Some Morphological Studies on the Jaw Joint of the Australian Saltwater Crocodile (Croco- Dylus Porosus)

Jaw joint of the saltwater Australian crocodile Saber and Hassanin

Some Morphological Studies on the Jaw Joint of the Australian Saltwater Crocodile (Croco- dylus porosus)

A. S. Saber1 and A. Hassanin2

1 Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Uni- versity of Sadat City, Sadat City, Egypt & Dicipline of Veterinary Sciences, College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Australia 2 Department of Cytology and Histology, Faculty of Veterinary Medicine, Univer- sity of Sadat City, Sadat City, Egypt.

______15 16 With 10 figures, 4 tables Received May, accepted for publication June 2014

Fig (15): Photomicrograph of the nail in ostrich depicting, part of keratin layer (K), thick articular surfaces, which were layer of epidermis (E) with multiple cell layers laying on the basal lamina (BL) and the Abstract fibrocartilage in nature at the dermis layer (D) with some vacuoles (v). (X 400, H&E stain). The saltwater crocodile is the periphery of the articular sur- largest of all living reptiles. It is Fig (16): Photomicrograph of the nail in ostrich showing: the dense and thick keratin face, hyaline in the rest of the also known and proved that it articular surface, and ossifies on layer (K), the epidermis (E) and the dermis (D). Note the fat cells forming vacuoles (v) of has the largest biting forces. The reaching the underlying bone. the dermis just under the epidermal layer. (X 400, H&E stain). magnitude of the biting force exerted by the jaw leads to The thick lateral and thin medial

thoughts about the anatomical collateral ligaments were formed structure and construction of the of collagenous fibers. An articu- jaw joint in this reptile. Thirteen lar disc was missing in the croc- skulls of the saltwater crocodile odile quadrate/articular joint. (C. porosus) were used for this The joint was surrounded by a study. Some skulls were used complex massive group of mus- for X-raying and morphology, cles responsible for the firm clo- and the others for histological sure and opening of the mouth. slides which were prepared from The results were supported by the articular cartilages, capsule 10 images and 4 tables, and and collateral ligaments. The were discussed with other am- quadrate/articular joint (jaw joint) phibians, domestic animals and was diarthroidal, formed by two man when needed.

J. Vet. Anat. 55 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin Keywords: Jaw joint, quad- trast, Hyenas, lions and tigers Its constituent bones, the man- Material and Methods rate-articular joints, morphology, generate around 100 psi (4.450 dible and the squamous tem- Ten saltwater crocodile heads saltwater crocodile newton). poral, are intramembranous in (Crocodylus porosus) donated origin. Thus, the tissue that co- by a crocodile farm in Cairns, Introduction Animals, which must exert pow- vers each articulating surfaces is Queensland, Australia, as well The saltwater crocodile, also erful bite forces, such as croco- a secondary cartilage with a fi- as four skulls bought at the known as the Estuarine or Indo- diles, often have rigid skulls with brous coat, derived from the per- Kotter Market, Townsville, and Pacific crocodile, is the largest little or no kinesis for maximum iosteum. Another feature is the one skull kept in the anatomy of all living reptiles. It is known strength (Iordansky, 1964). This disc, which even when incom- museum in the School of Veteri- and it has been proven that it author added that most reptile plete, is associated with the lat- nary and Biomedical Sciences, has the strongest biting forces. skulls are dikinetic, having both eral pterygoid muscle (Sprinz, JCU, Townville, were used in Comparison of Alligator missis- meta- and meso-kinetic joints. 1965). This arrangement has led this study. sippiensis biting forces with The mandibulo-quadrate joint some authors to speculate that it One crocodile head was used some of the large known values also articulates with the (pala- arose as a tendon, which be- for x-raying; two heads were cut in the literature for other gnatho- tine-pterygoid) bar, which, then came pinched, by the new joint sagittaly for x-raying and jaw stomes (measured using bite connects to the maxilla, so that (Du Brul, 1964). The third fea- muscle study. The other 7 heads bars and theoretical measures when the quadrate is pulled to- ture of the TMJ is its role in were dissected from both sides employing various modeling wards the skull by the muscles growth: i.e. the secondary con- to study the jaw joint (its liga- techniques) (Snodgrass and the bar pushes on the base of dylar cartilage is a major growth ments, joint capsule, articular Gilbert, 1967; Dechow and Carl- the maxilla and causes the up- site in addition to being an artic- surfaces) as well as the muscles son, 1983; Thomson and Holm, per jaw to open. ular covering. surrounding the joint and acting 1992; Binder and Van Valken- on it. Small pieces from the ar- This magnitude of the biting Among the great number of pa- burgh, 2000) suggests that ticular surface, joint capsule and force exerted by the jaw is the pers published on crocodiles crocodile bite forces are the collateral ligaments were pro- reason for our investigation of and alligators and their relatives, highest known for any living tax- cessed with routine histological the anatomical structure and only two very old manuscripts on (Tables 1, 2). Singha (2013) methods, cut with the microtome construction of this jaw in this were found which dealt with the also mentioned that certain bite (5 µm thick) and stained with reptile. anatomy of the crocodile’s quad- tests in laboratory settings con- H&E, Periodic acid Schiff (PAS) rate/articular joint (Parsons, ducted by experts have con- and Masson's trichrome stains, The temporomandibular joint 1900) and the cranial muscula- firmed the saltwater crocodile as and finally photographed with an (TMJ), also known as jaw joint ture (Edgeworth, 1935). Hence, the ultimate chomper of the wild; Olympus microscope equipped or mandibular joint in mammals, the aim of this study is to ex- the reptile can shut its jaw with with a camera (Imaging, Micro is an ellipsoid variety of synovial plore the nature and give more an unbelievable force of 3.700 Publisher 5.0 RTV). joint, paired right and left to form morphometric measurements pounds per square inch (PSI). a bicondylar articulation (Wil- and morphological description of The skulls were prepared using Erickson (2012) also measured liams et al, 1999). the saltwater crocodile’s bite this joint in the saltwater croco- the boiling maceration technique power at 3,700 psi (16.460 Herring (2003) mentioned three dile. for skeleton preparation de- newtons). He added that by con- interesting facts about the TMJ. scribed by Simoens et al., (1994) and the measurements J. Vet. Anat. 56 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin Keywords: Jaw joint, quad- trast, Hyenas, lions and tigers Its constituent bones, the man- Material and Methods rate-articular joints, morphology, generate around 100 psi (4.450 dible and the squamous tem- Ten saltwater crocodile heads saltwater crocodile newton). poral, are intramembranous in (Crocodylus porosus) donated origin. Thus, the tissue that co- by a crocodile farm in Cairns, Introduction Animals, which must exert pow- vers each articulating surfaces is Queensland, Australia, as well The saltwater crocodile, also erful bite forces, such as croco- a secondary cartilage with a fi- as four skulls bought at the known as the Estuarine or Indo- diles, often have rigid skulls with brous coat, derived from the per- Kotter Market, Townsville, and Pacific crocodile, is the largest little or no kinesis for maximum iosteum. Another feature is the one skull kept in the anatomy of all living reptiles. It is known strength (Iordansky, 1964). This disc, which even when incom- museum in the School of Veteri- and it has been proven that it author added that most reptile plete, is associated with the lat- nary and Biomedical Sciences, has the strongest biting forces. skulls are dikinetic, having both eral pterygoid muscle (Sprinz, JCU, Townville, were used in Comparison of Alligator missis- meta- and meso-kinetic joints. 1965). This arrangement has led this study. sippiensis biting forces with The mandibulo-quadrate joint some authors to speculate that it One crocodile head was used some of the large known values also articulates with the (pala- arose as a tendon, which be- for x-raying; two heads were cut in the literature for other gnatho- tine-pterygoid) bar, which, then came pinched, by the new joint sagittaly for x-raying and jaw stomes (measured using bite connects to the maxilla, so that (Du Brul, 1964). The third fea- muscle study. The other 7 heads bars and theoretical measures when the quadrate is pulled to- ture of the TMJ is its role in were dissected from both sides employing various modeling wards the skull by the muscles growth: i.e. the secondary con- to study the jaw joint (its liga- techniques) (Snodgrass and the bar pushes on the base of dylar cartilage is a major growth ments, joint capsule, articular Gilbert, 1967; Dechow and Carl- the maxilla and causes the up- site in addition to being an artic- surfaces) as well as the muscles son, 1983; Thomson and Holm, per jaw to open. ular covering. surrounding the joint and acting 1992; Binder and Van Valken- on it. Small pieces from the ar- This magnitude of the biting Among the great number of pa- burgh, 2000) suggests that ticular surface, joint capsule and force exerted by the jaw is the pers published on crocodiles crocodile bite forces are the collateral ligaments were pro- reason for our investigation of and alligators and their relatives, highest known for any living tax- cessed with routine histological the anatomical structure and only two very old manuscripts on (Tables 1, 2). Singha (2013) methods, cut with the microtome construction of this jaw in this were found which dealt with the also mentioned that certain bite (5 µm thick) and stained with reptile. anatomy of the crocodile’s quad- tests in laboratory settings con- H&E, Periodic acid Schiff (PAS) rate/articular joint (Parsons, ducted by experts have con- and Masson's trichrome stains, The temporomandibular joint 1900) and the cranial muscula- firmed the saltwater crocodile as and finally photographed with an (TMJ), also known as jaw joint ture (Edgeworth, 1935). Hence, the ultimate chomper of the wild; Olympus microscope equipped or mandibular joint in mammals, the aim of this study is to ex- the reptile can shut its jaw with with a camera (Imaging, Micro is an ellipsoid variety of synovial plore the nature and give more an unbelievable force of 3.700 Publisher 5.0 RTV). joint, paired right and left to form morphometric measurements pounds per square inch (PSI). a bicondylar articulation (Wil- and morphological description of The skulls were prepared using Erickson (2012) also measured liams et al, 1999). the saltwater crocodile’s bite this joint in the saltwater croco- the boiling maceration technique power at 3,700 psi (16.460 Herring (2003) mentioned three dile. for skeleton preparation de- newtons). He added that by con- interesting facts about the TMJ. scribed by Simoens et al., (1994) and the measurements J. Vet. Anat. 57 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

were taken using a normal cali- about 1 cm long. Both surfaces (Figs 4/A & 6/B). The tangential articular bones. The capsule is per. Gross photographs were were firmly adhering to the con- layer is the superficial layer of capacious enough to permit taken by a Samsung digital dyle of the quadrate bone (Figs the articular surface, similar to easy movement of the joint (Fig camera WB 700. Nomina Ana- 2, 8). the perichondrium of other carti- 7). tomica Veterinaria (2005) was lages; it is formed of small, flat- utilized for denominating the an- In two cases (smaller skulls) out tened chondrocytes and colla- Articular ligaments atomical terms in the study. of ten, the articular cartilage was gen fibers that run parallel to the found loosely attached to the Two collateral ligaments were articular surface (Fig 4). The col- found to tightly bind the joint sur- articular bone of the mandible in lagen fibers stained deep blue faces together. The lateral col- Results the first case, and in the other while the cartilage matrix was lateral ligament is thick, 20 mm The jaw or quadrate/articular case only the lateral part was light blue with Masson's tri- long and 7 mm wide, covering joint of the saltwater crocodile loose and its medial facet was chrome (Fig 6/A). The hyaline nearly the whole lateral side sur- (C. porosus) was a synovial, el- attaching the bone (Fig 2/B). cartilage formed from chondro- face of the joint. Microscopically, lipsoidal, condylar joint. The An articular disc like found in the cytes inside lacunae either sin- it was formed of dense regular measurements taken for the majority of the mammalian and gly or in groups (isogenous) connective tissue formed of col- crocodile skulls which house the reptilian jaw joints could not be embedded in the matrix (Figs 4, lagen bundles and fibrocytes run joint (skull length, skull weight observed in the jaw joint of the 5, 6). The deep calcified layer parallel with axis of the collagen with the mandible and without it) rests on the underlying cortex of crocodiles of this study. fibers as shown in (Fig 5/B). The are given in table (3). The the bone. It is transit zone be- medial collateral ligament was measurements of the articular (ii) Cranial component tween the articular cartilage and thinner and shorter than the lat- surfaces of the joint are given in The articular surface of the the bone structure of the mandi- eral one, measuring 13 mm long table (4). The quadrate/articular quadrate bone was formed of a ble. The chondrocytes are ar- and 3 mm wide. It was attached joint was formed of the following transversely oriented oval sur- ranged in rows perpendicular to at the middle of the medial sur- components: face (1.7-2.5 cm in length), the articular surface, it show face of the joint (Fig 7). which was constricted in its mid- pyknotic dark nuclei (Figs 4/A & Articular surfaces dle leaving a larger lateral con- 5/A). The matrix of the calcified Surrounding muscles dyle and medial smaller one cartilage layer stains slightly (i) Mandibular component (Fig. 3). darker (PAS) than the matrix of The quadrate/articular joint was The mandible of the crocodile the other layers (Fig 6/A). supported by a powerful muscu- was formed of six fused bones (iii) Histological structure of lar mass encircling it and helping (dentary, angular, sur-angular, the articular surface its action of opening and closing splenial, coronoid, and articular) Microscopic examination of the Articular capsule (fibrous & firmly the mouth. The muscles (Fig. 1). The articular was the articular surface of the condyles synovial) mostly arose from the lateral bone which presents the con- illustrated that it is formed of an wall of the braincase, to end in cave articular surface (1.5-2.8 The articular capsule was a tight outer fibrous tangential layer; the mandible (Figs 9,10). These cm long) configured as two sur- sleeve investing the mandibular middle hyaline cartilage layer muscles namely are: faces: the larger lateral one joint completely. It is attached at and deep calcified layer termi- measuring about 1.5 cm long the margins of the articular sur- a) M. adductor mandibularis nate in the bone of the mandible and smaller medial surface face of both the quadrate and externus superficialis,

J. Vet. Anat. 58 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin were taken using a normal cali- about 1 cm long. Both surfaces (Figs 4/A & 6/B). The tangential articular bones. The capsule is per. Gross photographs were were firmly adhering to the con- layer is the superficial layer of capacious enough to permit taken by a Samsung digital dyle of the quadrate bone (Figs the articular surface, similar to easy movement of the joint (Fig camera WB 700. Nomina Ana- 2, 8). the perichondrium of other carti- 7). tomica Veterinaria (2005) was lages; it is formed of small, flat- utilized for denominating the an- In two cases (smaller skulls) out tened chondrocytes and colla- Articular ligaments atomical terms in the study. of ten, the articular cartilage was gen fibers that run parallel to the found loosely attached to the Two collateral ligaments were articular surface (Fig 4). The col- found to tightly bind the joint sur- articular bone of the mandible in lagen fibers stained deep blue faces together. The lateral col- Results the first case, and in the other while the cartilage matrix was lateral ligament is thick, 20 mm The jaw or quadrate/articular case only the lateral part was light blue with Masson's tri- long and 7 mm wide, covering joint of the saltwater crocodile loose and its medial facet was chrome (Fig 6/A). The hyaline nearly the whole lateral side sur- (C. porosus) was a synovial, el- attaching the bone (Fig 2/B). cartilage formed from chondro- face of the joint. Microscopically, lipsoidal, condylar joint. The An articular disc like found in the cytes inside lacunae either sin- it was formed of dense regular measurements taken for the majority of the mammalian and gly or in groups (isogenous) connective tissue formed of col- crocodile skulls which house the reptilian jaw joints could not be embedded in the matrix (Figs 4, lagen bundles and fibrocytes run joint (skull length, skull weight observed in the jaw joint of the 5, 6). The deep calcified layer parallel with axis of the collagen with the mandible and without it) rests on the underlying cortex of crocodiles of this study. fibers as shown in (Fig 5/B). The are given in table (3). The the bone. It is transit zone be- medial collateral ligament was measurements of the articular (ii) Cranial component tween the articular cartilage and thinner and shorter than the lat- surfaces of the joint are given in The articular surface of the the bone structure of the mandi- eral one, measuring 13 mm long table (4). The quadrate/articular quadrate bone was formed of a ble. The chondrocytes are ar- and 3 mm wide. It was attached joint was formed of the following transversely oriented oval sur- ranged in rows perpendicular to at the middle of the medial sur- components: face (1.7-2.5 cm in length), the articular surface, it show face of the joint (Fig 7). which was constricted in its mid- pyknotic dark nuclei (Figs 4/A & Articular surfaces dle leaving a larger lateral con- 5/A). The matrix of the calcified Surrounding muscles dyle and medial smaller one cartilage layer stains slightly (i) Mandibular component (Fig. 3). darker (PAS) than the matrix of The quadrate/articular joint was The mandible of the crocodile the other layers (Fig 6/A). supported by a powerful muscu- was formed of six fused bones (iii) Histological structure of lar mass encircling it and helping (dentary, angular, sur-angular, the articular surface its action of opening and closing splenial, coronoid, and articular) Microscopic examination of the Articular capsule (fibrous & firmly the mouth. The muscles (Fig. 1). The articular was the articular surface of the condyles synovial) mostly arose from the lateral bone which presents the con- illustrated that it is formed of an wall of the braincase, to end in cave articular surface (1.5-2.8 The articular capsule was a tight outer fibrous tangential layer; the mandible (Figs 9,10). These cm long) configured as two sur- sleeve investing the mandibular middle hyaline cartilage layer muscles namely are: faces: the larger lateral one joint completely. It is attached at and deep calcified layer termi- measuring about 1.5 cm long the margins of the articular sur- a) M. adductor mandibularis nate in the bone of the mandible and smaller medial surface face of both the quadrate and externus superficialis,

J. Vet. Anat. 59 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

b) M. adductor mandibularis shares in the formation of the Parsons (1900) stated that the articular disc is fibro-fatty rather externus media, jaw joint. Iordansky (1964) men- meniscus is a very constant than vascular, as human. c) M. adductor mandibularis tioned that animals, which must structure in Mammalia but may externus profundus, exert powerful bite forces such be “suppressed or underdevel- The articular cartilages of the d) M. adductor mandibularis as crocodiles, often have rigid oped” in a very small number of crocodile jaw joint were of both caudalis (posterior). skulls with little or no kinesis for animals. He found no evidence fibrocartilaginous nature at the e) M. pseudotemporalis su- maximum strength of a disc in the mandibular joints articular surface and merged perficialis, Douglas (1999) comparing be- of Dasypus (armadillo), Dasy- into the hyaline nature then cal- f) M.pseudotemporalis pro- tween reptiles and mammals urus ursinus (Tasmanian devil), cified transit zone at the attach- fundus, mentioned that reptiles have at Ornithorhynchus (duck-bill plat- ment of the underling bone. g) M. pterygoideus dorsalis, least four bones in the lower jaw ypus) and Tachyglossus (Echid- Samuelson (2007) mentioned h) M. pterygoideus ventra- (e.g. the dentary, articular, angu- na or spiny anteater). that fibrocartilage is found at in- lis, lar, surangular, and coronoid), tervertebral discs and certain i) M. intramandibularis, while mammals have only one Sprinz (1965) confirmed the ab- ligamentous and tendinous at- j) M. depressor mandibu- (the dentary). In the crocodile of sence of the disc in Dasyurus tachments to bones and menisci lae. this study, six fused bones form- (native Australian rat) and the of stifle joints. He added that the ing the mandible were identified. presence of remnants of discs fibers bundles often assume a Discussion represented by fine fibrous herringbone pattern as individual In man, the adult mandibular strands in Tachyglossus (Echid- bundles crisscross each other in (N.B. due to the paucity of re- condyle varies considerably in na), Ornithorhynchus (Platypus) an interwoven V shape. Fibro- search found on the jaw joint form from that found in the and Sarcophilus (Tasmanian cartilage is often associated with anatomy in crocodiles, compari- young child. In the former, the devil). He added that complete both dense connective tissue son was made to some domes- neck is thin and elongated and discs, which are attached to the and hyaline cartilage, typically tic animals and man when is readily fractured (Patnaik, joint surfaces, are present in merging imperceptibly with needed) 2000). In the infant the condyle Didelphus (Virginian opossum) them. The same author con- The temporomandibular joint is short and stubby having a co- and Metachirus (rat-tailed opos- firmed that the matrix of the fi- (TMJ) is a cardinal feature that pious blood supply (Blackwood, sum). The disc ensures friction- brocartilage is basically similar defines the class Mammalia and 1965). reduced sliding, damping and to that of the hyaline cartilage, separates mammals from other diversion of peak load (Mc Don- and the chondrocytes are vertebrates (Herring, 2003). The Absence of the articular disc in ald (1989). A reduction in disc aligned in rows, much like fibro- crocodile skull, including the the crocodilian jaw joint of this thickness increases strain cytes within tendons and liga- mandible, is pneumatized in na- study may be interpreted to the (Nickel and Mc Lachlan, 1994). ments. Kerr (2009) mentioned ture with plenty of foramina on very close and firm adaptation of that the band of striations (Fig the dorsal aspect and lateral both articular surfaces forming Herring et al., (2002) mentioned 5/A of this work) that correspond sides of the skull and the lateral the joint to each other, prevent- that the pig TMJ is better sup- to aggregates of mineral (calci- sides of both rami of the mandi- ing any possibility to a lateral ported than that of humans lat- um) depositing by matrix vesi- ble. The mandible is formed of movement. erally and medially, but more cles produced by nearby chon- six completely fused bones, vulnerable caudally. The caudal drocytes is called tidemark. He from which the articular bone attachment area of the intra- added that calcium and hydrox-

J. Vet. Anat. 60 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin b) M. adductor mandibularis shares in the formation of the Parsons (1900) stated that the articular disc is fibro-fatty rather externus media, jaw joint. Iordansky (1964) men- meniscus is a very constant than vascular, as human. c) M. adductor mandibularis tioned that animals, which must structure in Mammalia but may externus profundus, exert powerful bite forces such be “suppressed or underdevel- The articular cartilages of the d) M. adductor mandibularis as crocodiles, often have rigid oped” in a very small number of crocodile jaw joint were of both caudalis (posterior). skulls with little or no kinesis for animals. He found no evidence fibrocartilaginous nature at the e) M. pseudotemporalis su- maximum strength of a disc in the mandibular joints articular surface and merged perficialis, Douglas (1999) comparing be- of Dasypus (armadillo), Dasy- into the hyaline nature then cal- f) M.pseudotemporalis pro- tween reptiles and mammals urus ursinus (Tasmanian devil), cified transit zone at the attach- fundus, mentioned that reptiles have at Ornithorhynchus (duck-bill plat- ment of the underling bone. g) M. pterygoideus dorsalis, least four bones in the lower jaw ypus) and Tachyglossus (Echid- Samuelson (2007) mentioned h) M. pterygoideus ventra- (e.g. the dentary, articular, angu- na or spiny anteater). that fibrocartilage is found at in- lis, lar, surangular, and coronoid), tervertebral discs and certain i) M. intramandibularis, while mammals have only one Sprinz (1965) confirmed the ab- ligamentous and tendinous at- j) M. depressor mandibu- (the dentary). In the crocodile of sence of the disc in Dasyurus tachments to bones and menisci lae. this study, six fused bones form- (native Australian rat) and the of stifle joints. He added that the ing the mandible were identified. presence of remnants of discs fibers bundles often assume a Discussion represented by fine fibrous herringbone pattern as individual In man, the adult mandibular strands in Tachyglossus (Echid- bundles crisscross each other in (N.B. due to the paucity of re- condyle varies considerably in na), Ornithorhynchus (Platypus) an interwoven V shape. Fibro- search found on the jaw joint form from that found in the and Sarcophilus (Tasmanian cartilage is often associated with anatomy in crocodiles, compari- young child. In the former, the devil). He added that complete both dense connective tissue son was made to some domes- neck is thin and elongated and discs, which are attached to the and hyaline cartilage, typically tic animals and man when is readily fractured (Patnaik, joint surfaces, are present in merging imperceptibly with needed) 2000). In the infant the condyle Didelphus (Virginian opossum) them. The same author con- The temporomandibular joint is short and stubby having a co- and Metachirus (rat-tailed opos- firmed that the matrix of the fi- (TMJ) is a cardinal feature that pious blood supply (Blackwood, sum). The disc ensures friction- brocartilage is basically similar defines the class Mammalia and 1965). reduced sliding, damping and to that of the hyaline cartilage, separates mammals from other diversion of peak load (Mc Don- and the chondrocytes are vertebrates (Herring, 2003). The Absence of the articular disc in ald (1989). A reduction in disc aligned in rows, much like fibro- crocodile skull, including the the crocodilian jaw joint of this thickness increases strain cytes within tendons and liga- mandible, is pneumatized in na- study may be interpreted to the (Nickel and Mc Lachlan, 1994). ments. Kerr (2009) mentioned ture with plenty of foramina on very close and firm adaptation of that the band of striations (Fig the dorsal aspect and lateral both articular surfaces forming Herring et al., (2002) mentioned 5/A of this work) that correspond sides of the skull and the lateral the joint to each other, prevent- that the pig TMJ is better sup- to aggregates of mineral (calci- sides of both rami of the mandi- ing any possibility to a lateral ported than that of humans lat- um) depositing by matrix vesi- ble. The mandible is formed of movement. erally and medially, but more cles produced by nearby chon- six completely fused bones, vulnerable caudally. The caudal drocytes is called tidemark. He from which the articular bone attachment area of the intra- added that calcium and hydrox-

J. Vet. Anat. 61 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

yapatite crystals accumulate in the condyle. The Muscle ptery- mississippiensis) by Holliday et macroscopic and microscopic the matrix vesicles, and their goideus caudalis was relatively al. (2013) variations in the human TMJ lig- contents of specific glycoprotein, smaller in three species com- aments. In the crocodiles of the abundant in the tidemark zone, pared with many short-snouted Patnaik (2000) mentioned that present study, the lateral collat- induce calcium phosphate (hy- crocodiles. It suggests that the the smooth slippery, pressure- eral ligament was formed only of droxyapatite) deposition in as- masticatory power in a fish- bearing tissue carpeting the one thick layer, while the medial sociation with binding to matrix eating long-snouted species is bearing areas of the jaw joint of collateral ligament was thinner collagen. not as high as in the short- humans varies in thickness and shorter. snouted crocodiles. The false across different articular areas. Patil and Bindra (2012) stated gavial and the African slender- It is essentially a bed of tough Conclusion that the ligaments on the lateral snouted crocodiles had the pter- collagen fibers bound by special  The quadrate/articular side of the sheep TMJ attach to ygoid bone well developed ex- glycoproteins. He also described joint of the saltwater cro- the zygomatic arches and retro- tending dorso-ventrally and it is the histological structure of the codile is diarthroidal, and articular processes, and ventral- suggested that the M. adductor articular surface as consisting of its articular surfaces ly to the mandibular neck. These mandibulae caudalis attached to 4 successive layers; (1) horizon- match very well to each ligaments are incorporated into the pterygoid bone may be tal, thick tightly packed, collagen other, preventing any the joint capsules and stabilize much larger than the Indian ga- fibers, (2) oblique fibers leading side movement. the intra-articular discs (May- vial. (Endo et al., 2002). into (3) strong vertical fibers with  The articular cartilage is scattered cartilage cells emerg- nard and Savage, 1959 & Joch- of the fibrocartilage type en and Tomasz, 2007) The Mm. adductor mandibulae ing from (4) calcified cartilage at the periphery of the ar- externus, adductor mandibulae overlying thin layer of cortical In monotremes, the pterygoid ticular surface, hyaline in posterior (caudalis), and ptery- bone. In the crocodile of this muscles have fused into a single nature at the rest of the goideus activate bilaterally and study only three layers were dis- unit (Edgeworth, 1935). Accord- surface, and ossifies on simultaneously during rapid tinguished; tangential layer, hya- ing to Abbie (1939) in macropo- reaching the underlying closing or crushing. The M. pter- line cartilage and calcified carti- dians the complex masseter, bone. ygoideus does not act during lage layers. pterygoid and temporalis muscu-  The joint capsule is tight prey holding whereas the Mm. lature are closely set together, Patnaik (2000) described two and the collateral liga- adductor mandibulae externus, and separation into distinct layers forming the lateral collat- ments are two; lateral adductor mandibulae caudalis muscles is not possible by dis- eral ligament of the human TMJ; and medial shorter and continue to be active. The Mm. section (as the case in the croc- a wide outer or superficial layer thinner. depressor mandibulae and in- odile of the present study). Ride (fan-shaped) and a narrow inner  There is no articular disc tramandibularis are variably ac- (1959), whilst agreeing with Ab- or deep band. He added that in the crocodile jaw joint. tive during both jaw opening and bie (1939), stated however that there is no comparable double-  The peculiar anatomical closing (Busbey, 1989). the muscle acted as if they were layered reinforcement on the feature of the crocodile isolated units. Sprinz (1965) medial side of condyle, but a jaw joint together with The complex grouping of the jaw added that in all joint studies a medial horizontal band is pre- the interdigitating ar- muscles found in this study re- muscle (lateral pterygoid) was sent at a lower level. Nell et al., rangement of the man- sembles that described for the attached to the medial pole of (1996) had described various dibular and maxillary American alligator (Alligator J. Vet. Anat. 62 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin yapatite crystals accumulate in the condyle. The Muscle ptery- mississippiensis) by Holliday et macroscopic and microscopic the matrix vesicles, and their goideus caudalis was relatively al. (2013) variations in the human TMJ lig- contents of specific glycoprotein, smaller in three species com- aments. In the crocodiles of the abundant in the tidemark zone, pared with many short-snouted Patnaik (2000) mentioned that present study, the lateral collat- induce calcium phosphate (hy- crocodiles. It suggests that the the smooth slippery, pressure- eral ligament was formed only of droxyapatite) deposition in as- masticatory power in a fish- bearing tissue carpeting the one thick layer, while the medial sociation with binding to matrix eating long-snouted species is bearing areas of the jaw joint of collateral ligament was thinner collagen. not as high as in the short- humans varies in thickness and shorter. snouted crocodiles. The false across different articular areas. Patil and Bindra (2012) stated gavial and the African slender- It is essentially a bed of tough Conclusion that the ligaments on the lateral snouted crocodiles had the pter- collagen fibers bound by special  The quadrate/articular side of the sheep TMJ attach to ygoid bone well developed ex- glycoproteins. He also described joint of the saltwater cro- the zygomatic arches and retro- tending dorso-ventrally and it is the histological structure of the codile is diarthroidal, and articular processes, and ventral- suggested that the M. adductor articular surface as consisting of its articular surfaces ly to the mandibular neck. These mandibulae caudalis attached to 4 successive layers; (1) horizon- match very well to each ligaments are incorporated into the pterygoid bone may be tal, thick tightly packed, collagen other, preventing any the joint capsules and stabilize much larger than the Indian ga- fibers, (2) oblique fibers leading side movement. the intra-articular discs (May- vial. (Endo et al., 2002). into (3) strong vertical fibers with  The articular cartilage is scattered cartilage cells emerg- nard and Savage, 1959 & Joch- of the fibrocartilage type en and Tomasz, 2007) The Mm. adductor mandibulae ing from (4) calcified cartilage at the periphery of the ar- externus, adductor mandibulae overlying thin layer of cortical In monotremes, the pterygoid ticular surface, hyaline in posterior (caudalis), and ptery- bone. In the crocodile of this muscles have fused into a single nature at the rest of the goideus activate bilaterally and study only three layers were dis- unit (Edgeworth, 1935). Accord- surface, and ossifies on simultaneously during rapid tinguished; tangential layer, hya- ing to Abbie (1939) in macropo- reaching the underlying closing or crushing. The M. pter- line cartilage and calcified carti- dians the complex masseter, bone. ygoideus does not act during lage layers. pterygoid and temporalis muscu-  The joint capsule is tight prey holding whereas the Mm. lature are closely set together, Patnaik (2000) described two and the collateral liga- adductor mandibulae externus, and separation into distinct layers forming the lateral collat- ments are two; lateral adductor mandibulae caudalis muscles is not possible by dis- eral ligament of the human TMJ; and medial shorter and continue to be active. The Mm. section (as the case in the croc- a wide outer or superficial layer thinner. depressor mandibulae and in- odile of the present study). Ride (fan-shaped) and a narrow inner  There is no articular disc tramandibularis are variably ac- (1959), whilst agreeing with Ab- or deep band. He added that in the crocodile jaw joint. tive during both jaw opening and bie (1939), stated however that there is no comparable double-  The peculiar anatomical closing (Busbey, 1989). the muscle acted as if they were layered reinforcement on the feature of the crocodile isolated units. Sprinz (1965) medial side of condyle, but a jaw joint together with The complex grouping of the jaw added that in all joint studies a medial horizontal band is pre- the interdigitating ar- muscles found in this study re- muscle (lateral pterygoid) was sent at a lower level. Nell et al., rangement of the man- sembles that described for the attached to the medial pole of (1996) had described various dibular and maxillary American alligator (Alligator J. Vet. Anat. 63 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

teeth is responsible for havior in juvenile spotted hyenas long-snouted crocodiles. Anato- http://www.plosone.org/article/inf the tremendous biting (Crocuta crocuta). J. Zool. mia, Histologia, Embryologia o%3Adoi%2F10.1371%2Fjourna force performing by (Lond.) 252: 273–283. 31(4): 206-213. l.pone.0062806 crocodiles. (retrieved 26/10/2013) Busbey, B. (1989): Form and Erickson, G.M. (2012): Croco- Acknowledgement function of the feeding appa- diles have strongest bite ever Iordansky, N.N. (1964): The We want to express our appre- ratus of Alligator mississip- measured, hands-on tests show. jaw muscles of the crocodiles ciation and thanks to Mrs. Elaine piensis. Journal of Morphology, http://www.news.nationalgeogra and some relating structures of Wright and Mr. Bruce Clark, Volume 202, Issue 1, pages 99– phic.com/news/2012/03/120315. the crocodile skull. Anat Anz., Farm managers in Cairns Croc- 127, October (Retrieved 22.10.2012) Oct 13, 115: 256-280 odile Farm, QLD, Australia for donating the crocodile heads of Dechow, P. C. & Carlson, D. S. Erickson, G.M.; Lappin, A.K. Jochen, F. and Tomasz, G. this study. Our thanks are also (1983): A method of bite force and Vliet, K.A. (2003): The on- (2007): “On the Development, extended to Mrs. Kerry Johns for measurement in primates. J. togeny of bite-force performance Morphology and Function of the preparing the crocodile skulls Biomech. 16: 797–802. in American Alligator (Alligator Temporomandibular Joint in the and to Mr. Laurie Reilly, the sen- mississippiensis). J. Zool. Lond, Light of the Orofacial System”. ior histology technicians officer, Douglas, T (1999): Evidences 260: 317-327 Annals of Anatomy- Anato- School of Veterinary and Bio- for Macroevolution, Part 1: The mischer Anzeiger, Vol.189, No. medical Sciences, JCU, Towns- Unique Universal Phylo- Herring S.W. (2003): TMJ anat- 4: 314-319 ville, for preparing the histologi- genicTree. omy and animal models. J Mus- http://www.talkorigins.org/faqs/c culoskelet Neuronal Interact, 3 Kerr, J.B. (2009): Functional cal slides, and to Dr. Fernando nd Histology. 2 ed., Mosby, Else- Liste Burillo for the x-ray imag- omdesc/section1.html (retrieved (4): 391 vier. ing. 28/10/2013) Herring S.W., Decker J.D., Liu Maynard, S.J. and Savage, Du Brul E.L. (1964): Evolution Z.J. and Ma T. (2002): Tem- of the temporomandibular joint. R.J.G. (1959): “The Mechanics References poromandibular joint in miniature in: Sarnat BG, editor. The tem- of Mammalian Jaws”, School Abbie, A.A. (1939): A mastica- pigs: anatomy, cell replication, poro-mandibular joint. Charles C Science Review, Vol. 40, No. 4: tory adaptation peculiar to some and relation to loading. Anat Thomas; Springfield, IL: 3-27 289-301. diprotodond marsupials. Proc. Rec., 266: 152-166 zool. Soc. Lond., B 109: 261- Edgeworth, F.H. (1935): The Mc Donalnd, F. (1989): The 279 cranial muscles of vertebrates. Holliday CM, Tsai HP, Skiljan condylar disc as controlling fac- Blackwood, H.J.J. (1965): Vas- Cambridge: University Press. RJ, George ID, Pathan S tor in form of condylar head. cularization of the condylar carti- (2013): A 3D Interactive Model J.Craniomandibular. Dosoral. 3: lage in the human mandible. Endo, H., R. Aoki, H. Taru, J. and Atlas of the Jaw Muscula- 83-86 Journal of Anatomy, 99: 551-63. Kimura, M. Sasaki, M. Yama- ture of Alligator mississippiensis. moto, K. Arishima, and Y. PLoS ONE 8(6): e62806. Nell, A; Niebauer, W; Sperr, W. Binder, W. J. & Van Valken- Hayashi (2002): Comparative doi:10.1371/journal.pone.00628 and Firbas, W. (1996): Special burgh, B. (2000): Development functional morphology of the 06 variation of lateral ligament of of bite strength and feeding be- masticatory apparatus in the

J. Vet. Anat. 64 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin teeth is responsible for havior in juvenile spotted hyenas long-snouted crocodiles. Anato- http://www.plosone.org/article/inf the tremendous biting (Crocuta crocuta). J. Zool. mia, Histologia, Embryologia o%3Adoi%2F10.1371%2Fjourna force performing by (Lond.) 252: 273–283. 31(4): 206-213. l.pone.0062806 crocodiles. (retrieved 26/10/2013) Busbey, B. (1989): Form and Erickson, G.M. (2012): Croco- Acknowledgement function of the feeding appa- diles have strongest bite ever Iordansky, N.N. (1964): The We want to express our appre- ratus of Alligator mississip- measured, hands-on tests show. jaw muscles of the crocodiles ciation and thanks to Mrs. Elaine piensis. Journal of Morphology, http://www.news.nationalgeogra and some relating structures of Wright and Mr. Bruce Clark, Volume 202, Issue 1, pages 99– phic.com/news/2012/03/120315. the crocodile skull. Anat Anz., Farm managers in Cairns Croc- 127, October (Retrieved 22.10.2012) Oct 13, 115: 256-280 odile Farm, QLD, Australia for donating the crocodile heads of Dechow, P. C. & Carlson, D. S. Erickson, G.M.; Lappin, A.K. Jochen, F. and Tomasz, G. this study. Our thanks are also (1983): A method of bite force and Vliet, K.A. (2003): The on- (2007): “On the Development, extended to Mrs. Kerry Johns for measurement in primates. J. togeny of bite-force performance Morphology and Function of the preparing the crocodile skulls Biomech. 16: 797–802. in American Alligator (Alligator Temporomandibular Joint in the and to Mr. Laurie Reilly, the sen- mississippiensis). J. Zool. Lond, Light of the Orofacial System”. ior histology technicians officer, Douglas, T (1999): Evidences 260: 317-327 Annals of Anatomy- Anato- School of Veterinary and Bio- for Macroevolution, Part 1: The mischer Anzeiger, Vol.189, No. medical Sciences, JCU, Towns- Unique Universal Phylo- Herring S.W. (2003): TMJ anat- 4: 314-319 ville, for preparing the histologi- genicTree. omy and animal models. J Mus- http://www.talkorigins.org/faqs/c culoskelet Neuronal Interact, 3 Kerr, J.B. (2009): Functional cal slides, and to Dr. Fernando nd Histology. 2 ed., Mosby, Else- Liste Burillo for the x-ray imag- omdesc/section1.html (retrieved (4): 391 vier. ing. 28/10/2013) Herring S.W., Decker J.D., Liu Maynard, S.J. and Savage, Du Brul E.L. (1964): Evolution Z.J. and Ma T. (2002): Tem- of the temporomandibular joint. R.J.G. (1959): “The Mechanics References poromandibular joint in miniature in: Sarnat BG, editor. The tem- of Mammalian Jaws”, School Abbie, A.A. (1939): A mastica- pigs: anatomy, cell replication, poro-mandibular joint. Charles C Science Review, Vol. 40, No. 4: tory adaptation peculiar to some and relation to loading. Anat Thomas; Springfield, IL: 3-27 289-301. diprotodond marsupials. Proc. Rec., 266: 152-166 zool. Soc. Lond., B 109: 261- Edgeworth, F.H. (1935): The Mc Donalnd, F. (1989): The 279 cranial muscles of vertebrates. Holliday CM, Tsai HP, Skiljan condylar disc as controlling fac- Blackwood, H.J.J. (1965): Vas- Cambridge: University Press. RJ, George ID, Pathan S tor in form of condylar head. cularization of the condylar carti- (2013): A 3D Interactive Model J.Craniomandibular. Dosoral. 3: lage in the human mandible. Endo, H., R. Aoki, H. Taru, J. and Atlas of the Jaw Muscula- 83-86 Journal of Anatomy, 99: 551-63. Kimura, M. Sasaki, M. Yama- ture of Alligator mississippiensis. moto, K. Arishima, and Y. PLoS ONE 8(6): e62806. Nell, A; Niebauer, W; Sperr, W. Binder, W. J. & Van Valken- Hayashi (2002): Comparative doi:10.1371/journal.pone.00628 and Firbas, W. (1996): Special burgh, B. (2000): Development functional morphology of the 06 variation of lateral ligament of of bite strength and feeding be- masticatory apparatus in the

J. Vet. Anat. 65 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

human TMJ. Clinical Anatomy, can Journal of Veterinary Re- Churchill Livingstone, London: 2) http://listverse.com/201 7: 267-70. search, 55: 33-39. pp 578-82 2/11/05/top-10-animal- bites-that-will- Nickel, J.L. and Mc Lachlan, Singha, R. (2013): Animals with completely-destroy- K.R. (1994): In vitro of the tem- the most powerful bite force you/ poromandibular joint disc. http://www.buzzle.com/articles/a Internet links: (Retrieved 11/2/2014) Arch.Oral Biol., 39: 323-331. nimals-with-the-most-powerful- 3) http://www.pawnation.c bite-bite-force.html 1) http://forums.sherdog.c Parsons F.G. (1900): The joints om/2012/12/18/12-most- Retrieved 17.10.2013 om/forums/f48/top-20- of mammals compared with powerful-bites-in-the- worlds-strongest- those of man. J. Anat., London, animal-kingdom/12 Snodgrass, J. M. & Gilbert, P. animal-bite-forces-new- (Retrieved 11/2/2014) 34: 41-68 (Retrieved W. (1967): A shark bite meter. In 2393047/ 11/2/2014) Patil, A.S. and Bindra, G.K. Sharks, skates, and rays: 331– ______(2012): Morphology of the tem- 337. Gilbert, P. W., Mathew-

poromandibular joint (TMJ) of son,R. F. & Rall, D. P. (Eds).

sheep (Ovis aries), Open Jour- Baltimore: Johns Hopkins Uni- Table (1): Comparison of Alligator mississippiensis biting forces with some the largest versity Press. nal of Veterinary Medicine, Vol. values in the literature for other gnathostomes estimated in Newton (N). Source: (Erik- 2 No. 4,242-244 son et al., 2003) Sprinz R.A. (1965): A note on Tyrannosaurus rex † (giant thero- Patnaik V.V.G. (2000): Anatomy the mandibular intra-articular pod dinosaur) of Temporomandibular Joint? A disc in the joints of marsupialia Allosaurus fragilis † (large thero- Review. J Anat. Soc. India 49(2) and Monotremata. Proc Zool pod dinosaur) 191-197 Soc London; Vol. 144, Issue 3: Alligator mississippiensis (croco- 327-337 dilian) Ride, W.D.L. (1959): Mastica- Canis familiaris (labrador dog)

tion and taxonomy in the macro- Crocuta crocuta (spotted hyena) Thomson, D. & Holm, S. podine skull. In Function and Panthera leo (African lion) (1992): Bite force development, taxonomic importance. Publ. Carcharhinus obscurus (dusky metabolic and circulatory re- Syat. Ass., No 3: 33-59 shark) sponse to electrical stimulation Canis lupus (grey wolf) Samuelson, D.A. (2007): Text in the canine and porcine mas- Homo sapiens (human) Pongo pygmaeus (orangutan) Book of Veterinary Histology. seter muscles. Arch. Oral Biol. Saunders, Elsevier 37: 997–1006. 0 2000 4000 6000 8000 10 000 12 000 14000 Bite force (N) Simoens, R., Poles, R. and Williams P.L.; Bannister, L.H.; `lauwers, H. (1994): Morpho- Berry, M.M; Collins, P. Dyson, metric analysis of foramen mag- M; Dussek, J.E; Ferguson, num in Pekingese dogs. Ameri- M.W.J.(1999): Gray’s Anatomy In: Skeletal System 38th Edn,

J. Vet. Anat. 66 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin human TMJ. Clinical Anatomy, can Journal of Veterinary Re- Churchill Livingstone, London: 2) http://listverse.com/201 7: 267-70. search, 55: 33-39. pp 578-82 2/11/05/top-10-animal- bites-that-will- Nickel, J.L. and Mc Lachlan, Singha, R. (2013): Animals with completely-destroy- K.R. (1994): In vitro of the tem- the most powerful bite force you/ poromandibular joint disc. http://www.buzzle.com/articles/a Internet links: (Retrieved 11/2/2014) Arch.Oral Biol., 39: 323-331. nimals-with-the-most-powerful- 3) http://www.pawnation.c bite-bite-force.html 1) http://forums.sherdog.c Parsons F.G. (1900): The joints om/2012/12/18/12-most- Retrieved 17.10.2013 om/forums/f48/top-20- of mammals compared with powerful-bites-in-the- worlds-strongest- those of man. J. Anat., London, animal-kingdom/12 Snodgrass, J. M. & Gilbert, P. animal-bite-forces-new- (Retrieved 11/2/2014) 34: 41-68 (Retrieved W. (1967): A shark bite meter. In 2393047/ 11/2/2014) Patil, A.S. and Bindra, G.K. Sharks, skates, and rays: 331– ______(2012): Morphology of the tem- 337. Gilbert, P. W., Mathew- poromandibular joint (TMJ) of son,R. F. & Rall, D. P. (Eds). sheep (Ovis aries), Open Jour- Baltimore: Johns Hopkins Uni- Table (1): Comparison of Alligator mississippiensis biting forces with some the largest versity Press. nal of Veterinary Medicine, Vol. values in the literature for other gnathostomes estimated in Newton (N). Source: (Erik- 2 No. 4,242-244 son et al., 2003) Sprinz R.A. (1965): A note on Tyrannosaurus rex † (giant thero- Patnaik V.V.G. (2000): Anatomy the mandibular intra-articular pod dinosaur) of Temporomandibular Joint? A disc in the joints of marsupialia Allosaurus fragilis † (large thero- Review. J Anat. Soc. India 49(2) and Monotremata. Proc Zool pod dinosaur) 191-197 Soc London; Vol. 144, Issue 3: Alligator mississippiensis (croco- 327-337 dilian) Ride, W.D.L. (1959): Mastica- Canis familiaris (labrador dog) tion and taxonomy in the macro- Crocuta crocuta (spotted hyena) Thomson, D. & Holm, S. podine skull. In Function and Panthera leo (African lion) (1992): Bite force development, taxonomic importance. Publ. Carcharhinus obscurus (dusky metabolic and circulatory re- Syat. Ass., No 3: 33-59 shark) sponse to electrical stimulation Canis lupus (grey wolf) Samuelson, D.A. (2007): Text in the canine and porcine mas- Homo sapiens (human) Pongo pygmaeus (orangutan) Book of Veterinary Histology. seter muscles. Arch. Oral Biol. Saunders, Elsevier 37: 997–1006. 0 2000 4000 6000 8000 10 000 12 000 14000 Bite force (N) Simoens, R., Poles, R. and Williams P.L.; Bannister, L.H.; `lauwers, H. (1994): Morpho- Berry, M.M; Collins, P. Dyson, metric analysis of foramen mag- M; Dussek, J.E; Ferguson, num in Pekingese dogs. Ameri- M.W.J.(1999): Gray’s Anatomy In: Skeletal System 38th Edn,

J. Vet. Anat. 67 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

Table (2): Comparison of saltwater crocodile biting forces with some the largest values Table (4): Measurements of the articular surfaces taken on both the skull (quadrate estimated for other mammals expressed in pound per square inch (psi). (Source: com- bone) and the mandible (articular bone) piled from Singha, 3013& 1,2,3) Skulls Measurement on the Measurement on the Animal Bite force (psi) Skull (quadrate) Mandible (articular) Skulls Human 150 Side/ Front/ Front/ Front/ Side/ Front/ Front/ Front/ side back back back side back back back Tasmanian devil 181 lengt length length length length length length length Grey Wolf 406 h (M) (Mi) (L) (M) (Mi) (L) Mastiff Dog 235 Skull 1 1.9 1.1 0.6 0.9 2.1 1.5 1.3 0.8 Great white Shark 669 Skull 2 2.2 1.0 0.5 2.3 1.5 2.5 1.0 1.5 Lion 650-691 Skull 3 2.5 1.0 0.7 1.0 2.8 1.2 1.4 1.9 Alligator Sn apping turtle 1.000 Skull 4* 3.5 1.5 0.9 1.5 4.0 2.4 1.7 1.9 Grizzly bear 1.050 Skull 5 2.3 0.9 0.7 0.8 2.3 1.0 1.2 1.7 Hyena 1.100 Skull 6 2.4 0.9 0.6 0.9 2.7 1.8 1.4 1.7 Gorilla 1.300 Skull 7 1.9 0.7 0.5 0.7 1.8 1.4 1.1 1.5 Jaguar 1.350 Skull 8 2.0 0.6 0.3 0.8 2.0 0.7 1.1 1.3 Hippopotamus 1.825 Skull 9 1.8 0.7 0.5 0.6 1.7 0.9 1.0 1.2 Alligator 2.125 Skull 10 1.7 0.7 0.4 0.6 1.6 1.0 0.9 1.4 Saltwater crocodile 3.700 Skull 11 2.0 1.1 0.6 0.8 1.7 1.5 1.1 1.4 Skull 12 2.1 1.6 1.1 1.6 1.9 1.0 0.6 0.9 Table (3): Measurements of the skulls used in this study Skull 13 1.7 1.1 0.6 1.0 1.6 1.2 1.2 1.3 Skulls Mandible weight/gm Maxilla weight/gm Skull Length/cm MEAN 1.98 0.98 0.59 0.87 1.9 1.17 1.07 1.38 Skull 1 103.85 171.82 27.00 SD 0.23 0.92 0.21 0.29 1.35 0.32 0.2 0.23 Skull 2 168.74 259.29 30.00 Max 2.4 1.6 1.1 1.6 2.7 1.8 1.1 1.7 Skull 3 169.08 264.80 30.00 Min 0.23 0.29 0.21 0.29 0.35 0.32 0.21 0.23 Skull 4* 536.70 799.97 40.00 Skull 5 130.00 348.00 26.3 N.B. Crocodile No 4 was excluded from the calculations as it is the only very big- Skull 6 146.00 288.00 27.00 Skull 7 106.00 175.00 24.6 sized one. Skull 8 97.00 153.00 24.5 Skull 9 104.00 167.00 25.00 Skull 10 83.00 185.00 24.00 Skull 11 104.00 165.00 24.00 Skull 12 109.00 172.00 26.00 Skull 13 98.00 158.00 25.00 MEAN 118.22 208.90 26.12 SD 17.89 64.63 1.03 Max 168.74 348 30 Min 83 153 24

N.B. Crocodile No 4 was excluded from the calculations as it is the only very big- sized one

J. Vet. Anat. 68 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin Table (4): Measurements of the articular surfaces taken on both the skull (quadrate bone) and the mandible (articular bone) Skulls Measurement on the Measurement on the Skull (quadrate) Mandible (articular) Skulls Side/ Front/ Front/ Front/ Side/ Front/ Front/ Front/ side back back back side back back back lengt length length length length length length length h (M) (Mi) (L) (M) (Mi) (L) Skull 1 1.9 1.1 0.6 0.9 2.1 1.5 1.3 0.8 Skull 2 2.2 1.0 0.5 2.3 1.5 2.5 1.0 1.5 Skull 3 2.5 1.0 0.7 1.0 2.8 1.2 1.4 1.9 Skull 4* 3.5 1.5 0.9 1.5 4.0 2.4 1.7 1.9 Skull 5 2.3 0.9 0.7 0.8 2.3 1.0 1.2 1.7 Skull 6 2.4 0.9 0.6 0.9 2.7 1.8 1.4 1.7 Skull 7 1.9 0.7 0.5 0.7 1.8 1.4 1.1 1.5 Skull 8 2.0 0.6 0.3 0.8 2.0 0.7 1.1 1.3 Skull 9 1.8 0.7 0.5 0.6 1.7 0.9 1.0 1.2 Skull 10 1.7 0.7 0.4 0.6 1.6 1.0 0.9 1.4 Skull 11 2.0 1.1 0.6 0.8 1.7 1.5 1.1 1.4 Skull 12 2.1 1.6 1.1 1.6 1.9 1.0 0.6 0.9 Skull 13 1.7 1.1 0.6 1.0 1.6 1.2 1.2 1.3 MEAN 1.98 0.98 0.59 0.87 1.9 1.17 1.07 1.38 SD 0.23 0.92 0.21 0.29 1.35 0.32 0.2 0.23 Max 2.4 1.6 1.1 1.6 2.7 1.8 1.1 1.7 Min 0.23 0.29 0.21 0.29 0.35 0.32 0.21 0.23

N.B. Crocodile No 4 was excluded from the calculations as it is the only very big- sized one.

J. Vet. Anat. 69 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

Palatine fenestra

Inferior temporal fossa

Occipital Quadrato- condyle jugal M Quadrate L Mi

A A

Mi L

M Quadrate (articular surface) Fig (1): Medial surface of the mandible right ramus (A) and lateral surface of the mandi- Fig (3): Left articular surface of the quadrate bone of Crocodylus porosus. A-A side ble left ramus (B) showing its six fused bony components (dentary, articular, angular, su- to side length, M-M medial front to back length, Mi-Mi middle front to back length, L-L lat- rangular, coronoid and splenial). eral front to back length.

Retroarticular Retroarticular Retroarticular process Retroarticular process process process L L M Mi M Mi A A

L L A A H

M Mi M Mi 1 1 Articular Articular 2 2

Angular Angular B A B A

: Fig (2, A) Articular surface of the left ramus of the mandible in Crocodylus po- A C B rosus. A-A side to side length, M-M medial front to back length, Mi-Mi middle front to back length, L-L lateral front to back length. : Fig �(�4) Light micrograph of the articular�� surface of the crocodile quadrate/articular joint showing: A. three distinct layers; (T) tangential layer, (H) hyaline cartilage and (C) Fig (2, B): Rostral view of a fresh left articular part of the quadrate/articular joint calcified cartilage layer (H&E stain; x20). B. higher magnification showing the tangential showing: 1 un-fused articular cartilage covering the articular surface of the bone, 2 ros- fibrocartilaginous layer (arrows) and proper cartilage layer with chondrocytes (ch) singly tral border of the articular surface on the articular bone. or in isogenous (I) imbedded in matrix (m). (H&E stain; x40) J. Vet. Anat. 70 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

Palatine fenestra

Inferior temporal fossa

Occipital Quadrato- condyle jugal M Quadrate L Mi

A A

Mi L

M Quadrate (articular surface) Fig (3): Left articular surface of the quadrate bone of Crocodylus porosus. A-A side to side length, M-M medial front to back length, Mi-Mi middle front to back length, L-L lateral front to back length.

A C B

: Fig �(�4) Light micrograph of the articular�� surface of the crocodile quadrate/articular joint showing: A. three distinct layers; (T) tangential layer, (H) hyaline cartilage and (C) calcified cartilage layer (H&E stain; x20). B. higher magnification showing the tangential fibrocartilaginous layer (arrows) and proper cartilage layer with chondrocytes (ch) singly or in isogenous (I) imbedded in matrix (m). (H&E stain; x40) J. Vet. Anat. 71 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

A B

�� Fig (5): Light micrograph of the crocodile quadrate-articular joint, A. higher magnification of (Fig. 4/A) showing the transitional layer (H) and the radial zone (O) between the cartilage and bone of the mandible, (arrows) indicate beginning of the process of ossifica- tion of the chondrocytes. . lateral collateral ligament showing fibrocytes (fb, arrows) in- B terspersed between the layers of the extracellular collagen fibers (c) (H&E stain; x40) Fig (7): Fresh dissected head of the C. porosus showing: lateral (1) and medial (2) collateral ligaments of the left quadrate/articular joint (3) retro-articular process, (4) remnants of the M. depressor mandibulae. The oval circle indicates the joint area; the yellow H arrow indicates the opened joint capsule and part of the articular surface covered by the T articular cartilage. � �

�

� Fig (8): Latero/medial radiograph of the saltwater crocodile (Crocodylus porosus) showing: A B C 1 articular bone, 2 quadrate bone, 3 retro-articular process 4 angular bone, 5 external mandibular fenestra, 6 dentary, 7 cranio-quadrate passage. Arrow indicates the quad- � rate/articular joint,. Fig (6): Light micrograph of the articular surface of the crocodile quadrate/articular �� joint showing A. intensive PAS reaction at the end of the calcified cartilage layer de- ______notes the bone (arrow) (PAS reaction; X40). B. showing the three distinctive layers; (T) Correspondence address: tangential layer, (H) hyaline cartilage layer and (C) calcified layer (Masson's trichrome Prof. Dr. A. S. Saber Email: [email protected] stain; X20) J. Vet. Anat. 72 Vol 7 No 2, (2014) 55 - 74 Jaw joint of the saltwater Australian crocodile Saber and Hassanin

Fig (7): Fresh dissected head of the C. porosus showing: lateral (1) and medial (2) collateral ligaments of the left quadrate/articular joint (3) retro-articular process, (4) remnants of the M. depressor mandibulae. The oval circle indicates the joint area; the yellow arrow indicates the opened joint capsule and part of the articular surface covered by the articular cartilage.

Fig (8): Latero/medial radiograph of the saltwater crocodile (Crocodylus porosus) showing: 1 articular bone, 2 quadrate bone, 3 retro-articular process 4 angular bone, 5 external mandibular fenestra, 6 dentary, 7 cranio-quadrate passage. Arrow indicates the quadrate/articular joint,.

______Correspondence address: Prof. Dr. A. S. Saber Email: [email protected]

J. Vet. Anat. 73 Vol 7 No 2, (2014) 55 - 74

Jaw joint of the saltwater Australian crocodile Saber and Hassanin Morphometric Analysis of the Mandible of Tuj and Morkaraman Sheep

Yasin Demiraslan1** Filiz Gülbaz2 Sami Özcan1 Mustafa Orhun Dayan3 Yalçın Akbulut4

1Department of Anatomy, Faculty of Veterinary Medicine, Kafkas University, 36100 Kars -TURKEY 2Ataturk Vocational School of Health Services, Kafkas University, 36100 Kars - TURKEY 3Department of Anatomy, Faculty of Veterinary Medicine, Selcuk University, 42100 Kon- ya -TURKEY 4Kars Collage of Health, Kafkas University, 36100 Kars -TURKEY

Fig (9): Superficial dissection of the jaw musculature of the C. proposes. With 2 figures, 4 tables Received June, accepted for publication September 2014 1 M. adductor mandibularis externus superficialis, 2 M. depressor mandibulae, 3 quadra- to/articular joint, 4 retroarticular process, 5 quadrate bone. Abstract and the mandible height at the level of the rear alveolar edge with 3rd In the present study, it was aimed to molar tooth (L14) had a significant determine morphometric differences statistical difference (p<0.05). Ac- of the mandible of Tuj and Morka- cording to the correlation values, it A 1 raman sheep having widespread C was seen that A2 values (the angle breeding area in the Eastern Anato- between the proc. condylaris and B lia Region. In this study, 20 mandi- ramus mandibulae) of the both 2 bles of the male Tuj and Morkara- sheep breeds were in negative rela- man sheep were used. The 16- 3 tion with the other mandible meas- lenghts taken to the mandible were urements. As a result, the obtained measured by electronic digital calli- data indicate that genetic doesn't per. Furthermore, after the mandible 5 4 significantly affect the morphometry were photographed and printed to of the mandible of the Morkaraman milimetric paper, the 4-angles stud- and Tuj sheeps. ied were measured with gonimeter. Fig (10): Sagittal section in the caudal part of a frozen head of C. proposes show- The results of this study proved that Keywords: Mandibula, Morkara- ing the voluminous complex muscles surrounding the quadrate/articular joint. the means of the length and angle man sheep, Morphometry, Tuj 1 M. depressor mandibulae, 2 M. adductor mandibularis (externus superficialis, media, profundus), 3 M. adductor mandibularis caudalis & 4 M. pterygoideus ventralis, 5 M. in- measurements obtained from sheep tramandibularis, Morkaraman sheep were mostly A quadrate bone, B articular bone. C retro-articular process. The arrow indicates the joint higher than Tuj sheep. The angle of Introduction position. margo ventralis mandibulae (A4) In Turkey, Morkaraman sheep, which is the dominant race of East-

J. Vet. Anat. 74 Vol 7 No 2, (2014) 55 - 74