a review on the avian chondrocranium
TRANSCRIPT
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nium of birds including a full description
bital region and ethmoid region.he Egyptian German Society for Zoology.
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Beer and Barrington (1934), De Beer
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The Journal of Basic & Applied Zoology (2013) 66, 109–120
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review on the avian chondrocranium
ostafa M. Zaher *, Amir M. Abu-Taira
partment of Zoology, Faculty of Science, Cairo University, Giza, Egypt
ceived 9 April 2013; revised 2 October 2013; accepted 2 October 2013
ailable online 19 December 2013
EYWORDS
hondrocranium;
irds
Abstract This review article is a review on the chondrocra
about basal plate and occipital region, auditory region, or� 2013 Production and hosting by Elsevier B.V. on behalf of T
ntents
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The neurocranium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .The basal plate and the occipital region . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .The auditory region . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The orbital region . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .The ethmoid region . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
roduction (1907), Rice (1920), De
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e chondrocranium of birds in general is now well known asattracted the interest of many Zoologists such as Sonies
(1937), Lutz (1942), Lang (1952), Frank (1954), Engelbrecht
(1958), May (1961), Muller (1961), Macke (1969), Mokhtar(1975), Mokhtar et al. (1983) and Vorster (1989).
Moreover, Zaher et al. (1991, 1993), Abu-Taira (1996,
1997), Nakane and Tsudzuki (1999), Abd El-Hady (2008),Atalgin and Kurtul (2009), Marugan-Lobon and Buscalioni(2009), Zaher and Riad (2009), El-Shikha (2011) and Zaher
and Riad (2012a,b,c) added more to the accurate and detailedknowledge of the avian chondrocranium.
In addition to all these above mentioned works, there areother articles dealing with certain elements of some regions
of the avian chondrocranium such as those of Zaher and Riad
Corresponding author. Tel.: +20 1005297098.-mail address: [email protected] (M.M. Zaher).
r review under responsibility of The Egyptian German Society for
ology.
Production and hosting by Elsevier
0-9896 � 2013 Production and hosting by Elsevier B.V. on behalf of The Egyptian German Society for Zoology.
p://dx.doi.org/10.1016/j.jobaz.2013.10.001
(2012d, in press, f) on the cranial ribs, parapolar cartilage andta
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De Beer and Barrington (1934) found, in the 138 h stage ofordal cartilages projecting immediatelyal on each side of the notochord. These
ely form part of the basal plate, and willl fenestra between them when they havewith the parachordal and the cochlear
peaks in favour of the formation of thecartilage in an embryo of Phalacrocorax
th. However, as it is evident from hisof formation of the anterior parachor-quite different from that mentioned inBarrington, 1934). In Phalacrocorax
ral end of the parachordal plate developsof two anterior diverging parachordalsotochord. They pass more in the rostral
hey produce two masses of condensedeet medially in the form of a transversehe origin of the acrochordal cartilage.
ior basicranial fenestra is encounteredrtilage anteriorly, the basal plate posteri-rior parachordals laterally on both sides.
achordals in both Anas and Phalacroco-t origins.schkin, 1899), Pyromelana (Engelbrecht,rops (Mokhtar, 1975), Pterocles (Mokh-
ser (Zaher et al., 1991), Corvus (Zaherlia (Zaher and Riad, 2009) and Columbabasal plate lacks a basicranial fenestra in
tal stages, but later on by resorption ofis formed. Among the other described
z, 1942), the night-jar and the ostrich
ica atra (Macke, 1969), a posterior basi-pletely absent in all ontogenetic stages.tion that the initial absence of the pos-
stra, observed in the early stages of thebirds, is reminiscent with what is re-early developmental stages of Urodela,ocodilia (De Beer, 1937) and Ophidia
da, 1965). It is thus possible to considerfenestra in some birds (either in earlyor during all ontogenetical stages) as a
character. If the fenestra later appearstion of cartilage in some of these forms,d as a secondary modification. If such a
e, it will be difficult to explain the condi-r and Barrington, 1934), Gallus (Sonies,ax (Slaby, 1951). Also it seems bewilder-e condition of crocodilia as why no sec-
has been realised when compared with
110 M.M. Zaher, A.M. Abu-Taira
he precarotid plate of Passer, Pterocles and Streptopelia. Theuthors concluded that a review on the development of the
vian chondrocranium would be very useful to enrich knowl-dge of this subject.
he neurocranium
he basal plate and the occipital region
he study of the early stages of the avian neurocranium cor-oborates that the basal plate is the product of three distinct
lements. These are the parachordal plate, the acrochordal car-ilage and two discrete occipital vertebrae; Vorster (1989) inallus, Zaher and Abdeen (1991) in Charadrius, Zaher et al.
1993) in Corvus, Nakane and Tsudzuki (1999) in Japaneseuail, Abd El-Hady (2008) in Coturnix, Zaher and Riad2009) in Streptopelia and El-Shikha (2011) in Columba.
The verdict that the acrochordal anlage and the parachor-
al plate have a simultaneous appearance prior to any otherhondrocranial element, and that the former has an acceler-ted chondrification than the latter seems unique among the
o far studied birds. This fact does not confirm the findingsf Parker (1891) in Apteryx, Sonies (1907) and Van Wijhe1907) in Anas and Gallus, De Beer and Barrington (1934) in
nas, Mokhtar (1975) in Upupa and Merops, Mokhtar et al.1983) in Pterocles, Zaher et al. (1991) in Passer, Zaher andbdeen (1991) in Charadrius, Zaher et al. (1993) in Corvus,
nd Abd El-Hady (2008) in Coturnix that the acrochordal an-age is the first chondrocranial element to appear. In Phala-rocorax, as maintained by Slaby (1951) the parachordallate appears first, and soon grows rostrally as two anterior
arachordals, which enclose the posterior basicranial fenestra.his latter is closed anteriorly when the anterior parachordalshare in developing a transverse bar, which represents the
crochordal anlage. Crompton (1953) refers that the blastema-ous anlage of the acrochordal cartilage, which arises in Sphe-iscus forms the anterior end of the parachordals. Frank
1954) asserts that the acrochordal cartilage in Struthio devel-ping after the perichordal plate has been laid down.The fact that the parachordal plate has one centre of chon-
rification in birds (Sonies, 1907; Jager, 1926; Slaby, 1951;
okhtar, 1975; Zaher and Riad, 2009) contradicts the viewf Goodrich (1930) and De Beer (1937) about the exact naturef the parachordal plate in vertebrates in general. Even De
eer and Barrington (1934) confirm the single origin of thearachordal plate in Anas, but indicate it as a secondary mod-fication. However, among birds so far described, the only
xception is the condition mentioned by Parker (1891) in
Anas, anterior parachbehind the acrochord
cartilages will ultimatenclose the basicraniaestablished connection
capsule.Slaby (1951) also s
anterior parachordal
of 10 mm body lengdescription, the modedals in this species isAnas (De Beer and
(Slaby, 1951), the rostanteriorly in the formon both sides of the n
direction, and then tmesenchyme which mbar that represents t
Accordingly, a posterby the acrochordal caorly, and the two ante
Thus, the anterior parrax have two differen
In Tinnunculus (Su1958), Upupa and Me
tar et al., 1983), Paset al., 1993), Streptope(El-Shikha, 2011), the
the early developmencartilage, the fenestrabirds; the Emu (Lut
(Frank, 1954) and Fulcranial fenestra is com
It is worthy to men
terior basicranial fenemajority of describedcorded in Dipnoi, theAnura, Lacertilia, Cr
(Kamal and Hammouthe absence of such adevelopmental stages
primitive phylogeneticby a process of absorpit should be considere
supposition comes trution of Anas (De Bee1907) and Phalacrocoring to comment on th
ondary modification
pteryx, where the parachordals remain distinctly paired untillate ontogenetic stage.In the avian literature, the unified formation of the basallate from the very beginning is also a subject of much contro-ersy. In the authors’ opinion, these controversies are adjustedn considering how and when a posterior basicranial fenestra
s formed. In Lacerta, Gaupp (1906) feels that the fenestra re-ults from the resorption of cartilage. In Gallus, Sonies (1907)s of the opinion that the basal plate is a composite structure.
rompton (1953) has also the same view in Spheniscus beyondhe fact that this latter bird lacks a basicranial fenestra.
other lower forms as Urodela, Lacertilia and Ophidia.What seems peculiar in all birds in general is the strong
ventral curvature of the rostral end of the notochord shortlybefore it leaves the acrochordal cartilage. On the contrary,during the early developmental stages in Squamata, such a
ventral bent of the notochord is unnoticeable (El-Toubi andKamal, 1961; Kamal and Hammouda, 1965). Gaupp (1906)found that, in common with all vertebrates with extreme cra-
nial flexure, the anterior most tip of the notochord curves ven-trally, project from the ventral surface of the parachordalplate. Gaupp’s view confirms the condition in birds, but lizards
and snakes seem to deviate probably due to the fact that theyare related to those forms with the least cranial flexure.
The S-shaped curvature of the basal plate occurs early dur-
ing ontogeny in all the birds so far described. Lang (1952), inher work on the cranial flexure of birds, has termed this curva-ture ‘‘lordosis” of the basal region. Also the notochord runs in
an S-shaped fashion corresponding to the flexure of the basalplate. In older embryos, this lordosis is no clearer due to theregression of nearly the whole dorsal portion of the acrochor-
dal cartilage, as well as to the far less pronounced condition ofthe cranial flexure. Also by the regression of the anterior re-gion of the notochord, it loses its S-shaped pattern.
The atrophy of the acrochordal cartilage is first described
by Parker (1891) in Apteryx. In Gallus, Sonies (1907) describesthe degeneration of the acrochordal plate till only narrowbridge remains forming the anterior border to the basicranial
fenestra. This condition is also observed in the majority of de-scribed forms; Vorster (1989) in Gallus, Zaher et al. (1991) inPasser, Zaher and Abdeen (1991) in Charadrius, Nakane and
Tsudzuki (1999) in Japanese quail, Abd El-Hady (2008) inCoturnix, Atalgin and Kurtul (2009) in turkey and Zaherand Riad (2012b) in Streptopelia.
The differentiation of the first and second occipital verte-brae in the early stages of development is a clear indicationthat the posterior end of the base of the skull will be formedby two included vertebrae which are differentiated from their
corresponding somites, this is mentioned by Mokhtar (1975),Mokhtar et al. (1983), Zaher and Riad (2009), El-Shikha(2011) in Upupa, Pterocles, Streptopelia and Columba, respec-
tively. This fact is of theoretical importance since it further val-idates the findings and observations of several authors aboutthe segmental nature of the head region in birds; Froriep
(1883, 1886), Suschkin (1899), Jager (1926), De Beer andBarrington (1934), Meier (1979, 1982), Kuratani et al. (1999)and Kuratani (2003, 2005).
Another potent evidence to the segmental nature of the ba-sal plate in birds is the development of the occipital arches andthe enclosure of the hypoglossal foramina. These foraminausually lie at the transitional area between the basal plate
and the occipital region. Muller (1961), Macke (1969), Mokh-tar (1975), Mokhtar et al. (1983), Zaher and Abdeen (1991),Zaher et al. (1991, 1993), Zaher and Riad (2009) as well as
El-Shikha (2011) stated that the number of these foramina inbirds may be taken as an approximate clue for the numberof the included vertebrae. It could be anticipated that the num-
ber of hypoglossal foramina during ontogeny is equal on bothsides of the basal plate. However, in the avian literature con-tradictory data, concerning the number of observed hypoglos-sal nerve roots, hypoglossal foramina and occipital arches are
generally met with.In Sturnus (Sonies, 1907), Gallinula (Abu-Taira, 1996),
Bubulcus (Abu-Taira, 1997), Streptopelia (Zaher and Riad,
2009) and Columba (El-Shikha, 2011), the number of the hypo-glossal foramina is rendered constant throughout ontogenybeing only three on both sides of the basal plate. This implies
the development of four occipital arches. In Pterocles(Mokhtar et al., 1983), there is a variation in the number ofthe hypoglossal foramina being four in the early stages, which
decreases to three in the optimum stage. Also during ontogeny,Pterocles (Mokhtar et al., 1983) shows a peculiar condition,where in its fourth stage (30.6 mm total body length embryo),
three hypoglossal foramina are found on the dorsal surface atthe right side, while the ventral surface shows four foramina.
It is thus evident that commonly in birds the number of the
hypoglossal foramina manifests a considerable range of varia-tion. The number may also differ in different developmentalstages of the same species and also on both sides of the basal
plate of the same embryo. However, Muller (1961) and Macke(1969) have referred that the majority of birds possess twohypoglossal foramina in the adult stage. Again, the above
mentioned data speak strongly in favour of Rice (1920) view.Rice gave a list of the number of the hypoglossal foraminain various reptiles, and mentioned that the contradictionsfound in the list are due to specific differences or to individual
variation either dependent upon age or seemingly accidental.Thus Rice (1920) supports the probability that the numberof the occurring foramina may differ regardless of the age of
the embryo.In all described birds without exception, the metotic carti-
lage joins the basal plate forming a homocontinuous bridge
(Vorster, 1989 in Gallus; Nakane and Tsudzuki, 1999 in Japa-nese quail; Atalgin and Kurtul, 2009 in turkey and Zaher andRiad, (2012b) in Streptopelia). Beyond its origin which shows a
considerable variation, the anterior portion of the latter bridgeforms a floor to the recessus scalae tympani. Its commissurapraevagalis separates the foramen jugulare from the latterrecess. As maintained by Muller (1961), this commissura prae-
vagalis is thus analogous to the processus recessus of mam-mals. In mammals, the processus recessus grows posteriorlyfrom the ventral border of the cochlear portion and merges
with the floor of the prominentia utriculoampullaris inferiorof the canalicular portion. In birds, the commissura praevagal-is represents a connection between the basal plate and the
metotic cartilage; Vorster (1989) in Gallus, Zaher et al.(1991) in Passer, Zaher and Abdeen (1991) in Charadrius, Za-her et al. (1993) in Corvus, Nakane and Tsudzuki (1999) in
Japanese quail, Abd El-Hady (2008) in Coturnix and Atalginand Kurtul (2009) in turkey.
In the avian literature, there seems an agreement that thelateral side of the occipital arch indistinguishably fuses with
the medial edge of the metotic cartilage to form a continuouscartilaginous plate below the auditory capsule, the recessusscalae tympani and the cavum metoticum; Mokhtar et al.
(1983) in Pterocles, Zaher and Abdeen (1991) in Charadrius,Abu-Taira, (1996, 1997) in Gallinula and Bubulcus, Atalginand Kurtul (2009) in turkey and Zaher and Riad (2012b) in
Streptopelia.In Streptopelia (Zaher and Riad, 2012b), the tectum synot-
icum is mainly a tectum posterius formed when the two occip-ital arches fuse together in the mid-dorsal line. The extensive
commissura supraoccipitocapsularis is the line of fusion be-tween the auditory capsule and the occipital arch at a pointdorsal to the fissura exoccipitocapsularis. The commissura
supraoccipitocapsularis is interrupted by a wide elongatedforamen for the passage of a blood vessel. Further posteriorlyand upwards the commissura supraoccipitocapsularis becomes
indistinguishable when the medial surface of the prominentiacanalis semicircularis anterior merges with the wall of the audi-tory capsule at this particular region. Thus, it can be said that
the hind walls of the auditory capsule may contribute with theleast share of chondrin matrix to the formation of the tectum.It is thus conceivable to admit that the tectum of Streptopelia
A review on the avian chondrocranium 111
(Zaher and Riad, 2012b) is a tectum synoticum plus posteriusalthough it has a pure occipital origin.
This finding is of a real theoretical importance, since it val-
idates the finding of Mokhtar et al. (1983) in Pterocles, Zaherand Abdeen (1991) in Charadrius and Abu-Taira, (1996, 1997)in Gallinula and Bubulcus, but does not go in pair with what is
met with in the previous works. Sonies (1907) described pairedisolated centres for the tectum synoticum in Anas and Gallus.In Spheniscus (Crompton, 1953), Struthio and Nyctisyrigmus
(Frank, 1954), the anlage of the tectum synoticum is anunpaired procartilaginous bridge between the two auditorycapsules, and it would seem that a tectum posterius is welldeveloped. This latter fuses without definite boundary with
the tectum synoticum anterior to it. Laterally, the two tectiin Struthio and Nyctisyrigmus (Fourie, 1955) are separatedby a pair of foramina. A closer finding has been drawn by
Macke (1969) in Fulica and Muller (1961) in Rhea. The tectumsynoticum has an unpaired anlage, and a tectum posterius ispresent. Both are transformed to cartilage and finally they
form a broad bridge which unites the auditory capsules andthe occipital arches together. In Strix, May (1961) doubtsthe unpaired origin of the tectum synoticum on account of
the presence of a median incisure in the tectum. In Pyromelana(Engelbrecht, 1958) and Upupa (Mokhtar, 1975), the tectumsynoticum has paired centres of pure otic origin.
From what has been stated above, it is evident that Ptero-
cles (Mokhtar et al., 1983), Gallinula as well as Bubulcus (Abu-Taira, 1996, 1997) and Streptopelia (Zaher and Riad, 2012b)are the only birds which have a tectum synoticum of pure
occipital origin. This fact could explain the delayed appearanceof the tectum in these birds. In Streptopelia (Zaher and Riad,2012b), the referred tectum lacks a processus anterior tecti.
However, Pterocles (Mokhtar et al., 1983) is unique in havingsuch a process projecting from the tectum. This is a typical lac-ertilian character (El-Toubi and Kamal, 1961).
The auditory region
In all birds so far described, the structure of the auditory cap-sule seems conservative, regardless of the insignificant varia-
tions which may exist from one bird to another.Of special interest is the dispositional relation of the audi-
tory capsule to the basal plate, and that of the cochlear portion
to the canalicular portion during ontogeny. These relationsseem to be constant in all birds. They are principally controlledby three consecutive movements: the encroachment of the co-
chlear portion onto the lateral surface of the basal plate, theposterior rotation of the canalicular portion and the medialrotation of its hind portion. The final picture is that the co-chlear portion vigorously invades the antero-lateral portion
of the basal plate and comes to lie anteriorly, medially andventrally. Their anterior poles strongly converge towards themedio-sagittal line and in some forms the basicranial fenestra
is the only area that separates them. Meantime, the canalicularportion is disposed later vertically on the lateral edge of the ba-sal plate, but the cochlear portion declines anteriorly with the
latero-ventral border of the basal plate and the acrochordalcartilage.
The development of the auditory capsule from two inde-
pendent centres of chondrification was observed in the major-ity of described birds; Struthio (Frank, 1954), Pyromelana,
Fulica (Macke, 1969), Upupa and Merops (Mokhtar, 1975),Pterocles (Mokhtar et al., 1983), Gallus (Vorster, 1989),Charadrius (Zaher and Abdeen, 1991), Passer (Zaher et al.,
1991), Corvus (Zaher et al., 1993), Japanese quail (Nakaneand Tsudzuki, 1999), Coturnix (Abd El-Hady, 2008), turkey(Atalgin and Kurtul, 2009), Streptopelia (Zaher and Riad,
2009) and Columba (El-Shikha, 2011). Thus the condition inbirds contradicts the view of Noordenbos (1905) who statesthat generally in vertebrates the cochlear part of the auditory
capsule chondrifies in continuity with the canalicular part.The fact that the cochlear portions, in their earlier develop-
ment, are initially discrete and quite independent of the basalplate is of theoretical importance since it presents potent evi-
dence against the verdict drawn by Gaupp (1906) that gener-ally in the development of Amniota, because of the intimatefusion between the cochlear portion of the auditory capsule
and the basal plate, the former is regarded as an integral partof the latter.
The condition found in Upupa and Merops (Mokhtar,
1975), Pterocles (Mokhtar et al., 1983), Passer (Zaher et al.,1991), quail-chick (Couly et al., 1993), Corvus (Zaher et al.,1993), Streptopelia (Zaher and Riad, 2009) and Columba
(El-Shikha, 2011) validates the view of Noordenbos (1905),Goodrich (1930) and De Beer (1937) who point out that theauditory capsule, during the development of the living verte-brates, almost, arises from a centre or centres of chondrifica-
tion. On the other hand, Romanoff (1960) is of the opinionthat the parachordal, almost from the moment of its appear-ance, is flanked at its anterior end by the anlagen of the
cochlear portions of the auditory capsules. Observers of thechick (Sonies, 1907) and Spheniscus (Crompton, 1953),although found isolated anlagen for the cochlear portions,
yet they considered them as related to the basal plate. In thisconnection, Crompton (1953) considered the basal plate tobe of a composite structure composed of the perichordal plate,
the median acrochordal plate and the paired cochlear portions.Parker (1891) in the Kiwi, has stated that the cochlear portionis an integral part of the parachordal from the beginning or atleast chondrifies in continuity with it. The same condition of
homo-continuous development exists in Tinnunculus (Suschkin,1899) and Pyromelana (Engelbrecht, 1958). In Struthio, Frank(1954) states that the cochlear capsule is small and fuses with
the basal plate from the earliest stages, so that it is impossibleto ascertain its actual extent.
In the authors’ opinion, the condition observed in the
majority of investigated birds and other vertebrate forms,leaves no doubt that the cochlear portion develops indepen-dent of the basal plate. The wide diversity of data found insome birds; Spheniscus (Crompton, 1953), Struthio (Frank,
1954), Pyromelana (Engelbrecht, 1958), Gallus (Vorster,1989), Corvus (Zaher et al., 1993), Japanese quail (Nakaneand Tsudzuki, 1999), Streptopelia (Zaher and Riad, 2009),
Columba (El-Shikha, 2011), or other vertebrate groups (Noor-denbos, 1905 and Hammouda and Kamal, 1965) is mainly as-cribed to the size of the cochlear portion. In these forms, where
an earlier fusion between the cochlear portion of the auditorycapsule and the basal plate has been achieved, one should re-gard that a large cochlear portion has appeared in the territory
of the basal plate, thus displacing its lateral margin from thevery beginning i.e., when the cochlear portion is stillmesenchymatous.
112 M.M. Zaher, A.M. Abu-Taira
In all birds without exception, the intermediate regionbetween the cochlear and canalicular portions is marked bya series of six or seven fenestrations, in addition to an extra
foramen that lies far posteriorly on the dorso-medial surfaceof the prominentia ampullaris posterior. This latter foramenis the endolymphatic one. The former anterior foramina are
a lateral fenestra ovalis, a latero-ventral perilymphatic fora-men and four or five acoustic foramina occupying the internalauditory meatus; Struthio (Frank, 1954), Fulica (Macke, 1969),
Upupa andMerops (Mokhtar, 1975), Pterocles (Mokhtar et al.,1983), Pyromelana, Gallus (Vorster, 1989), quail-chick (Coulyet al., 1993) and Japanese quail (Nakane and Tsudzuki, 1999).
The study of the majority of described birds shows that the
endolymphatic foramen and the five acoustic foramina areremnants of the cochlea-canalicular fissure, while the perilym-phatic foramen and the fenestra ovalis develop by resorption
in pre-existing cartilage. This is the condition recorded in themajority of described birds such as Struthio (Frank, 1954),Fulica (Macke, 1969), Upupa and Merops (Mokhtar, 1975),
Pterocles (Mokhtar et al., 1983), Pyromelana and Streptopelia(Zaher and Riad, 2009, 2012b).
Sonies (1907) in Gallus considers the fenestra ovalis as a
remnant of the cochlea-canalicular fissure, while in Anas, it isnot clear as to whether it develops from the cochlear or thecanalicular portions (De Beer, 1937).
The prefacial commissure has a general occurrence among
almost all sauropsidian forms. However, it is lacking in somespecies of Leptodeira (Brock, 1929). In Ophidia (Hammoudaand Kamal, 1965) as in lower vertebrates, it represents the line
of junction of the basal plate with the prominentia recessusutriculi. In Lacertilia (De Beer, 1937), it lies on the cochlearpart of the auditory capsule. In birds, although Sonies (1907)
points out that the prefacial canal is situated entirely in thewall of the otic capsule, yet the distinct position of the commis-sure slightly varies from one form to another. In Anas (De Beer
and Barrington, 1934), Struthio and Nyctisyrigmus (Frank,1954), Pyromelana (Engelbrecht, 1958), in Merops (Mokhtar,1975), the prefacial commissure connects both portions ofthe auditory capsule in the young stages. In old embryos the
commissure extends to fuse with the lateral edge of the basalplate. In Rhea (Muller, 1961), and Fulica (Macke, 1969), it ex-tends up to the acrochordal cartilage and joins the posterior
border of the hypophyseal foramen. In Spheniscus (Crompton,1953), the commissure is the connection between the processuslateralis paries cochlearis and the canalicular portion. In Strep-
topelia (Zaher and Riad, 2012b), it shows no relation to the ba-sal plate and lies entirely above the auditory capsule betweenthe cochlear and canalicular portions. This is similar to thecondition of Upupa (Mokhtar, 1975) and Pterocles (Mokhtar
et al., 1983).It is clear that among sauropsidian forms, there is a marked
change from one group to another in the exact disposition of
the prefacial commissure in relation to the auditory capsuleand the basal plate. It is also clear that in Squamata, it seemsto connect the basal plate with the auditory capsule, but in
birds it connects the two portions of the auditory capsule to-gether. Perhaps on these grounds that Engelbrecht (1958)maintains that the prefacial commissure in Pyromelana is not
homologous with the prefacial commissure of Lacerta. How-ever, the present authors feel that all these marked changesin the exact disposition of the prefacial commissure amongsauropsidian forms could be adjusted when considering the
exact extent of encroachment of the cochlear portion of theauditory capsule onto the lateral portion of the basal plate.
In birds, the series of commissures connecting the auditory
capsule with the surrounding cartilaginous structures are: thebasicapsular commissure, orbitocapsular commissure, thecommissura exoccipitocapsularis, and the commissura supra-
occipitocapsularis, Upupa and Merops (Mokhtar, 1975),Pterocles (Mokhtar et al., 1983), Gallus (Vorster, 1989),Charadrius (Zaher and Abdeen, 1991), Passer (Zaher et al.,
1991), Corvus (Zaher et al., 1993). The anterior two commis-sures are designated in the previous works, but the other twoare neglected in the avian literature, Japanese quail (Nakaneand Tsudzuki, 1999), Coturnix (Abd El-Hady, 2008), turkey
(Atalgin and Kurtul, 2009), Streptopelia (Zaher and Riad,2012b) and Columba (El-Shikha, 2011). Muller (1961) is thefirst to draw the attention that a straight analogy is present be-
tween these two latter commissures in birds and correspondingcommissures in mammals. Accordingly, Muller (1961) standar-dises their nominations in both birds and mammals and his
nomenclature is conceivably followed by the authors.Undoubtedly, the commissura orbitocapsularis is homologouswith the taenia marginalis of Lacerta (De Beer, 1937).
Other than these commissures, a commissura parietooccip-italis or a processus parietooccipitalis have a common occur-rence in birds. These are designated by Muller (1961) fromanalogous structures present in mammals. If the commissura
parietooccipitalis fuses intimately with the prominentia canalissemicircularis anterior, a fissura supraoccipitocapsularis is ab-sent as in Fulica (Macke, 1969), Upupa (Mokhtar, 1975). But if
the commissure runs aside the referred prominentia, a fissuresupraoccipitocapsularis, will represent the elongated narrowslit separating them as in Rhea (Muller, 1961). This commis-
sure, when present, usually joins the supracapsular cartilageand both merge with the commissura supraoccipitocapsularis.In Merops (Mokhtar, 1975), Gallinula (Abu-Taira, 1996),
Bubulcus (Abu-Taira, 1997) as well as in Streptopelia (Zaherand Riad, 2012b) this normal picture is not observed, sincethe processus parietooccipitalis fails to acquire the morpholog-ical significance of a true commissure.
Of special interest is the fact that the presence of a commis-sura praevagalis (=processus recessus of mammals), first des-ignated by Muller (1961), is a typical avian feature.
Muller (1961) and Macke (1969) are of the opinion that thebasicapsular commissure in Rhea and Fulica, respectively, haslost its character as a commissure. This is because the
encroachment of the cochlear portion on the basal plate causesthe loss of the demarcating line between the two entities. In fa-vour to this concept they add that if a line goes from the lateraledge of the basal plate anteriorly to the fissure metotica poste-
riorly it no longer passes on the border between the cochlearportion and the basal plate, but passes directly across the co-chlear portion however, the present authors feel that there is
nothing weighing against regarding the basicapsular commis-sure as a true commissure in birds, at least in the young devel-opmental stages, where the exact margin of the commissure
between the cochlear portion and basal plate could be easilyfollowed in Upupa and Merops (Mokhtar, 1975), Pterocles(Mokhtar et al., 1983), Charadrius (Zaher and Abdeen,
1991), Passer (Zaher et al., 1991), Corvus (Zaher et al.,1993), Coturnix (Abd El-Hady, 2008), turkey (Atalgin andKurtul, 2009), Streptopelia (Zaher and Riad, 2009) andColumba (El-Shikha, 2011).
A review on the avian chondrocranium 113
The term ‘‘metotic cartilage” was first used by Sonies(1907). Undoubtedly, the metotic cartilage is a typical new for-mation that characterises the skull of birds; Struthio (Frank,
1954), Fulica (Macke, 1969), Upupa and Merops (Mokhtar,1975), Pterocles (Mokhtar et al., 1983), Pyromelana, Gallus(Vorster, 1989), Charadrius (Zaher and Abdeen, 1991),
Japanese quail (Nakane and Tsudzuki, 1999) and turkey(Atalgin and Kurtul, 2009).
Investigation on Streptopelia (Zaher and Riad, 2012b), fully
supports the findings of Engelbrecht (1958) that the metoticcartilage in Pyromelana develops from a medial and lateralanlagen that soon goes into imperceptible fusion to form theacquainted full grown metotic cartilage to form the acquainted
full grown metotic cartilage of birds. The medial anlage devel-ops from the lateral edge of the hind region of the basal plate,while the lateral anlage is homo-continuous from the very
beginning with the ventro-lateral edge of the prominentiacanalis semicircularis lateralis.
The origin of the metotic cartilage varies from one form to
another. It develops either as an outgrowth of the occipital re-gion as in Tinnunculus (Suschkin, 1899), Phalacrocorax (Slaby,1951), Struthio (Frank, 1954) and Fulica (Mack, 1969), as an
outgrowth of the auditory capsule as in Spheniscus (Crompton,1953) or as two anlagen, one from the auditory capsule and theother from the occipital region as in Pyromelana (Engelbrecht,1958), Upupa and Merops (Mokhtar, 1975), Pterocles (Mokh-
tar et al., 1983), Coturnix (Abd El-Hady, 2008), turkey (Atal-gin and Kurtul, 2009) as well as Streptopelia (Zaher and Riad,2012b). But whatever the case may be, the final picture of the
metotic cartilage is amazingly the same in all the describedbirds, where it fuses with the basal plate and the occipital archto form a continuous floor below the canalicular portion of the
auditory capsule, the recessus scalae tympani and the cavummetoticum. Also in all birds, the formation of the metotic car-tilage regardless of its origin in some forms encloses the vagus-
accessory nerve into a separate foramen. This means that thecommissura praevagalis is expected in all birds, Gallus(Vorster, 1989), Japanese quail (Nakane and Tsudzuki,1999), turkey (Atalgin and Kurtul, 2009) and Streptopelia (Za-
her and Riad, 2012b).The homology of the metotic cartilage is a subject of con-
troversy. De Beer and Barrington (1934) and Slaby (1951) have
the opinion that the metotic cartilage develops as a modifica-tion of a number of cranial ribs. Accordingly, they homologiseit with the subcapsular process of crocodiles and the parac-
ondylar process of mammals. On the other hand, Crompton(1953), Frank (1954) and Macke (1969) could show that thereis no evidence for such a homology since in the majority ofinvestigated birds the metotic cartilage is either an outgrowth
of the auditory capsule or has a separate centre of chondrifica-tion. Also, Engelbrecht (1958), Mokhtar (1975) and Mokhtaret al. (1983) refute the referred homology and could show that
the medial anlage develops simultaneous with the developmentof the cranial ribs in Pyromelana, Upupa, Merops and Ptero-cles. In Streptopelia (Zaher and Riad, 2012b), this homology
is not accepted since it has been proved that the medial anlageof the metotic cartilage in Streptopelia is developed after theregression of the cranial ribs and both structures are quite
apart from each other. Muller (1961) holds the concept thatthe metotic cartilage is analogous with the lamina alaris ofmammals and accordingly, the process of the metotic cartilageshould be analogous with the paracondylar process.
The orbital region
The orbital region of birds, as in reptiles, is divided into twoparts; an anterior interorbital part joining the nasal capsules,and a posterior part which represents the connection of the
intertrabecula and the trabeculopolar complex with the basalplate. Gaupp (1906) calls the latter part ‘‘the temporal region”,while Lang (1952) refers to it as the ‘‘sphenotemporalportion”. The border between both parts is clearly marked
by the incisura optica.The fact that the prechordal region of the chondrocranium
develops slightly later than the acrochordal and basal plate re-
gions seems to be a general character in all the birds so far de-scribed. But the majority of investigators have not strictlystated which of the prechordal elements have a prior appear-
ance, except Van Wijhe (1907) and Romanoff (1960), whomaintain that the trabeculae crania are the first cartilages toappear. Also Macke (1969) admits such an opinion in his first
stage of Fulica atra. On the other hand, Slaby (1951) assuredthe precocial development of the polar and supratrabecularcartilages in the 10 mm embryo of Phalacrocorax. In Upupa(Mokhtar, 1975), the isolated intertrabecula, the paired inde-
pendent trabeculae and the paired polar cartilages are alreadyfused to the acrochordal plate by the polar acrochordal junc-tions, and have a simultaneous appearance. These junctions
have a short duration. In Pterocles (Mokhtar et al., 1983),the first element of the prechordal region to appear is the iso-lated polar cartilages simultaneous with the parachordal plate
followed by the suprapolars and trabeculae, then the isolatedintertrabecula in a sequence manner. In Streptopelia, (Zaherand Riad, 2009), the isolated trabeculae and the polar carti-lages have a precocial appearance. The polars, which are al-
ready fused to the acrochordal plate by polar acrochordaljunctions, have a long duration. The intertrabecula appearssomehow late.
The independent origin of the trabeculae in birds was re-ferred to by Van Wijhe (1907). It was also observed in Anas(De Beer and Barrington, 1934), Phalacrocorax (Slaby,
1951), Spheniscus (Crompton, 1953), Fulica (Macke, 1969),Upupa (Mokhtar, 1975), Pterocles (Mokhtar et al., 1983),Passer (Zaher et al., 1991), Gallinula (Abu-Taira, 1996),
Bubulcus (Abu-Taira, 1997) and Streptopelia (Zaher and Riad,2009). On the other hand, in Tinnunculus (Suschkin, 1899),Struthio (Frank, 1954), Pyromelana (Engelbrecht, 1958),Gallus (Vorster, 1989), Charadrius (Zaher and Abdeen,
1991), Japanese quail (Nakane and Tsudzuki, 1999), Coturnix(Abd El-Hady, 2008) and Columba (El-Shikha, 2011), thetrabeculae and polar cartilages are already fused from the early
beginnings forming trabeculo-polar bars which originate incontinuity with the acrochordal plate.
The origin of the trabeculae is a subject of controversy in
birds. De Beer (1937) regards the trabeculae to be of visceralorigin. De Beer considers the parallel disposition of the trabec-ulae with the other visceral arches as positive evidence that theformer represent the premandibular arches. Allis (1923, 1924)
holds the same opinion and adds that the trabeculae may behomologous with the pharyngeo-premandibularis. Goodrich(1930) considers the trabeculae as structures of special kind
developed to support the fore-brain and nasal sacs. Holmgren(1943) considers the trabeculae to be of axial origin. InStreptopelia (Zaher and Riad, 2009) it has been observed that
114 M.M. Zaher, A.M. Abu-Taira
the trabeculae lie in a line nearly parallel with the other visceralarches. Thus, De Beer’s concept could be appreciated.
In the majority of the described birds, the intertrabecula is
formed as a clear well defined median isolated entity betweenthe two trabeculae cranii; Pyromelana (Engelbrecht, 1958),Gallus (Vorster, 1989), Passer (Zaher et al., 1991), Charadrius
(Zaher and Abdeen, 1991), Japanese quail (Nakane andTsudzuki, 1999), Coturnix (Abd El-Hady, 2008), Streptopelia(Zaher and Riad, 2009) and Columba (El-Shikha, 2011).
In Streptopelia (Zaher and Riad, 2009), the anterior orbitalcartilage has an isolated centre of chondrification, it lies fromthe very beginning quite apart from the trabecula and theintertrabecula. The trabecula retains a distinct outline;
meantime the anterior orbital anlage is fairly developed. Theanterior orbital cartilage has a prior appearance than the inter-orbital septum. This latter develops nearly after the anterior
orbital cartilage reached its optimum condition.Parker (1880) was the first to recognise an intertrabecular
element in his study on the development of the green turtle,
Chelone viridis. In other turtles, its existence is asserted bysome authors as a well marked wedge between the trabeculae,e.g., Lepidochelys and Chrysemys (Pehrson, 1945) and Chely-
dra serpentine (Bellairs, 1949). Its presence in crocodilia wasobserved by Parker (1883). Among other Sauropsida, it maybe of rare and transient occurrence, e.g., Anguis fragilis (Bella-irs, 1958), or absent as in snakes (Kamal and Hammouda,
1965).In the avian literature, many authors admit that the recog-
nition of an intertrabecular element, as a clear well defined en-
tity in the chondrocranium, seems dubious and still callsfurther investigation for the different species. Few others advo-cate its precocial existence as an independent element as in Gal-
lus (Bellairs, 1958), Merops and Upupa (Mokhtar, 1975) andPterocles (Mokhtar et al., 1983), while others have either de-nied it completely (Van Wijhe, 1907 and Engelbrecht, 1958)
or have doubted its appearance from the early beginning asin Rhea (Muller, 1961). However, Parker (1891) was the firstto record its presence as a discrete element in Gallus. Sonies(1907) was not able to recognise it as independent cartilaginous
element in the same species. In Gallus, Hamilton (1952) andBellairs (1958) maintained its independent existence in theinterorbital and internasal regions as a median keel-like plate,
which later fuses with the trabeculae. It forms the interorbitalseptum, nasal septum and prenasal process. The anterior orbi-tal cartilage, most probably, has an isolated centre in close
proximity to the intertrabecula. In Larus (De Beer and Bar-rington, 1934), Fulica (Macke, 1969), Upupa (Mokhtar, 1975)and Pterocles (Mokhtar et al., 1983) the same condition is con-served. Suschkin (1899) has the same opinion in Tinnunculus.
But De Beer (1937) for the latter species feels that it is morethan doubtful whether the intertrabecula could be regardedas a distinct element. Engelbrecht (1958) says ‘‘No trace of
the intertrabecular element is present in Pyromelana, and thetrabeculae fuse in midline to form the trabecula communiswithout the intrusion of an isolated intertrabecula”. Engelbr-
echt adds that the interorbital septum is the up growth ofthe dorsal border of the trabecula communis. The anteriororbital cartilages have isolated centres of chondrification and
later run in continuity with the interorbital septum. The prena-sal process grows out of the trabecula communis.
Bellairs (1958) adds that the intertrabecula is responsiblefor the formation of the interorbital and nasal septa as well
as the prenasal process, but the anterior orbital cartilage, mostprobably has an isolated origin. In Passer domesticus (Bellairs,1958), an intertrabecular keel is noticeable in the posterior part
of the interorbital septum.De Beer and Barrington (1934) who have had the opportu-
nity to investigate several early ontogenetic stages of Anas, de-
nied completely the existence of an intertrabecula. In all thedevelopmental stages described by Slaby (1951) for Phalacroc-orax, there is no evidence for the presence of an intertrabecular
element. For Rhea Americana, the older stages, which Muller(1961) dealt with admitted him for no comment. However, inhis discussion he doubted its presence in birds and added thatno intertrabecula was proved to exist in the ratites examined
up till now. Thus, in Anas (De Beer and Barrington, 1934),Phalacrocorax (Slaby, 1951), Spheniscus (Crompton, 1953),Struthio (Frank, 1954) and Rea (Muller, 1961) the anterior
orbital cartilage and the prenasal process develop from the tra-becula communis.
It could be deduced that the anterior orbital cartilage seems
in the majority of investigated birds to have a separate centreof chondrification; meantime the origin of the interorbital sep-tum, nasal septum and the prenasal process in birds follows
one of the following three probabilities:
1- They either originate from the intertrabecula, e.g.,Tinnunculus (Suschkin, 1899), Gallus (Bellairs, 1958),
Fulica (Macke, 1969), Upupa (Mokhtar, 1975), Pterocles(Mokhtar et al., 1983), Passer (Zaher et al., 1991) andColumba (El-Shikha, 2011).
2- They originate from the trabecula communis if an inde-pendent intertrabecula is absent, e.g., Anas (De Beer andBarrington, 1934), Phalacrocorax (Slaby, 1951), Sphenis-
cus (Crompton, 1953) and Struthio (Frank, 1954).3- Or the interorbital septum originates from the intertrab-
ecula and the trabecula communis, while the nasal
septum and the prenasal process develop from the intert-rabecula, e.g., Merops (Mokhtar, 1975) and Streptopelia(Zaher and Riad, 2009, 2012b).
A fenestra septi interorbitalis, which is formed by a processof resorption in pre-existing cartilage, is present in many birds,e.g., Spheniscus (Crompton, 1953), Pyromelana (Engelbrecht,
1958), Rhea (Muller, 1961), Fulica (Macke, 1969), Merops(Mokhtar, 1975), Pterocles (Mokhtar et al., 1983) andStreptopelia (Zaher and Riad, 2012b). In Anas (De Beer and
Barrington, 1934), two fenestrae septi interorbitales arepresent. On the other hand, in Struthio (Frank, 1954) as wellas in Upupa (Mokhtar, 1975), the fenestra is wanting.
Usually in birds, the anterior orbital cartilage undergoes a
very rapid regression, e.g., Upupa and Merops (Mokhtar,1975) and Streptopelia (Zaher and Riad, 2012b). Thus, athree-sided olfactory tunnel is formed, which is bounded dor-
sally by the back growing parietotectal cartilage, medially bythe interorbital septum and laterally by the regressed anteriororbital cartilage.
In the majority of described birds, such as Fulica (Macke,1969), Upupa (Mokhtar, 1975), Gallus (Vorster, 1989), Passer(Zaher et al., 1991), Japanese quail (Nakane and Tsudzuki,
1999) and Columba (El-Shikha, 2011), the posterior orbitalcartilage has no separate centre of chondrification. It usuallydevelops as a direct continuity of the lateral border of the pilaantotica of its side. This latter in its turn is a direct
A review on the avian chondrocranium 115
proliferation of the lateral border of the acrochordal platewithout any sign of interruption in their blasteme. This fact ad-mits regarding the posterior orbital cartilage, pila antotica and
the acrochordal cartilage to develop from one centre of chon-drification, e.g., Upupa andMerops (Mokhtar, 1975), Streptop-elia (Zaher and Riad, 2009) and Columba (El-Shikha, 2011).
The earliest recognition of anterior and posterior orbitalcartilages in birds is met with in the work of Parker (1891)who designates them as the orbitosphenoid and the alisphe-
noid, respectively. Suschkin (1899) in Tinnunculus calls thesecartilages the supraorbital plate and alisphenoid; meantimehe considers the planum supraseptale as an isolated elementand nominates it the orbitosphenoid plate. A further confusion
is found in the work of Lang (1952) who names them as theanterior orbitosphenoid and the posterior orbitosphenoid.The ontogeny of Anas (De Beer and Barrington, 1934) shows
that corresponding structures form a homogenous continuousstructure at a certain stage of development. Accordingly, DeBeer and Barrington suggest the term ‘‘orbital cartilage” for
this lateral wall of the neurocranium, which later is differenti-ated into anterior and posterior orbital cartilage. They desig-nate the temporary bridge connecting both cartilages as the
supraorbital cartilage. These terms are widely accepted nowa-days in Upupa and Merops (Mokhtar, 1975), Gallus (Vorster,1989), Japanese quail (Nakane and Tsudzuki, 1999), Streptop-elia (Zaher and Riad, 2009), and Columba (El-Shikha, 2011).
The polar cartilages were first observed by Sonies (1907) inthe chick. However, Suschkin (1899) did not differentiate thepolar cartilages from the trabeculae in Tinnunculus. According
to Sonies (1907), the connection between the polar cartilageand the basal plate takes place at the border between the co-chlear portions of the auditory capsules and the acrochordal
cartilage; thereafter it fuses anteriorly with the dorsal borderof the polar cartilage, while the ophthalmic incisures is turnedto a foramen.
The suprapolar cartilage has no separate centre of chondri-fication; Spheniscus (Crompton, 1953), Struthio (Frank, 1954),Pyromelana (Engelbrecht, 1958) and Fulica (Macke, 1969). Itoriginates from the posterodorsal surface of the polar cartilage
and extends forward with a free anterior end, thus creating anophthalmic incisure that opens anteriorly, i.e., the two struc-tures are initially connected posterior to the ophthalmic artery.
However, this is contrary to the condition found in Pterocles(Mokhtar et al., 1983) where the ophthalmic incisure opensposteriorly. Similarly in Upupa and Merops (Mokhtar, 1975),
the ophthalmic incisure opens backwards. It seems, thus thatUpupa and Merops (Mokhtar, 1975) and Pterocles (Mokhtaret al., 1983) are the only described birds that have the suprapo-lar cartilage initially connected to the polar cartilage at a point
lying anterior to the ophthalmic artery.The development of a pila antotica spuria seems to be a
universal character in birds. However, Kesteven (1942) has
pointed out that it does not develop in Emu or the grebe (Podi-ceps) although Frank (1954) admits its presence in the Emu.
In all investigated birds without exception, an ultimate con-
nection between the orbital and auditory regions does occur.This cartilaginous connection deserves to be designated as acommissura orbitocapsularis whatever its constituent elements
are. As to its exact homology, De Beer (1937) and Frank(1954) feel that it corresponds to a part of the taenia marginalisof Lacerta, which connects the planum supraseptale with thedorsal border of the auditory capsule. According to De Beer
(1937), the lamina parietalis of mammals is also homologouswith the taenia marginalis.
In the majority of described birds, the commissura orbito-
capsularis is formed when the processus orbitocapsularis ofthe posterior orbital cartilage comes to fuse side by side, orone below the other, with the processus prooticus that devel-
ops out of the auditory capsule as in Tinnunculus (Suschkin,1899), Gallus (Sonies, 1907 and De Beer, 1937), Fulica (Macke,1969), Upupa (Mokhtar, 1975), Pterocles (Mokhtar et al.,
1983), Passer (Zaher et al., 1991) and Columba (El-Shikha,2011). The exact extent of each process and its time of appear-ance vary considerably among the described birds. In Pyrom-elana (Engelbrecht, 1958) and Rhea (Muller, 1961), the
processus prooticus has a prior appearance. In Fulica (Macke,1969) the reverse is true similar to the condition of Merops(Mokhtar, 1975). In Pterocles (Mokhtar et al., 1983), the
two processes have a simultaneous late appearance. In Strix(May, 1961), Fulica (Macke, 1969), Merops (Mokhtar, 1975)and Pterocles (Mokhtar et al., 1983), the commissura orbito-
capsularis is relatively small, whereas in the majority of otherdescribed birds this latter process is considerably voluminousin proportion to the processus prooticus to which it is adhered
side by side.In Spheniscus (Crompton, 1953), Nyctisyrigmus (Frank,
1954), Upupa (Mokhtar, 1975) and Streptopelia (Zaher andRiad, 2012b) the commissura orbitocapsularis is formed out
of the processus orbitocapsularis only, which realises an inti-mate connection with the auditory capsule without the inter-vention of a processus prooticus. In these four birds only, up
till now, the latter process is completely wanting.The cartilaginous postorbital process is present in the most
described avian skulls; Dromiceius (Lang, 1952), Pyromelana
(Engelbrecht, 1958), Strix (May, 1961), Rhea (Muller, 1961),Fulica (Macke, 1969), Upupa and Merops (Mokhtar, 1975),Pterocles (Mokhtar et al., 1983), Bubulcus (Abu-Taira, 1997),
Columba (El-Shikha, 2011) and Streptopelia (Zaher and Riad,2012b). However in Struthio (Frank, 1954) and Spheniscus(Crompton, 1953), the cartilaginous postorbital process islacking. In Pterocles (Mokhtar et al., 1983), the postorbital
process is voluminous and has an anterior broad process. InStreptopelia (Zaher and Riad, 2012b), the postorbital processis reduced in size when compared with that of other birds.
The ethmoid region
Generally in birds, the ethmoid region has a delayed develop-
ment relative to the chondrification of other regions of thechondrocranium.
In birds, the cartilaginous elements of the nasal capsule are:the prenasal process, the nasal septum, the parietotectal carti-
lage, the paries lateralis nasi, the copula anterior, three distinc-tive conchae which are the atrioturbinal, the maxilloturbinaland the concha nasalis, the planum antorbitale and the solum
nasi.The long prenasal process is a characteristic feature of birds
so far investigated. In the older stages it does not show any
sign of ossification but undergoes resorption. Therefore, itshould be considered as a transitory structure. Its origin asthe anterior extension of the intertrabecular bar, validates
the findings in Gallus (Bellairs, 1958), Upupa and Merops(Mokhtar, 1975), Pterocles (Mokhtar et al., 1983), Gallinula(Abu-Taira, 1996), Coturnix (Abd El-Hady, 2008), Columba
116 M.M. Zaher, A.M. Abu-Taira
(El-Shikha, 2011) as well as Streptopelia (Zaher and Riad,2012b) and contradicts what seems to be prevalent in the avianliterature that the process grows out of the trabecula commu-
nis as in Phalacrocorax (Slaby, 1951), Spheniscus (Crompton,1953), Struthio (Frank, 1954), Pyromelana (Engelbrecht,1958) and Rhea (Muller, 1961). In Anas (De Beer and Barring-
ton, 1934), the prenasal process is the anterior prolongation ofthe nasal septum.
The circumstances that this process is transitory and subse-
quently, more or less, completely disappears seem to agreewith the fact that it is a definite active outgrowth of the intert-rabecula and not from the trabeculae. This finding could pos-sibly cast some light on the exact phylogeny of the prenasal
process. In Gallinaceae, Parker (1891) explains that the prena-sal process develops in front of the nasal capsules to serve as asubstratum around which the membrane bones of this region
are developed. Malan (1946) considers its presence in the Igua-nidae and Varanus as a rhynchocephalian character of someprimitive lacertilian families. Broom (1905) considers that the
prenasal process indicates the reptilian ancestry of the primi-tive mammals. On the contrary, Engelbrecht (1958) by analys-ing the condition found in Pyromelana regards the absence of
the prenasal process in this bird as the original reptilian condi-tion and not to be considered as a secondary feature resultingfrom the elongation of the snout. Relying on this conclusion,Engelbrecht (1958) has the opinion that the presence of the
prenasal process in birds is a secondary character broughtabout when the premaxillae come to lie in a position onceoccupied by the anterior part of the nasal capsules in their rep-
tilian predecessors.Although Engelbrecht’s conception seems phylogenetically
conceivable, yet the ontogeny of the prenasal process in Passer
(Zaher et al., 1991), Gallinula and Bubulcus (Abu-Taira, 1996,1997) and Streptopelia (Zaher and Riad, 2012b) reveals itsnecessity as a skeletal element preserving the anterior part of
the snout, to be later occupied by the premaxillae. Accord-ingly, Parker’s view (1891) seems also plausible. Moreover,the fact that the process originates from the intertrabecularformation raises a possibility in favour of its primitive charac-
ter since the intertrabecular formation is a typical chelonianaffinity. But its existence in variable groups among the Saur-opsida supports Engelbrecht’s proposition (1958) that it is a
parallel modification in accordance with the anterior part ofthe snout.
Ontogenetically, it has been proved that in birds the nasal
septum has no separate centre of chondrification, and in itsorigin it can simply be regarded as the dorsal extension ofthe intertrabecula in the region between the two nasal sacs.This finding goes in accordance with what Suschkin (1899),
Bellairs (1958), Mokhtar (1975), Mokhtar et al. (1983), Zaheret al. (1991), Abu-Taira (1996, 1997), Atalgin and Kurtul(2009) and Zaher and Riad (2012b) have mentioned for Tin-
nunculus, Gallus, Upupa, Merops, Pterocles, Passer, Gallinula,Bubulcus, Turkey and Streptopelia, respectively. However inthe chick (Sonies, 1907), the duck (De Beer and Barrington,
1934), the ostrich (Brock, 1937), Pyromelana (Engelbrecht,1958) and Fulica (Macke, 1969), the nasal septum is the dorsaloutgrowth of the trabecula communis and the anterior conti-
nuity of the interorbital septum.It is thus evident that in the majority of birds, the nasal sep-
tum originates either from the trabecula communis or from theintertrabecula, and the prenasal process appears slightly later.
In birds, a thickened trabecular bar (=intertrabecular bar)in the ethmoid region is a characteristic feature. This would en-tail a decrease in the flexibility of the ethmoid region and thus
restricts kinesis; Pyromelana (Engelbrecht, 1958), Fulica(Macke, 1969), Columba (El-Shikha, 2011) and Streptopelia(Zaher and Riad, 2012b). If kinesis is to be retained in birds,
as is actually the case, certain structural alterations have totake place in the ethmoid region in order to overcome this lackof flexibility; Upupa and Merops (Mokhtar, 1975) and Strep-
topelia (Zaher and Riad, 2012b).The parietotectal cartilage (tectum nasi) in the avian chon-
drocranium contributes to the formation of the whole roof ofthe nasal capsule, the paries lateralis nasi of the anterior por-
tion of the capsule, the atrioturbinal cartilage, the copula ante-rior, the lamina transversalis anterior as well as its processesparaseptalis anterior as in Pyromelana (Engelbrecht, 1958),
Fulica (Macke, 1969), Columba (El-Shikha, 2011) and Strep-topelia (Zaher and Riad, 2012b). Posteriorly, the parietotectalcartilage ends as processus tectalis. In Upupa (Mokhtar, 1975),
the posterior border of the process is smooth and blunt. InRhea (Muller, 1961) and Passer (Zaher et al., 1991) the proces-sus tectalis is slightly bifid. The bifid character of the process is
more exaggerated in Anas (De Beer and Barrington, 1934). InFulica (Macke, 1969), the process is tripartite. In Spheniscus(Crompton, 1953), the process is in a rudimentary form. Inother birds, e.g., Struthio (Brock, 1937 and Frank, 1954),
Sturnus (De Kock, 1955), Nyctisyrigmus (Fourie, 1955) andPyromelana (Engelbrecht, 1958), the processus tectalis seemsto be absent.
In the avian literature, there seems an agreement that anatrioturbinal cartilage is almost always developed in birds, asa derivative of the parietotectal cartilage, in the form of a ridge
stretching downwards from its ventral surface. It has a lateappearance being evident only in the optimum stage. It is tobe remembered that the paries lateralis nasi in the region of
the atrioturbinal is derived from the parietotectal cartilage;De Beer and Barrington (1934) in Anas, Macke (1969) inFulica, Mokhtar (1975) in Upupa, Mokhtar et al. (1983) inPterocles, Zaher and Riad (2012b) in Streptopelia.
De Beer and Barrington (1934) have the opinion that theatrioturbinal is a new formation for birds since it is absent inreptiles. It seems to correspond in position to the rudimentary
atrioturbinal found in some mammals and most probably bothof them follow a parallel line in their development.
In all described birds, the concha nasalis is of the simplified
type due to the absence of the extraconchal recess. It originatesfrom the paranasal cartilage. The former is considered as thedorsal component of the latter. The ventro-median componentis the rudiment of the maxilloturbinal cartilage. These two
components of the paranasal cartilage contribute to the forma-tion of the paries lateralis nasi of the main nasal cavity.
The fact that an isolated paranasal element contributes to
the formation of the lateral wall of the nasal capsule validatesthe findings of De Beer and Barrington (1934) in Anas, Macke(1969) in Fulica, Mokhtar (1975) in Upupa, Mokhtar et al.
(1983) in Pterocles, Zaher and Riad (2012b) in Streptopelia,as far as this point is concerned. Frank (1954) holds the sameopinion for Struthio, although Brock (1937) maintains the ab-
sence of the paranasal anlage in the same species. It should benoted that Sonies (1907) claims an independent anlage for theside wall of the capsule and its turbinals including the conchanasalis in the duck, fowl and sparrow. On the other hand, in
A review on the avian chondrocranium 117
Upupa and Merops, Mokhtar (1975) denies completely thepresence of a paranasal anlage as a component of the nasalcapsule. She ascribes, the formation of the lateral wall to the
parietotectal cartilage, and accordingly the concha nasalis, ifpresent, to be a mere infolding of the latter cartilage.
As to the exact homology of the concha nasalis of birds,
there seems diversity in opinion in the avian literature. De Beerand Barrington (1934) hold the view that the concha nasalis ofbirds is homologous to the same concha of reptiles. On the
other hand, Muller (1961) suggests that both the maxilloturbi-nal cartilage and the concha nasalis of birds are homologous tothe concha nasalis of reptiles. It is of interest to add that Mat-thes (1921), De Beer and Barrington (1934) and Schuller (1939)
homologise, respectively, the concha nasalis of birds with theethmoturbinal, crista semicircularis and nasoturbinal ofmammals.
Reviewing the avian literature, some birds have the maxil-loturbinal cartilage represented by an un-branched cartilagi-nous lamella which is rolled up laterally in the form of a
spiral. In its middle region, the spiral reaches its maximumextension and consists of a variable number of turns. An ex-treme reduction in the size of the maxilloturbinal is observed
in Phalacrocorax (Slaby, 1951), Fulica (Macke, 1969), as wellas in Streptopelia (Zaher and Riad, 2012b) where it is only rep-resented by a rudimentary lamella. In Upupa (Mokhtar, 1975)as well as Pterocles (Mokhtar et al., 1983), the simple primary
lamella of maxilloturbinal cartilage carries secondary lamellae.A more complicated maxilloturbinal lamella is found in Stru-thio (Frank, 1954), where its secondary lamellae curl dorsally
forming semicircular structures.As to the origin of the planum antorbitale, it has been
shown in Streptopelia (Zaher and Riad, 2012b) that this struc-
ture has no isolated centre of chondrification and it is sup-posed to originate from the dorso-lateral border of theparanasal cartilage. In Spheniscus (Crompton, 1953), it devel-
ops out of the lower posterior region of the side wall of the na-sal capsule. In Struthio (Frank, 1954), the planum antorbitale,from the outset, is intimately fused with the paranasal carti-lage. In Fulica (Macke, 1969), the planum antorbitale is first
laid as a vertical ledge in close contact to the nasal septumbut it is more clearly differentiated than other elements. Anintermediate condition between that of Streptopelia (Zaher
and Riad, 2012b) and the above described birds is found inUpupa and Merops (Mokhtar, 1975). In these two latter birds,the planum has an isolated centre of chondrification which
very soon runs in mesenchymal fusion with the closer elements(Parietotectal, paranasal and trabecula).
In the avian literature, the recognition of the maxillary pro-cesses and their exact homology is a subject of controversy. In
the 61 mm embryo of Spheniscus, Crompton (1953) describes asmall independent cartilage uncinatum, connected to the pla-num antorbitale by means of a thick strand of connective tis-
sue. The relationship of this process to the blastema of thepars pterygoidea (=processus orbitalis of the quadrate) in thislatter bird led Crompton (1953) to believe that the process is
homologous with the processus maxillaris posterior of reptiles.Relying on this, and on the fact that the process is later chond-rified than the wall of the nasal capsule to which it is attached,
Frank (1954) supports the theory that the process has a differ-ent origin. Frank’s results are supported by Brock (1937) forStruthio. But Lang goes too far in believing that the atrioturb-
inal cartilage participates in the formation of the process.Lang’s view seems untenable.
In other described birds, no author has discussed the origin
of the maxillary processes, but they merely mention whetherthey are present or not. In Merops (Mokhtar, 1975) they arecompletely absent. For Anas (De Beer and Barrington,
1934), Phalacrocorax (Slaby, 1951) and Pyromelana (Engelbr-echt, 1958), no mention of the processes is met with. In Sturnus(De kock, 1955) and Rhea (Muller, 1961), anterior and poster-
ior maxillary processes are found. In Dromiceius, only the pos-terior process is present, similar to the condition of Spheniscusand Struthio as well as Upupa (Mokhtar, 1975). In Fulica,Macke (1969) feels that the processus maxillaris does not show
any differentiation to anterior and posterior processes.The solum nasi of the anterior portion of the nasal vestibule
(vestibular floor) is uncommon in the described birds, e.g., it is
completely absent in Pterocles (Mokhtar et al., 1983). In Strep-topelia (Zaher and Riad, 2012b), it is present but in a rudimen-tary form. This vestibular floor seems to be complete only in
those forms which have the fenestra narina completely ringedby cartilage, e.g., Upupa and Merops (Mokhtar, 1975). Butwhat seems peculiar is the contradictory data about the mode
of formation of such a floor. In Streptopelia (Zaher and Riad,2012b), the medial edge of the roof, in the region of the fenes-tra narina curves downwards, in close contact to the lateralborder of the intertrabecular bar with a clear line of demarca-
tion between them to be imperceptibly fused together in thenestling stage, then projects outwards for a short distancebut never fuse with the ventral edge of the side wall of the nasal
capsule. In Upupa and Merops (Mokhtar, 1975), the vestibularfloor has the same origin as described for Streptopelia (Zaherand Riad, 2012b), but it extends more laterally than it does
in the latter bird and acquires fusion with the paries lateralisnasi to complete a cartilaginous ring around the fenestranarina.
The lamina transversalis anterior in birds and reptiles has atypical position, but most probably a different origin. It seemsto have a phylogenetic importance, since it is preserved fromthe reptilian stock.
In the majority of described birds, there is no evidence forthe formation of zona annularis in the sense as described byGaupp (1906), Backstrom (1931) and De Beer (1937). Accord-
ing to their view, a zona annularis is formed if the nasal cap-sule is encircled with cartilage whether in a transverse planeor an oblique plane. Therefore, the assumption of Engelbrecht
(1958) that a zona annularis is present in Pyromelana, in theregion of cupola anterior seems correct. Also in Upupa, Mokh-tar (1975) feels the presence of two transverse zonae annulares,one in the region of the lamina transversalis anterior formed
by the abutting of the processus paraseptalis anterior to theintertrabecular bar. The other transverse zona is temporaryand is found at the level where the planum antorbitale per-
forms a procartilaginous connection with the nasal septum.Moreover, an oblique zona annularis is present in the samebird in the region of the fenestra narina.
In the avian literature, the cited information on the par-aseptal cartilages is very confusing. In trying to interpret theexact definition of these elements, the present authors feel
the necessity of differentiating, morphologically, between twoparaseptal derivatives; the so called anterior and posterior par-aseptal processes and the additional paraseptal cartilages, as
118 M.M. Zaher, A.M. Abu-Taira
the vomero-paraseptals or the maxillo-palatine paraseptals(paraseptal 1 and 2).
Muller (1961) is the first to cast light on the exact homology
of these elements in birds. He draws the attention to a probableresemblance in topography between the paraseptal derivativesin both birds and reptiles, and considers those of birds to be
the remnants of those of reptiles. It is a well known fact thatparaseptal element in the majority of reptilian forms is repre-sented by a long strut of cartilage lying ventro-lateral to the na-
sal septum, and connects the lamina transversalis anterior withthe planum antorbitale (Kamal and Hammouda, 1965) inPsammophis, Cerastes and Eryx respectively. If a discontinuityin this connection takes place, the condition is encountered in
all birds without exception, Upupa and Merops (Mokhtar,1975), Pterocles (Mokhtar et al., 1983) and Streptopelia (Zaherand Riad, 2012b). In undescribed bird, a continuous paraseptal
element connecting the lamina transversalis anterior with theplanum antorbitale is present; Pyromelana (Engelbrecht,1958); Upupa and Merops (Mokhtar, 1975) and Streptopelia
(Zaher and Riad, 2012b). It is of interest to state that such a dis-continuity in the paraseptal element is also evident in many lac-ertilian families (Malan, 1946), and is also known in mammals.
As to the additional paraseptal cartilages, e.g., the vomero-paraseptal cartilages (=paraseptal. (I) found in Upupa (Mokh-tar, 1975) and Pterocles (Mokhtar et al., 1983), the maxillo-palatine paraseptal cartilage (=paraseptal. (II) of Upupa
(Mokhtar, 1975) or the vomerine cartilage of Pyromelana(Engelbrecht, 1958), are completely wanted in Merops (Mokh-tar, 1975) and Streptopelia (Zaher and Riad, 2012b).
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