 1 9 9 3 . T u rb u le n t boundary layers subjected to
m u ltip le cu rva tu re s and pressure gradients. Journal o f Fluid Mechanics 246:
503-527.
B annasch R. 1 9 9 5 . H ydrodynam ics o f penguins - an exp erim e nta l approach. In :
Dann, P. N orm an, I. Reilly, P. (E ds.), The penguins: Ecology and m anagem ent.
N orton, NSW: S urrey B eatty and Sons, pp. 141-176.
B arel CDN. 1 9 8 5 . A m a tte r o f space/ co n structional m orph o log y o f cichlid fishes.
Thesis, Univ Leiden.
B arel C D N , A n k e r GCh, W itt e F, H o o g e rh o u d RJC, G o ld s c h m id t T. 1 9 8 9 .
C onstructional
co n stra in ts
and
its
ecom orphological
im plications.
Acta
m orphologica N eerlando-S candinavica 27: 8 3-109.
B au c h o t M -L , S a ld a n h a L. 1 9 8 6 . Congridae (including H eterocongridae). In :
W hitehead P.J.P. Bauchot,
Fishes o f th e
M-L. H ureau, J-C. Nielsen, J. T ortonese, E. (Eds.),
n o rth -e a ste rn A tla n tic and th e
M editerranean. Vol
2.
Paris:
UNESCO, pp. 5 6 7-574.
BBC D o c u m e n ta ry s e rie s . 2 0 0 1 . Blue planet: Eposid2 - The Deep.
B elo u ze A. 2 0 0 1 . C om préhension m orphologique e t phylogénétique des taxons
actuels e t fossils rapports aux A n g uillifo rm e s (Poissons, Téléostéens). Thèse de
d o cto ra t p a lé o e nviro n m en t e t palèobiosphère l'U n ive rsité Claude Bernard Lyon
I, 407 p.
B e rte ls e n E, N ie ls e n JG. 1 9 8 7 . The deep sea eel fa m ily M onognathidae (Pisces,
A n g u illifo rm e s). S teenstrupia 1 3 (4 ): 141-198.
B e rte ls e n E, N ie ls e n JG, S m ith DG. 1 9 8 9 . S uborder Saccopharyngoidei: fam ilies
S accopharyngidae, E urypharyngidae, and M onognathidae. In : Böhlke EB. (E d.),
Fishes o f th e W estern North A tla n tic. Sears Foundation fo r M arine Research,
New Haven, pp. 6 3 6-6 5 5 .
B e rtin L. 1 9 3 4 . Les poissons apodes a p p a rte n a n t au sous-ordre des Lyom éres.
Dana Rep 3: 1-56
B ig e lo w HB, S c h ro e d e r W C . 1 9 5 3 . Fishes o f th e g u lf o f Maine. Fishery Bulletin
Fish & W ildlife Service 53, U.S. Printing Service, W ashington, D.C. 577 p.
138
LÍTRATURE C ÍT E d
B lache J. 1 9 6 8 . C on trib u tio n a la Connaissance de Poisons A n g uillifo rm e s de la
Cote O ccidentate d 'A friq ue (N euvièm e N ote/les H eterenchelyidae). Bulletien de
I'I.F.N .T. XXX, ser, A, no 4.
B ock W J, V on W a h le r t G. 1 9 6 5 . A daptation and th e fo rm -fu n c tio n com plex.
Evolution 19: 269-299.
B ock W J, S h e a r RC. 1 9 7 2 . A staining m ethod fo r gross dissection o f ve rte b ra te
muscles. A n a to m isch e r A nzeiger Bd 130: 2 2 2 -2 2 7 .
Boel CDN.
1 9 8 5 . A M a tte r o f Space [D is s e rta tio n ]. The N etherlands:
Leiden
U niversity.
B ö h lke JE. 1 9 6 6 . O rder In io m i and Lyom eri. In :
Fishes o f th e w estern north
A tla n tic Mem. M em oir Sears Foundation fo r Marine Research, pp. 6 0 3-628.
B ö h lke EB. 1 9 8 9 a . In : Fishes o f th e W estern North A tla n tic. Part 9. New Haven,
CT: Sears Foundation fo r M arine Research. 1055 p.
B ö h lke EB. 1 9 8 9 c . Methods and te rm in o lo g y . In : Böhlke EB. (E d), Fishes o f the
W estern North A tla n tic. New Haven: Sears Foundation fo r Marine Research, p.
1- 8 .
B ö h lke EB, M cC osker JE, B ö h lke JE. 1 9 8 9 . Fam ily M uraenidae. In : Böhlke E.B.
(Ed), fishes o f th e W estern North A tla n tic. New Haven: Sears Foundation fo r
Marine Research, pp. 104-206.
B o zzan o A. 2 0 0 3 . Vision in the rufus snake eel. O phichthus rufus', adaptive
m echanism s fo r a bu rro w ing life -style . Marine Biology 143: 167-174.
B ro ck JP. 2 0 0 0 . The Evolution o f a daptive system s. Academ ic Press. 642 p.
C aira JN , B enz G W , B o rucinska J, K o h le r NE. 1 9 9 7 . Pugnóse eels, S im enchelys
p a ra siticu s (S ynaphobranchidae) fro m th e h eart o f a s h o rtfin m ako, Is u ru s
oxyrin ch u s ( Lam nidae). E nvironm ental Biology o f Fishes 49: 139-144.
C a ld w e ll
MW.
2003.
"W ith o u t
d e velo p m en t o f axial
a
elongation
leg
and
to
stand
on":
lim blessness
on
th e
evo lu tio n
in te tra p o d s.
and
Canadian
Journal o f Earth Science 40: 573-588.
C arro ll AM . 2 0 0 4 . Muscle a ctiva tion and stra in d u ring suction feeding in the
largem outh bass M icropterus salm oides. Journal o f E xperim ental Biology 207:
9 8 3 -9 9 1 .
139
LÍTRATURE C ÍT E d
C arro ll RL. 1 9 9 7 a . Patterns and processes o f v e rte b ra te e vo lu tio n . C am bridge
Paleobiology Series. 447 p.
C arro ll RL. 1 9 9 7 b . The fossil record o f elongation and lim b reduction as a model
o f e v o lu tio n a ry patterns. Journal o f M orphology 232: 241.
C arson F, H la d ik C. 2 0 0 9 . H istotechnology: a se lf-in stru ctio n a l te x t, 3nd e d itio n ,
ASCP Press, Chicago, pp. 114-115.
C a s im ir MJ, F ric k e H W . 1 9 7 1 . Z u r fu n c tio n , m orphologie und histochem ie der
schwanzdrüse bei röhrenaalen (Pisces, Apodes, H eterocongridae). Marin Biology
9: 339-346.
C as tle PHJ. 1 9 6 1 . D ee p -w ate r eels fro m Cook S tra it, New Zealand. Zool. Pub.
Viet. Univ. N.Z. 27: 1-30.
C as tle PHJ. 1 9 6 8 . The w orld o f eels. T u a ta ra : Journal o f th e Biological Society
1 6 (2 ): 8 7 -97 .
C as tle PHJ, M cco sker JE. 1 9 9 9 . A new genus and tw o new species o f M yrophine
W orm -eels,
w ith
C om m ents
on
M uraenichthys
and
Scolecenchelys
(A n g u illifo rm e s: O phichthidae). Records o f th e A ustralian Museum 51: 113-122.
C as tle PHJ, R an d a ll JE. 1999. Revision o f Indo-P acific garden eels (C ongridae:
H eterocongrinae), w ith descriptions o f five new species. Indo-P acific Fishes 30:
2-53.
Chen Y -Y , M ok H -K . 2 0 0 1 .
A new s y n o p h o b ra n c h i eel, D ysom m a lo n g iro stru m
(A n g u illifo rm e s: syn o ph o branchidae), fro m th e n o rth ea stern coast o f Taiwan.
Zoological Studies 4 0 (2 ): 7 9 -83 .
Cohn
MJ,
T ic k le
C.
1999.
D evelopm ental
basis
of
lim blessness
and
axial
p a tte rn in g in snakes. N ature 399: 4 7 4 -4 7 9 .
C o llar
DC,
N ear
TJ,
W a in w r ig h t
PC.
2005.
C om parative
analysis
of
m orphological d iv e rs ity : does d is p a rity accum ulate a t th e sam e rate in tw o
lineages o f ce ntrarchid fishes? Evolution 59: 1783-1794.
D a rw in C. 1 8 5 9 . On th e O rigin o f Species by Means o f Natural Selection, o r
Preservation o f Favored Races in th e S truggle fo r Life. John M urray. London.
D e S c h e p p e r N. 2 0 0 7 . E vo lutin a ry m o rph o log y o f body elongation in teleosts:
aspects o f co n verg e n t evo lu tio n [d is s e rta tio n ]. G hent U niversity.
140
LÍTRATURE C ÍT E d
D e S c h e p p e r N, A d ria e n s D, T e u g e ls GG, D e v a e re S, V e rra e s W . 2 0 0 4 .
In tra sp e c ific va ria tio n in th e postcranial skeleton m o rph o log y in A frican clariids:
A case s tu d y o f e xtre m e phenotypic p la sticity. Zoological Journal o f th e Linnean
Society o f London 140: 4 3 7 -4 4 6 .
De
Schepper
N,
A d ria e n s
(M o rin g u id a e :A n g u illifo rm e s):
D, D e
K egel
B.
2005.
M oringua
edw ardsi
cranial specialization fo r h e a d -firs t burrow ing?
Journal o f M orphology 266: 3 5 6 -3 6 8 .
D e S c h e p p e r N , D e K egel B, A d ria e n s D. 2 0 0 7 a . M orphological specialization in
H eterocongrinae (A n g u illifo rm e s: C ongridae) related to bu rro w ing and feeding.
Journal o f M orphology 268: 3 4 3 -3 5 6 .
De
Schepper
N,
(O phichthidae:
De
K egel
B,
A n g u illifo rm e s ):
A d ria e n s
D. 2 0 0 7 b .
specialization
fo r
Pisodonophis
h e ad first
and
boro
ta il-firs t
burrow ing? Journal o f M orphology 268: 112-126.
D e S c h e p p e r N , V an W a s s e n b e rg h S, A d ria e n s D. 2 0 0 8 . M orphology o f th e ja w
system in tric h iu rid s : tra d e -o ffs betw een m outh closing and b itin g perform ance.
Zoological Journal o f th e Linnean S ociety 152: 7 1 7-7 3 6 .
D e v a e re S, A d ria e n s D, V e rra e s W , T e u g e ls GG. 2 0 0 1 . Cranial m orph o log y o f
th e
a n g u illifo rm
clariid
C hannallabes
apus
(G ü n th e r,
1873)
(Teleostei:
S ilu rifo rm e s ): A d aptations related to pow erful biting? Journal o f Zoology 255:
235-250.
D e v a e re S, T e u g e ls GG, A d ria e n s
Redescription
o f D olichallabes
D, H u y s e n tru y t F, V e rra e s W . 2 0 0 4 .
m ic ro p h th a lm u s (Poll,
1942)
(S ilu rifo rm es.
C lariidae). Copeia 1: 108-115.
D e V is s e r J, B arel CDN. 1 9 9 8 . The expansion apparatus in fish heads, a 3-D
kine tic deduction. N etherlands Journal o f Zoology 48: 361-395.
D iog o R. 2 0 0 4 . Muscles versus bones: catfishes as a case s tu d y fo r an analysis on
th e
co n trib u tio n
o f m yological
and
osteological
s tru c tu re s
in
phylogenetic
reconstructions. Anim al Biology 54: 373-391.
D iog o R. 2 0 0 5 . M orphological e vo lu tio n , a d ap tatio n s, hom oplasies, co n stra in ts and
e v o lu tio n a ry tre n d s:
catfishes as a case stu d y on general
m a croe vo lutio n . Science publisher, In c, NH, USA. 491 p.
141
phylogeny and
L ítrature C ítecI
D iog o R, H in its Y , H u g h es SN . 2 0 0 8 . D evelopm ent o f m a n dib u la r, hyoid and
hypobranchial m uscles in th e zebrafish:
hom ologies and evo lu tio n o f these
muscles w ith in bony fishes and te tra p o d s. BMC D evelopm ental Biology 8, 24.
D u e llm a n
W E,
T ru e b
L.
1986.
M usculoskeletal
system .
In :
Biology
of
A m phibians. D uellm an WE and Trueb L, e ditors. New York: M cGraw-Hill. pp.
2 8 9 -3 6 4 .
D u lle m e ije r P.
1974.
Concepts and approaches
in anim al
m orphology.
Van
g orcum , Assen.
D u lle m e ije r
P.
1991.
Evolution
of
biological
co n stru ction s:
concessions,
lim ita tio n s , and pathw ays. In : S c h m id t-K ittle r N, Vogel K, (Eds). C onstructional
M orphology and E volution, S pringer, Berlin, pp. 3 1 3 -3 2 9 .
E ag d eri S, A d ria e n s D. 2 0 1 0 a . Head m orph o log y o f th e duckbill Eel, H oplunnis
p u n cta ta
(Regan,
1915;
N etta sto m a tid ae :
A n g u illifo rm e s ):
a case
o f ja w
elongation. Zoology 1 1 3 (3 ): 148-157.
E ag d eri
S,
A d ria e n s
D.
2010b.
m a cruru s (H eterenchelyidae:
Cephalic
A n g u illifo rm e s ):
m o rph o log y
of
specializations
P ythonichthys
fo r
h e a d -first
bu rro w ing . Journal o f M orphology 2 7 1 (9 ): 1053-1065.
E ag d eri S, A d iria e n s D. (s u b m itte d ). Cephalic specialization in a parasitic eel,
S im enchelys p a rasiticu s (S im enchelyinae: S ynaphobranchidae). Copeia.
E a to n , T .H . J r., 1 9 3 5 . Evolution o f th e upper ja w m echanism in te le o s t fishes.
Journal o f M orphology 58: 157-72.
F e ls e n s te in
J.
1985.
Phylogenies
and
th e
co m p ara tive
m ethod.
Am erican
N aturalist 1 2 5 :1 -1 5 .
F e rry -G ra h a m LA, L a u d e r GV. 2 0 0 1 a . A quatic prey capture in ra y-finn e d fishes:
A ce n tu ry o f progress and new d irections. Journal o f M orphology 248: 9 9 -11 9 .
F e rry -G ra h a m LA, W a in w r ig h t PC, B ellw o o d DR. 2 0 0 1 b . Prey capture in longjaw e d b u tte rfly fis h e s (C ha e to d o ntid a e ): th e fu n ctio n al basis o f novel feeding
habits. Journal o f Experim ental Marine Biology and Ecology 256: 1 6 7 -1 8 4 .
F e rry -G ra h a m LA, W a in w r ig h t PC, H u ls e y CD, B ellw o o d DR. 2 0 0 1 c . Evolution
o f m echanics o f long ja w s in B u terflyfishes (Fam ily C haetodontidae). Journal o f
M orphology 248: 1 2 0 -1 4 3 .
142
L ítrature C ítecI
Fish FE. 1 9 9 8 . Im a g in a tiv e solutions by m arine organism s fo r drag reduction. In :
Meng, J.C.S. (E d .), Proceedings o f th e In te rn a tio n a l Sym posium on Seaw ater
Drag Reduction. N ew port, Rhode Isla n d, pp. 4 4 3 -4 5 0 .
F ish er RA. 1 9 3 0 . The genetical th e o ry o f natural selection. O xford Univ. Press
(C larendon), O xford.
F o rey PL. 1 9 7 3 . R elationships o f elopom orphs. In :
Patterson
C, (Eds).
In te rre la tio n s h ip s o f Fishes.
Greenwood PH, Miles RS,
Zoological Journal o f the
Linnean S ociety, 53 (S uppl. 1), Academ ic Press, New York, pp. 3 5 1 -3 6 8 .
F o rey PL, L ittle w o o d
Elopom orph
DTJ, R itc h ie P, M e y e r A.
1 9 9 6 . In te rre la tio n s h ip o f
In :
LR,
fishes.
S tiassny
MU,
Parenti
Johnson
GD,
(Eds).
In te rre la tio n s h ip s o f Fishes. Academ ic Press, San Diego, CA. pp. 1 7 5 -1 9 1 .
Gans
C.
1975.
Tetrapod
lim blessness:
e vo lution
and
fu n ctional
corollaries.
Am erican Zoologist 15: 4 5 5-4 6 7 .
Gans C, D e V re e F. 1 9 8 7 . Functional bases o f fib e r length and angulation in
m uscle. Journal o f M orphology 192: 6 3 -85 .
G e e rin c k x T, B ru n a in M, A d ia e n s D. 2 0 0 5 . D evelopm ent o f th e chondrocranium
in th e
su ckerm outh
arm ored
catfish A n cistru s cf.
trira d ia tu s
(Loricariidae,
S ilu rifo rm e s). Journal o f M orphology 2 6 6 (3 ): 3 3 1-355.
G e n te n F ,T e rw in g h e E, D a n g u y A. 2 0 0 9 . Atlas o f fish histology. Enfield (N H ):
Science Publishers, pp. 64-74.
G ili T , R yd e r JA. 1 8 8 3 . On th e a n a to m y and re la tio n sh ip o f th e Eurypharyngidae.
Proceedinf United S tates National Museum 6: 262-273.
G illis GB, L a u d e r GV. 1 9 9 5 . Kinem atics o f feeding in bluegill sunfish: is th e re a
general d istin ctio n betw een aquatic capture and tra n s p o rt behaviors? Journal o f
Experim ental Biology 198: 7 0 9 -7 2 0 .
G oode
GB,
B ean
TH .
1896.
Oceanic
ichth yolo g y.
S m ithsonian
C on tribution
Knowledge 9 8 1 :1 -5 5 3 .
G ordon SM . 1 9 5 4 . The eel genus S tilbiscus. Copeia 1: 1 1 -1 5 .
G o slin e W A . 1 9 6 1 . Some osteological o f m odern lowe teleostean fishes. S m ithson
Mise Colins 1 4 2 ( 3 ) :l- 4 2 .
G o slin e W A . 1 9 6 5 . Teleostean phylogeny. Copeia 1: 1 8 6 -1 9 4 .
143
L ítrature C ítecI
G o slin e W A . 1 9 7 1 . Functional m orph o log y and classification o f teleostean fishes.
U nive rsity Press o f Hawaii, H onolulu. 208 p.
G o slin e W A . 1 9 8 0 . The evo lu tio n o f som e s tru c tu ra l system s w ith reference to the
in te rre la tio n sh ip s o f m odern low e r teleostean fish groups. Japanese Journal o f
Ic h th y o lo g y 21: 1-24.
G ould SJ, V rb a E. 1 9 8 2 . E xaptation - a m issing te rm in th e science o f fo rm .
Paleobiology 8: 4 -15.
G re e n w o o d PH , Rosen DE, W e itz m a n S H , M y e rs G. 1 9 6 6 . Phyletic studies o f
teleostean fishes, w ith a provisional classification o f living fo rm s , B ulletin o f the
Am erican Museum o f Natural H istory 131: 3 3 9-456.
G re g o ry W K . 1 9 3 3 . Fish skulls: a s tu d y o f th e evo lu tio n o f natural m echanism s.
Transactiosn o f th e A m erican Philosophical S ociety 2 3 (2 ): 7 5 -481.
G rub ich
J, Rice A N , W e s tn e a t
MW.
2008.
Functional
m orph o log y o f bite
m echanics in th e g re at barracuda (S phyraena b a rra cu d a ). Zoology 111: 16-29.
H anken
J, W a s s e rs u g
R.
1981.
The
visible
skeleton,
a
new
d o ub le-stain
technique reveals th e nature o f th e "h a rd " tissues. Functional Photography 16:
22-26.
H e e m s tra PC, H is s m a n n K, F ric k e H, S m a le MJ. 2 0 0 6 .
Fishes o f th e deep
dem ersal h a b ita t a t Ngazidja (Grand C om oro) Isla n d, W estern In dian Ocean.
South African Journal o f Science 102: 4 4 4 -4 6 0 .
H e lfm a n
GS, C la rk
JB.
1986.
R otational
feeding:
overcom ing
g a p e -lim ite d
fo ra g in g in a n gu illid eels. Copeia 3: 6 7 9-685.
H e lfm a n GS, C o lle tte BB, Facey DE. 1 9 9 7 . The D ive rsity o f fishes. Blackwell
Science, Inc. USA, 597 p.
H e rn a n d e z
LP,
Bird
NC,
S ta a b
KL.
cyp rin ifo rm e v o lu tio n a ry novelties:
2007.
Using
zebrafish
to
inve stig a te
Functional d e velo p m en t and e v o lu tio n a ry
d ive rsifica tion o f th e kine thm o id . Journal o f Experim ental Zoology 308B: 625641.
H e rre i A, A d ria e n s D, V e rra e s W , A e rts P. 2 0 0 2 . Bite perform ance in clariid
fishes w ith h yp e rtro p h ie d ja w adductors as deduced by bite m odelling. Journal
o f M orphology 253: 1 9 6 -2 0 5 .
144
L ítrature C ítecI
H e rtw ig
ST.
2008.
Phylogeny
of
th e
C yprin o do n tifo rm e s
(Teleostei,
A th e rin o m o rp h a ): th e c o n trib u tio n o f cranial s o ft tissue characters. Zoologica
Scripta 3 7 (2 ): 1 4 1 -1 7 4
H ild e b ra n d M. 1 9 9 5 . Analysis o f v e rte b ra te stru c tu re . Fourth E dition.W iley, New
York.
H o u sto n KA, H a e d ric h RL. 1 9 8 6 . Food habits and intestinal parasites o f deep
dem ersal
fishes fro m
th e
upper co n tine n ta l
slope
east o f N ew foundland,
n o rth w e st A tla n tic Ocean. Marine Biology 92: 563-574.
H u le t W M , R obison RC. 1 9 8 9 . The e v o lu tio n a ry significance o f th e leptocephalus
larva. In : Böhlke EB, (Ed). Fishes o f th e W estern North A tla n tic. Part 10, Sears
Foundation fo r M arine Research, New Haven, pp. 6 6 9-6 7 7 .
H u tc h in s M, T h o n e y DA, L o is elle PV, N eil S c h la g e r N. 2 0 0 3 . G rzim ek's anim al
life encyclopedia. Second ed itio n . Volum es 4 - 5 , Fishes I —II. Farm ington Hills,
MI: Gale Group.
In o u e JG, M iya M, T s u k a m o to K, N is h id a M. 2 0 0 3 . E volution o f th e deep-sea
g u ip e r eel m ito ch on d ria l genom es: large-scale gene rea rra n g e m e n ts orig in ate d
w ith in th e eels. M olecular Biology and Evolution 2 0 (1 1 ): 1917-1924.
In o u e JG, M iya M. 2 0 0 1 . Phylogeny o f th e basal te le osts, w ith special reference
to th e Elopom orpha. Japanese Journal o f Ic h th y o lo g y 48: 75-91 [in Japanese
w ith English a b s tra c t].
In o u e JG, M iya M, M ille r MJ, S ad o T, H an e l R, H a to o k a K, A o y a m a J, M a rk
In o u e JG, M iya M, T s u k a m o to K, N is h id a M. 2 0 0 4 . M ltogenom lc evidence fo r
th e m o n op h yly o f elopom orph fishes (Teleostei) and th e e v o lu tio n a ry origin o f
th e leptocephalus larva. M olecular Phylogenetics and Evolution 32: 274-286.
In o u e JG, M iya M , M ille r MJ, S ad o T , H an el R, H a to o k a
K, A o y a m a J,
M in eg is h i Y, N is h id a M , T s u k a m o to K. 2 0 1 0 . Deep-ocean origin o f the
fre s h w a te r eels. Biological Letters, doi: 1 0 .1 0 9 8 /rs b l.2009.0989
Ja m es R, A tk in s o n A, R o g e r S, P ullin V. 1 9 9 5 . O bservations on th e burrow s and
burrow ing b e havior o f th e red band-fish. Sepola rubescens L. Marine Ecology
1 7 (1 -3 ): 23-40.
Ja m ies o n
BGM.
1991.
Fish
evo lu tio n
and
system atics:
sperm atozoa. C am bridge u n iv e rs ity press, C am bridge, UK.
145
evidence
fro m
L ítrature C ítecI
Jaquet
M.
1920.
C on trib u tio n
á l'a na to m ie
du S im enchelys p a ra siticu s
Gili.
R ésultat des Cam pagnes S cientifiques par A lb e rt I, Prince Souverian de Monaco,
56: 1-77.
Jones EC. 1 9 7 1 . Is itiu s brasiliensis, a squaloid shark, th e probable o f cra te r
w ounds on fishes and cetaceans. U.S. Fishery Bulletin 69: 79 1-7 9 8
K a jiu ra SM , Forni BJ, S u m m e rs AP. 2 0 0 5 . O lfactory m o rph o log y o f carcharhinid
and sphyrnid sharks: does th e cephalofoil co nfer a sensory advantage? Journal
o f M orphology 264: 25 3-2 6 3 .
K a m m e re r CF, G ra n d e L, W e s tn e a t M W . 2 0 0 5 . C om parative and developm ental
fu n ctio n al m orph o log y o f th e ja w s o f living and fossil gars (A c tin o p te ryg ii:
Lepisosteidae). Journal o f M orphology 267: 1017-1031.
K lages M, M u y a k s h in S, S o ltw e d e l T, A rn tz W E . 2 0 0 2 . M echanoreception, a
possible m echanism fo r food fall detection in deep-see scavengers. Deep-SEA
Res I 49: 143-155.
K o n o w IM, B ellw o o d
DR. 2 0 0 5 .
P rey-capture in Pom acanthus se m icircu la tus
(Teleostei, P om acanthidae): fu n ctio n al im plicatio n s o f in tra m a n d ib u la r jo in ts in
m arine angelfishes. Journal o f Experim ental Biology 208: 1421-1433.
K o n o w IM, S a n fo rd CPJ. 2 0 0 8 . Is a co n ve rg e n tly derived m u s c le -a c tiv ity p a ttern
drivin g
novel raking
behaviours in te le o s t fishes? Journal o f E xperim ental
Biology 211: 9 8 9-9 9 9
K ra m e r MO. 1 9 6 0 . Boundary laye r sta b iliza tion by d is trib u te d dam ping. Journal o f
Am erican Society o f Naval Engineers 72: 25-33.
Lauder
GV.
1979.
Feeding
m echanism s in
p rim itiv e
teleosts
and
in
the
halecom orph fish A m ia calva. Journal o f Zoology 187: 543-578.
L a u d e r GV. 1 9 8 0 a . H ydrodynam ics o f prey capture by te le o s t fishes. In : Schneck
D. e d itor. Biofluid Mechanics, vol. 2 New York: Plenum Press, pp. 161-181.
Lauder
GV.
1981a.
Form
and
fu n c tio n : s tru c tu ra l
analysis
in
e v o lu tio n a ry
m orphology. Paleobiology 7: 4 3 0-4 4 2 .
L a u d e r GV. 1 9 8 1 b . In tra s p e c ific fu n ctio n al re p ertoire s in th e feeding m echanism
o f characoid fishes: Lebiasina, Hoplias and Chalceus. Copeia 1981: 154-168.
Lauder
GV. 1 9 8 2 .
H istorical
biology and th e
T heoretical Biology 97: 57-67.
146
problem
o f design. Journal o f
L ítrature C ítecI
L a u d e r GV. 1 9 8 2 . Pattern o f evo lu tio n in th e feeding m echanism o f actin op terg ian
fishes. A m erican Zoologist 22: 275-282.
L a u d e r GV. 1 9 8 5 . A quatic feeding in low e r ve rte b ra te s. In : Functional V e rte b rate
M orphology.
H ildebrand
M,
Bram ble
DM,
Liem
KF,
W ake
DB,
editors.
C am bridge, MA: Belknap Press, pp. 210-229.
L a u d e r GV. 1 9 9 0 . Functional m orph o log y and system atics: stu d ying fu n ctional
p a tte rn s in an historical co n te xt. Annual Review o f Ecology and S ystem atics 21:
317-340.
L a u d e r GV. 1 9 9 5 . On th e inference o f fu n ctio n fro m s tru c tu re . In : M orphology in
V e rte b rate Paleontology (J. Thom ason, e d ), pp. 1-18. C am bridge, England:
C am bridge U nive rsity Press.
L e B o e u f BJ, M cC o sker JE, H e w itt J. 1987. C rater w ounds on no rth ern elephant
seals: th e co o k ie c u tte r sh a rk strike s again. U.S. Fishery B ulletin 85: 38 7-3 9 2 .
L eib y M M . 1 9 8 1 . Larval m o rph o log y o f th e eels Bascanichthys bascanium , B.
scuticaris,
O phichthus
m e lanoporus
and
O.
ophis
(O p h ichthid a e),
w ith
a
discussion o f larval ide n tifica tio n m ethods. Bulletin o f Marine Science 31: 4 6 -71 .
Liem K. 1 9 6 7 . Functional m orph o log y o f th e head o f th e anabantoid te le o s t fish
H elostom a te m m in cki. Journal o f M orphology 121: 135-158.
Liem KF, O sse JW M . 1 9 7 5 . Biological v e rs a tility , e v o lu tio n , and food resources
e xp lo ita tio n in African cichlid fishes. A m erican Z oologist 15: 427-454.
Lindell LE. 1 9 9 4 . The evo lu tio n o f ve rte b ra l n u m be r and body size in snakes.
Functional Ecology 8: 7 0 8-7 1 9
Lopez JA, W e s tn e a t M W , H an e l R. 2 0 0 7 . The p h ylogenetic a ffin itie s o f the
m yste riou s a n g u illifo rm genera C oloconger and Thalassenchelys as supported
by m tDNA sequences. Copeia 4: 9 5 9 -9 6 6
M a rs h a ll NB. 1 9 6 2 . O bservation on th e H eterom i, an o rd e r o f te le o s t fishes.
Bulletin o f th e British Museum Natural H istory (Z o ology) 9: 24 9-2 7 0 .
M a s sc h a e le
BC,
C n udd e
V,
V la s s e n b ro e c k J. 2 0 0 7 .
D ie ric k
UGCT:
M,
Jacobs
P,
Van
H o o re b e k e
L,
New X -ra y ra d io g rap h y and to m o g ra p h y
fa c ility . Nuclear In s tru m e n ts and Methods in Physics Research Section A 580:
266-269.
147
L ítrature C ítecI
M a y r E. 1 9 8 3 . Darwin intellectual re vo lu tio n a ry. Bendall, DS. (E d.). Evolution from
Molecules to Men. C am bridge U nive rsity Press, pp. 23-42.
M cC osker JE. 1 9 9 8 . Eels and th e ir allies. In : Paxton JR and Eschm eyer WN, (Eds).
Encyclopedia o f Fishes. San Diego: Academ ic Press, pp. 85-90.
M cC osker JE, B ö h lke EB, B ö h lke JE. 1 9 8 9 . Fam ily O phichthidae. In : Böhlke EB,
e d itor. Fishes o f th e W estern North A tla n tic. New Haven, CT: Sears Foundation
fo r M arine Research, pp. 254-412.
M is h le r
B.
2003.
d evelopm ental
Phylogeny.
biology.
Haii
In :
Keywords
BK,
Olson
and
M, eds.
concepts
H arvard
in
e vo lu tio n a ry
U nive rsity
Press,
London, pp. 29 7-3 0 8 .
M e h ta RS. 2 0 0 9 . E com orphology o f th e m oray b ite: re la tio n sh ip betw een d ie ta ry
e xtre m e s and m orphological d ive rsity. Physiological and Biochem ical Zoology
8 2 (1 ): 9 0 -103.
M e h ta RS, W a in w r ig h t PC. 2 0 0 7 a . Raptorial ja w s in th e th ro a t help m o ray eels
sw allow large prey. Nature 449: 7 9 -83 .
M e h ta RS, W a in w r ig h t PC. 2 0 0 7 b . Biting releases co n stra in ts on m o ray eel
feeding kinem atics. Journal o f Experim ental Biology 210: 4 9 5-5 0 4 .
M e h ta RS, W a in w r ig h t PC. 2 0 0 8 . Functional m orph o log y o f th e pharyngeal ja w
apparatus in m o ray eels. Journal o f M orphology 269: 6 0 4-6 1 9 .
M ille r MJ. 2 0 0 9 . Ecology o f a n g u illifo rm leptocephali: rem arkable tra n s p a re n t fish
larvae o f th e ocean surface layer. Aqua-BioScience M onographs (ABSM) 2 (4 ):
1-94.
M o n tg o m e ry JC. 1 9 8 9 . Lateral line detection o f pla n kto n ic prey. In : Coombs S,
G örner P, Münz H, editors. The
M echanosensory Lateral
Line.
New York:
S pringer-V erlag. C hapter 28.
N a k a e M , S asaki K. 2 0 0 4 . H om ologies o f th e a d d u cto r m andibulae m uscles in
T e tra o d o n tifo rm e s as indicated
by nerve branching p a tterns. Ich th yo lo gica l
Research 51: 3 2 7 -3 3 6 .
N arici M , M a g n a ris C. 2 0 0 6 . Muscle a rch ite ctu re and a d ap tatio n s to fu n ctio n al
re q uirem ents. In : B ottinelli R, Reggiani C, (Eds). Advances in m uscle research:
Skeletal m uscle p la sticity in health and disease, pp. 25 6-2 8 8 .
148
L ítrature C ítecI
N elson GJ. 1 9 6 6 . Gili arches o f th e teleostean fishes o f th e o rd e r A n g uillifo rm e s
Pacific S cientific 20: 391-408.
N elson GJ. 1 9 6 7 . Branchial m uscles in re p re se n ta tive s o f live eel fam ilies. Pacific
Science, 2 1 (3 ): 348-363.
N elson GJ. 1 9 7 3 . R elationship o f clupeom orphs, w ith rem arks on th e s tru c tu re o f
th e low er ja w in fishes.. In : M.L.J. Stiassny, L.R. Parenti and G.D. Johnson,
Editors, In te rre la tio n s h ip s o f Fishes, Academ ic Press, San Diego, CA.
pp. 3 3 3 -
349.
N elson JS. 2 0 0 6 . Fishes o f th e w orld. Fourth e d itio n . John W iley & Sons, INC. 600
PN ie ls e n JG, B e rte ls e n E. 1 9 8 5 . The g ulper-eel fa m ily Saccopharyngidae (Pisces,
A n g u illifo rm e s). S teenstrupia 1 1 (6 ): 157-206.
N ie ls e n JG, B e rte ls e n
E, J e sp ersen A.
1 9 8 9 . The biology o f E u ryp h a ryn x
pelecanoides (Pisces, E u rypharyngidae). Acta Zoologica 70: 187-197.
N o rd e n y H. 1 9 7 1 . Is th e local o rie n ta tio n o f anadrom ous fishes d e te rm in e d by
herom ones? Nature (Lond.) 233: 41 1- 413.
N o rm a n JR. 1 9 2 6 . The D evelopm ent o f th e chondrocranium o f th e eel (A nguilla
vu lg a ris), w ith observations on th e co m p ara tive m orph o log y and de velo p m en t
o f th e chondrocranium in bony fishes. Philosophical Transactions o f th e Royal
Society o f London Series B 214: 36 9-4 6 4
N o rto n
SF,
B ra in e rd
EL.
1993.
Convergence
in th e
feeding
m echanics
of
ecom orphologically s im ila r species in th e C entrarchidae and Cichlidae. Journal
o f Experim ental Biology 176: 1 1 -2 9 .
N u s b a u m -H ila ro w ic z J. 1 9 2 3 .
Etudes d 'a na tom ie com paree sur les poissons
p ro ven a n t des cam pagnes scientifiques de S.A.S. le Prince de Monaco. Camp
Scient Prince A lb e rt I 15: 1-100.
O b e rm ille r LE, P fe ile r E. 2 0 0 3 . Phylogenetic relationships o f elopom orph fishes
inferred fro m m ito ch on d ria l ribosom al DNA sequences. M olecular Phylogenetics
and Evolution 26: 2 0 2 -2 1 4 .
P a rk e r GHO.
1922.
Sm ell, ta ste
and th e
allied
senses
in th e ve rte b ra te s,
m onographs on E xperim ental Biology, D.B. Lippincelf, Philadelphia.
149
L ítrature C ítecI
P a n k u rs t N W , L y th g o e JN. 1 9 8 3 . Changes in vision and olfaction d u ring sexual
m a tu ra tio n in th e European eel. Journal o f Fish Biology 23: 22 9-2 4 0 .
P a tte rs o n C. 1 9 7 5 . The braincase o f pholidophorid and leptolepid fishes, w ith a
review o f th e a ctin o p te ryg ia n braincase. Philosophical Transactions o f th e Royal
Society o f London. Series B, Biological Sciences 269: 2 7 5-579.
P a tte rs o n C., Rosen DE. 1 9 7 7 . Review o f ichth yo d e ctifo rm and o th e r Mesozoic
te le o st fishes and th e th e o ry and practice o f classifying fossils. B ulletin o f the
Am erican Museum o f Natural H istory 158: 8 1-172.
P fe ile r
E.
1986.
Tow ards
an
explanation
o f th e
developm ental
s tra te g y
in
leptocephalus larvae o f m arine fishes. E nvironm ental Biology o f Fishes 15: 3 13.
P fe ile r E. 1 9 9 7 . Effect o f Ca2+ on survival and d e velo p m en t o f m etam orphosing
bonefish (A lbula sp.) leptocephali. Marine Biology 127: 5 7 1 -5 7 8 .
P fe ile r
E.
1999.
D evelopm ental
physiology
of
elopom orph
leptocephali.
C om parative B iochem istry and Physiology A 1 2 3 :113-128.
P fe ile r
E, Luna
u tiliza tio n
A.
d u ring
1984.
Changes
in
biochem ical
m etam orphosis o f leptocephalous
com position
and
larvae o f th e
energy
bonefish
{A lbula). E nvironm ental Biology o f Fishes 10: 243-251
Poll M. 1 9 7 3 . Les ye u x des poissons aveugles A fricains e t de C aecom astacem belus
brichardi Poli en p a rticu lie r. Ann du Spéléologie 28: 221-230.
P o rte r H T, M o tta PJ. 2 0 0 4 . A com parison o f s trike and prey capture kinem atics o f
th re e species o f piscivorous fishes: Florida g a r {Lepisosteus p la ty rh in c u s ), redfin
needlefish {S tro n g y lu ra n o ta ta ), and g re a t barracuda {S phyraena barracuda).
Marine Biology 145: 9 8 9-1 0 0 0.
Pough HF, A n d re w s RM , C ad le JE, C ru m p ML, S a v itz k y A H , W e lls KD. 1 9 9 8 .
Body su p p o rt and locom otion. In : Pough HF, e d itor. H erpetology. New Jersey:
Prentice Haii. C hapter 8.
R egan CT. 1 9 0 9 . The classification o f teleostean fishes. Annals and Magazine o f
Natural H istory 3: 75-86.
R egan CT. 1 9 1 2 . The osteology and classification o f th e teleostean fishes o f the
O rder Apoda. Annals and Magazine o f N atural H istory 10: 377-387.
150
L ítrature C ítecI
R enous
S,
H ö flin g
appendicular
E,
system s
Gase
in
JP.
1998.
relation
to
Respective
th e
tra n s itio n
role
to
o f th e
axial
lim blessness.
and
Acta
B iotheorethica 46: 141-156.
R ice A N , W e s tn e a t M W . 2 0 0 5 . C oordination o f feeding, loco m o to r and visual
system s in pa rro tfishe s (Teleostei: Labridae). Journal o f Experim ental Biology
208: 3 5 03 -3 5 18 .
R iep p el OC. 1 9 8 8 . Fundam entals o f co m p ara tive biology. Basel: Birkhauser.
R id le y M. 2 0 0 4 . Evolution. 3rd ed. W iley-B lackw ell, 751 p.
R obins CH. 1 9 7 1 . The co m p ara tive m orph o log y o f th e s y n a p h o b ra n c h i eels o f the
S tra its o f Florida. Proceeding o f th e Academ y o f Natural Science o f Philadelphia.
1 2 3 (7 ): 153-205.
R obins CH. 1 9 8 9 . Fam ily D erichthyidae. In :
Böhlke, E.B. (E d .), Fishes o f the
w estern North A tla n tic. New Haven, CT: Sears Foundation fo r Marine Research,
pp. 4 2 0 -4 3 1 .
R obins CH, R obins CR. 1 9 8 9 .
Fam ily S ynaphobranchidae. In :
Fishes o f the
w estern North A tla n tic. Böhlke EB, e d itor. New Haven, CT: Sears Foundation fo r
Marine Research, pp. 207-253.
R obinson CR. 1 9 8 9 . The p h ylogenetic relationships o f th e a n g u illifo rm fishes. In :
Böhlke EB, e d itor. Fishes o f th e w estern North A tla n tic. New Haven: Conn
Search Found Mar Res pp. 9-23.
R ojo AL. 1 9 9 1 . D ictionary o f e v o lu tio n a ry o f fish osteology. Florida: CRC Press.
273 p.
R o h lf FJ. 2 0 0 4 a . tpsS pline, th in -p la te spline, version 1.16. D ep a rtm e n t o f Ecology
and E volution, S tate U nive rsity o f New York a t S tony Brook.
R o h lf FJ. 2 0 0 4 b . tp s U til, file u tility program , version 1.26. D ep a rtm e n t o f Ecology
and E volution, S tate U nive rsity o f New York a t S tony Brook.
R o h lf FJ. 2 0 0 5 . tp sD ig , d igitize landm arks and o u tlin e s, version 2.08. D ep a rtm e n t
o f Ecology and E volution, S tate U nive rsity o f New Y ork a t S tony Brook.
R o s e n b la tt RH.
1 9 5 8 . The status and syn o no m y o f th e eastern
Pacific eel
A riosom a g ilb e rti (O g ilb y). Copeia 1958: 52-54.
R o s e n b la tt RH. 1 9 6 7 . The osteology o f th e congrid eel Gorgasia p u n c ta ta and th e
elationships o f th e H eterocongrinae. Pacific S cientific 21: 9 1 -9 7 .
151
L ítrature C ítecI
R ussell A P, B au e r AM .
2005.
V ariation in s tru c tu re and its re la tio n sh ip to
fu n ctio n : co rre la tio n , explanation and e x tra p o la tio n .
C hapter 17, In : V a ria tio n :
A Central Concept in Biology, B. H allgrim sson and B.K. Haii (E ds.), Academ ic
Press, New York. pp. 399-434.
S a ld a n h a L, B au c h o t M -L. 1 9 8 6 . Synaphobranchidae (including N ettodaridae and
S im enchelyidae).
In :
Fishes
of
th e
n o rth -e a ste rn
A tla n tic
and
the
M editerranean. W hitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese
E, editors. UNESCO, Paris. Vol. 2. pp. 58 6-5 9 2 .
S a n fo rd , CPJ, W a in w r ig h t PC. 2 0 0 2 . Use o f so n o m ic ro m e try de m on stra tes link
betw een prey capture kinem atics and suction pressure in largem outh bass.
Journal o f E xperim ental Biology 205: 3 4 45 -3 4 57 .
S a n to s FB, C as tro RMC. 2 0 0 3 . A c tiv ity , h a b ita t u tiliz a tio n , feeding behavior, and
d ie t o f th e sand m o ray G ym n o th o ra x ocellatus (A n g u illifo rm e s, M uraenidae) in
th e South W estern A tla n tic. Biota Neatropica 3: 1-7.
S c h a e ffe r B, Rosen DE. 1 9 6 1 . M ajor adaptive levels in th e e vo lution o f the
actin o p te ryg ia n feeding m echanism . Am erican Z oologist 1: 187-204.
S c h u ltze
H -P ,
Cum baa
SL.
2001.
D ialipina
and
th e
characters
o f basal
a ctin op teryg ian s. I n : A hlberg PE (Ed). M ajor events in v e rte b ra te e vo lution.
London, UK/ T a ylo r & Francis, pp. 315-332.
S h ira i S, N a k a y a K. 1 9 9 2 . Functional m orph o log y o f feeding apparatus o f the
co o k ie -c u tte r shark, Is is tiu s brasiliensis (E lasm obranchii, D alatiinae). Zoological
Science 9: 8 1 1-8 2 1 .
S ib b in g FA, O sse J W M , T e rlo u w A. 1 9 8 6 . Food handling in th e carp ( C yprinus
ca rp io ):
its
m o ve m e n t
p a tte rn s,
m echanism s
and
lim ita tio n s .
Journal
of
Zoology, London A 210: 1 6 1 -2 0 3 .
S m ith DG. 1 9 8 9 a . Fam ily congridae. In : Böhlke, E.B. (E d.), Fishes o f th e W estern
North A tla n tic. Sears Foundation fo r Marine Research, New Haven, pp. 4 6 0 -6 1 2 .
S m ith DG. 1 9 8 9 b . Fam ily N ettastom atidae. In : Böhlke, E.B. (E d .), Fishes o f the
w estern North A tla n tic. New Haven, CT: Sears Foundation fo r Marine Research,
pp. 5 6 8 -5 6 7 .
152
L ítrature C ítecI
S m ith DG. 1 9 8 9 c . Fam ily M uraenesocidae. In : Böhlke, E.B. (E d .), Fishes o f the
w estern North A tla n tic. New Haven, CT: Sears Foundation fo r Marine Research,
pp. 4 3 2 -4 4 0 .
S m ith
DG.
1989d.
Fam ily M oringuidae. In :
Böhlke EB, e d itor.
Fishes o f the
W estern North A tla n tic. A n g u illifo rm e s and S accopharyngiform es. New Haven,
CT: Sears Foundation fo r Marine Research, pp. 55-71.
S m ith DG. 1 9 8 9 e . Fam ily H eterenchelyidae. In : Böhlke EB, e d itor. Fishes o f the
W estern North A tla n tic. A n g u illifo rm e s and S accopharyngiform es. New Haven,
CT: Sears Foundation fo r Marine Research, pp. 4 8 -54 .
S m ith
DG.
1999.
S ynaphobranchidae.
C u tth ro a t
eels.
In :
FAO
species
ide n tifica tio n guide fo r fis h e ry purposes. The living m arine resources o f the
WCP. Vol. 3. Batoid fishes, chim aeras and bony fishes p a rt 1 (Elopidae to
Linophrynidae). C arpenter KE, Niem VH, editors. FAO, Rome. pp. 1658-1661.
S m ith
DG.
2004.
A
new
genus
and
species
of
congrid
eel
(Teleostei:
A n g uillifo rm e s: C ongridae) fro m W estern A ustralia. Records o f th e A ustralian
Museum 5 6 (2 ): 143-146.
S m ith DG, C as tle PHJ. 1 9 7 2 . The eel genus N eoconger G irard: S ystem atics,
osteology, and life h isto ry. The B ulletin o f Marine Science 22: 196-249.
S m ith DG, K a rm o v s k a y a ES. 2 0 0 3 . A new genus and tw o new species o f congrid
eels (Teleostei: A n g uillifo rm e s: C ongridae) fro m th e In d o -W e st Pacific, w ith a
redescription and osteology o f C hiloconger d entatus. Zootaxa 343: 1-19.
S m ith DG, K a n a z a w a RH. 1 9 7 7 . Eight new species and a new genus o f congrid
eels fo rm th e W estern North A tla n tic w ith redescriptions o f A riosom a analis,
H ildebrandia g u pp yi, and Rhechias vicinalis. B ulletin o f M arine Science 2 7 (3 ):
530-543.
S m ith DG, N ie ls e n JG. 1 9 8 9 . Fam ily n e m ichthyidae. In : Böhlke EB, e d itor. Fishes
o f th e w estern North A tla n tic. New Haven, CT: Sears Foundation fo r Marine
Research, pp. 4 4 1 -4 5 9 .
S o lo m o n -R a ju
N,
R o s e n b la tt
S im enchelys p a ra siticu s fro m
RH.
th e
1971.
central
m e ta m o rph ic fo rm . Copeia 2: 3 1 2-314.
153
New
record
n orth
o f th e
pacific
w ith
parasitic eel,
notes
on
its
L ítrature C ítecI
S o lo m o n
EP,
B erg
LR,
M a rtin
DW.
2005.
Biology,
7th
Ed.,
Brooks/C ole,
Thom son Learning, USA.
S u b ra m a n ia n A. 1 9 8 4 . Burrow ing b e ha vio r and ecology o f th e cra b -e a tin g Indian
snake eel Pisodonophis boro. E nvironm ental Biology o f Fishes 10: 195-202.
S u m m e rs A P, K oob TJ, B ra in e rd EL. 1 9 9 8 . S tin g ra y ja w s s tru t th e ir stu ff.
N ature 3 9 5 (6 7 0 1 ): 4 5 0-4 5 1 .
Sw anson
JR.
1996.
A n a to m y
and
h istology
of
norm al
skin.
h ttp ://w w w .m e d d e a n .lu c .e d u /lu m e n /M e d E d /m e d ic in e /d e rm a to lo g y /m e lto n /s k in l
sn /skn ls n .h tm
T a y lo r W R , V a n D y k e GC. 1 9 8 5 . Revised procedures fo r staining and clearing
sm all fishes and o th e r ve rte b ra te s fo r bone and cartilage study. C ybium 9: 107119.
T c h e ra n v ia n V V . 1 9 4 7 . Further notes on th e s tru c tu re o f th e bony fishes o f o rd e r
Lyom eri ( E u ryp h a ryn x). Journal o f th e Linnean Society (Z o o lo g y) 41: 37 7-3 9 3 .
Tesch F -W . 2 0 0 3 . The Eel. Third e d itio n . O xford: Blackwell Science. 408 p.
T ig h e KA, 1 9 8 9 . Fam ily S e rrivom eridae. In :
Böhlke EB, e d itor. Fishes o f the
w estern North A tla n tic. New Haven, CT: Sears Foundation fo r Marine Research,
pp. 6 1 3-6 2 7 .
T ila k
R,
K an ji
SK.
1969.
Studies
on
th e
osteology
o f Pisodonophis
boro
(H a m ilto n ). Gegenbaurs m o rph o lo- gisches Jahrbuch 113: 5 0 1 -5 2 3 .
T u rin g a n RG, W a in w r ig h t PC, H e n s le y DA. 1 9 9 5 . In te rp o p u la tio n v a ria tio n in
prey use and feeding biom echanics in Caribean T riggerfishes. Oecologia 102:
296-304.
T s u k a m o to Y , O k iy a m a M. 1 9 9 7 . M etam orphosis o f th e Pacific ta rp o n , Megalops
cyprinoides (E lopiform es, M egalopidae) w ith rem arks on d e velo p m en t p a tte rn s
in th e Elom orpha. The Bulletin o f M arine Science 60: 2 3 -3 6
V a n d e w a lle P, G lu c k m a n I , W a g e m a n s F. 1 9 9 8 . A critical assessm ent o f the
Alcian blu e /A liza rin e double staining in fish larvae and fry . Belgian Journal o f
Zoology 1 2 8 :9 3 -9 5 .
V a n d e w a lle P, P a rm e n tie r E, C hard o n M. 2 0 0 0 . The branchial basket in te le o st
feeding. Cybium 2 4 (4 ): 3 1 9-342.
154
L ítrature C ítecI
V a n W a s s e n b e rg i! S, H e rre i A , A d ria e n s D, A e rts P. 2 0 0 4 . Effects o f ja w
ad d u cto r h y p e rtro p h y on buccal expansion during feeding o f a ir breathing
catfishes (Teleostei, C lariidae). Z oo m o rph o log y 123: 8 1 -93 .
V a n W a s s e n b e rg i! S, A e rts P, A d ria e n s D, H e rre i A. 2 0 0 5 . A dynam ical model
o f m outh closing m ovem ents in clariid catfishes: th e role o f enlarged ja w
adductors. Journal o f Theoretical Biology 234: 4 9 -65 .
V e tte r B. 1 8 7 8 . U ntersuchungen zu r vergleichende a natom ie der kiem en und
kie fe rm u s k u la tu r d e r fische. II. Jenaische Z e its c h rift fü r N aturw issenschaft 12:
4 3 1-5 5 0 .
V id e le r JJ. 1 9 9 5 .
E llington,
C.P.
Body surface a d ap tatio n s to
Pedley, T.J.
(E ds.),
b o u n d a ry -la y e r dynam ics. In :
Biological
Fluid
Dynam ics.
Society fo r
Experim ental Biology, pp. 1-20.
V ig lio la
L,
G a lzin
R,
H a rm e lin -V iv e n
ML,
M a ze a s
F,
S a lv a t
B.
1996.
H étérocongerina (Téléostei : C ongridae). De la pente exte rn e de Moorea (II de
la société, Polynésie Française): d is trib u tio n e t biologie. C ybium 20: 3 7 9-393.
V a illa n t
L.
1882.
Sur un
poisson
des grandes
profondeurs
de
l'A tla n tiq u e ,
l'E u ryp h a ryn x pelecanoides. C om ptes Rendus H ebdom adaires des séances de
l'Académ ie des sciences 95: 1226-1228.
V la s s e n b ro e c k J, D ie ric k M, M a s sc h a e le B, C n u d d e V , V a n H o o re b e k e L,
Jacobs P. 2 0 0 7 . S oftw are tools fo r q u a n tifica tio n o f X -ra y m icro to m o g ra p h y a t
th e UGCT. Nuclear In s tru m e n ts and M ethods in Physics Research A 580: 44 2445.
W a in w r ig h t
PC,
B ellw o o d DR. 2 0 0 2 . E com orphology o f feeding in coral reef
fishes. In : Sale, P.F. (E d.) Coral Reef Fishes: Dynam ics and D ive rsity in a
Com plex Ecosystem . San Diego: Academ ic Press, pp. 33-55.
W a in w r ig h t P, C a rro ll A N , C o lla r DC, D ay S W , H ig h a m TE, H o lz m a n RA.
2007.
Suction
feeding
m echanics,
perform ance,
and
d iv e rs ity
in
fishes.
In te g ra tiv e and C om parative Biolog 47: 9 6 -10 6 .
W ake
MH.
1986.
G ym nophiona),
w ith
The
m orph o log y
com m ents
on
Journal o f M orphology. 1 8 9 (1 ): 1-16.
155
of
Id io c ra n iu m -Russeli
m in ia tu riz a tio n
th ro u g h
(A m phibia,
heterochrony.
L ítrature C ítecI
W a n g CH, Kuo CH, M o k HK, Lee SC. 2 0 0 3 . M olecular phylogeny o f elopom orph
fishes inferred fro m
m ito ch on d ria l 12S ribosom al RNA sequences. Zoologica
S cripta, 32: 2 3 1-241.
W a rd AB, B ra in e rd EL. 2 0 0 7 . Evolution o f axial p a tte rn in g in elongate fishes.
Biological jo u rn a l o f th e Linnean Society. 9 0 (1 ): 9 7-116.
W e b b JF. 2 0 0 2 . Functional evo lu tio n o f th e lateral line system : im plicatio n s fo r
fish bioacoustics. Bioacoustics 12 ( 2 /3 ): 145-147.
W e s tn e a t
MW.
1990.
"Feeding
m echanics
of
te le o s t
fishes
(Labridae;
P erciform es): a te s t o f fo u r-b a r linkage m odels." Journal o f M orphology 205:
269-295.
W e s tn e a t
MW.
1994.
Transm ission
of
force
and
v e lo c ity
in
th e
feeding
m echanism s o f labrid fishes (Teleostei, P erciform es). Z oo m o rph o log y 1 1 4 :1 0 3 118.
W e s tn e a t M W . 2 0 0 4 . Evolution o f levers and linkages in th e feeding m echanism s
o f fishes. In te g ra tiv e and C om parative Biolog 44: 3 78-89.
W e s tn e a t M W . 2 0 0 7 . Twice b itte n . Nature 449: 33-34
W ilg a CD. 2 0 0 5 . M orphology and evo lu tio n o f th e ja w suspension in lam n ifo rm
sharks. Jornal o f M orphology 265: 102-19.
W in te rb o tto m , R., 1 9 7 4 . A descrip tive syn o nym y o f th e s tria te d m uscles o f the
Teleostei. Proceeding o f th e A cadem y o f Natural Sciences o f Philadelphia 125:
225-317.
You ng RF, W in n HE. 2 0 0 3 . A c tiv ity p a tte rn s, d ie t, and sh e lte r site use fo r tw o
species o f m oray eels. G ym n o th o ra x m o rin g a and G ym n o th o ra x vicinus, in
Belize. Copeia 2003: 4 4 -55 .
Y u k ih ira H, S h ib u n o T , H a s h im o to H , G u sh im a K. 1 9 9 4 . Feeding habits o f
m oray eels (Pisces: M uraenidae) a t K uchierabujim a. Journal o f th e Faculty o f
Applied Biological Science - H iroshim a U nive rsity (Japan) 33: 159-166.
156
Pu b lic a tio n Lis t o f So h e il Ea g d er i
E agd eri S, M o ja zi A m iri B, M irv a g h e fi A. 2 0 0 6 . A h is to lo g ic a l s tu d y on te s tis
s tru c tu re and s p e rm a to g e n e s is o f B u la tm a i b arbel ( Barbus capito) m ig ra to ry to
S e fid ro o d and Polrood R ivers. Jo u rn a l o f th e Ira n ia n N a tu ra l R esources 1 3 9 150. (In Farsi - English A b s tra c t)
E agd eri S, De S ch e p p e r N, A d ria e n s D. 2 0 0 7 . Head m o rp h o lo g y o f a d u c k b ill eel,
Hoplunnis punctata (N e tto s to m a tid a e : A n g u illifo rm e s ). Journal o f M o rp h o lo g y
2 6 8 (1 2 ): 1 0 6 9 -1 0 7 0 .
A k b a rz a d e h A, K a ram i M, N e za m i SA, E aa d e ri S. B a k h tiy a ri M, K hara H.
2 0 0 7 . A n a lysis o f p o p u la tio n s tru c tu re o f p ike p e rch ( Sander lucioperca), in
Ira n ia n w a te rs o f C aspian Sea and A nzali w e tla n d using tru s s s y s te m . Jo u rn a l o f
th e Ira n ia n N a tu ra l R esources 6 0 (1 ): 1 2 7 -1 3 9 . (In Farsi - English A b s tra c t)
K am al
S, B a k h tiy a ri
M, A bdoli A , E aad eri
v a ria tio n s o f k illifis h
S. K a ram i
M.
2009.
L ife -h is to ry
(Aphanius sophiae) p o p u la tio n s in tw o e n v iro n m e n ta lly
d iffe re n t h a b ita ts in c e n tra l Ira n . Jo u rn a l o f A p plied Ic h th y o lo g y 2 5 (4 ): 4 7 4 478.
E agd eri S, A d ria e n s D. 2 0 1 0 . Head m o rp h o lo g y o f th e d u c k b ill e e l, Hoplunnis
punctata (R eg a n, 1 9 1 5 ; N e tta s to m a tid a e : A n g u illifo rm e s ) in re la tio n to ja w
e lo n g a tio n . Z o o lo g y 1 1 3 (3 ): 1 4 8 -1 5 7 .
E agd eri
S,
A d ria e n s
D.
2010.
macrurus (H e te re n c h e ly id a e :
C ephalic
A n g u illifo rm e s ):
m o rp h o lo g y
of
s p e c ia liza tio n s
Pythonichthys
fo r
h e a d -firs t
b u rro w in g . Jo u rn a l o f M o rp h o lo g y 2 7 1 (9 ): 1 0 5 3 -1 0 6 5 .
E agd eri S, A d ria e n s D, M o ja zi A m iri B, K h o m e ira n i R. D e scrip tio n o f th e o v a ria n
fo llic le m a tu ra tio n o f th e m ig ra to ry a d u lt fe m a le B u la tm a i B arbel ( Barbus capito
(G ü ld e n s tä d t 1 7 7 2 )) (C y p rin id a e , C y p rin ifo rm e s ) in c a p tiv ity . B elgian Jo u rn a l o f
Z o o lo g y . U n d e r R evision.
E agd eri S, C h ris tia e n s J, Boone M, Jacobs P, A d ria e n s D. To be s u b m itte d .
C e ph alic
s p e c ia liz a tio n
in
a
p a ra s itic
eel,
Simenchelys
parasiticus
(S im e n c h e ly in a e : S y n a p h o b ra n c h id a e ). Copeia.
E agd eri S, M e h ta RS, D o m in iq u e A d ria e n s D. In prep. C ephalic s p e c ia liz a tio n s in
re la tio n to second s e t o f ja w s in m u ra e n id s.
E agd eri S, D ie ric k M, V a n H o o re b e k e L, A d ria e n s D. In prep. Head m o rp h o lo g y
of
a
Pelican
E u ry p h a ry n g id a e ).
e e l,
Eurypharynx
pelecanoides
(S a c c o p h a ry n g o id e i:
FACULTY OF SCIENCES
UNIVERSITEIT
GENT
D e p a r tm e n t o f Biology
E volutionary M orphology o f V e rte b ra te s
Structural diversity in the cranial
musculoskeletal system in Anguilliformes:
an evolutionary-m orphological study
P a rt 2 - F ig u re s
Soheil Eagderi
T h es is s u b m itte d to o b ta in th e d e g re e
o f D o c to r in S ciences (B io lo g y )
A ca d e m ic y e a r 2 0 0 9 - 2 0 1 0
R ector: P rof. D r. P aul v a n C a u w e n b e rg e
D ean : P rof. D r. H e rw ig D e jo n g h e
P ro m o te r: P rof. D r. D o m in iq u e A d ria e n s
nun
UNIVERSITEIT
GENT
FACULTY OF SCIENCES
DEPARTMENT OF BIOLOGY
EVOLUTIONARY MORPHOLOGY OF VERTEBRATES
S tru ctu ral d iversity in th e cranial m usculoskeletal system
in A nguilliform es: an evo lu tio n ary-m o rp h o lo g ical study
Part 2 - Figures
Soheil Eagderi
Thesis s u b m itte d to o b ta in th e d e g re e
o f D o c to r in Sciences (B io lo g y )
A cadem ic y e a r 2 0 0 9 -2 0 1 0
R ector: P rof. Dr. Paul van C a u w e n b e rg e
D ean: Prof. D r. H e rw ig D ejo n g h e
P ro m o te r: Prof. D r. D o m in iq u e A driaen s
T able o f c o n ten ts
1. Introduction ........................................................................................................... 1
2. Head Morphology of the Duckbill E e l.................................................................. 8
3. Cephalic Morphology of Pythonichthys m a c ru ru s ............................................ 22
4. Cephalic Specialization in a Parasitic E e l.......................................................... 40
5. Cephalic Specializations in Relation to a Second Set of Jaws in Muraenids
........................................................................................................................................ 56
6. Head Morphology of the Pelican Eell................................................................... 81
7. General D iscussion................................................................................................. 90
F ig u re 1.1. D iv e rs e e e ls , (a ) Conger conger (C o n g rin a e : C o n g rid a e ), (b )
Heteroconger hassi (H e te ro c o n g rin a e : C o n g rid a e ), (c ) Eurypharynx pelecanoides
( E u r y p h a r y n g id a e ) , ( d ) Moringua edwardsi (M o rin g u id a e ), (e ) Strophidon sathete
(M u ra e n in a e : M u ra e n id a e ), ( f ) Ariosoma gilberti (B a th y m y r in a e : C o n g rid a e ), (g )
Simenchelys
parasiticus
(S im e n c h e ly in a e :
S y n a p h o b ra n c h id a e ),
(h )
Gymnothorax prasinus (M u ra e n in a e : M u ra e n id a e ), ( j) Pisodonophis boro
( O p h ic h th id a e ).
1
Adult
Larva
Elopoides
Elopiform es
Albuloides
N otacanthiform es
Anguilloidei
A n guilliform es
Saccopharyiiooult'i
F ig u re 1 .2 . H y p o th e s iz e d
in te r r e la tio n s h ip s o f th e s u p e ro r d e r E lo p o m o rp h a
b ase d on G re e n w o o d e t al. ( 1 9 6 6 ) , w ith th e le p to c e p h a lu s la rv a e o f th e
r e p r e s e n ta tiv e ta x a ( a f t e r W a n g e t al. 2 0 0 3 ).
2
Megalopida
Elopidae
Albulidae
Notacanthidae
Nelson (1973)
Anguilloidei
Forey (1973)
Saccopharyngoidei
Forey et al. (1996)
(1977)
F ig u re 1.3. A-D . Four hypothetical interrelationships among elopomorph fishes.
(A) Nelson (1973), (B) Forey (1973), (C) Patterson and Rosen (1977) and (D)
Forey e ta /. (1996) (after Forey et al. 1996).
3
Thalassenchelys coheni (m eenae sedis)
Serrivomer beani!
I
Serrivomeridae
Ichthyapus ophioneus
Myrichthys breviceps
Ophichthus puncticeps
Echiophis punctifer
Ophichthus rex
Ophichthidae
Myrophis platyrhynchus
Myrophis punctatus B
Myrophis punctatus A
AnAva egmontis
Conger oceanicus
Conger japonicus
Hoplunnis tenuis
Facciolella gilbertii
Chilorhinus suensonii
Kaupichyhys hyoprotoides
Congridae
N ettastom atidae
Chlopsidae
Kaupichthys nuchalis
Moringua edwardsi
Anguilla anguila
Anguilla rostrata
M o rin g u id a e
Anguillidae
Avocettina infans
Nemichthyidae
Gymnothorax moringa
M uraenidae
G y m n o th o ra x c a s ta n e u s
Ariosoma balearicum
Congridae
Eurypharynx pelecanoides
Saccopharyngiformes
Albula vulpes
Notocanthusbonapartei
Albuliformes
Clupea Iw/engus
Limnothrissa miodon
Clupeomorpha
Stolothrissa tanganicae
Elops saurus
Elops sp
Elops affinis
Elopiformes
Elops hawaiiensis
Megalops atlanticus
Chitala ornata
Mormyrops nigricans
Petrocephalus Dovei
Petrocephalus sp
Osteoglossomorpha
Pollimyrus petrtcolus
Xenomystus nigri
Osteoglossum (erronea
Pantodon buchholzi
Hiodon alosoides
F ig u re 1.4. S in g le m o s t p a rs im o n io u s (M P ) tr e e f o r th e c o m b in e d 12S a n d 16S
rR N A d a ta s e t fr o m ta x a c o m p ris in g th e s u p e ro rd e rs E lo p o m o rp h a (o r d e r
E lo p ifo rm e s ,
A lb u lifo r m e s ,
S a c c o p h a ry n g ifo rm e s ,
and
A n g u illifo r m e s ) ,
C lu p e o m o rp h a , a n d O s te o g lo s s o m o rp h a ( a fte r O b e rm ille r a n d P fe ile r, 2 0 0 3 )
4
A n g u illa la p o n ic a
A n g u illa m a rm o ra ta
S e rrivo m e r sam o e n sis
I
S crriv o m c rid a r
C h ilo rh in u s p la tyrh yn ch u s
I
C hbpuda«
N e m ich th ys scolop a ce u s
I
V rm ic h ih y id a r
R hechias retrotincta
I
C ongridae (C ongrinae)
T roconger le p tu ru s
G a via lice p s taeniola
S a u re n ch e lys fie ra s fe r
G orgasia taiw a n ce n sis
N esso rh a m p h u s ingo lfia n u s
Anago anago
P a rapa th ym y ru s m acro p h th a lm u s
I
I
I
I
I
M u ra rn ru x -ld a c
Nel la ii om atidac
C ongridae (H eterocongrinae)
D erichthyidae
C ongridae (B a th ym yrin a e )
O x yco n g e r lepto g n a th u s
M u ra e n e s o x cinereus
M it H M ie t ld ir
C iado III
(A ngu illifo rm es)
O p h ich th u s e ve rm a n n i
P iso d o n o p h is ca n crivo ru s
O p hichthida e (O ph ichth ina e)
X ynas revulsus
MP tree
M ura e n ich th ys sp.
F u ry p h a ry n x p e le c a n o id e s
O p hichthida e (M yrop hin ae )
Saccvphar vasiform e«
D yso m m a ang u illa re
M eadia roseni
S yn aphobranchidae (I>y «ommatln«)
S ynapho b ra n ch u s affinis
Sy naphobranchidae (S ynaphobranchinae)
S im e n ch e lyin a e para siticu s
syna ph ob ran chida e (Sim enchelyinae)
G ym n o th o ra x re ticu la ris
E ch id n a xantho sp ilo s
M uraenidae
U ro p te ryg iu s m icropterus
A lb u la gio ssa d o n ta
P te ro th n ssu s gissu
(Hade II
N o ta ca n th u s a b b o tti 1
(A lbuliform es)
N o ta ca n th u s a b b o tti 2
M e g a lo p s cypnno>ds
M egalopidae
E lo p s h a w a ie n sis
Elopidae
E lo p s m ach n a ta
Ciadi-1
(E lopiform es)
S ard in e lla h a lie n sis
E n g ra u lis ja p o n ic u s
C lup eifo rm es
G o n o ryn ch u s abb re via tu s
C onors n ch îfo r m m
C ha n o s c hanos
C rossostom a lacustre
S chistura fasciolata
C yrp ia ¡formes
N o to p te ru s chitala
O stoglossum b ic irrh o su m
O tleogloatiform ea
F ig u re 1.5. Maximum parsimony cladogram inferred from 12S rRNA sequence
data. Support for clades with 500 bootstrap values (after Wang et al. 2003).
5
Scyliorhinus canicula
Polypierus ornatipinnis
Osteoglossomorpha
Pantodon buchholzi
O steoglossum bicirrhosum
'ops hawaiensis
'ops saurus
Elopiformes
Megalops cyprinoides
Megalops atlanticus
Albula glossodonta
P te ro f) riss us gissu
Albuli'o'm es
To coste
vandia affmrs
Notacanthus chem nitzi
--
•_
<J*
G ym nothorax kidako
Synap/ioi>fanchus kaupii
J<0
C
C
o
E
â
o
l
LU
"™
A n g u illifo rm e s
Ophisurus macrorhynchus
C onger m yriaster
A nguilla japonica
E o p c c o p ra a
•
Sacoop/iaryrur tevenbergr
S a-xoprü ryrg Termes
Eurypfta/yn# petecanwdas
Engraulis japonicus
^
^
7- ^
Clupeomorpha
Sardinops m eünosffcius
Chanos chanos
Anotophysi
Otocephala
G onorynchus greyi
C yprinus carpio
<ÍSPSstí3
Crossostom a lacustre
<£*=2so
O rc o rfiy n rfiu s m ykiss
UWPOOOBOMII
S alm o solar
Otophysi
* ï - ~ 7- r r K !
<f c
^
J^t ï
Protacanthopterygii
Coregonus lavaretus
EutelöostGi
Neoteleostei
Chlorophthalm us agassizi
~ '
i j o a ja p o n ic a
Pagrus m ^jor
Figure 1.6. The 50% m ajority rule consensus tree of the 50,000 pooled trees
from the two independent Bayesian analyses of mitogenomic data (14,040 bp)
from 30 teleosts and three outgroup species using MrBayes 3.0b4 (Huelsenbeck
and Ronquist, 2001; Ronquist and Huelsenbeck, 2003) with GTR+I +C model
(Yang, 1994) of sequence evolution (after Inoue et al. 2004).
6
Elops
Notacanthus
C ongroides 1
Simenchelys
Ilyophis
. qq
Pythonichthys
Myroconger
loo
Anarchias
Gymnothorax
Rhinomuraena
M u r a e n o id e s 1
M u ra e iv k le i _
Kaupichthys
Robinsia
Ariosoma
Thalassenchelys
Nessorhamphus
Derichthys
Coloconger
Congroidei-2
Chlopsidae
I C ongridae-1
I u n id e n tifie d -1
I D erichthyidae
Colocongridae
Nettastom atidae-1
Conger
Congridae-2
Myrichthys
Muraenesox
Cynoponticus
Moringua e.
Congroidei-3
Muraenidae
unidentified-2
Paraconger
Ophisurus
100
M yrocongridae
type II
Facciolella
Heteroconger
A n g u illo id e s2
Heterenchelyidae
Nettastoma
Hoplunnis
‘saccophary ngi form s
Synaphobranchidae
Synaphobranchus
A n g u illo id e s I
Nettastomatidae-2
Congridae-3
Ophichthidae
Muraenesocidae
M oringuidae
Moringua m.
Saccopharynx
Saccopharyngidae
Eurypharynx
Cyema
Cyematidae
Monognathus
Monognathidae
Nemichthys
Avocettina
Nem ichthyidae
Eurypharyngidae '
Labichthys
Serrivomer b.
Serrivomer s.
Stemonidium
A. mossambica
Serrivom eridae
A. borneensis
A.
A.
A.
A.
A n g u illo id e i-3
anguilla
rostrata
dieffenbachii
australis a.
A. australis s.
A. reinhardtii
A. japonica
A n g uillid ae
A. celebesensis
(= Anguilla)
A. megastoma
A. marmorata
A. nebulosa l.
A. nebulosa n.
A. interioris
A. obscura
A. bicolor b.
A. bicolor p.
Figure 1.7. The best-scoring maximum likelihood (ML) tree of 58 elopomorph
species based on unambiguously aligned whole mitogenome sequences (after
Inoue et al. 2010).
7
(Heteroconger hassi)
Heterocongrinae
Derichthyidae
(Derichthys serpentinus)
Congrinae
(Conger conger)
Muraenesocidae
(Oxyconger leptognathus)
Nettastomatidae
(Hoplunnis punctata)
Notacanthiformes
(Notacanthus bonaparti)
F ig u re 3 .1 : Phylogeny o f th e taxa considered in th is stu d y, based on m itochondrial
12S ribosom al RNA and m tDNA sequences (m o difie d a fte r Wang e t al., 2002).
o-Epi
o-Par
o-F
o-Pt
o-BOc
o-ExOc
SOc ri o-SOc o-Sph
af susp A
o-PSph fr-Opt
o-F
fr-Jug
Oo
o-BOc
o-ExOc
o-Par Vo
Vomeral teeth
o-Pt o-Pro o-PtSph o-BSph
fr-Tri.fac fr-Olf
1mm
F ig u re 3 .2 : Neurocranial bones o f H oplunnis p u n cta ta , (a) Dorsal view and (b)
ve n tra l view , a f susp A, a n te rio r suspensorial a rticu la tio n fa c e t; fr-Ju g , foram en
ju g u la ris ; fr-O p t, fo ra m e n o p tic u m ; fr-O lf, foram en o lfa c to riu s ; fr-T ri.fa c , foram en
trig e m in o -fa c ia lis ; o-BOc, basioccipital; o-B Sph, basisphenoid; o-E pi, e p io tic; oExOc, e xo ccip ita l; o-F, fro n ta l; o-Par, p a rie ta l; o-Par Vo, pars vo m e ra lis o f
p re m a xillo -e th m o vo m e ra l com p le x; o-P M x-E tv, p re m a xillo -e th m o vo m e ra l com plex;
o-Pro, p ro o tic; o-PSph, parasphenoid; o-P t, p te ro tic ; o-PtSph, p te ro sphenoid; oSoc, su p rao ccip ital; o-S ph, sp henotic; SOc ri, supraoccipital ridge.
9
o-PtSph
af susp P 0-par o-Sph
o-BSph
0 _f
o-Mx
o-PMx-Etv
o-Op
o-SOp
-Ang-IOp
o-IOp
1-Ang-POp
o-POp
o-PSph
o-D
2 mm
l-M x-P M x-E tv-In fö rb
ae susp P
o-Op ae Op 0-Hm
ae susp A 1-PP
afO p
o-SOp l-Op-IOp
o-Q
o-POp
Ctis
o-PP
2 mm
F ig u re 3 .3 : Cranial skeleton in H oplunnis p u n c ta ta (Lateral v ie w ), (a) C om plete
skull (rig h t side) and (b) Suspensorium (rig h t side), ae Op, o p ercu la r a rtic u la r
condyle; a f Op, o p ercu la r a rtic u la r fa ce t ; ae susp A, a n te rio r suspensorial condyle;
ae susp P, p o ste rio r suspensorial condyle; a f susp P, p o ste rio r suspensorial
a rticu la tio n fa ce t ; Ctis, connective tissu e ; l-A n g -Io p , a n g u lo -in te ro p e rcu la r
lig a m e n t; l-Ang-Pop, a n g u lo -p re o p e rcu la r lig a m e n t; 1-M x-P M x-E tv-InfO rb, m a xillop re m a x illo -e th m o v o m e ro -in fra o rb ita l lig a m e n t; l-O p -IO p , o p e rc u lo -in te ro p e rcu la r
lig a m e n t; l-PP, pala to p te ryg o id a l lig a m e n t; o-BSph, basisphenoid; o-D , d e n ta ry
com p le x; o-Epi, e p io tic; o-F, fro n ta l; o-H m , h yo m an d ibu la ; o -Io p , inte rop e rcle ; oMx, m a x illa ry ; o-O p, opercle; o-Par, p a rie ta l; o-PM x-Etv, p re m a xillo -e th m o vo m e ra l
com p le x; o-POp, preopercle; o-PP, p a la to p te ryg o id ; o-Pro, p ro o tic; o-PSph,
parasphenoid; o-P t, p te ro tic ; o-PtSph, p te ro sphenoid; o-Q, q u a d ra te ; o-SOp,
subopercle; o-S ph, sp h enotic; Sy, ca rtila g ino u s sym plectic.
10
(a)
o-Nas
La Nas W
1 mm
1-InfOrb-PMx-Etv c AdNas
/V A A K A A A Ä A / A
o-InfOrb
(b)
F ig u re 3 .4 : The cranial lateral line system o f H oplunnis p u n cta ta , (a) Dorsal view
o f th e le ft nasal bone, (b) lateral view o f th e com posing canals (rig h t side). Circles
show e xte rn al sensory pores. B LL, body lateral line syste m ; c AdNas, adnasal
canal; c IO , in fra o rb ita l canal; c POM, p reopercular m a n d ib u la r canal; c SO,
su p rao rb ita l canal; c T, te m p o ral canal; cm ST, su p ratem p o ra l co m m issure; La Nas
W, lateral nasal w in g s; 1-InfO rb-PM x-Etv, in fra o rb ito -p re m a x illo -e th m o v o m e ra l
lig a m e n t; o-Nas, nasal; o -In fo O rb , in fra o rb ita l.
11
' \.Vll
-mV
.v.-^y>v
,Acím5A>A
12
F ig u re 3 .5 : Lateral view o f th e cranial m uscles o f H oplunnis p u n cta ta , (a) Skin is
re m oved; (b ) m a x illa ry , Prim ordial lig a m e n t and subsections o f A2, w ith exception
o f A2ßd re m oved; (c) A2ßd and A3 are re m oved; (d ) ve n tra l view o f th e cranial
m uscles (Skin is rem oved). I-Ang-Pop, a n g u lo -p re o p e rcu la r lig a m e n t; l-CH -Ang,
ce ra to h ya lo -a n g u la r lig a m e n t; l-C H -H m , ce ra to h y a lo -h y o m a n d ib u la r lig a m e n t; IM x-P M x-E tv-InfO rb, m a x illo -p re m a x illo -e th m o v o m e ro -in fra o rb ita l lig a m e n t; l-p rim ,
p rim o rd ia l lig a m e n t; m - A l, A Í section o f th e a d d u cto r m andibulae m uscle com plex;
m -A 2, A2 section o f th e a d d u cto r m andibulae m uscle co m p le x; m -A 2a, ve n tra l
subsection o f A2; m -A 2ad, dorsal subsection o f A 2a; m -A 2 a v, ve n tra l subsection o f
A2a; m -A2ß, dorsal subsection o f A 2; m -A2ßa, a n te rio r subsection o f A2ß; m -A2ßp,
p o ste rio r subsection o f A2ß; m -A 3, A3 section o f th e a d d u cto r m andibulae m uscle
com p le x; m-AAP, a d d u cto r arcus palatini m uscle; m -AO , a d d u cto r operculi m uscle;
m -D O , d ila ta to r operculi m uscle; m -E pax, epaxial m uscles; m -H H, hyohyoideus
m uscle; m -H yp, hypaxial m uscles; m-LAP, le v a to r arcus palatini m uscle; m -LO,
le va to r operculi m uscle; m-PH, p ro tra c to r hyoidei m uscle; m -SH , sternohyoideus
m uscle; o-BH, basihyal; o-CH A, a n te rio r ce ra to h ya l; o-CI, c le ith ru m ; o-D , d e n ta ry
com p le x; o-F, fro n ta l; o -Io p , inte rop e rcle ; o-M x, m a x illa ry ; o-PM x-E tv, p re m a xillo e th m o vom e ra l co m p le x; o-O p, opercle; o-POp, preopercle; o-PP, p a la to p te ryg o id ;
o-PSph, parasphenoid; o-Q, q u a d ra te ; o-SO p, subopercle; o-UH, u ro hya l; Sy,
ca rtila g ino u s sym p le ctic; t A 2av, tendon o f A 2av; t A2ß, tendon o f A2ß; t LAP,
tendon o f le v a to r arcus p a la tin i; t LO, tendon o f le v a to r o p ercu li; t.a PH, a n te rio r
tendon o f p ro tra c to r hyo id e i; t.p PH, p o ste rio r tendon o f p ro tra c to r hyoidei; t SH,
tendon o f sternohyoideus.
13
o-Mx
af Mx-Etv
lmm
prC or o-Ang
pr Ang
af Md
1-Ang-POp
1-Ang-IOp
2mm
o-D
Mcc F
pr ra
F ig u re 3 .6 : Jaw o f H oplunnis p u n c ta ta (rig h t side, m edial v ie w ), (a) Lower ja w and
(b ) m a xilla ry, a f Md, m a n d ib u la r a rtic u la tio n fa c e t; a f M x-Etv, m a xilloe th m o vo m e rin e a rticu la tio n fa c e t; l-A n g -Io p , a n g u lo -in te ro p e rc u la r lig a m e n t; l-A ngPop, a n g u lo -p re o p e rcu la r lig a m e n t; o-A ng, a n g u la r com plex ; o-D , d e n ta ry
com p le x; o-M x, m a x illa ry ; Mee F, m eckelian fossa; pr Ang, a n g u la r process; p r Cor,
coronoid process; p r ra, process o f re tro a rtic u la r.
14
o-SOp
o-Op
pr D Op af Op
o-BH
o-UH
Pr A Op
1mm
1-CH-Hm
1-CH-Ang
■Pr A POp
o-POp
2mm
1mm
o-C H P
o-R B R
o-CHA
l-CH-BH
a f CH
Figure 3.7: Hyoid and o p ercu la r series in H oplunnis p u n cta ta , (a) Dorsal view o f
th e basihyal and u ro h ya l; (b) th e a n te rio r and p o ste rio r ceratohyal in a m edial view
(rig h t sid e ); (c) th e o p ercu la r series in th e lateral view (rig h t side), a f CH,
ceratohyal a rtic u la r fa c e t; a f Op, o p ercu la r a rtic u la r fa c e t; l-CH -Ang, ce ra to hya lo a n gu la r lig a m e n t; l-CH-BH, ce ra to hya lo -ba sih yal lig a m e n t; l-C H -H m , ce ra to hya lo h yo m a n d ib u la r lig a m e n t; o-BH, basihyal; o-CH A, a n te rio r ce ra to h ya l; o-CH p,
p o ste rio r ce ra to h ya l; o -Io p , in te ro p e rcle ; o-O p, opercle; o-POp, preopercle; o-SOp,
subopercle; o-R Br, branchiostega! rays; o-UH, u ro h ya l; p r A Op, a n te rio r process
o f opercle; pr A POp, a n te rio r process o f preopercle; p r D Op, dorsal process of
a n te rio r process o f opercle.
15
(Heteroconger hassi)
(Hoplunnis punctata)
(Conger conger)
16
F ig u re 3 .8 : Cranial shape differences betw een H oplunnis p u n cta ta , C onger conger
and H eteroconger h a s s i: d e fo rm atio n grids show to ta l shape difference going,
specially ja w elo n g a tion , fro m species w ith sm a lle r ja w length to w a rd species w ith
longer one (in a d irection as indicated by th e big a rrow s). The lengths o f green
arrow s in th e grids re present th e s h ift in hom ologous lan d m a rk (red points)
positions am ong th e th re e studied species. The hom ologous landm arks were
selected to d e pict an overall shape o f th e neurocranoim .
17
m-Epax
m -A 2a tA l-A 2 a -A 3
tA 2 m -A l
1-prim
t LO
m-LO
(a)
1-Ang-POp
20 mm
m -DO
m-LAP
l-M x-D
m-PH
m -A 3a m -A 3ß
m-LO
l-POp-Op
o-SOp
20 mm
(b)
o-POp
m-AO t AO
t DO m -DO t LAP
m -A 3ß
l-PP-Mx
m-Epax
'-Hyp
20 mm
(c)
m-HH
l-A ng-10p tA 2 ß
m-LAP m-AAP
18
F ig u re 3 .9 : Lateral view o f th e cranial m uscles o f C onger conger, (a ) Skin is
re m oved; (b) p rim o rd ia l lig a m e n t and subsections o f A2 exception A2ßd are
re m oved; (c) lateral view o f th e cranial m uscles a fte r rem oving skin, A l, A2 and A3
muscles, (m o difie d a fte r De Schepper, 2007). I-Ang-Pop, a n g u lo -p re o p e rcu la r
lig a m e n t; l-A n g -Io p , a n g u lo -in te ro p e rc u la r lig a m e n t; l-M x-D , m a x illo -d e n ta ry
lig a m e n t; l-POp-Op, p re op e rcu lo -o p ercu la r lig a m e n t; l-POp-Op, preoperculoo p ercu la r lig a m e n t; l-PP-Mx, p a la to p te ryg o id e o -m a xilla lig a m e n t; l-p rim , prim ordial
lig a m e n t; m - A l, A Í section o f th e a d d u cto r m andibulae m uscle co m p le x; m -A 2a,
ve n tra l subsection o f A 2; m -A 3, A3 section o f th e a d d u cto r m andibulae m uscle
com p le x; m -A 3a, ve n tra l subsection o f A 3; m -A3ß, dorsal subsection o f A3; m-AAP,
a d d u cto r arcus palatini m uscle; m -AO , a d d u cto r operculi m uscle; m -DO , d ila ta to r
operculi m uscle; m -Epax, epaxial m uscles; m -H H, hyohyoideus m uscle; m -H yp,
hypaxial m uscles; m-LAP, le v a to r arcus palatini m uscle; m-PH, p ro tra c to r hyoidei
m uscle; m -LO, le v a to r operculi m uscle; o -Io p , inte rop e rcle ; o-POp, preopercle; oSOp, subopercle; t A l-A 2 a -A 3 , tendon o f t A l-A 2 a -A 3 ; t A2, tendon o f A 2; t A2ß,
tendon o f A2ß;
t AO, tendon o f a d d u cto r o p ercu li; t DO, tendon o f d ila ta to r
o p ercu li; t LAP, tendon o f le v a to r arcus p a la tin i; t LO, tendon o f le v a to r operculi.
19
Epi
A2
Par
F
AA D
TA2 TA3
TLAP
TPH P
Psph
T Do
Op
(c)
HH Ad
H H in f
PtSph
Susp
20
F ig u re 3 .1 0 (A d d itio n a l p ic tu re ): Lateral view o f th e cranial m uscles o f
H ete roco n g er hassi, (a) Skin is rem oved, (b ) A2 section is rem oved, and (c)
Levator arcus palatini is rem oved (m o difie d a fte r De Schepper, 2007).
21
hf (1-6) and u (1-7)
o3
H eterenchelyidae
Pythonichthys macrurus
>-------------
1 cm
o (3-5)
Anguillidae
A n g uilla anguilla
M oringuidae
o (1, 3 & 6)
M o rin g u a edw ardsi
hf ( 1, 3, 4, 5 S. 6) and 0 (3 , 5 & 6)
O phichthidae
Pisodonophis boro
O th er Anguilliform es
22
F ig u re 4 .1 : C ladogram o f th e taxa exam ined in th is stu d y (m o difie d a fte r Böhlke
(1 9 8 9 a ). A nguillidae and M oringuidae are m o n op h yletic fo llo w ing O b e rm ille r and
Pfeiler (2 0 0 3 ). F e a tu re s re la te d to h e a d -fir s t b u rro w in g : Eye reduction ( h f l) ,
W idened cephalic lateral line system th a t extends into th e derm al cavities (h f2 ),
V entral positioning o f gili opening (h f3 ), C audoventral o rie n ta tio n o f th e a n te rio r
section o f th e a d d u cto r m andibulae m uscle com plex (h f4 ), Skull w ith sh o rt and
sharp sn o ut (h f5 ), Large insertion sites o f body m uscles on th e neurocranium (h f 6 );
U n iq u e c h a ra c te rs o f P y th o n ic h th y s m a c r u r u s : Frontal arches ( u l) , Preopercle
w ith a rch -like s tru c tu re s (u 2 ), T u b u la r and a rch -like circum o rb ita l bones (u 3 ), A rch ­
like su p rap re o pe rcu lar bone (u 4 ), Two rin g -lik e e xtra sca p u la r bones (u 5 ) and
Caudal positioning o f th e le v a to r arcus palatini m uscle (u 6 ), M erging le ft and rig h t
bundles o f th e ste rn o hyo id eu s and p ro tra c to r hyoidei m uscles (u 7 ); O th ers :
Absence o f basisphenoid ( o l) , Separate vom eronasal bone (o 2 ), Prem axilloe th m o vo m e rin e com plex (o 3 ), Connection o f th e p a la to p te ryg o id a t its tw o ends
(o 4 ), W ell-developed pectoral fins (o 5 ), Absence o f A Í section o f th e a d du ctor
m andibulae m uscle com plex ( 0 6 ).
23
Pt
P M x-E t
Par
E xO c
1 mm
(a)
SO c
Sph
Pro
Sph
F
PSph
F
PM x-Et
ExO c
BO c
1 mm
a f susp A P tS ph
B Sph
F ig u re 4 .2 . N eurocranial bones o f P yth onichthys m acrurus, (a) Dorsal view and (b)
ve n tra l view . a f susp A, a n te rio r suspensorial a rticu la tio n fa c e t; a f susp p, p o ste rio r
suspensorial a rticu la tio n fa c e t; fr-T ri.fa c , foram en trig e m in o -fa c ia lis ; Lat exp-F,
lateral expansion o f fro n ta l bone; o-BOc, basioccipital bone; o-B Sph, basisphenoid;
o-Epi, epioccipital bone; o-ExOc, exoccipital bone; o-F, fro n ta l bone; o-Par, parietal
bone; o-PM x-Et, p re m a x illo -e th m o id com plex; o-Pro, p rootic bone; o-PSph,
parasphenoid; o-P t, p te ro tic bone; o-PtSph, p te ro sphenoid; o-SOc, supraoccipital
bone; o-S ph, sphenotic bone; o-Vo, vom eral bone.
24
SOc
Par
s ph
F
BSph
Vo
Orb
Mx PMx-Et
T Do
\V > r
-
—
w m /h
^
------ 1
1mm
\
Op
SOp
PSph
Sup POp
ae
ae susp P
Hm ae susp A
PP
af Op
mm
(b)
SOp
IOp
Pr D Op pop
0 ae Md
F ig u re 4 .3 . Cranial skeleton in P yth onichthys m a cruru s (la te ra l v ie w ), (a)
C om plete skull (rig h t side) and (b) Suspensorium (rig h t side), ae Op, o percular
a rtic u la r condyle; a f Op, o p ercu la r a rtic u la r fa ce t ; ae susp A, a n te rio r suspensorial
condyle; ae susp P, p o ste rio r suspensorial condyle; fs Olf, o lfa c to ry fossa; o-BSph,
basisphenoid bone; o-D , d e n ta ry co m p le x; o-E pi, epioccipital bone; o-F, fro n ta l
bone; o-H m , h yo m a n d ib u la r bone; o -Io p , inte rop e rcle ; o-M x, m a x illa ry bone; o-O p,
opercle; o-Par, parietal bone; o-PM x-Et, p re m a x illo -e th m o id co m p le x; o-POp,
preopercle; o-PP, p a la to p te ry g o id ; o-PSph, parasphenoid; o-P t, p te ro tic bone; oPtSph, pterosphenoid bone; o-SOc, supraoccipital bone; o-Q , q u a d ra te ; o-SOp,
subopercle; o-S ph, sphenotic bone; o-S up Pop, suprap re o pe rcla r bone; o-S y,
sym p le ctic bone; o-V o, vom eral bone; Orb, o rb it.
25
cm ST
cm F
Fare a
Fare p
c SO
•£>, <zzz>
(a)
cT
c POM
C 5 > n <s»r=r<atf>y
c IO
L Nas W
Nas
InfOrb
1 mm
Lae
26
F ig u re 4 .4 . The cranial lateral line system o f P yth onichthys m acrurus, (a) Lateral
view o f th e com posing canals (rig h t side), (b ) Dorsal view o f th e le ft nasal bone,
lacrim al bone and in fra o rb ita l bones, c IO , in fra o rb ita l canal; c POM, p reopercular
m a n d ib u la r canal; c SO, su p rao rb ita l canal; c T, te m p o ra l canal; cm F, Frontal
co m m issure; cm ST, su p ratem p o ra l co m m issu re ; F arc a, a n te rio r fro n ta l arch; F
arc p, p o ste rio r fro n ta l arch; La Nas W, lateral nasal w ings; o-Nas, nasal bone; oIn fo O rb, in fra o rb ita l bone ; o-Lac, lacrim al bone.
27
Pr Cor
Ang
af Md
— .sp ----- L Ang-Pop
1 mm
D
(a)
Mee f
Pr ra
Mx
1 mm
(e)
af Mx-PMx-Et
F ig u re 4 .5 . Jaw o f P yth onichthys m a cru ru s (rig h t side) (a -b ) m a x illa ry bone;
lateral view (a ), m edial view (b ) and (c) low er ja w (m edial v ie w ), a f Md, m a n dib u la r
a rticu la tio n fa c e t; ae M x-Et, m a xillo -e th m o id a l a rtic u la tio n condyle; ca-CorMec,
coronom eckelian ca rtila g e , L Io p -A n g , in te ro p e rcu lo -a n g u la r lig a m e n t; L Pop-Ang,
pre op e rcu lo -a n gu la r lig a m e n t; o-A ng, a n gu la r bony com plex ; o-D , d e n ta ry ; o-M x,
m a xilla ry bone; fs Mec, m eckelian fossa; pr Cor, coronoid process; pr ra, process o f
re tro a rtic u la r bone.
28
BH
i---------------1
1 mm
TSH
UH
1 mm
CH P
LHm-CH
afCH
L BH-CH
1 mm
CHA
R Br
(b)
F ig u re 4 .6 . Hyoid apparatus o f P yth onichthys m acrurus, (a) Dorsal view o f the
basihyal and urohyal bones; (b ) The a n te rio r and p o s te rio r ceratohyal bones in a
m edial view (rig h t side), a f CH, ceratohyal a rtic u la r fa c e t; L BH-CH, ce ra to hya lo basihyal lig a m e n t; L CH-Hm , ce ra to hya lo - h yo m a n d ib u la r lig a m e n t; o-BH, basihyal
bone; o-CH A, a n te rio r ceratohyal bone; o-CH P, p o s te rio r ceratohyal bone; o-R Br,
branchiostega! rays; o-UH, urohyal bone.
29
T A2a-A2ß
m-A3
m-SH
m-HH
IOp
CHA
LBH -CH BH
m-PH
(b) m-HH
T LOm
m-LO m
L IOp-Ang L prim m-Au)
m-LO a
Pop
m-Do
T DO L POp-Ang
30
L F-Nas
L Po-Mx
m-PH
Mx
F ig u re 4 .7 . The cranial m uscles o f P yth onichthys m acrurus, (a) V entral view o f the
cranial m uscles (skin is re m o ve d ); (b) Skin is rem oved (late ra l v ie w ); (c) M axillary
bone, p rim o rd ia l lig a m e n t and sections o f A2 are rem oved (late ra l v ie w ); (d )
section A3 are rem oved (la te ra l v ie w ). L CH-Hm , ce ra to h y a lo -h y o m a n d ib u la r
lig a m e n t; L F-Nas, fro n ta l-n a s a l lig a m e n t; L Hm-PP, h y o m a n d ib u la -p a la to p te ryg o id
lig a m e n t; L Io p -A n g , in te ro p e rc u lo -a n g u la r lig a m e n t; L Po-Mx, p re o rb ita l-m a x illa ry
lig a m e n t; L p rim , p rim o rd ia l lig a m e n t; L Pop-Ang, p re op e rcu lo -a n gu la r lig a m e n t;
m -A 2a, ve n tra l subsection o f A2; m -A2ß, dorsal subsection o f A2; m -A 3, A3 section
o f th e a d d u cto r m andibulae m uscle co m p le x; m-AAP, a d d u cto r arcus palatini
m uscle; m-Aco, Aco section o f a d d u cto r m andibulae m uscle com p le x; m -DO,
d ila ta to r operculi m uscle; m -E pax, epaxial m uscles; m -H H, hyohyoideus m uscle;
m -H yp, hypaxial m uscles; m-l_AP, le v a to r arcus palatini m uscle; m -b/AO la,
la te ro a n te rio r bundle o f le v a to r/a d d u c to r operculi m uscle; m -L/A O m , m esial bundle
o f le v a to r/a d d u c to r operculi m uscle; m -L/A O Ip, la te ro p o s te rio r bundle o f
le v a to r/a d d u c to r operculi m uscle;
m -L/A O
m p, m e d io p o ste rio r bundle o f
le v a to r/a d d u c to r arcus palatini m uscle; m -b/AO m a, m e d io a n te rio r bundle o f
le v a to r/a d d u c to r operculi m uscle; m-PH, p ro tra c to r hyoidei m uscle; m -SH ,
sternohyoideus m uscle; o-BH, basihyal bone; o-BSph, basisphenoid; o-CH A,
a n te rio r ceratohyal bone; o-CI, c le ith ru m ; o-ExOc, exoccipital bone; o -IO p ,
inte rop e rcle ; o-M x, m a x illa ry bone; o-PM x-Et, p re m a x illo -e th m o id co m p le x; o-POp,
p reopercle; o-UH, urohyal bone ; Orb, o rb it; r-T b/AO, rest o f le v a to r/a d d u c to r
operculi m uscle te n d o n ; T A2, tendon o f A2; T A3, tendon o f A 3; T DO, tendon o f
d ila ta to r operculi m uscle; T LAP, tendon o f le v a to r arcus p a la tin i; T b/AO, tendon of
le v a to r/a d d u c to r o p e rcu li; T L/AO m , tendon o f m esial bundle o f le v a to r/a d d u c to r
operculi m uscle; T.a PH, a n te rio r tendon o f p ro tra c to r hyo id e i; T SH, tendon o f
sternohyoideus.
31
Orobranchial tongue-like organ
500 pm
Blood-vessel
Goblet cells
32
Central cavity
F ig u re 4 .8 . The orobranchial organ o f P ythonichthys m acrurus, (a) Two to n g u e -like
appendages o f the orobranchial organ on the ro o f o f the m o u th ; (b) Closer view o f
the tw o to n g u e -lik e appendages o f th e orobranchial organ; (c -d ) sagittal section o f
th e orobranchial organ (m e d ia l) (c) base region; (d ) apex region.
33
-HH
m-Epax
m_i 0
m_A2
m -A 2 d
TA2
m -A 2 a
L POp-Ang L IOp-Ang
m-Ao
TDo
m-Do Sph
L prim
m-A3
PP
m-PH
F
NX
5 mm
Iop
TA2m
m-A2m Pop
EpiSOc m-Do m-L.AP
BSph
PSph
PMx-Etv
m
5 mm
Sop
Pt LOp-Iop
UM
m-AAP
10 mm
(d)
m-HH
m-SH
m-LO TSH m-Al-A2
TA1-A2 LPrim m-PH T PH
L IOp-Ang
34
F ig u re 4 .9 . The cranial m uscles o f A n g uilla anguilla, (a) Skin is rem oved (late ra l
v ie w ); (b ) sections A2 except th e m edial fibers o f subsection A 2m , hyohyoideus
m uscle, le v a to r operculi m uscle, epaxial m uscles, hypaxial m uscles, m a x illa ry bone
and p rim o rd ia l lig a m e n t are rem oved (late ra l v ie w ); (c) subsection A2m and
subsection A3 are rem oved (late ra l v ie w ); (d) ve n tra l view o f th e rig h t side o f the
cranial muscles (Skin is re m ove d ), (M odified a fte r De Schepper (2 0 0 7 )). L Io p -A n g ,
in te ro p e rc u lo -a n g u la r lig a m e n t; L O p -Io p , p re o p e rcu lo -in te ro p e rcu la r lig a m e n t; L
p rim , p rim o rd ia l lig a m e n t; L Pop-Ang, p re op e rcu lo -a n gu la r lig a m e n t; m -A2 a,
a n te rio r subsection o f A 2; m -A2 d, dorsal subsection o f A2; m -A 2 v, ve n tra l
subsection o f A 2; m -A2 m, m edial subsection o f A2; A3 section o f th e a d du ctor
m andibulae m uscle com p le x; m-AAP, a d d u cto r arcus palatini m uscle; m -DO ,
d ila ta to r operculi m uscle; m -E pax, epaxial m uscles; m -H H, hyohyoideus m uscle;
m-LAP, le v a to r arcus palatini m uscle; m -AO , a d d u cto r operculi m uscle; m-LO m,
le va to r operculi m uscle; m-PH, p ro tra c to r hyoidei m uscle; m -SH , sternohyoideus
m uscle; o-B Sph, basisphenoid; o-D , d e n ta ry co m p le x; o-Epi, epioccipital bone; o-F,
fro n ta l bone; o -IO p , inte rop e rcle ; o-O p, opercle;
POp, preopercle; o-PP,
p a la to p te ry g o id ; o-PSph, parasphenoid; o-P t, p te ro tic bone; o-M x, m a x illa ry bone;
SOc, supraoccipital bone; o-SO p, subopercle; o-S ph, sphenotic bone; o-UH, urohyal
bone ; T A2, tendon o f A2; T A2 m , tendon o f A2 m ; T DO, tendon o f d ila ta to r
operculi m uscle; T PH, tendon o f p ro tra c to r hyo id e i; T SH, tendon o f
sternohyoideus.
35
SOc
T A1
A1
L prim
PMx-Etv
ExOc
T LO
LO
A
IOp
T PH P
PH
A2
T PH A
A3
Epi
B
SOp
POp T A 2
Aco
D
Pt
AO
C
Op
T DO Hm
T LAP
36
Mx
F ig u re 4 .1 0 (A d d itio n a l p ic tu re ): 3D reconstruction o f th e cranial m uscles o f
Pisodonophis boro. The nasal is indicated by an arrow . A: The skin is rem oved, B:
th e A Í o f th e a d d u cto r m andibulae com plex is rem oved, C: A2 and Aco o f the
a d d u cto r m andibulae com plex and LO are rem oved (a fte r De S chepper., 2007).
37
A3m
T A2m
Al
A3
PMx-Etv
A2v
LO
L prim F
A2v A2m
A2b
A3
Pop
A'U)
T LO DO T LAP A3
Mx
Orb
Sco
ExOc
Boc
LO T DO LAP
Epax AH
Sph AAP Pt
AO
Op
Q
PtSph
38
1 mm
F ig u re 4 .1 1 (A d d itio n a l p ic tu re ): Lateral view o f th e cranial m uscles M oringua
edw ardsi. D otted lines indicate parts o f s tru c tu re s being covered by o th e r elem ents.
A: Skin is rem oved. B: Prim ordial lig a m e n t and A Í are rem oved, exposing the
a d d u cto r m andibulae com plex w ith dorsal (A 2d), m edial (A 2 m ), ve n tra l (A 2v) and
m a n d ib u la r (Aco) part. C: The a d d u cto r m andibulae com plex is rem oved, e xcept fo r
th e A3. D: O percular m uscles are rem oved (a fte r De Schepper, 2007).
39
o-PtSph
o-Par
o-PMx-Et
o-Epi
o-SOc
o-ExOc
1 mm
o-Pt
o-Sph
o-F
fr-Olf
fr-Tri.fac
a f susp P
a f susp A o-F o-PSph
o-PMx-Et
o-BOc
o-ExOc
1mm
o-Pt
o-Pro
o-Sph o-PtSph
40
o-BSph
o-V
F ig u re 5 .1 : N eurocranium o f S im enchelys parasiticus. (A) Dorsal vie w , and (B)
Ventral view , a f susp A, a n te rio r suspensorial a rtic u la tio n fa c e t; a f susp P, p o ste rio r
suspensorial a rticu la tio n fa c e t; fr-O lf, foram en o lfa c to riu s ; fr-T ri.fa c , foram en
trig e m in o -fa c ia lis ; o-BOc, basioccipital; o-BS ph, basisphenoid; o-E pi, e p io c c ip ita l;
o-ExOc, e xo ccip ita l; o-F, fro n ta l; o-Par, p a rie ta l; o-PM x-Et, p re m a xillo -e th m o id a l
com plex;
o-Pro, p ro o tic;
o-PSph, parasphenoid; o-P t, p te ro tic ; o-PtSph,
p te ro sphenoid; o-Soc, su p rao ccip ital; o-S ph, sp henotic; o-V, vo m e r.
41
o-SOc
o-Par
o-Sph
o-PtSph o-BSph o-F
o-M x
o-Hm
ae susp P
ae susp A
o-PMx-Et
o-Epi
Pr Hm
o-Pt
ae Op
o-Hm
1 mm
o-SOp o-O p
1-Op-IOp o-PO p
1
o-IOp
I-CH-Ang
o-V
o-D
l-prim
(C )
42
o-POp
1 mm
o-Q
o-PP
F ig u re 5 .2 : Cranial skeleton o f S im enchelys p a ra siticu s (la te ra l v ie w ), (a)
C om plete skull except th e circum o rb ita l bones (rig h t side), (b ) Suspensorium (rig h t
side) and (c) position o f th e skull in th e head. Cranial skeleton o f S im enchelys
pa ra siticu s (late ra l v ie w ). (A) C om plete skull except th e circu m o rb ita l bones (rig h t
side), (B) Suspensorium (rig h t side) and (C) position o f th e skull in th e head, ae
Op, o p ercu la r a rtic u la r condyle; ae susp A, a n te rio r suspensorial condyle; ae susp P,
po ste rio r suspensorial condyle; a .I.d.M x, a n te ro la te ra l depression o f m a x illa ry ; d mPMx-Et, distance betw een a n te rio r tip o f m outh and p re m a xillo -e th m o id a l com plex
(so ft tis s u e ); l-Io p -A n g , in te ro p e rc u lo -a n g u la r lig a m e n t; l-CH -Ang, ce ra to hya lo a n gu la r lig a m e n t; l-O p -IO p , o p e rc u lo -in te ro p e rc u la r lig a m e n t; l-p rim , p rim o rd ia l
lig a m e n t; o-Nas, nasal; o-BSph, basisphenoid; o-D , d e n ta ry co m p le x; o-Epi,
epiocci pital ; o-F, fro n ta l; o -H m , h yo m an d ibu la ; o -Io p , in te ro p e rcle ; o-M x,
m a x illa ry ; o-O p, opercle; o-Par, p a rie ta l; o-PM x-Et, p re m a xillo -e th m o id a l com plex;
o-POp, preopercle; o-PP, p a la to p te ry g o id ; o-PSph, parasphenoid; o-P t, p te ro tic ; oPtSph, p te ro sphenoid; o-Q, q u a d ra te ; o-Soc, su p rao ccip ital; o-SO p, subopercle; oSph, sp h en o tic; o-V , v o m e r; Orb, o rb it; Pr Hm, h yo m a n d ib u la r lateral process.
43
cm ST c T
o-Hm
o-PoOrb I-IV
o-F
Cm F
c SO
c POM
I mm
o-PoOrb I
F ig u re 5 .3 : The cranial lateral line system o f S im enchelys p a rasiticus, (a) Position
o f th e com posing canals in relation to th e skull (rig h t side, lateral v ie w ), and (b )
lateral view o f th e nasal bone, p re orb ita l bone, in fra o rb ita l bone and firs t postorbital
bone (rig h t side), c IO , in fra o rb ita l canal; c POM, p reopercular m a n d ib u la r canal; c
SO, su p rao rb ita l canal; c T, te m p o ral canal; cm F, fro n ta l co m m issure; cm ST,
su p ratem p o ra l co m m issure; o -In fO rb , in fra o rb ita l; o-D , d e n ta ry com p le x; o-F,
fro n ta l; o -H m , h yo m an d ibu la ; o-Nas, nasal; o-O p, opercle; o-Porb, p re o rb ita l; oPoOrb, p o s to rb ita l, o-POp, preopercle.
44
Pr Cor
cutting-edge teeth
(A)
af Md
1-CH-Ang
o-ra
mm
1-IOp-Ang
o-D
(B)
af Mx-PMx-Et
o-Mx
cutting-edge teeth
F ig u re 5 .4 : Jaws o f S im enchelys p a ra siticu s (rig h t side), (a) Lower ja w ; medial
view , and (b ) m a x illa ry ; m edial view , a f Md, m a n d ib u la r a rtic u la tio n fa c e t; a f Mx-Et,
m a xillo -p re m a x illo -e th m o id a l a rtic u la r fa c e t; l-Io p -A n g , in te ro p e rcu lo -a n g u la r
lig a m e n t; l-CH -Ang, ce ra to h ya lo -a n g u la r lig a m e n t; o-A ng, a n g u la r com plex ; o-D ,
d e n ta ry com plex; o-M x, m a x illa ry ; o-cM ec, coronom eckelian; pr Cor, coronoid
process; o -ra , re tro a rtic u la r.
45
D erm al
c a v ity
m -A 2 ß
t-A 2 ß
m -A 3
(c )
m -A A P
A secretory unit of tongue
m -L A P a
m -A 2 a
Epidermis
Stratum spongiosum
Stratum compactum
m -SPH
Tongue
o-D
c POM
l-IO p -A n g
m -P H
m -P H
m -SH
(d ) M u ltila y e r e p ith e lia l tissue
m -H H i n f
(b )
2m m
Im m
46
F ig u re 5 .5 : (a ): Cross section o f th e head o f S im enchelys p a ra s itic u s : (a) a t th e
level o f th e a n te rio r p a rt o f th e low er ja w : (b) a t th e level o f th e a n te rio r p a rt o f the
large to n g u e ; (c) detail o f th e g la n d u la r tissue large in th e to n g u e -lik e s tru c tu re o f
S. parasiticus-, and (d ): m u ltila ye re d epithelial tissue o f th e skin around th e m outh,
c POM, pre op e rcu la r m a n dib u la r canal; l-IO p -A n g , in te ro p e rc u lo -a n g u la r lig a m e n t;
m -A 2a, ve n tra l subsection o f A2; m -A2ß, dorsal subsection o f A2; m -A 3, A3 section
o f th e a d d u cto r m andibulae m uscle co m p le x; m-AAP, a d d u cto r arcus palatini
m uscle; m-HH inf, hyohyoideus inte rio ris m uscle; m-LAPa, a n te rio r subsection o f
le va to r arcus palatini m uscle;
m-PH, p ro tra c to r hyoidei m uscle;
m -SH,
sternohyoideus m uscle; m-SPH, p h aryn g o cle ith ra lis m uscle; o-D , d e n ta ry com plex;
t A2ß, tendon o f A2ß.
47
o-Op
(a)
a f Op
o-SOp
o-Hhy D o-Hhy V
Pop W
o-POp
o-CH A
o -C H P
l-C II-A n g
o-lOp
o -U II
(Ventral view)
ae I Ihy
Pr UH
(b)
o-CH A o-Hhy V o-Hhy D
F ig u re 5 .6 : O percular series and hyoid a pparatus o f S im enchelys p a ra s itic u s : (a)
O percular series; lateral view (rig h t side ), and (b ) hyoid a p pa ra tu s; ve n tra l and
dorsal view s o f th e dorsal hypohyal, ve n tra l hypohyal, a n te rio r ceratohyal and
p o ste rio r ceratohyal bones, ve n tra l and dorsal view s o f u ro hya l, and dorsal view o f
basihyal. a f Hhy, hypohyal a rtic u la r fa c e t; a f Op, o p ercu la r a rtic u la r fa c e t; ae Hhy,
hypohyal a rtic u la r condyle ; l-C H -Ang, ce ra to h ya lo -a n g u la r lig a m e n t; o-BH,
b asihyal; o-CH A, a n te rio r ceratohyal bone; o-CH p, p o s te rio r ceratohyal bone; oHhy D, dorsal hypohyal bone; o -H hy V, ve n tra l hypohyal bone; o -Io p , inte rop e rcle ;
o-O p, opercle; o-POp, preopercle; o-SOp, subopercle; o; o-UH, u ro hya l; p r UH,
urohyal process; Pop W, p reopercular w ing.
48
o-Hb 1
o-Cb I
o-Eb I o-Ib II
o-Ib IV
o-UP
o-Cb V
1mm
o -B b l
O-LP
B b lll
m -L e
m-Li
m -APTp
m-PHC
1mm
m-SPH
m-Trans.v
F ig u re 5 .7 : Gili arches o f S im enchelys p a rasiticus, (a ) Dorsal view o f th e ve n tra l
p a rt and th e ve n tra l view o f th e dorsal p a rt o f th e gili arch, and (b ) gili arch
muscles. o-B b, basibranchia! bone; o-Cb, ceratobranchia! bone; o-Eb, epibranchial
bone; o-H b, hypobranchial bone; o -Ib , infra ph a ryn go b ra n chia l bone; o-LP, low er
pharyngeal to o th plates; o-UP, upper pharyngeal to o th plates; m-APTp, pharyngeal
to o th plate a d d u cto r m uscle; m -Le, le v a to r e xte rn u s m uscle; m -Li, le v a to r inte rnu s
m uscle; m-PHC, p h aryn g o cle ith ra lis m uscle; m-SPH, subpharyngealis m uscle; m T ra n s.v, tra n sve rsus v e n tra lis muscle.
49
m -A 2 ß
o-Mx
m-LAPp
m-LAPa m-A3
o-PMx-Et
m-Epax
m -L O
m-HH sup
o-O p
o-S O p
2 miri
2 mm
m-SH
m -LO
o-Par
m-DO
m -A 2a m-HH in f m -PH 1-prim
t-LAPa
o-D
t-L A P p m -A 2 a m
m-AAP o-F
tongue-like
secretory structure
o-CH A
1-lOp-Ang
o-Hb III m-SPH
o-Cb V
o-Cb IV
o-Cl
m-AO
t-DO
2 mm
o-POp
m-PH
m-LAPa
50
o-Hhy
m-SH
m-HH inf
m-Trans.v
m-PHC
F ig u re 5 .8 : The cranial m uscles o f S im enchelys p a rasiticus, (a) Skin rem oved
(la te ra l vie w ), (b) sections A2 except fo r th e m edial fib e rs o f subsection A2a,
hyohyoideus m uscle, hyohyoideus inte rio ris m uscle, epaxial m uscles, hypaxial
m uscles, ve n tra l m uscles o f th e head and p rim o rd ia l lig a m e n t are rem oved (lateral
v ie w ), (c) subsection A2a, section A3, lateral fib e rs o f th e le v a to r arcus palatini
m uscle and le v a to r operculi m uscle are rem oved (late ra l v ie w ), and (d ) ve n tra l
m uscles o f head (sa g itta l le ft c u t), hyohyoideus m uscle is rem oved. I-Io p -A n g ,
in te ro p e rc u lo -a n g u la r lig a m e n t; l-p rim , p rim o rd ia l lig a m e n t; m -A 2a, ve n tra l
subsection o f A 2; m -A2ß, dorsal subsection o f A 2; m -A 2 a m , m edial fib e rs o f ve n ta I
subsection o f A2; m -A 3, A3 section o f th e a d d u cto r m andibulae m uscle com plex;
m-AAP, a d d u cto r arcus palatini m uscle; m -AO , a d d u cto r operculi m uscle; m -DO ,
d ila ta to r operculi m uscle; m -Epax, epaxial m uscles; m-HH inf, hyohyoideus
inte rio ris m uscle; m-HH sup, hyohyoideus s u p e rio r m uscle; m-l_APa, a n te rio r
subsection o f le v a to r arcus palatini m uscle; m-LAPp, p o s te rio r subsection o f le va to r
arcus palatini m uscle; m -LO, le v a to r operculi m uscle; m-PH, p ro tra c to r hyoidei
m uscle; m -SH, sternohyoideus m uscle; m-SPH, subpharyngealis m uscle; m T ra n s.v, tra n sve rsus v e n tra lis m uscle; o-Cb, ceratobranchia! bone; o-CH A, a n te rio r
ceratohyal bone; o-CI, cle ith ru m bone; o-D , d e n ta ry co m p le x; o-F, fro n ta l bone; oHb, hypobranchial bone; o -H hy V, ve n tra l hypohyal bone; o-M x, m a x illa ry bone; oOp, opercle; o-Par, parietal bone ; o-PM x-Et, p re m a xillo -e th m o id a l co m p le x; o-POp,
p reopercle; o-PP, p a la to p te ryg o id bone; t-A 2 ß , tendon o f A2ß; t-D O , tendon o f
d ila ta to r operculi m uscle; t-LAPa, tendon o f a n te rio r subsection o f le v a to r arcus
p a la tin i; t-LAPp, tendon o f p o s te rio r subsection o f le v a to r arcus p a la tin i; t-LO ,
tendon o f le v a to r operculi.
51
m-Epax
m-L/AOI
m-A2a
m-A2ß
t-A2ß
o-Mx 1-Mx-PMx-Et
n v XTrrr^-
2 mm
(a)
m-HH
o-IOp
1-I0p-Ang
1-prim
o-Op m-L/AOm m-DO m-LAP
m-A3
o-D
m-PH
o-F
///
o-SOp
o-Cl
o-POp 1-CH-Ang
m-HH
o-IOp
o-D
m-SPH
(c)
52
o-CH A
l P-pH
t.a-PH
Figure 5.9: The cranial m uscles o f Ily o p h is brunneus, (a) Skin rem oved (late ra l
v ie w ); (b ) sections A2, hyohyoideus m uscle, lateral fib e rs o f th e le v a to r/a d d u c to r
operculi m uscle, epaxial m uscles, hypaxial m uscles, m a x illa ry bone, branchiostega!
rays and p rim o rd ia l lig a m e n t are rem oved (late ra l v ie w ); (c) ve n tra l view o f th e
rig h t side o f th e cranial m uscles (Skin is rem oved and subpharyngealis m uscle is
cu t). I-Io p -A n g , in te ro p e rc u lo -a n g u la r lig a m e n t; l-CH -Ang, c ra to h y a lo -a n g u la r
lig a m e n t; l-p rim , p rim o rd ia l lig a m e n t; l-M x-P M x-E t, m a x illo -p re m a x illo -e th m o id a l
lig a m e n t; l-UH-BH, u rohyalo-basihyal lig a m e n t; m -A 2a, ve n tra l subsection o f A2;
m -A2ß, dorsal subsection o f A2; m -A 3, A3 section o f th e a d d u cto r m andibulae
m uscle co m p le x; m -D O , d ila ta to r operculi m uscle; m -Epax, epaxial m uscles; m -H H,
hyohyoideus m uscle com p le x; m-l_AP, le v a to r arcus palatini m uscle; m -b/A O l,
lateral fibers o f le v a to r/a d d u c to r operculi m uscle; m -L/A O m , m edial fib e rs o f
le v a to r/a d d u c to r operculi m uscle; m-PH, p ro tra c to r hyoidei m uscle; m -SH ,
sternohyoideus m uscle; m-SPH, subpharyngealis m uscle; o-CH A, a n te rio r
ceratohyal bone; o-CI, cle ith ru m bone; o-D , d e n ta ry co m p le x; o-F, fro n ta l bone; oIO p, in te ro p e rcle ; o-M x, m a xilla ry bone; o-O p, opercle; o-POp, preopercle; o-SOp,
subopercle; o-UH, urohyal bone; t-A 2 ß , tendon o f A2ß; t.a-P H , a n te rio r tendon o f
p ro tra c to r hyoidei m uscle; t.p-P H , p o ste rio r tendon o f p ro tra c to r hyoidei m uscle; tSH, tendon o f sternohyoideus m uscle.
53
m-Epax
m-LO
m-A2ß
m-A3 m-AAP
o-Mx
o-PMx-Et
'v W V \ / 1 / V P ~ P V
1 mm
m-HH o-IOp 1-I0p-Ang
m-A2a
o-Op m-AO t-DO m-DO
o-Pg
1-prim
m-LAP m-A3
o-D
o-F
1 mm
o-SOp
o-D
m-AAP
1-Pg-Q m-AAP
m-PH
o-Hhy
o-D
o-UH
m-PH.I
m-PHC
1 mm
o-BH
o-CH A
54
t-SH
m-SH
o-Cl
Figure 5.10: The cranial m uscles o f S ynaphobranchus brevidorsalis, (a) Skin
rem oved (la te ra l v ie w ), (b) Sections A2, hyohyoideus m uscle, le v a to r operculi
m uscle, epaxial m uscles, hypaxial m uscles, m a x illa ry bone and p rim o rd ia l lig a m e nt
are rem oved (late ra l v ie w ), and (c) ve n tra l m uscles o f head; le ft low er ja w , a n te rio r
and p o ste rio r ce ra to hya l, and le ft m uscle bundle o f th e p ro tra c to r hyoidei (m -P H ),
and sternohyoideus (m -S H ) are rem oved. I-Io p -A n g , in te ro p e rc u lo -a n g u la r
lig a m e n t; l-p rim , p rim o rd ia l lig a m e n t; l-P g -Q , p te r y g o id e o - q u a d r a te lig a m e n t;
m -A A P , a d d u c to r a rc u s p a la tin i; m -A 2a, ve n tra l subsection o f A2; m -A2ß, dorsal
subsection o f A 2; m -A 3, A3 section o f th e a d d u cto r m andibulae m uscle com plex;
m -D O , d ila ta to r operculi m uscle; m -E pax, epaxial m uscles; m -H H, hyohyoideus
muscle c o m p le x ; m -L A P , le v a to r arcus palatini m uscle; m -A O , a d d u c to r operculi
m uscle; m -LO , le v a to r operculi m uscle; m -PH .I, la te ra l fib e rs o f p ro tra c to r hyoidei
m uscle; m -P H C , p h a r y n g o c le ith r a lis ; m -SH, ste rnohyoideus m uscle; o -B H ,
b a s ih y a l; o-CH A, a n te rio r ceratohyal bone; o-CI, cle ith ru m bone; o-D , d e n ta ry
com p le x; o-F, fro n ta l bone; o -H h y , h y p o h y a l b o n e ; o -IO p , in te ro p e rc le ; o-M x,
m a xilla ry bone; o-O p, opercle; o-PM x-Et, p re m a xillo -e th m o id a l co m p le x; o -P g ,
p te ry g o id b o n e ; o -S O p , s u b o p e rc le ; o -U H , u ro h y a l b o n e ; t-D O , te n d o n
o f d ila ta to r operculi m u s c le ;t-S H , te n d o n o f s te rn o h y o id e u s m u s c le .
55
a
b
c
56
Figure 6.1. Functional m orphological model o f pharyngeal ja w m o ve m e n t in M.
re tife ra . The le ft d e n ta ry has been rem oved in a -c , and th e le ft m axilla has been
rem oved in b and c. a, Pharyngeal ja w apparatus a t rest, b, Pharyngeal ja w
p ro tra cte d : th e le v a to r inte rnu s (L I) and le v a to r e xte rn u s (LE) p ro tra c t th e upper
ja w into th e oral c a vity, w hereas th e rectus com m unis (RC) p ro tra cts th e low er ja w .
D uring p ro tra c tio n , th e upper pharyngobranchial is d orsally ro tated by co ntraction
o f th e LI and th e obliqus dorsalis (OD). c, A fte r prey co n ta ct, th e a d d u cto r (AD)
co n tra cts to bring th e upper and low e r ja w s to g e th e r to d e liv e r a second bite. The
dorsal re tra c to r (DR) and p h aryn g o cle ith e ralis (PHC) re tra c t th e pharyngeal ja w s
back to th e ir resting position behind th e skull. Scale bar, 1 cm (a fte r Mehta and
W a in w rig h t, 2007a).
57
o-Epi
o-Par
o-ExOc
1mm
o-Pro
afsu sp P
o-Pro
afsuspA
o-PMx-Etv
o-F
fr-Opt
o-F
o-BOc
o-ExOc
fr-Tri.fac
1mm
o-ExOc
o-Sph o-PtSph o-BSph
o-PSph
Figure 6.2: N eurocranium o f A riosom a g ilb e rti, (a) Dorsal view and (b ) ve n tra l
view , af susp A, a n te rio r suspensorial a rticu la tio n fa ce t; a f susp p, p o ste rio r
suspensorial a rtic u la tio n fa c e t; fr-O p t, foram en o p tic u m ;fr-T ri.fa c , foram en
trig e m in o -fa c ia lis ; o-BOc, basioccipital bone; o-B Sph, basisphenoid; o-Epi,
epioccipital bone; o-ExOc, exoccipital bone; o-F, fro n ta l bone; o-Par, parietal bone;
o-PM x-Etv, p re m a xillo -e th m o vo m e ra l com plex; o-Pro, p ro otic bone; o-PSph,
parasphenoid; o-Pt, p te ro tic bone; o-PtS ph, p te ro sphenoid; o-S ph, sphenotic bone.
58
o-Pro
af susp P
o-Par
o-PtSph
o-Sph
o-BSph
o-Mx o-PMx-Etv
o-F
o-Epi
o-Pt
o-ExOc
o-Op
o-SOp
1 mm
o-IOp
ae Op ae susp P
0-Hm
o-POp o-PSph o-Ang o-PP
o-D
ac SUSP A
1 mm
o-PP
Figure 6.3: Cranial skeleton o f A riosom a g ilb e rti (Lateral v ie w ), (a) C om plete skull
(rig h t side) and (b) Suspensorium (rig h t side), ae Op, o p ercu la r a rtic u la r condyle; a f
susp p, p o ste rio r suspensorial a rticu la tio n fa c e t; ae susp A, a n te rio r suspensorial
condyle; ae susp P, p o ste rio r suspensorial condyle; o-A ng, a n gu la r bony com plex ;
o-BSph, basisphenoid bone; o-D , d e n ta ry co m p le x; o-Epi, epioccipital bone; oExOc, exoccipital bone; o-F, fro n ta l bone; o-H m , h yo m an d ibu la r bone; o -Io p ,
inte rop e rcle ; o-M x, m a x illa ry bone; o-O p, opercle; o-Par, parietal bone; o-PM x-Etv,
p re m a xillo -e th m o vo m e ra l co m p le x; o-POp, preopercle; o-PP, p a la to p te ryg o id ; oPro, p ro otic bone; o-PSph, parasphenoid; o-P t, p te ro tic bone; o-PtSph,
pterosphenoid bone; o-Q, q u a d ra te ; o-SOp, subopercle; o-S ph, sphenotic bone.
59
cm ST
cT
c SO
mm
(a)
c POM
c IO
o-Nas
o-InfOrb
o-Lac
Figure 6.4: The cranial lateral line system o f A riosom a g ilb e rti, (a) position o f th e
com posing canals in relation to th e skull (rig h t side, lateral vie w ) and (b ) lateral
view o f th e nasal bone, lacrim al bones and in fra o rb ita l bones (rig h t side) (re la tive
position o f bones do not correspond to th e ir real p o sitio n ), c IO , in fra o rb ita l canal; c
POM, pre op e rcu la r m a n d ib u la r canal; c SO, su p rao rb ita l canal; c T, te m p o ral canal;
cm ST, su p ratem p o ra l co m m issure; o-Nas, nasal bone; o -In fO rb , in fra o rb ita l bone;
o-Lac, lacrim al bone.
60
af Mx-Etv
lmm
o-Mx
(a)
pr Cor
o-Ang
af Md
lmm
(b)
o-D
o-CorMec
fs-Mec
o-ra
F ig u re 6 .5 : Jaws o f A riosom a g ilb e rti (rig h t side) (a -b ), m a x illa ry ; m edial view (a ),
and low er ja w ; m edial view (b ). a f Md, m a n dib u la r a rticu la tio n fa c e t; a f M x-Etv,
m a xillo -e th m o vo m e ra l a rtic u la r fa c e t; o-A ng, a n g u la r bony com plex ; o-D , d e n ta ry
com p le x; o-M x, m a x illa ry bone; o-CorM ec, coronom eckelian bone; fs-M ec,
m eckelian fossa; p r Cor, coronoid process; o -ra , re tro a rtic u la r bone.
61
o-SOp
o-Op
a f Op
o-BH
o-UH
lm m
■apo-Op
1mm
o-IOp
o-POp
1mm
o -C H P
o-CH A
F ig u re 6 .6 : O percular series and hyoid apparatus o f A riosom a g ilb e rti, (a)
O percular series; lateral view (rig h t side) and (b ) hyoid a p pa ra tu s; lateral view s o f
th e a n te rio r ceratohyal and p o ste rio r ceratohyal bones, dorsal view s o f urohyal, and
lateral view o f basihyal (rig h t side), a f Op, o p ercu la r a rtic u la r fa c e t; apo-O p,
apophysis o f opercle; o-BH, basihyal bone; o-CH A, a n te rio r ceratohyal bone; o-CH
P, p o ste rio r ceratohyal bone; o -Io p , inte rop e rcle ; o-O p, opercle; o-POp, preopercle;
o-SOp, subopercle; o-UH, urohyal bone.
62
I--------1
1mm
m-Trans.v
o-LP
(b) o-Bb 1 o-Hb I
m-Ob.v II
o-Cb I
m-Rc
m-PHC
F ig u re 6 .7 : Gili arches and associated m uscles o f A riosom a g ilb e rti, (a) Dorsal view
o f th e ve n tra l p a rt and (b) ve n tra l view o f th e dorsal p a rt o f th e gili arch. o-Bb,
basibranchia! bone; o-Cb, ceratobranchia! bone; o-Eb, epibranchial bone; o-Hb,
hypobranchial bone; o -Ib , infra ph a ryn go b ra n chia l bone; o-LP, low er pharyngeal
to o th plates; o-UP, upper pharyngeal to o th plates; m -O b .d .m , m edial obliqus
dorsalis
m uscle;
m -O b .v,
ve n tra l
obliqus
dorsalis
m uscle;
m-PHC,
p h aryn g o cle ith ra lis m uscle; m -Rc, rectus com m unis m uscle; m -RD, rectus dorsalis
m uscle; m -R D .m , m edial rectus dorsalis m uscle; m -T ra n s.v, tra n sve rsus v e n tra lis
muscle.
63
m-Epax
m-LO
m-HH
t-LO m-A2ßp m-A2ßa t-A2ß
o-PSph o-Mx
m-HH sup m-A2a 1-Iop-Ang t-A2
m-AO
m-DO
m-A3
m-AAP
4
*\ \
l-prim
11- 1 \ I \ 1 i\
__ -
M
1------1
2 mm
o-SOp
t-PH
o-IOp
m-PH
t-Do
o-D
m-LAP
-
t-A3
o-UH
IB I
(b)
1-CH-Ang
m-HH sup
1 mm
l-BH-CH
64
m-SH m-Hyp o-IOp (c)
F ig u re 6 .8 : The cranial m uscles o f A riosom a g ilb e rti, (a) Skin rem oved (lateral
v ie w ), (b ) sections A2, hyohyoideus m uscle com plex, epaxial m uscles, hypaxial
m uscles, ve n tra l m uscles o f th e head, branchiostega! rays and p rim o rd ia l lig a m e nt
are rem oved (late ra l vie w ) and (c) ve n tra l m uscles o f head (sa g itta l left cu t),
hyohyoideus m uscle com plex is rem oved and (d) Position o f th e m uscles on the
m edial face o f th e Suspensorium . I-CH-Ang, c e ra to h y a lo -a n g u la r lig a m e n t; l-BH-CH,
b asihyalo-ceratohyal lig a m e n t; l-Io p -A n g , in te ro p e rc u lo -a n g u la r lig a m e n t; l-p rim ,
p rim o rd ia l lig a m e n t; m -A 2a, ve n tra l subsection o f A2; m -A2ßa, a n te rio r p a rt o f
dorsal subsection o f A2ß; m -A 2ßp, p o s te rio r p a rt o f dorsal subsection o f A2ß; mA3, A3 section o f the a d d u cto r m andibulae m uscle co m p le x; m-AAP, a d d u cto r arcus
palatini m uscle; m -AO , a d d u cto r operculi m uscle; m -D O , d ila ta to r operculi m uscle;
m -Epax, epaxial m uscles; m -H H, hyohyoideus m uscle com p le x; m-HH sup,
hyohyoideus su p e rio r m uscle; m -H yp, hypaxial m uscles; m-LAP, le v a to r arcus
palatini m uscle; m -LO, le v a to r operculi m uscle; m-PH, p ro tra c to r hyoidei m uscle;
m -SH , ste rnohyoideus m uscle; o-BH, basihyal bone; o-D , d e n ta ry com plex; o -IO p ,
inte rop e rcle ; o-M x, m a x illa ry bone; o-P M x-E tv, p re m a xillo -e th m o vo m e ra l com plex;
o-PSph, parasphenoid bone; o-SO p, subopercle; o-UH, urohyal bone ; t-A 2 , tendon
o f A2 ; t-A 2 ß , tendon o f A2ß; t-A 3 , tendon o f A3; t-D O , tendon o f d ila ta to r operculi
m uscle; t-LO , tendon o f le v a to r o p ercu li; t-PH , tendon o f p ro tra c to r hyoidei.
65
o-Sph
o-PtSph 0_F o-BSph
o-Mx
o-PMx-Etv
o-Pt
o-Hm
Op-tuberosity
o-Op
2 mm
o-
o-IOp o-POp
"p
o-PP
I-Q-Mx
o-PSph
‘o-Ang
o-Hm
ae susp P ae susp A
ac Op
af Op
1 mm
o-Op
o-SOp o-POp
66
o-Q
o-PP
F ig u re 6 .9 : Cranial skeleton o f G ym n o th o ra x pra sin u s (late ra l v ie w ), (a ) C om plete
skull (rig h t side) and (b) Suspensorium (rig h t side), ae Op, o p ercu la r a rtic u la r
condyle; a f Op, o p ercu la r a rtic u la r fa c e t; ae susp A, a n te rio r suspensorial condyle;
ae susp P, p o s te rio r suspensorial condyle; l-Q -M x, q u a d ra to -m a x illa ry lig a m e n t; oAng, A n g ula r bony co m p le x; o-B S ph, basisphenoid bone; o-D , d e n ta ry co m p le x; oF, fro n ta l bone; o -H m , h yo m a n d ib u la r bone; o -Io p , inte rop e rcle ; o-M x, m a xilla ry
bone; o-O p, opercle; o-Par, parietal bone; o-PM x-E tv, p re m a xillo -e th m o vo m e ra l
com p le x; o-POp, preopercle; o-PP, p a la to p te ry g o id ; o-PSph, parasphenoid; o-Pt,
p te ro tic bone; o-PtS ph, pterosphenoid bone; o-Q , q u a d ra te ; o-SO p, subopercle; oSoc, supraoccipital bone; o-S ph, sphenotic bone ; O p -tu b e ro sity, o p ercu la r
tu b e ro sity.
67
o-SOc o-Par o-Sph
o-PtSph
0-F
o-BSph
0-Mx
o-PMx-Etv
o-Epi
o-ExOc
o-Pt
o-Op
o-SOp
I mm
o-IOp
o-Ang
o-PP
o-PSph
fr-Opt
ae susp P o-Hm
ae susp A
ae Op
a f Op
o-Op
o-SOp o-POp
68
o-Q
F ig u re 6 .1 0 : Cranial skeleton o f A narchias a lla rd ice i (late ra l v ie w ), (a) C om plete
skull (rig h t side) and (b) Suspensorium (rig h t side), ae Op, o p ercu la r a rtic u la r
condyle; a f Op, o p ercu la r a rtic u la r fa c e t; ae susp A, a n te rio r suspensorial condyle;
ae susp P, p o ste rio r suspensorial condyle; fr-O p t, foram en o p tic u m ; o-A ng, a n gu la r
bony com plex ; o-BS ph, basisphenoid bone; o-D , d e n ta ry co m p le x; o-ExOc,
exoccipital bone; o-F, fro n ta l bone; o -H m , h yo m a n d ib u la r bone; o -Io p ,
inte rop e rcle ; o-M x, m a x illa ry bone; o-O p, opercle; o-Par, parietal bone; o-PM x-Etv,
p re m a xillo -e th m o vo m e ra l co m p le x; o-POp, preopercle; o-PP, p a la to p te ryg o id ; oPSph, parasphenoid; o-P t, p te ro tic bone; o-PtSph, pterosphenoid bone; o-Q,
q u a d ra te ; o-SOp, subopercle; o-Soc, supraoccipital bone; o-S ph, sphenotic bone.
69
o-Epi
o-Par
o-F
o-Pt
ri-SOc
o-ExOc
lmm
o-PMx-Etv
o-SOc
a f susp P
o-Sph
a f susp A o-PSph
o-F
fr-Tri.fac
o-BOc
1mm
(b)
o-Pt
o-Pro
o-Sph
o-PtSph
F ig u re 6 .1 1 : N eurocranium o f G ym n o th o ra x prasinus, (a ) Dorsal view and (b)
ve n tra l view , a f susp A, a n te rio r suspensorial a rticu la tio n fa c e t; a f susp p, p o ste rio r
suspensorial a rticu la tio n fa c e t; fr-T ri.fa c , foram en trig e m in o -fa c ia lis ; o-BOc,
basioccipital bone; o-Epi, epioccipital bone; o-ExOc, exoccipital bone; o-F, fro n ta l
bone; o-Par, parietal bone; o-PM x-E tv, p re m a xillo -e th m o vo m e ra l co m p le x; o-Pro,
prootic bone; o-PSph, parasphenoid; o-P t, p te ro tic bone; o-PtSph, pterosphenoid;
o-Soc, supraoccipital bone; o-S ph, sphenotic bone ; ri-S oc, supraoccipital crest.
70
o-Epi
o-Par
lmm
o-Pt
ri-SOc
o-ExOc
o-SOc
af susp P
o-PMx-Etv
o-Sph
a f susp A o-PtSph
o-F
oO O
o-BOc
o-ExOc
lmm
(b)
o-Pt o-Pro
fr-Tri.fac
o-PSph
o-BSph
F ig u re 6 .1 2 : N eurocranium o f A narchias allardicei, (a) Dorsal view and (b ) ve n tra l
view , a f susp A, a n te rio r suspensorial a rticu la tio n fa c e t; a f susp p, p o ste rio r
suspensorial a rticu la tio n fa c e t; fr-T ri.fa c , foram en trig e m in o -fa c ia lis ; o-BOc,
basioccipital bone; o-B Sph, basisphenoid; o-Epi, epioccipital bone; o-ExOc,
exoccipital bone; o-F, fro n ta l bone; o-Par, parietal bone; o-PM x-Etv, p re m a xillo e th m o vom e ra l com p le x; o-Pro, p ro otic bone; o-PSph, parasphenoid; o-Pt, p te ro tic
bone; o-PtSph, pterosphenoid; o-Soc, supraoccipital bone; o-S ph, sphenotic bone ;
ri-S oc, supraoccipital crest.
71
m-Epax
m-LO
m-A2al
t-A2al m-A3
o-Mx
m-LO l-LO
m-LAP
o-F
m-A3
o-PMx-Etv
m-Epax
C-*
-JTi\irg_
(a)
1-A2-Q
n-HH
l-PH
l-Q-Mx o-CH A o-D m-PH
m-A2al
(medial fibers)
Pr Cor
m-RC
o-D
m-DO in-A2y
iA2y
t-A3
o-D
m-L¡
m-APh.I
2 miri
o-ExOc
o-Pro
m-AH
m-AAP
o-O
m-HH sup
m-PH
o-CH A
o-CHP
m-SH
m -A O
o-CI
o-Op
(c)
<d)
72
F ig u re 6 .1 3 : The cranial m uscles o f G ym n o th o ra x prasinus, (a) Skin rem oved
(late ra l vie w ), (b ) sections A2 except th e subsection A 2m , hyohyoideus m uscle
com plex, hypaxial m uscles, ve n tra l elem ents o f th e head and q u a d ra te -m a x illa ry
lig a m e n t and branchiostega! rays are rem oved (la te ra l v ie w ), (c) V entral m uscles o f
head (sa g itta l le ft c u t), hyohyoideus m uscle com plex is rem oved. I-Q -M x, q u ad ra to m a xilla ry lig a m e n t; m -A 2al, lateral subsection o f A 2a; m -A 2 y, m edial subsection o f
A2; m -A 3, A3 section o f th e a d d u cto r m andibulae m uscle co m p le x; m-AAP,
a d d u cto r arcus palatini m uscle; m -AH , a d d u cto r hyom andibulae m uscle; m -AO,
a d d u cto r operculi m uscle; m-APhJ, a d d u cto r m uscle o f th e pharyngeal ja w ; m -DO,
d ila ta to r operculi m uscle; m -Epax, epaxial m uscles; m -H H, hyohyoideus muscle
com p le x; m-HH sup, hyohyoideus su p e rio r m uscle; m-LAP, le v a to r arcus palatini
m uscle; m -Li, le v a to r inte rnu s m uscle; m -LO, le v a to r operculi m uscle; m-PH,
p ro tra c to r hyoidei m uscle; m-RC, rectus com m unis m uscle; m -SH , sternohyoideus
m uscle; o-CH A, a n te rio r ceratohyal bone; o-CH P, p o ste rio r ceratohyal bone; o-CI,
c le ith ru m ; o-D , d e n ta ry co m p le x; o-ExOc, exoccipital bone; o-F, fro n ta l bone; oMx, m a xilla ry bone; o-O p, opercle; o-P M x-Etv, p re m a xillo -e th m o vo m e ra l com plex;
o-Pro, p rootic bone; o-Q, qu ad ra te bone; t-A 2 a l, tendon o f A2al ; t-A 2 -Q , A2quadrate te n d o n ; t-A 2 y , tendon o f A 2 y; t-A 3 , tendon o f A 3; t-E p a x, tendon o f
epaxial m uscles ; t-LO , tendon o f le v a to r o p ercu li; t-PH , tendon o f p ro tra c to r
hyo id e i; pr Cor, coronoid process.
73
mm
o-Mx
af Mx-Etv
pr Cor
o-Ang
af Md
lmm
(b)
o-D
fs-Mec
pr ra
F ig u re 6 .1 4 : Jaws o f G ym n o th o ra x pra sin u s (rig h t side) (a -b ), m a x illa ry ; lateral
view (a ), and low er ja w ; m edial view (b ). a f Md, m a n d ib u la r a rtic u la tio n fa c e t; a f
M x-Etv, m a x illo -e th m o v o m e ra l a rtic u la r fa c e t; o-A ng, a n gu la r bony com plex ; o-D ,
d e n ta ry co m p le x; o-M x, m a x illa ry bone; fs-M ec, m eckelian fossa; p r Cor, coronoid
process; pr ra, re tro a rtic u la r process.
74
lmm
(a)
o-Mx
afM x-Etv
pr Cor
o-Ang
af Md
1-POp-Ang
lmm
o-D
fs-Mec
o-CorMec
pr ra
F ig u re 6 .1 5 : Jaws o f A narchias a lla rd ice i (rig h t side) (a -b ), m a x illa ry ; m edial view
(a ), and low er ja w ; m edial view (b ), a f Md, m a n d ib u la r a rticu la tio n fa c e t; a f MxEtv,
m a xillo -e th m o vo m e ra l
a rtic u la r fa ce t;
l-P op-A ng,
p re op e rcu lo -a n gu la r
lig a m e n t; o-A ng, a n gu la r bony com plex ; o-D , d e n ta ry co m p le x; o-CorM ec,
coronom eckelian bone; o-M x, m a x illa ry bone; fs-M ec, m eckelian fossa; p r Cor,
coronoid process; pr ra, re tro a rtic u la r process.
75
m-HH
o-POp t-A2-0 m-SH t-A2
m-LO t-LO
o-CH A
m-PH
o-PMx-Etv
m-A3
m-LAP
o-D
o-Op
t-DO m-DO
o-CH A
o-CH P
76
m-SH
(c)
F ig u re 6 .1 6 : The cranial m uscles o f A narchias allardicei, (a) Skin rem oved (late ra l
vie w ), (b ) sections A2, hyohyoideus m uscle com plex, epaxial m uscles, hypaxial
muscles, ve n tra l elem ents o f th e head and q u a d ra to -m a x illa ry lig a m e n t and
branchiostega! rays are rem oved (late ra l v ie w ) and (c) ve n tra l m uscles o f head
(sa g itta l le ft cu t) and position o f th e pharyngeal ja w s in relation to th e low e r ja w
and hyoid apparatus, hyohyoideus m uscle com plex is rem oved. m -A 2a, ve n tra l
subsection o f A2; m -A2ß, dorsal subsection o f A 2; m -A 3, A3 section o f th e a d du ctor
m andibulae m uscle com plex; m-APhJ, a d d u cto r m uscle o f th e pharyngeal ja w ; m DO, d ila ta to r operculi m uscle; m -Epax, epaxial m uscles; m -H H, hyohyoideus
muscle co m p le x; m-l_AP, le v a to r arcus palatini m uscle; m -LO, le v a to r operculi
m uscle; m-PH, p ro tra c to r hyoidei m uscle; m-RC, rectus com m unis m uscle; m -SH ,
sternohyoideus m uscle; o-CH A, a n te rio r ceratohyal bone; o-CH P, p o ste rio r
ceratohyal bone; o -D , d e n ta ry co m p le x; o-F, fro n ta l bone; o-M x, m a x illa ry bone; oOp, opercle; o-PM x-E tv, p re m a xillo -e th m o vo m e ra l co m p le x; o-POp, preopercle; tA2, tendon o f A2; t-A 2 -Q , A 2 -q ua d ra te te n d o n ; t-A 3 , tendon o f A3; t-D O , tendon of
d ila ta to r operculi m uscle; t-LO , tendon o f le v a to r o p e rcu li; t-PH , tendon o f
p ro tra c to r hyoidei; p r Cor, coronoid process.
77
o-SOrb
o-Införb
1 mm
o-Nas
o-Adn
a)
cm ST
cT
c SO
c Adnas
c Et
1 mm
c IO
cPOM
(b)
F ig u re 6 .1 7 : The cranial lateral line system and circu m o rb ita l bones o f
G ym n o th o ra x prasinus, (a) Lateral view o f th e nasal bone, p re orb ita l bones,
in fra o rb ita l bone, p o storbital bones and su p rao rb ita l bones (rig h t side) and (b )
position o f th e com posing canals in relation to th e skull (rig h t side, lateral v ie w ), c
Adnas, adnasal canal; c Et, eth m o id canal; c IO , in fra o rb ita l canal; c POM,
pre op e rcu la r m a n d ib u la r canal; c SO, su p rao rb ita l canal; c T, te m p o ral canal; cm
ST, su p ratem p o ra l co m m issure; o-N as, nasal bone; o-A dn, adnasal bone; o -In fO rb ,
in fra o rb ita l bone; o-Lac, lacrim al bone; o-SO rb, su p rao rb ita l bone.
78
o-Nas
o-Lac
1 mm
(a)
cm ST
cT
cm F
c SO
<x.
1 mm
(b)
c POM
c IO
F ig u re 6 .1 8 : The cranial lateral line system and circu m o rb ita l bones o f A narchias
allardicei, (a) lateral view o f th e nasal bone, p re orb ita l bones and p o sto rbita l bones
(rig h t side) and (b ) position o f th e com posing canals in relation to th e skull (rig h t
side, lateral v ie w ), c IO , in fra o rb ita l canal; c POM, pre op e rcu la r m a n dib u la r canal; c
SO, su p rao rb ita l canal; c T, te m p o ral canal; cm F, fro n ta l co m m issure; cm ST,
su p ratem p o ra l co m m issure; o-Nas, nasal bone; o -In fO rb , in fra o rb ita l bone; o-Lac,
lacrim al bone.
79
o-Eb I
o-Eb IV
o-UP
lmm
o-LP
=s-----—~~
o-Cb IV
o-C bl
F ig u re 6 .1 9 : Gili arches o f G y m n o th o ra x prasinus, (a) V entral view o f th e dorsal
elem ents and (b ) dorsal view o f th e ve n tra l elem ents. o-Cb, ceratobranchia! bone;
o-Eb, epibranchial bone; o-LP, low er pharyngeal to o th plates; o-UP, upper
pharyngeal to o th plates.
o-Eb IV
o-Ib I
lmm
-o -U P
o-LP
o-Cb IV
o-Cb I
o-Eb II
F ig u re 6 .2 0 : Gili arches o f A narchias allardicei. Lateral view o f th e ve n tra l and
dorsal p a rt o f th e gili arches (rig h t side). o-Cb, ceratobranchia! bone; o-Eb,
epibranchial bone; o -Ib , infra ph a ryn go b ra n chia l bone; o-LP, low er pharyngeal to o th
plates; o-UP, upper pharyngeal to o th plates.
80
(lat)Cond-Q
o-Q
(a)
(med)Cond-Q
Mand
o-Man o-Mx
l-(med)Man-Q
1-Mx-Mand
F ig u re 7 .1 : Cranial skeleton in E u ryp h a ryn x pelecanoides (Lateral v ie w ), (a)
C om plete scanned skull (rig h t side), and (b) m edial view th e q u ad ra to -m a nd ib u la
jo in t (rig h t side), c -o rb ito -e th m o id ca rtila g e ; (lat)C o n d -Q , lateral condyle o f
q u a d ra te ; (m ed)C ond-Q , m edial condyle o f q u a d ra te ; l-(m e d )M a n-Q , medial
m a n dib u lo -q u ad ra te lig a m e n t; l-S e-M an, Sesam oid bone-m andibula lig a m e n t; oBOc, basioccipital; o-E pi, ep io ccipita l; o-ExOc, e xo ccip ita l; o-F, fro n ta l; o-H m ,
h yo m an d ibu la ; Mand, m andíbula; o-M x, m a x illa ry ; o-Par, p a rie ta l; o-P t, p te ro tic ; oQ, q u a d ra te ; o-Se, sesam oid bone; o-S ph, sphenotic; o-V, v o m e r; o - V e l, firs t
v e rte b ra ; m -A m , a d d u cto r m andibulae m uscle; t-A m , tendon o f th e a d d u cto r
m andibulae m uscle.
81
o-Pt
o-Par
o-Sph
c-Orb-Et
o-ExOc
o-Vel
o-BOc
fr-Mag
o-F
o-Epi
o-Pt
a f susp
o-Sph
0_v
o-ExOc
o-BOc
2mm
(b)
o-PSph
o-Pro
82
c-Orb-Et
F ig u re 7 .2 : N eurocranium o f E u ryp h a ryn x pelecanoides, (a) Dorsal view , and (b)
Ventral view , a f susp, suspensorial a rticu la tio n fa c e t; c -o rb ito -e th m o id ca rtila g e ; frMag, foram en m a g nu m ; o-BOc, basioccipital; o-Epi, ep io ccipita l; o-ExOc,
e xo ccip ita l; o-F, fro n ta l; o-Par, p a rie ta l; o-Pro, p ro o tic; o-PSph, parasphenoid; o-Pt,
p te ro tic ; o-S ph, sp henotic; o-V, v o m e r; o - V e l, firs t ve rte b ra.
83
c-Orb-Et
t-( lat)LAP
t-(vent)p.DM
a-DM-m
o-Hm
l-(iü t)M an -Q
m-Epax
84
t-(lat)Epax
m-AH
F ig u re 7 .3 : The cranial m uscles o f E u ryp h a ryn x pelecanoides, (a) Skin rem oved
(late ra l vie w ) and does not show e n tire length o f th e m andíbula, and (b ) m uscles o f
th e ve n tra l view o f neurocranium . m-AAP, a d d u cto r arcus palatini m uscle; m -A m ,
a d d u cto r m andibulae m uscle; m -AH , a d d u cto r hyom andibulae m uscle; a-D M -m ,
a n te rio r depressor m andibulae m uscle; p-D M -m , p o ste rio r depressor m andibulae
m uscle; m -E pax, epaxial m uscles; m -H yp, hypaxial m uscles; m-l_AP, le v a to r arcus
palatini m uscle; c -o rb ito -e th m o id ca rtila g e ; o-BOc, basioccipital; o-Epi, e p io c c ip ita l;
o-ExOc, e xo ccip ita l; o-F, fro n ta l; o -H m , h yo m a n d ib u la r bone; Mand, m andíbula; oMx, m a xilla ry bone; o-Par, p a rie ta l; o-Pro, p ro o tic; o-P t, p te ro tic ; o-Q , q u a d ra te ; oSe, sesam oid bone; o-S ph, sp henotic; o-V , v o m e r; o - V e l, firs t v e rte b ra ; Orb, o rb it;
t-A m , a d d u cto r m andibulae te n d o n ; t(v e n t)p .D M , ve n tra l tendon o f p o ste rio r
depressor m andibulae m uscle; t(d o r)p .D M , dorsal tendon o f p o ste rio r depressor
m andibulae m uscle; t(la t)E p a x , lateral tendon o f epaxial m uscles; t-H y p , tendon o f
h yp axia l; t-LAP, tendon o f le v a to r arcus palatini m uscle.
85
External epiderm is contains
dense m elanophores
Internal
dermis
External dermis
M uscle fiber
hyalin cartilage
Lamella o f
cartilage
Perichondral bone
(b)
F ig u re 7 .4 : Histological section o f th e skin and bone in E u ryp h a ryn x p e le ca n oid e s:
(a) cross section o f th e skin around th e m o u th , and (b) cross section o f the
hyom andibula.
86
(a)
(b)
F ig u re 7 .5 : Stages o f supposed feeding s tra te g y by Nielsen e t al. (1 9 8 9 ) (a fte r
Nielsen e t al. 1989).
87
88
F ig u re 7 .6 : Stages o f feeding in E u ryp h a ryn x p e le ca n oid e s: (a) S w im m in g, (b )
detecting th e prey and s ta rtin g p o in t o f m outh opening, (c) firs t stage o f m outh
opening, (d ) opened m outh a t nearly a rig h t angle, (e) m oving to w a rds th e prey
w ith th e m outh opened, (f) engulfing o f th e prey, (g ) closing m o u th ,(h ) food item s
stay in th e ve n tra l pouch o f th e buccal c a v ity (a fte r Blue planet: Eposid2 - The
Deep, 2001).
89
F ig u re . 8 .1 . Photographs show ing typ ica l head and ja w shapes o f m any typ e s o f
a n g u illifo rm leptocephali. These taxa are A n g uilla m a rm o ra ta (A ), A riosom a m a jo r
(B ), H ete roco n g er hassi (C ), C onger sp. (D ), B athycongrus sp. (E), G nathophis sp.
(F), M uraenesox cinereus (G ), S errivo m e rid a e sp. (H ), M uraenidae sp. ( I) ,
Chlopsidae sp. (J), N ettenchelys sp. (K ), and S ynaphobranchinae sp. (L),
Ilyo p h in a e , Synaphobranchidae (M ), E u ryp h a ryn x pelecanoides (N ), Cyema a tru m
( 0 ) . (a fte r M iller and T sukam oto, 2004).
90
F ig u re . 8 .2 . S chem atic illu s tra tio n o f th e generated forces by th e a d d u cto r
m andibulae A2 (F2) and A2 (F3) w ith , respectively, th e ir horizontal (Fh 2 and Fh 3)
and ve rtica l com ponents (Fv 2 and Fv 3). The horizontal com ponents run in the
opposite d ire ctio n , reducing th e pressure in th e jo in t betw een th e low er ja w and the
q u adrate (encircled) (a fte r De Schepper e t al, 2005).
91