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Scientific article on the topic MORPHOFUNCTIONAL ASPECTS OF FOOD SPECIALIZATION OF THE FRUIT-eating hornbeak CALYPTOMENA VIRIDIS (PASSERIFORMES, EURYLAIMIDAE), COMPARATIVE ANALYSIS Biology

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Text of the scientific article on the topic "MORPHOFUNCTIONAL ASPECTS OF FOOD SPECIALIZATION OF THE FRUIT-eating hornbeak CALYPTOMENA VIRIDIS (PASSERIFORMES, EURYLAIMIDAE), COMPARATIVE ANALYSIS"

ZOOLOGICAL JOURNAL, 2014, volume 93, no. 6, p. 754-767

MORPHOFUNCTIONAL ASPECTS OF FOOD SPECIALIZATION OF THE FRUIT-eating hornbeak CALYPTOMENA VIRIDIS (PASSERIFORMES, EURYLAIMIDAE), COMPARATIVE ANALYSIS

© 2014 E. N. Zubkova1, L. P. Korzun1,2

1 Faculty of Biology, Moscow State University M.V. Lomonosov, Moscow 119991, Russia e-mail: 1 [email protected], 2 [email protected] Received July 15, 2013

Morphofunctional analysis of the jaw apparatus of the small green beak (Calyptomena viridis), a representative of the archaic family Eurylaimidae, crying passerine birds of the Old World, revealed a deep adaptation to the consumption of a wide range of fruits. This adaptation was formed on the basis of the key structural features of the jaw apparatus for robebeaks, adapted to the consumption of relatively large food items of animal origin. Within the framework of fructivorous adaptation, we received a consistent biomechanical interpretation of all the main specific morphological features of the jaw apparatus of the caliptomene, such as the unusual shape of the zygomatic arch, the structure of the jaw joint, the shape and orientation of the square bone, the external articular ligament, which is gently oriented in the transverse plane and vertical in the parasagittal plane, a feature attachment of the postorbital ligament, the role of the lacrimal bone and the structure of the lower jaw.

Key words: suboscines, Eurylaimidae, morphofunctional analysis, oral apparatus, fructo-venom, Calyptomena viridis.

This work is devoted to representatives of the family of Afro-Asian hornbeaks (Eurylaimidae) - one of three families of primitive screaming (Suboscines) passerine birds of the Old World. Unlike the screaming passerine birds of the New World, which demonstrate a relatively wide range of trophic adaptations in very species-rich families, each of the three families of the screaming passerines of the Old World contains a small number of species with very similar trophic specificity within each group.

In the Afro-Asian hornbeak family, which includes 16 species distributed over 10 genera and 5 subfamilies (Bruce, 2003), the overwhelming majority of species feed on animal food (arthropods, sometimes small vertebrates). Against the background of forest songbirds, all hornbeaks, especially large representatives of this family, are distinguished by weak locomotor activity. They hunt, collecting prey from branches, leaves, trunks. Sometimes they catch large insects in the air, looking out for them from the perch. Occasionally, fruit remains are also found in the stomachs of these hornbeaks (Lambert and Woodcock, 1996). Representatives of the Asiatic genus Calyptomena (3 species) stand out clearly from other hornbeaks in that they mainly feed on relatively large fruits, mainly

thus, ficuses (Lambert and Woodcock, 1996, Bruce, 2003). The birds either pluck them or, less commonly, collect them on the ground. The fruits are usually swallowed whole. Caliptomena can also vary their diet with invertebrates, for example, during the rearing period (Fogden, 1972). There is very little information about the diet of the extremely rare, small African Grauer's hornbeak (Pseudoca-lyptomena graueri); it is only known that these birds eat small fruits, flowers, and small invertebrates (Lowe, 1931).

Earlier, while studying the morphofunctional features of the mouth apparatus of insectivorous hornbeaks, we revealed a pronounced monomorphism of this group (Zubkova, Korzun, 2006, Zubkova, Korzun, 2006). Against this background, it is of particular interest to understand the depth of adaptation of the jaw apparatus of fructivorous hornbeaks to fruit feeding. The results of the morphofunctional analysis of this biomechanical node in one of the species of fructivorous hornbeak - the small green hornbeak Calyptomena viridis (hereinafter referred to as the caliptomene), determined the content of the proposed article.

At the moment, works considering the functional significance of morphological

There are practically no features of the screaming passerine birds of the Old World, with the exception of the one given above. Comparatively recent studies of the morphology of the hind limbs (Raikow, 1987) and syrinx (Prum, 1993) dealt primarily with issues of taxonomy. Earlier works (Forbes, 1880, Lowe, 1924, 1931) superficially touch on the features of the jaw apparatus, but contain errors.

We used museum specimens of the small green beak, or caliptomena, Calyptomena viridis from the subfamily Ca-lyptomeninae: mummy (MNHN), as well as the skull and skeleton of the tongue (No. 143-1 PIN). To carry out a comparative morphological and functional analysis, we also used alcoholic specimens of other hornbeaks - 7 species from 6 genera, representing two other subfamilies, namely: Eurylaiminae (brown - Corydon sumatranus (No. R2533 ZMMU), Javanese - Eurylaimus javani-cus (VZMSU), black and yellow - E. ochromalus (MNHN), red-bellied - Cymbirhynchus macro-rhynchos (no R2547 ZMMU), gray-breasted - Serilophus lunatus (no R2156 ZMMU) and long-tailed - Psa-risomus dalhousiae (ZMMU) variegated, or Cape hornbeak - Smithornis capensis (No. 94.338 ZMUC)). We used the heads of birds fixed in alcohol (one specimen of each species). In the listed species, the muscles were prepared in detail and the skeleton of the jaw and hypoglossal apparatus was studied. In addition, mounted skeletons (NBC) were additionally studied: blue-bellied green beak - Calyptomena hosei (no. 1130), red-sided speckled beak - Smithornis rufolateralis (no. 54), E. javanicus, C. macrorhyn-chos and C. sumatranus - 1 each copies, as well as 2 copies. E. ochromalus. The designations and descriptions of the muscles and aponeuroses of the jaw apparatus were made in accordance with the work of Dzerzhinsky and Potapova (1974). In the functional analysis of the oral apparatus, the methods of graphic statics developed by Dzerzhinsky (1972) were used.

Unfortunately, the authors did not have the opportunity to study the biology of calyptomene in the natural environment; this information was taken from the literature (Lambert, Woodcock, 1996, Bruce, 2003). To compare the behavioral and feeding characteristics of fructivorous calyptomena and insectivorous hornbeaks, in 2010, 2011, and 2012. We carried out targeted observations of three species of insectivorous hornbeaks (C. macrorhynchos, C. sumatranus and E. javanicus) in the Cat Tien National Park in the south of Vietnam on the basis of the Russian-Vietnamese Tropical Center. Environmental data was collected from

using classical methods of ornithology.

Explanation of the abbreviation used: MNHN - Museum of Natural History of Paris, France, NBC - Center for Biodiversity of the Museum of Natural History, Leiden, Netherlands, PIN - Institute of Paleontology. A.A. Borisyak RAS, Moscow, Russia, ZMMU - Ornithology Sector of the Scientific Research Zoological Museum of Moscow State University, Moscow, Russia, ZMUC - Zoological Museum of the University of Copenhagen, Denmark, VZMSU - Department of Vertebrate Zoology, Faculty of Biology, Moscow State University, Moscow, Russia.

GENERAL FEATURES OF THE HORNBEAK ORAL APPARATUS

All hornbills are distinguished by a disproportionately large head (Zubkova, Korzun, 200b, Zubkova, Korzun, 200b). Their specifically wide massive beak ends in a nail-like hook. A large, relatively soft tongue with a very weakly keratinized dorsal surface is located in the voluminous oral cavity. Without going into details, we can list the following general features of the hornbeak skull. First of all, this is the relative massiveness of the skull bones, which is especially pronounced in the preorbital region (as an example, we chose the most generalized representative of the hornbeak, E. javanicus, Fig. 1, 1). The structure of the beak determined the tendency towards the formation of a monolithic vaulted structure. For example, in C. macrorhynchos, this led to a significant overgrowth of the bony nostrils, and in the largest, C. sumatranus, it manifested itself in a very strong thickening of the arch ridge of the beak. The growth of bone tissue is also pronounced in the posterolateral parts of the upper jaw. In these areas, the edges of the beak can descend significantly below the dorsal edge of the strong lower jaw (this is most pronounced also in C. sumatranus).

The prokinetic flexible zone (pra, prokinetic area), located between the beak and the axial skull, in all members of the family is formed by a mobile syndesmosis. This zone is marked by a clearly visible deep transverse fissure between the frontal (Fr, frontale) and nasal (Ns, nasale) bones. At their junction, the nasal bones are depressed under the "overhanging" swollen frontal bones (Figs. 1 and 2). At the edges, the gap is widened and filled with loose connective tissue. In this place, their maxillary processes (mxns, proc. Maxillaris nasalis) depart steeply downward from the lateral bulges of the nasal bones (Fig. 1, 2, 1 and 2, 3). When squeezing the object, these processes play the role of struts, effectively transmitting pressure from the edge of the over-

Fig. 1. Skull, lateral view: 1 - Javanese hornbeak (Eryvichtm] al> amétus, 2 - Cape hornbeak (^ tmorrn ^ capensis): b - axis of the prokinetic flexible zone, OQ - vertical axis of the square bone, q - conditional center of the jaw joint, x is the conditional center of the square-cranial joint.

beaks to the frontal bones and further to the axial skull, thereby insuring the flexible zone. The fact that the jaw apparatus of the beak is specifically adapted to the forceful compression of the object at the base of the beak, in addition, is evidenced by some other features of its structure. The extended posterolateral parts of the maxillary bones, together with the ends of the maxillary processes of the nasal bones (tmu), approximately at the level of the flexible zone, form a kind of platform, which corresponds to the thickened areas of the branches of the lower jaw.

zun, 2006; Zubkova, Korzun, 2006) (Fig. 1, 1). These bony sites are capable of receiving pressure from an object clamped at the base of the beak.

The general plan of the structure of the jaw muscles is also characteristic of all hornbeaks (Zubkova, Kor-zun, 2006; Zubkova, Korzun, 2006). We regard it as with

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