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The role of cranial kinesis in birds

Identifieur interne : 000039 ( Istex/Corpus ); précédent : 000038; suivant : 000040

The role of cranial kinesis in birds

Auteurs : Ron G. Bout ; Gart A. Zweers

Source :

RBID : ISTEX:00AB7A351166C7CE48A265D5CBF660C621F66C6F

English descriptors

Abstract

Abstract: In birds, the ability to move the upper beak relative to the braincase has been the subject of many functional morphological investigations, but in many instances the adaptive significance of cranial kinesis remains unclear. Alternatively, cranial kinesis may be considered a consequence of the general design of the skull, rather than an adaptive trait as such. The present study reviews some results related to the mechanism and functional significance of cranial kinesis in birds. Quantitative three-dimensional X-ray has shown that in skulls morphologically as divers as paleognaths and neognaths the mechanism for elevation of the upper beak is very similar. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw movement by the postorbital ligament. Such a mechanical coupling would necessitate upper beak elevation. However, independent control of upper and lower jaw has been shown to occur during beak movements in birds. Moreover, kinematic modeling and force measurements suggests that the maximum extensibility of collagen, in combination with the short distance of the insertion of the postorbital ligament to the quadrato-mandibular articulation do not constitute a block to lower jaw depression. The lower jaw ligaments serve to limit the maximal extension of the mandibula. It is suggested here that cranial kinesis in avian feeding may have evolved as a consequence of an increase in eye size. This increase in size led to a reduction of bony bars in the lateral aspect of the skull enabling the transfer of quadrate movement to the upper jaw. The selective forces favoring the development of a kinetic upper beak in birds may be subtle and act in different ecological contexts. Simultaneous movement of the upper and lower jaw not only increases the velocity of beak movements, but with elevated upper beak also less force is required to open the lower jaw. However, the penalty of increased mobility of elements in a lightweight skull and a large eye is potential instability of skull elements during biting, smaller bite forces and limitations on joint reaction forces. Such a lightly built, kinetic skull may have evolved in animals that feed on small plant material or insects. This type of food does not require the resistance of large external forces on the jaws as in carnivores eating large prey.

Url:
DOI: 10.1016/S1095-6433(01)00470-6

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ISTEX:00AB7A351166C7CE48A265D5CBF660C621F66C6F

Le document en format XML

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<div type="abstract" xml:lang="en">Abstract: In birds, the ability to move the upper beak relative to the braincase has been the subject of many functional morphological investigations, but in many instances the adaptive significance of cranial kinesis remains unclear. Alternatively, cranial kinesis may be considered a consequence of the general design of the skull, rather than an adaptive trait as such. The present study reviews some results related to the mechanism and functional significance of cranial kinesis in birds. Quantitative three-dimensional X-ray has shown that in skulls morphologically as divers as paleognaths and neognaths the mechanism for elevation of the upper beak is very similar. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw movement by the postorbital ligament. Such a mechanical coupling would necessitate upper beak elevation. However, independent control of upper and lower jaw has been shown to occur during beak movements in birds. Moreover, kinematic modeling and force measurements suggests that the maximum extensibility of collagen, in combination with the short distance of the insertion of the postorbital ligament to the quadrato-mandibular articulation do not constitute a block to lower jaw depression. The lower jaw ligaments serve to limit the maximal extension of the mandibula. It is suggested here that cranial kinesis in avian feeding may have evolved as a consequence of an increase in eye size. This increase in size led to a reduction of bony bars in the lateral aspect of the skull enabling the transfer of quadrate movement to the upper jaw. The selective forces favoring the development of a kinetic upper beak in birds may be subtle and act in different ecological contexts. Simultaneous movement of the upper and lower jaw not only increases the velocity of beak movements, but with elevated upper beak also less force is required to open the lower jaw. However, the penalty of increased mobility of elements in a lightweight skull and a large eye is potential instability of skull elements during biting, smaller bite forces and limitations on joint reaction forces. Such a lightly built, kinetic skull may have evolved in animals that feed on small plant material or insects. This type of food does not require the resistance of large external forces on the jaws as in carnivores eating large prey.</div>
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<abstract>Abstract: In birds, the ability to move the upper beak relative to the braincase has been the subject of many functional morphological investigations, but in many instances the adaptive significance of cranial kinesis remains unclear. Alternatively, cranial kinesis may be considered a consequence of the general design of the skull, rather than an adaptive trait as such. The present study reviews some results related to the mechanism and functional significance of cranial kinesis in birds. Quantitative three-dimensional X-ray has shown that in skulls morphologically as divers as paleognaths and neognaths the mechanism for elevation of the upper beak is very similar. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw movement by the postorbital ligament. Such a mechanical coupling would necessitate upper beak elevation. However, independent control of upper and lower jaw has been shown to occur during beak movements in birds. Moreover, kinematic modeling and force measurements suggests that the maximum extensibility of collagen, in combination with the short distance of the insertion of the postorbital ligament to the quadrato-mandibular articulation do not constitute a block to lower jaw depression. The lower jaw ligaments serve to limit the maximal extension of the mandibula. It is suggested here that cranial kinesis in avian feeding may have evolved as a consequence of an increase in eye size. This increase in size led to a reduction of bony bars in the lateral aspect of the skull enabling the transfer of quadrate movement to the upper jaw. The selective forces favoring the development of a kinetic upper beak in birds may be subtle and act in different ecological contexts. Simultaneous movement of the upper and lower jaw not only increases the velocity of beak movements, but with elevated upper beak also less force is required to open the lower jaw. However, the penalty of increased mobility of elements in a lightweight skull and a large eye is potential instability of skull elements during biting, smaller bite forces and limitations on joint reaction forces. Such a lightly built, kinetic skull may have evolved in animals that feed on small plant material or insects. This type of food does not require the resistance of large external forces on the jaws as in carnivores eating large prey.</abstract>
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<note>This paper was originally presented as part of the ESCPB Congress symposium ‘Learning about the Comparative Biomechanics of Locomotion and Feeding’, Liège July 26–27, 2000.</note>
<note type="content">Section title: Review</note>
<note type="content">Fig. 1: Lateral view of the skull of Anas platyrhynchos with several ligaments. POM=lig. postorbitale; LM=lig. lacrimomandibulare; OM=lig. occipitomandibulare; JM=lig. jugomandibulare; LJ=lig. lacrimojugulare; SO=lig. suborbitale.</note>
<note type="content">Fig. 2: Force (in Newton) measured at the tip of the mandible required to depress the lower beak of the mallard over a range of 30°. The upper beak is fixed in the rest or elevated position. The curves are fitted through data points of 6–8 birds (12 measurements per bird). The top panel shows that the force increases continuously, without a clear ‘block’. Cutting the ligaments shows that the contribution of the ligaments PO and LO to the total force is small up to 20–25°. When the upper beak is elevated the ligaments are slack or at their resting length and do not resist jaw opening (middle panel). As a consequence less opening force for the lower jaw is required when the upper jaw is elevated than when it is at the rest position (lower panel).</note>
<note type="content">Fig. 3: 2D kinematic model. The model takes an upper (UB) and lower beak (LB) angle, and a quadrate (Q) position within the mandibular articulation groove as input and calculates the positions of skeletal and ligamentous elements. S=skull, Pa=palatine, Pt=pterygoid, Ju=jugal. Head morphology is characterized by the XY co-ordinates of the projection on the lateral plane of 14 skeletal points and the origo and insertion of the postorbital, lacrimomandibular and occipitomandibular ligaments (not shown). Skeletal points: 1, articulation of the quadrate with the skull; 2, hinge of the upper jaw; 3, articulation of the jugal bar and the upper jaw; 4, articulation of the jugal bar and the quadrate; 5, articulation of the palatine and the upper jaw; 6, articulation of the palatine and the pterygoid; 7, articulation of the pterygoid and the quadrate; 8, tip upper beak; 9, caudal point culmen of the upper beak; 10, tip lower beak; 11, dorsal point culmen lower beak; 12, quadratomandibular articulation (lateral condyle); 13, caudal border mandibular groove; 14, rostral border mandibular groove.</note>
<note type="content">Fig. 4: (a) Two ways to increase the range of lower jaw angles by limiting the strain in the postorbital ligament (PO). M=mandible, Q=quadrate, S=skull, Pa=palatine, Pt=pterygoid, Ju=jugal. A. The mandible moves forward and upward with the quadrate and PO shortens. (b) The mandible remains stationary with respect to the skull and the quadrate moves over a curved articular groove on the mandible decreasing the distance to the insertion of PO.</note>
<note type="content">Fig. 5: Calculated maximal strain in jaw ligaments of the mallard as a function of lower and upper beak angle, and position of the quadrate. Lines indicate beak angles for which the strain in PO and OM is 1.06. In the top panel the quadrate is kept at the most caudal position of the articulation groove. In this situation upper beak elevation results in a forward movement of the mandible, which is limited by OM. Lower jaw depression is limited by PO (and LOM). Maximal strain limits the possible combinations of upper and lower jaw angles to the area between the curves. Note that the lower jaw can depress 25° without elevating the upper jaw before PO reaches its maximal strain. As the quadrate moves forward along the articulation groove (half-way: middle panel) the area between the curves increases: upper beak elevation is effected without moving the mandible and the shorter distance between the quadrate and the insertion of PO allows larger opening angles for the mandible. At the most rostral point in the articulation groove (bottom panel) the distance between quadrate condyle and PO attachment is zero and for large upper beak elevations there are no constraints on lower jaw depression. However, for small elevation angles the mandible has to be retracted (also moving downward) for the quadrate to reach its rostral position in the articulation groove. This stretches PO and effectively blocks lower jaw movement.</note>
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<p>In birds, the ability to move the upper beak relative to the braincase has been the subject of many functional morphological investigations, but in many instances the adaptive significance of cranial kinesis remains unclear. Alternatively, cranial kinesis may be considered a consequence of the general design of the skull, rather than an adaptive trait as such. The present study reviews some results related to the mechanism and functional significance of cranial kinesis in birds. Quantitative three-dimensional X-ray has shown that in skulls morphologically as divers as paleognaths and neognaths the mechanism for elevation of the upper beak is very similar. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw movement by the postorbital ligament. Such a mechanical coupling would necessitate upper beak elevation. However, independent control of upper and lower jaw has been shown to occur during beak movements in birds. Moreover, kinematic modeling and force measurements suggests that the maximum extensibility of collagen, in combination with the short distance of the insertion of the postorbital ligament to the quadrato-mandibular articulation do not constitute a block to lower jaw depression. The lower jaw ligaments serve to limit the maximal extension of the mandibula. It is suggested here that cranial kinesis in avian feeding may have evolved as a consequence of an increase in eye size. This increase in size led to a reduction of bony bars in the lateral aspect of the skull enabling the transfer of quadrate movement to the upper jaw. The selective forces favoring the development of a kinetic upper beak in birds may be subtle and act in different ecological contexts. Simultaneous movement of the upper and lower jaw not only increases the velocity of beak movements, but with elevated upper beak also less force is required to open the lower jaw. However, the penalty of increased mobility of elements in a lightweight skull and a large eye is potential instability of skull elements during biting, smaller bite forces and limitations on joint reaction forces. Such a lightly built, kinetic skull may have evolved in animals that feed on small plant material or insects. This type of food does not require the resistance of large external forces on the jaws as in carnivores eating large prey.</p>
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<ce:simple-para>In birds, the ability to move the upper beak relative to the braincase has been the subject of many functional morphological investigations, but in many instances the adaptive significance of cranial kinesis remains unclear. Alternatively, cranial kinesis may be considered a consequence of the general design of the skull, rather than an adaptive trait as such. The present study reviews some results related to the mechanism and functional significance of cranial kinesis in birds. Quantitative three-dimensional X-ray has shown that in skulls morphologically as divers as paleognaths and neognaths the mechanism for elevation of the upper beak is very similar. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw movement by the postorbital ligament. Such a mechanical coupling would necessitate upper beak elevation. However, independent control of upper and lower jaw has been shown to occur during beak movements in birds. Moreover, kinematic modeling and force measurements suggests that the maximum extensibility of collagen, in combination with the short distance of the insertion of the postorbital ligament to the quadrato-mandibular articulation do not constitute a block to lower jaw depression. The lower jaw ligaments serve to limit the maximal extension of the mandibula. It is suggested here that cranial kinesis in avian feeding may have evolved as a consequence of an increase in eye size. This increase in size led to a reduction of bony bars in the lateral aspect of the skull enabling the transfer of quadrate movement to the upper jaw. The selective forces favoring the development of a kinetic upper beak in birds may be subtle and act in different ecological contexts. Simultaneous movement of the upper and lower jaw not only increases the velocity of beak movements, but with elevated upper beak also less force is required to open the lower jaw. However, the penalty of increased mobility of elements in a lightweight skull and a large eye is potential instability of skull elements during biting, smaller bite forces and limitations on joint reaction forces. Such a lightly built, kinetic skull may have evolved in animals that feed on small plant material or insects. This type of food does not require the resistance of large external forces on the jaws as in carnivores eating large prey.</ce:simple-para>
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<abstract lang="en">Abstract: In birds, the ability to move the upper beak relative to the braincase has been the subject of many functional morphological investigations, but in many instances the adaptive significance of cranial kinesis remains unclear. Alternatively, cranial kinesis may be considered a consequence of the general design of the skull, rather than an adaptive trait as such. The present study reviews some results related to the mechanism and functional significance of cranial kinesis in birds. Quantitative three-dimensional X-ray has shown that in skulls morphologically as divers as paleognaths and neognaths the mechanism for elevation of the upper beak is very similar. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw movement by the postorbital ligament. Such a mechanical coupling would necessitate upper beak elevation. However, independent control of upper and lower jaw has been shown to occur during beak movements in birds. Moreover, kinematic modeling and force measurements suggests that the maximum extensibility of collagen, in combination with the short distance of the insertion of the postorbital ligament to the quadrato-mandibular articulation do not constitute a block to lower jaw depression. The lower jaw ligaments serve to limit the maximal extension of the mandibula. It is suggested here that cranial kinesis in avian feeding may have evolved as a consequence of an increase in eye size. This increase in size led to a reduction of bony bars in the lateral aspect of the skull enabling the transfer of quadrate movement to the upper jaw. The selective forces favoring the development of a kinetic upper beak in birds may be subtle and act in different ecological contexts. Simultaneous movement of the upper and lower jaw not only increases the velocity of beak movements, but with elevated upper beak also less force is required to open the lower jaw. However, the penalty of increased mobility of elements in a lightweight skull and a large eye is potential instability of skull elements during biting, smaller bite forces and limitations on joint reaction forces. Such a lightly built, kinetic skull may have evolved in animals that feed on small plant material or insects. This type of food does not require the resistance of large external forces on the jaws as in carnivores eating large prey.</abstract>
<note>This paper was originally presented as part of the ESCPB Congress symposium ‘Learning about the Comparative Biomechanics of Locomotion and Feeding’, Liège July 26–27, 2000.</note>
<note type="content">Section title: Review</note>
<note type="content">Fig. 1: Lateral view of the skull of Anas platyrhynchos with several ligaments. POM=lig. postorbitale; LM=lig. lacrimomandibulare; OM=lig. occipitomandibulare; JM=lig. jugomandibulare; LJ=lig. lacrimojugulare; SO=lig. suborbitale.</note>
<note type="content">Fig. 2: Force (in Newton) measured at the tip of the mandible required to depress the lower beak of the mallard over a range of 30°. The upper beak is fixed in the rest or elevated position. The curves are fitted through data points of 6–8 birds (12 measurements per bird). The top panel shows that the force increases continuously, without a clear ‘block’. Cutting the ligaments shows that the contribution of the ligaments PO and LO to the total force is small up to 20–25°. When the upper beak is elevated the ligaments are slack or at their resting length and do not resist jaw opening (middle panel). As a consequence less opening force for the lower jaw is required when the upper jaw is elevated than when it is at the rest position (lower panel).</note>
<note type="content">Fig. 3: 2D kinematic model. The model takes an upper (UB) and lower beak (LB) angle, and a quadrate (Q) position within the mandibular articulation groove as input and calculates the positions of skeletal and ligamentous elements. S=skull, Pa=palatine, Pt=pterygoid, Ju=jugal. Head morphology is characterized by the XY co-ordinates of the projection on the lateral plane of 14 skeletal points and the origo and insertion of the postorbital, lacrimomandibular and occipitomandibular ligaments (not shown). Skeletal points: 1, articulation of the quadrate with the skull; 2, hinge of the upper jaw; 3, articulation of the jugal bar and the upper jaw; 4, articulation of the jugal bar and the quadrate; 5, articulation of the palatine and the upper jaw; 6, articulation of the palatine and the pterygoid; 7, articulation of the pterygoid and the quadrate; 8, tip upper beak; 9, caudal point culmen of the upper beak; 10, tip lower beak; 11, dorsal point culmen lower beak; 12, quadratomandibular articulation (lateral condyle); 13, caudal border mandibular groove; 14, rostral border mandibular groove.</note>
<note type="content">Fig. 4: (a) Two ways to increase the range of lower jaw angles by limiting the strain in the postorbital ligament (PO). M=mandible, Q=quadrate, S=skull, Pa=palatine, Pt=pterygoid, Ju=jugal. A. The mandible moves forward and upward with the quadrate and PO shortens. (b) The mandible remains stationary with respect to the skull and the quadrate moves over a curved articular groove on the mandible decreasing the distance to the insertion of PO.</note>
<note type="content">Fig. 5: Calculated maximal strain in jaw ligaments of the mallard as a function of lower and upper beak angle, and position of the quadrate. Lines indicate beak angles for which the strain in PO and OM is 1.06. In the top panel the quadrate is kept at the most caudal position of the articulation groove. In this situation upper beak elevation results in a forward movement of the mandible, which is limited by OM. Lower jaw depression is limited by PO (and LOM). Maximal strain limits the possible combinations of upper and lower jaw angles to the area between the curves. Note that the lower jaw can depress 25° without elevating the upper jaw before PO reaches its maximal strain. As the quadrate moves forward along the articulation groove (half-way: middle panel) the area between the curves increases: upper beak elevation is effected without moving the mandible and the shorter distance between the quadrate and the insertion of PO allows larger opening angles for the mandible. At the most rostral point in the articulation groove (bottom panel) the distance between quadrate condyle and PO attachment is zero and for large upper beak elevations there are no constraints on lower jaw depression. However, for small elevation angles the mandible has to be retracted (also moving downward) for the quadrate to reach its rostral position in the articulation groove. This stretches PO and effectively blocks lower jaw movement.</note>
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