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Abstract
The present study contrasts available biological data and results of morphofunctional analyses of the bill and hyoid apparatus in motmots. It shows that these omnivorous birds, which take relatively large food items, possess osteomuscular peculiarities that enable them to process these items as a whole in order to soften or cut them, and make them suited for easy ingestion. For that, they use the crenate edges of their rhamphotheca. Their jaws work as a highly mobile saw-like system. Their mutual movements, enhanced by the fact that particular dispositions of the hyoid apparatus rise the tongue and the supported items high up into buccal cavity, facilitate an effective clamping of items that can be moved along the jaws and be quite appropriately processed. To cite this article: L.P. Korzun et al., C. R. Biologies 327 (2004).
... Arnall and Keymer (1975), Tindall (1975) andMcLelland (1990) described the hyobranchial apparatus as a delicate framework of bones supports the tongue and responsible for its movement except in parrots, swallowing, breathing and voice production. Korzun, Erard and Gase (2004) added that, the mutual movements of the jaws enhanced by the fact of, particular disposition of the hyoid apparatus rise the tongue and the supporting items high up into the buccal cavity, facilitate an effective clamping of items that can be moved along the jaws. ...
The present study describes in detail for the first time the skeleto-muscular system of the jaw and hyoid apparatus (i.e. feeding apparatus) of seedsnipes (Thinocoridae), a small (two genera, four species) South-American bird family the biology and particularly the diet of which are still barely known. Morpho-functional analyses interpreted in the light of presently available behavioural and diet data show a strongly developed adaptation to the removal of attached plant items based on the acquisition of the separate control of jaws. In order to acquire this mechanism and because they are separated in two very different size-classes, large Attagis and small Thinocorus species did not modify the same osteo-muscular structures. Attagis species expanded m. pseudotemporalis superficialis of which they increased the intricacy of the internal aponeurotic system. Thinocorus species evolved a specific orbito-zygomatic process (mainly by expansion and fusion of postorbital and zygomatic processes by ossification of aponeuroses), expanded the medial portion of the external adductor of the mandible and increased the complexity of the aponeuroses of this medial portion. Seedsnipes appear to be well specialized in the continuous removal of small plant fragments thanks to a tongue raising mechanism joint to enlarged salivary glands and crenate areas in the buccal cavity. Thinocoridae seem to have followed a morpho-functional evolutionary pathway similar to that followed by sandgrouse (Pteroclididae) in the course of the adaptation of their bill and hyoid apparatus to a vegetarian diet essentially based on the removal of small attached plant fragments in rather similar habitat conditions.
For the present study, 15 species of pigeons representing the 5 sub-families usually recognized, and 3 species of sandgrouse were examined. The skeleton and musculature of the bill and hyoid apparatus are described. Morpho-functional analyses show that from a key adaptation to the removal and deglutition (without processing) of attached plant items, pigeons would have followed two pathways, one based on the joint muscular control of the movement of the jaws (Columbinae, Treroninae, Gourinae), the other on the separate muscular control (Didunculinae, Otidiphabinae). Sandgrouse would have diverged from this latter, developing the ability to very selectively remove attached plant items as well as to peck particularly small seeds on the ground. Unexpected differences appeared between sandgrouse species which raise eco-ethological problems.
The jaw muscles are described in detail in a primitive representative of plovers, Squatarola squatarola, taken as a standard subject, with references to the jaw muscle patterns in 3 other plovers (Stercorarius pomarinus, Cepphus grille, Uria aalge). The main attention is paid to muscle aponeuroses for which a nomenclature is suggested. The essence of internal differentiation of jaw muscles and, first of all, external adductor and pterygoid muscle consists in their complicated pinnate structure which represents a method of packing relatively short fibers (their length corresponds to the necessary amplitude of contraction) in the complex volume of the muscle. The complicated pinnate muscle can be visualized as a continuous layer of short fibers forming deep folds where aponeuroses cutx in. The construction of aponeurotic carcass reflects, therefore, most completely and precisely the morphological specificity of the muscle related to its functional abilities and spatial conditions.
A morphofunctional analysis of the feeding apparatus was conducted from an evolutionary perspective on the hoatzin (Opisthocomidae), some cuckoos (Cuculidae) and some turacos (Musophagidae). These goups share a common ancestral adaptation of the bill apparatus linked to starting food processing at base of the bill. The morphofunctional analyses give results different from what is known for the Galliformes and allow the construction of the hypothesis of two trophic adaptive pathways. One followed by the Cuculidae would have led to the consumption of a large range of arthropods, including toxic species; the other, followed by the Musophagidae and Opisthocomidae, would have led to the consumption of plant parts.
Although membership in broad diet categories is a standard feature of community analyses of Neotropical birds, the bases for assignments to diet categories are usually not stated, or they are derived from anecdotal information or bill shape. We used notations of stomach contents on museum specimen labels to assess membership in broad diet categories ("fruit only," " arthropods only," and "fruit and arthropods") for species of four families of birds in the Neotropics usually considered to have a mixed diet of fruit and animal matter: trogons (Trogonidae), motmots (Momotidae), New World barbets (Capitonidae), and tou- cans (Ramphastidae). An assessment of the accuracy of label data by direct comparison to independent microscopic analysis of actual stomach contents of the same specimens showed that label notations were remarkably accurate. The specimen label data for 246 individuals of 17 species of Trogonidae showed that quetzals (Pharomachrus) differ significantly from other trogons (Trogon) in being more fiugivorous. Significant differences in degree of fru- givory were found among various Trogon species. Within the Trogonidae, degree of frugivory is strongly correlated with body size, the larger species being more frugivorous. The more frugivorous quetzals (Pharomachrus) have relatively flatter bills than other trogons, in ac- cordance with predictions concerning morphology of frugivores; otherwise, bill morphology correlated poorly with degree of fiugivory. An analysis of label data from 124 individuals of six species of motmots showed that one species (Electron platyrhynchum) is highly in- sectivorous, differing significantly from two others that are more frugivorous (Baryphthengus martii and Momotus momota). An analysis of 135 individuals of 12 species of barbets showed that although "fruit only" predominated among almost all species, arthropods are more frequently recorded in the stomachs of species in the genera Eubucco and Capito than in Semnornis. The highly frugivorous diet of Semnornis species is yet another parameter in which they resemble toucans more than New World barbets. Data from 326 individuals of 32 species of toucans showed that the family is remarkably homogeneous in the predomi- nance of fruit in the stomachs of all species. These data suggest that the degree to which toucans prey upon bird eggs and nestlings, and animal matter in general, is overemphasized. Although our data suggest that it is safe to assign toucans to a "fruit only" category in community analyses, such assignments must be taken on a genus-by-genus or species-by- species basis in trogons, motmots, and barbets.
A morphofunctional analysis of the bill apparatus was conducted on some African forest flycatchers (Muscicapidae, Platysteiridae, Monarchidae) in relation to detailed eco-ethological data available on these species. The aim was to evaluate relationships between anatomical structures and habitat constraints and also identify the most pertinent trophic adaptations. If forest Muscicapidae have essentially conserved the generalized passerine structures and occupy open-habitat niches in the forest, Platysteiridae and Monarchidae have adapted to forest conditions and show a key-adaptation based on specific changes in the structure of the bill apparatus in response to particular light patterns and habitat clogginess, constraints that require speed and precision for the capture of prey and protection of the skull against collisions.
The present study points to morpho-anatomical features that allow vegetarian but mainly frugivorous turacos to fill at best their specific feeding requirements. Mechanisms are analysed which the bird can use to detach a fruit and avoid it rolls out of the bill. It is also examined how vegetable items can be processed particularly when they have to be cut, and what can facilitate their ingestion particularly when they are fruits that have to be swallowed entirely and are large and/or have dry or fibrous skin or flesh. The skeletal and muscular anatomy of the bill and hyoid apparatus is described in details and illustrated. The particularly short and stout bill coupled with a relatively simple system of aponevroses of the adductors reflects a trade-off between two important jaw functional requirements: huge efforts for clamping, and a wide opening for plucking, processing and swallowing relatively large fruit. The clearly oblique orientation of the modified outer adductor seems an adaptation to the detachment of fruits. The os uncinatum, particularly developed in this bird family, is interpreted as maintaining transversal stability, particularly when jaws act as a pair of scissors. Most food items being processed near the base of the bill, mechanisms have been developed which contribute to overcome the risk of breakage at the level of the prokinetic hinge because of a vertically oriented force there. Hyoid apparatus features are related to the tongue role during the detachment of the fruit and its processing in the bill.
