Morphology of the feeding apparatus in nestlings of Merops

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1 Italian Journal of Zoology ISSN: (Print) (Online) Journal homepage: Morphology of the feeding apparatus in nestlings of Merops Andrea Brusaferro & Alberto Mario Simonetta To cite this article: Andrea Brusaferro & Alberto Mario Simonetta (1998) Morphology of the feeding apparatus in nestlings of Merops, Italian Journal of Zoology, 65:3, , DOI: / To link to this article: Copyright Taylor and Francis Group, LLC Published online: 22 Oct Submit your article to this journal Article views: 128 View related articles Citing articles: 1 View citing articles Full Terms & Conditions of access and use can be found at Download by: [ ] Date: 07 January 2018, At: 18:58

2 Irai. J. Zool., 65: (1998) Morphology of the feeding apparatus in nestlings of Merops ANDREA BRUSAFERRO Dipartimento di Biologia Molecolare, Cellulare e Anímale, Università di Camerino, via Camerini 2, I Camerino (MC) (Italy) ALBERTO MARIO SIMONETTA Dipartimento di Biologia Animale e Genetica "Leo Pardi", Università di Firenze, via Romana 17, I Firenze (Italy) ABSTRACT The morphological comparison of the facial skeleton and tongue between young nestlings and subadults has shown that Merops desmognatism is due to the ossification of the processus prenasalis and solum nasi. The maxillo-palatines are not fused along the midline and the pterigoid is fused to the vomer. The heterochrony in the development of the skull of Merops was suggested to be due to protracted parental care so that only when the bird captures its prey, do the stresses produced in the killing actions induce ossification of the solum nasi and of the processus prenasalis. KEY WORDS: Aves - Coraciiformes - Merops - Skull morphology. ACKNOWLEDGEMENTS For part of the material used in this investigation, we are indebted to Or. Robert Prys-Jones of the British Museum (Natural History) who loaned two heads of nestlings (Merops viridis and Merops ornatiis) and to Dr. Annamaria Nistri of the "La Specola" Museum in Florence (Italy) for one subadult skull of Merops cipiaster. Thanks to the British Museum (Natural History) of Tring and to the "La Specola" Museum of Florence (Italy), it was possible to examine some nestlings of different families of the Coraciiformes. (Received 1 April Accepted 4 May 1998) INTRODUCTION The morphology of the feeding apparatus is highly. varied and strongly adaptive in birds. The heterogeneity of the feeding apparatus of the Coraciiformes represents an excellent example because it is very difficult to identify any palatal character common to all the families. The few common characters, such as the desmognathic condition of the palate and the strong medial ligament of the quadrate (this is not true for the Alcedinidae; Burton, 1984) are insufficient to lead to an evolutionary interpretation or to assess systematic relationships. The crucial point is whether the investigation of developmental pathways leading to the desmognathic condition are or are not important with respect to the varieties of desmognatism (Parker, 1876). The desmognathism of Merops is different with respect to that of Nyctiornis (Meropidae), and to that of Alcedinidae as well. The cranial morphology of the Meropidae and that of the Coraciiformes has been studied since the last century by several anatomists (Huxley, 1867; Sharpe, ; Murie, 1872b, c, 1873; Garrod, 1874, 1878; Shufeldt, 1884, 1903; Fürbringer, 1888, 1902; Gadow, 1892; Beddard, 1893; Stresemann, 1934, 1959; Wetmore, 1934, I960; Lowe, 1946, 1948; Verheyen, 1955; Rawal, 1970; Cracraft, 1971; Rawal & Bhatt, 1974; Soliman et al., 1975; Burton, 1984; Bhattacharyya, 1987), but the available knowledge concerns only the adult skull and so far we know nothing about the nestlings and the post-natal development of Coraciiformes except for that of Upupa epops (Soliman et al, 1975). Indeed the study of post-natal development deserves more attention. During the nestling stage, while the cartilages are already well developed, the dermal bones are incompletely developed and they are neither fused nor completely ossified, so that it is possible to see clearly the connections between the different structures. Comparison with the adult stage, and as far as possible with an intermediate stage, help us in learning the adaptive changes of the entire feeding apparatus, as well as identifiyng homologous structures that are most important factors for understanding systematic relationships. The present paper concerns the morphology of the Meropidae and is part of a systematic attempt to clarify the adaptive pathways of the feeding apparatus and contribute to the debate on the systematics of Coraciiformes. MATERIALS AND METHODS Four specimens of Merops apiaster, one of M. viridis, and one of M. ornatus were studied. Of the specimens of M. apiaster, three were nestlings collected by one of us (A. M. Simonerta) in 1977 from Afgoi (Somalia) and one was a subadult on loan from the Museo "La Specola" of Florence (collection No. 3017). The specimen of M. viridis was a nestling (unregistered) loaned by the British Museum (Natural History) of Tring and the specimen of M. ornatus was a subadult (collection No. A\ ) loaned by the British Museum (Natural History) of Tring.

3 250 A. BRUSAFERRO, A. M. SIMONETTA With the exception of the skull of one nestling of M. apiaster, that was stained in toto by the Wassersug method (1976), the skulls were prepared for microscopical analysis after décalcification in "Top Decal" (Pabish) and embedding in paraffin-celloidin. The skulls of the nestlings were microtomized in 12-H-thick serial section and the subadult skulls in sections of 14 u.m. The preparations were stained with Mallory's triple stain method (1900) and the graphics reconstructions were made with the PC3D recstruction software of Jandel Scientific Corporation. RESULTS Topography of palatal bones In the nestling of Merops the corpora of the fused premaxillaries form the anterior tip of the beak. Each corpus premaxillaris extends backwards in a dorsal processus nasalis (processus frontalis, Marinelli, 1936; processus prenasalis, Erdmann, 1940; processus ascendens, de Beer, 1937), in a ventral processus palatinus (palato-maxillary, W. K. Parker, 1866) and in a ventrolateral processus maxillaris (processus labialis, Jollie, 1957; processus palatinus, Webb, 1957; processus alveolaris, de Beer, 1937). The proc. maxillaris extends backwards and forms the lateral edge of the beak just behind the corpora of the fused premaxillaries and in front of the proc. zygomaticus of the maxillary bone. The proc. maxillaris for the whole of its length.has a syndesmotically medial contact with the maxillary bone. The proc. palatinus does not fuse medially with its corresponding controlateral process and extends backwards ventro-medially to the palatine and medially to the maxillary (Fig. 1). The anterior tip, as well as the anterior portion of the corpus maxillaris is syndesmotically united with the lateral proc. maxillaris of the premaxillary bone, with the ventral palatine bone and with the medio-ventral proc. palatinus of the premaxillary bone. The greater portion of corpus maxillaris is ventral to the atrioturbinal region of the nasal capsules; the corpus is located dorsally to the palatine and medio-ventrally to the proc. maxillaris of the premaxillary bone. More posteriorly, each maxillary bone thins off into two posteriorly directed processes: the processus jugalis (processus labialis, Jollie, 1957; zygomatic process, Müller, 1963) and the processus maxillopalatinus (palatine process, Gadow & Selenka, 1891, de Beer, 1937, Hofer, 1945, Jollie, 1957). The palatine process of the maxillary is a short process that originates from the median surface of the maxillary and is directed medially and dorsally to the palatine; each maxillopalatine is separated from the other one and its posterior portion leaves a broad fissure (the choanae) between the two structures (Fig. 1). Each palatine consists of a narrow anterior part in the nasal region of the skull, while in the orbital region it broadens to a flat plate-like structure. From its anterior tip, the palatine continues backwards ventrally to the maxillary and laterally to the proc. palatinus ossis premaxillaris; where the maxillary thins off into a proc. maxillapalatinus and proc. zygomaticus, the palatine bends inwards ventrally to the maxillapalatinus. Therefore the palatine has a simple morphology in the nasal region: it is a bony rod with an elliptical cross section. Behind the choanae, the palatine becomes more complex and it broadens to a flat plate-like structure; here the medial edge of the palatine is produced medially to form a dorsal processus ethmopalatinus and a processus ventralis. The medial edge of the ethmopalatine lies against the anterior tip of the parasphenoid (Fig. 2); more posteriorly, the distal edge of the ethmopalatine is wedged between the parasphenoid and the anterior tips of the vomers. Posteriorly the ethmopalatine becomes larger and it forms the most developed part of the palatine. The proc. ventralis palatini remains unchanged for its whole length, but, for a short length, its distal edge bends inwards approaching the respective counterpart. Between these two processes, the medial surface of the palatine has a concavity; in the orbital region a processus medialis palatini develops from the concavity and its distal edge is located ventral to the pterygoid. More caudally the process is in syndesmosis with the respective process of the corresponding bone. The vomers are a paired structures placed ventrally to the ethmopalatine; short and kidney shaped in cross section (Fig. 2), they continue backwards and are synostotically fused with the pterygoids. The pterygoid reaches from the palatine to the quadrate to which it is articulated by means of a synovial joint ventral to the proc. orbitoquadratus (proc. orbitalis) of the quadrate. This joint is of a ball-and-socket type and the posterior tip of the pterygoid bears a cupshaped concavity with no articular cartilage; this fits into a cartilaginous protuberance on the medial surface of the quadrate. Anteriorly, the pterygoid overlaps the posterior end of the palatine dorsally and its anterior end is synostotically fused with the vomer. Dorsally the pterygoids are separated from the rostrum by a narrow fissure V-shaped in cross section. More posteriorly each pterygoid is articulated with a short secondary basipterygoid process of the basisphenoid; the basipterygoid joint is synovial (Fig. 3) and the articular surfaces are covered by cartilage and located in an articular cavity enclosed by a synovial membrane. The proc. jugalis ossis maxillaris is a long, slender process tapering posteriorly; it overlaps the jugal and the anterior half of the quadratojugal and the bones are in syndesmosis. The jugal is a short bony rod; its anterior portion is dorsal to the processus jugalis ossis maxillaris and the posterior portion is dorsal to the quadratojugal. The quadratojugal is a slender bony rod; its posterior end fits into a cup-shaped fossa of the quadrate and no synovial cavity is present. A limited amount of movement between the two elements is possible, but there is no real diarthrosis. The nasal capsules In the nestling of Merops, the nasal capsule is almost entirely cartilaginous. A certain amount of ossification

4 FEEDING APPARATUS OF MEROPS 251 POP TN PNAS fn PP BO POP MT SN PP Fig. 1 - Graphic reconstruction of the skull of a young nestling of Merops aptaster. A, dorsal view, above chondrocranium; B, lateral view, nasal capsule without parietotectal cartilage; C, ventral view, below chondrocranium. Abbreviations BO, basioccipital; BTP, basitemporal plate; EC, ectethmoid; EO, exoccipital; FC, fenestra craniofacialis; FM, foramen magnum; FN, fenestra narina; FR, frontal; IS, interobital septum; L, lacrimal; MA, maxillary; MP, maxillopalatine; MT, maxilloturbinal; NA, nasal; NT, nasal septum; OC, occipital condyle; PAR, parietal; BPTA, basipterigoid articulation; PL, palatine; PLS, pleurosphenoid; PM, premaxillary; P.MAX, processus maxiltaris of the premaxillary; P.NAS, processus nasalis of the premaxillary; POP, postorbital process; PP, processus prenasalis P.PAL, processus palatinus of the premaxillary; PS, parasphenoid; PSR, parasphenoid rostrum; PT, pterygoid; Q, quadrate; QJ, quadratojugal; SN, solum nasi; SO, supraoccipital; SQ, squamosal; TN, tectum nasi; V, vomers. Roman numerals indicate foramen for cranial nerves. Bar, 2 mm. has taken place in the septum and in the roof of the capsule posteriorly. The anterior end of the nasal capsule is produced into a very prominent azygous processus prenasalis (Fig. 1); the premaxillary bones surround the anterior end of this process. Posteriorly the proc. prenasalis merges into the septum nasi lengthening dorsally to assume a drop-shape in cross section (Fig. 4A); more posteriorly, the processus fuses dorsally with nasal cartilages forming a clear crest on the ventral surface of the nasal capsule (Fig. 4B). Therefore the proc. prenasalis does not arise from the anterior end of the nasal capsule but from its ventral surface and the posterior

5 252 A. BRUSAFERRO, A. M. SIMONETTA Fig. 2 - Transverse section showing the anterior end of the vomers and the palatine in a young nestling of Merops viridis. Abbreviations: IS, interorbital septum; PL, palatine; PSR, parasphenoidal rostrum; V, vomers. Bar, 0.5 mm. BSPH SEC.C Fig. 3 - Transverse section showing the basipterigoid articulation in a young nestling of Merops aptaster. Abbreviations: BSPH, basisphenoid; PT, pterigoyd; S.CAV, synovial cavity; SEC.C, secondary cartilage. Bar, 0.5 mm. end of the process appears to be the swollen ventral surface of the septum nasi. In this region, each nasal vestibulum is separated by connective tissue covered with epithelium. Behind the fenestra internasalis, the septum nasi increases in height fusing with the parietotectal cartilage. The cupola anterior is absent because the fenestra narina opens anteriorly (Figs 1-4B). The anterior two-thirds of the septum in front of the fissura craniofacialis are cartilaginous and thin, but in the atrioturbinal region its ventral edge is swollen. More posteriorly, in the region of maxilloturbinal cartilage, the ventral edge of septum nasi has two cartilaginous bulges, the dorsal one being fused with the solum nasi. In front of the fissura, the septum nasi is again thin with no ventral bulge. The roof of the nasal capsule is complete and the parietotectal cartilage continues laterally downwards to form the side wall of the capsule. Posterior to the fenestra narina the parietotectal cartilage decreases in height, so that the lower portion of the atrioturbinal (de Beer, 1937) may be seen laterally. At the posterior end of the atrioturbinal, however, the side wall is extended ventrally again to cover the maxilloturbinal laterally (de Beer, 1937). The floor of the nasal capsule is complete and cartilaginous in the region of the atrioturbinal and maxtlloturbinal cartilage, but it completely disappears in front of coanae. The atrioturbinal extends from a distance behind the fenestra narina up to some distance in front of the anterior tip of the maxilloturbinal. For almost its entire length it is attached to the side wall of the nasal capsule and projects freely into the vestibulum of the nasal capsule. The anterior portion consists of a thin primary lamella bearing two secondary lamellae: a well-developed ventrally direct one and a smaller dorsal one. Posteriorly, the primary lamella becomes shorter and thicker, the secondary ventral one lengthens and the dorsal one is reduced to a low cartilaginous ridge, which disappears near the hinder end of the turbinai (Fig. 4C-D). The posterior end of the atrioturbinal is a bulge located on the floor of the nasal capsule. The maxilloturbinal is cartilaginous and is fused to the dorsal surface of the side wall of the nasal capsule. The anterior end is located immediately behind the posterior end of the atrioturbinal cartilage and consists of a short cartilaginous lamella. More posteriorly, the maxilloturbinal presents a peculiar arched shape with the convexity directed toward the septum nasi. In the region of the concha nasalis (de Beer, 1937), the maxilloturbinal is located on the medial surface of the side wall of the nasal capsule and its distal end borders the choanae (Fig. 4E-F). Wedged in between the tectum nasi and the dorsal surface of the maxilloturbinal cartilage is a well developed concha nasalis; it is thin and entirely cartilaginous (Fig. 4G-H). In the posterior region of the nasal capsule, the nasal cavity is smaller and protected dorsally by the tectum nasi, while laterally and ventrally it is surrounded by connective tissue. More posteriorly, each vestibulum is subdivided into two smaller cavities; the medial one opens into the orbital region thus forming a paranasal sinus, while the lateral one is a caecum close to the lacrimal duct. The planum antorbitale is a cartilaginous plate extending ventrolaterally from the septum-, it does not close the posterior wall of the nasal capsule, but is a thin cartilage strip that points the passage from the nasal to the orbital region. Dorsomedially, it is closely connected to the lateral surfaces of the septum, while the distal edge is syndesmotically connected to the

6 FEEDING APPARATUS OF MEROPS 253 B H 22 -^ V Fig. 4 - Outline of the series of anterior-posterior transverse sections through different regions of nasal capsule in a young nestling. 1, processus nasalis ossispremaxillaris-, 2, processus maxillaris ossispremaxillaris; 3, maxillary; 4, palatine; 5, processuspalatinus ossispremaxillaris; 6, processusprenasalis-, 7, fenestra narina; 8, septum nasi; 9, parietotectal cartilage; 10, atrioturbinal cartilage; 11, solum nasi; 12, processus maxillaris ossis nasalis-, 13, processus premaxillaris ossis nasalis; 14, maxilloturbinal cartilage; 15, concha nasalis; 16, processus maxillopalatinus; 17, processus zygomaticus; 18, nasal; 19, planum antorbitale; 20, fenestra craniofacialis; 21, lacrimal; 22, jugal; 23, frontal; 24, parasphenoid; 25, vomers. Bar, 2 mm.

7 254 A. BRUSAFERRO, A. M. SIMONETTA lacrimal. The planum tapers rapidly to form a short process closely adjacent to the septum (Fig. 4I-J). The membrane bones of the nasal capsules The premaxillaries are fused to form a single bony structure strengthening the tip of the beak; each premaxillary possesses three backward directed processes: a proc. frontalis, a proc. palatalis and a proc. alveolaris. The latter two have been dealt with in the description of the palate. The proc. frontalis ossis premaxillaris continues backwards, dorsal to the nasal capsule, for the entire length of the bill, while the caudal tip of the proc. frontalis is placed at the level of the nasal-frontal hinge (Fig. 1). The nasal is a thin bony plate lateral to the posterior third of the proc. frontalis ossis premaxillaris; at its fore end, the nasal is bifurcated to form a median proc. premaxillaris and a lateral proc. maxillaris. The proc. maxillaris ossis nasalis is a ventrally directed, long, slender, tapering process extending forwards dorsally to the maxillary and mediodorsally to the proc. lateralis ossis premaxillaris (Fig. 1). The fenestra narina is bounded anteriorly by the premaxillaries and dorsally by the proc. frontalis ossis premaxillaris and by the proc. premaxillaris ossis nasalis; posteriorly it is bounded by the nasal and ventrally by the proc. maxillaris ossis nasalis and the proc. lateralis ossis premaxillaris. The lacrimal is well developed and is formed by a dorsal portion (head of the lacrimal), joining with the nasal and the frontal and by a descending process. The distal end of the descending process widens into a small basal plate that adjoins the jugal. The foot of the descending process overlaps for a short length with the distal edge of the planum antorbitale. The frontals are in syndemosis along the dorsal midline, except for their anteriorly diverging ends; anteriorly, the frontal is overlapped by the nasal but the mesokinetic hinge is not restricted to this region; the dorsal bending is located at the level of the nasal immediately dorsally to the fissura craniofacialis, and here both nasals are very thin forming a restricted line of bending. The lower jaw The following dermal bones occur in the lower jaw of Merops: dentary, splenial (opercular; Gadow, 1892), gonial (complementary; Suschkin, 1899; Gaupp, 1911), angular and surangular (Fig. 5). The different dermal bones surround a central canal in which lies Meckel's cartilage (Fig. 6A). In the nestling of Merops, the different bony elements are in syndemosis, except the gonial and the surangular which show an incipient synostosis. The left and the right dentaries join anteriorly between the dentary internal surface. The dentary extends backwards for half the length of the mandible and has a ventral process reaching far backwards and lying lateral to the anterior portion of the angular. The dentary cov- MC RLD SA CMF ART ANG ART Fig. 5 - Graphics reconstruction of the mandible in a young nestling of Merops apiaster. A, lateral view; B, medial view; C, medial view without the splenial and gonial bones. Abbreviations: ANG, angular; ART, articular; CMF, caudal mandibular fenestra; D, dentary; GON, gonial; MC, Meckel's cartilage; RLD, ramus lateralis of the dentary; RMD, ramus medialis of the dentary; SA, surangular; SPL, splenial; V.PROC.D, ventral processus of the dentary. Bar, 2 mm. ers the anterior half of Meckel's cartilage dorso-laterally and ventrally and it is thicker in the dorsal surface. More posteriorly, the dorsal edge of the dentary displays a groove in which lies the anterior end of the surangular. Going backwards, the groove becomes deeper and turns into a fissure which separates the dentary in the ramus lateralis and the ramus medialis. Behind to the anterior end of the surangular the ramus lateralis separates in dorsal and ventral processes (Fig. 6B). The dorsal process of the ramus lateralis and the ramus medialis of the dentary continue backwards dorsally to Meckel's cartilage, their tapering distal ends half way along the lower jaw. The ventral process is longer and continues backwards lying laterally to the Meckel's cartilage. Posteriorly, the ventral process of the dentary becomes thin and it ends beyond the angular and the surangular. The anterior end of the surangular lies wedged between the dorsal processes of the dentary (Fig. 6A-B). The surangular broadens posteriorly and covers dorsolaterally the posterior half of the Meckel's cartilage. It is bordered ventrally by the angular. The splenial is a thin bony plate that medially covers Meckel's cartilage (Fig. 6A-B). The anterior half of the splenial is bordered dorsally by the ramus medialis of the dentary and ventrally by the ventral process of the dentary. The posterior half of the splenial is bordered dorsally by the surangular and ventrally by the angular. Posteriorly the splenial displays synostosis with the angular.

8 FEEDING APPARATUS OF MEROPS 255 SPL SPL MC R.MAND. V MC VPROC.D MC VPROC.D Fig. 6 - Series of anterior-posterior transverse sections through different regions of the lower jaw in a young nestling of Merops viridis. Abbreviations: ANG, angular; D, dentary; GON, gonial; MC, Meckel's cartilage; RLD, ramus lateralis of the dentary; RMD, ramus meclialis of the dentary; SA, surangular; SPL, splenial; V.PROC.D, ventral processus of the dentary. Bar, 2 mm. The gonial (Fig. 6C) medially covers the posterior half of Meckel's cartilage. Its anterior end lies between the ramus meclialis and the splenial, medio-dorsal to the cartilage. Posteriorly, it is fused with the angular. For its entire length the gonial is bordered dorsally by the surangular and ventrally by the splenial. The angular is a bony plate ventral to Meckel's cartilage. Its anterior end lies immediately in front of the anterior end of the gonial. The angular broadens posteriorly between the dorsal Meckel's cartilage and the ventral splenial and dentary bones. Behind the posterior ends of the dentary and splenial bones, the angular is a large bony plate ventral to Meckel's cartilage. Here it is bordered laterally by the surangular and medio-dorsally by the gonial. The posterior end of Meckel's cartilage is covered medially by the gonial, ventrally by the angular and dorsolaterally by the surangular. The posterior portion of Meckel's cartilage is not yet ossified to form the articular; it just shows signs of pericordal ossification. The articular part of the cartilage shows a short lateral process and a medial process. Approaching the basitemporal bone, the medial process extends medially and its medial edge fits into a cup-shaped concavity limited dorsally by the lateral process of the basitemporal bone. Each articular surface is covered by a thin layer of connective tissue. The hyoid skeleton The hyoid of birds consists of an unpaired corpus (.copula) made up usually by fused copula I and copula II; the copula articulates with paired cornua branchialia, each consisting of a proximal hypobranchial (ceratobranchial; Suschkin, 1899) and a distal ceratobranchial (epibranchial; Suschkin, 1899). The hyoid of Merops is typically avian (Fig. 7). The paraglossum supports the tongue as generally in Aves, and before Reichert (1837) it was called either an os linguale or an os entoglossale. According to Owen (1866), T. J. Parker (1892) and Pycraft ( ), the paraglossum is a Y-shaped cartilage and the posterior prongs correspond with the ceratohyals, while the anterior slender unpaired structure is the basihyal. All authors except Kallius (1905) believed this; Crompton (1953) corroborates the original claim of Kallius (1905) and states that "...the anläge of the paraglossal cartilage, is situated dorsally to the anterior region of the copula. On either side if this plate a centre of condensation of the tissue is observable. These indicate the paired nature of the paraglossal cartilage". In the nestling of Merops, the only evidence of its paired origin is the two anteriorly directed prongs. In a dorsal view, the paraglossum is an A-shaped cartilage. In fact, each prong converges anteriorly and fuses in a slender cartilaginous unpaired structure. More posteriorly, the paraglossum articulates with the dorsal surface of the copula, and in this region the two prongs of paraglossum are connected by a cartilaginous bridge. The copula consists of a fused copula I and copula II and is flattened laterally. Its anterior portion lies between the two prongs of the paraglossum, and midway along its length the copula is constricted laterally, form-

9 2% A. BRUSAFERRO. A. M. SIMONETTA PAR. COR I COPII HPB. CTB. Ify. 7 - Graphics reconstruction of the ventral aspect of the hyoid complex in a young nestling of Merops apiaster. Abbreviations: COM, copula I; COP.II, copula II; CTB, ceratobranchial; HTB, hypobranchial; PAR, paraglossa. Bar, 1 mm. ing an articular fossa for the hypobranchial on either side. Posteriorly the copula is flattened laterally again and has a long posteriorly directed process. The hypobranchial and the ceratobranchial are articulated to form a long, slender, rod-like cornu branchiale f. In the stages investigated, the cornu branchiale I is in an advanced stage of perichondral ossification whereas its terminal portions are cartilaginous. The cornua branchialia extend backwards and outwards from the copula in the form of a V. The posterior third of the cornu branchiale curves upwards and its distal end slightly inwards. DISCUSSION Cranial kinesis The kinetic mechanism in the skull of Merops is typically prokinetic, the most common form of kinesis in birds, in which the upper jaw maintains its shape as it pivots about the craniofacial hinge (Hérissant, 1752; Uoecher, 1951; Bock, 1964; Bühler, 1981; Zusi, 1993). Rotation upwards of the upper jaw begins by the contraction of the Musculus protractor pterygoidei. According to Burton (1984), the M. protractor of Meropidae is large, its insertion is over the entire medial surface of the orbital process, and the muscle shows no differentiation into two parts. The study of the transverse sections in the nestlings corroborates Burton's statements (1984). The quadrate is pulled forward and slightly inwards by the contraction of M. protractor pterygoidei. Forward movements of the quadrate are transferred to the maxillary and the premaxillary by way of the palatine which attaches in syndesmosis with these bones, and by the lower temporal arch. The pterygoid and the palatine are in syndesmosis and they can slide along the rostrum. The beak is rotated dorsally but the amount of dorsal rotation of the beak in the nestling cannot be very considerable, as a true mesokinetic joint is absent. In the nestlings investigated, there is no 'real fracturing' of the septal apparatus, but the bending of the nasal septum is perhaps possible to a very limited extent as the septum is still cartilaginous. In addition bending is facilitated by the presence of a large fenestra septi nasi posterior (Fig. 1) which is filled with connective tissue. The ventral borders of the fenestra septi nasi posterior and that of fenestra septi nasi anterior are formed by the fused trabeculae and in front of the nasal capsule this trabecular bar is elongated into a very prominent processus prenasalis. In the subadult skull, the ventral border of the fenestra septi nasi posterior is still cartilaginous and partially resorbed. In the adult skull, the nasal septum has become ossified but the bending is possible because the ventral border of the fenestra septi nasi posterior is totally resorbed (it is now called fissura craniofacialis) so that there is a real 'fracturing' of a septal apparatus (de Villiers, 1946) and there is a dorsal line of bending. Both in the nestling and adult skull, bending is limited to the nasal and to the processus frontalis ossis premaxillaris. The frontals do not take any active part in the dorsal hinge. The movements of the upper jaw are also limited, in the nestling, by the presence of a true basipterygoid articulation (Fig. 3). Given the proportions of the skull, the mesokinetic flex line lies cranially with respect to the basipterygoid articulation so that this not only cannot work as a pivot, but actually restrains kinesis, as it is clear that in Merops an efficient kinetic mechanism involves the rotation of the pterygoid away from the basisphenoid. The résorption or modification of the basipterygoid articulation is therefore necessary. In the nestling of Merops, the basipterygoid joint, probably in relation with the comparative shortness of the beak, is synovial with small articular surfaces, and this implies little movement of the upper jaw. In the subadult skull, the basipterygoid process is reduced to a small spine of a basisphenoid (Fig. 8) and the joint is substituted by a delicate ligament allowing an increase in the amount of kinetic movements. However the structural continuity of the septal apparatus is still an impediment to the movements of the jaw. To sum up: the nestling and the subadult of Merops technically have a kinetic upper jaw, but the movements of the jaws are limited and apparently they are basically passive and function as a sort of shock absorber. An efficient kinetic mechanism is obtained in the adult skull with active food-getting.

10 FEEDING APPARATUS OF MEROPS 257 BSPH PT Fig. 8 - Transverse section showing the regression of the basipterigoid articulation in a subadult of Merops ornatus. Abbreviations: BSPH, basisphenoid; PT, pterigoyd; S.CAV, synovial cavity; SEC.C, secondary cartilage. Bar, 0.5 mm. The quadrate condyles are arranged in horseshoe pattern and the cavities between the lateral and medial ones are poorly defined. The articular surfaces on the mandible are flat and lack the knob that fits into the cavity between the lateral and medial condyles of the quadrate. So the articular surfaces on the quadrate-articular hinge do not offer protection against possible disarticulation of the mandible when the bill is opened, and probably when the bill is beaten on a branch with lateral movements for killing the prey. Hence a medial brace is present and the morphology of the quadrate-articular hinge of Merops is similar to that of Charadrius hiaticula described by Bock (I960), but the contact between the medial brace and the basitemporal bone is really different. This is a secondary articulation, but not a centre of rotation of the mandible and probably works primarily as a shock absorber. Indirect desmognathism The subadult shows better development of the dermal bones and more advanced ossification of the cartilages; the premaxillary, the maxillary and the palatine are stronger and more developed. Anyway, the relationships of the bones are the same as those in the young nestling: the premaxillo-palatines and the maxillopalatines are still separated, the vomer is longer but maintains its paired structure and the pterygo-palatine articulation is the same as in the young nestling with the synostotical fusion between pterygoid and vomers. The same is true for the membrane bones dorsal to the nasal capsules. On the contrary, a most important feature is the heterochronous development of the chondrocranium; the braincase and the orbital region show adult features while the nasal region has a juvenile morphology. Microscopic study of the young nestling and of the subadult skulls of Merops has outlined the presence in the young nestling of a long proc. prenasalis. Posteriorly, the processus prenasalis merges with the septum nasi fusing dorsally with the nasal cartilagines and forming a definite crest on the ventral surface of the nasal capsule. According to Engelbrecht (1958), the proc. prenasalis of Pyromelana does not arise from the anterior end of the nasal capsule (as maintained as a general rule by de Beer & Barrington, 1934; Swart 1946 in Anas; Grewe, 1951), but in ventral view it looks like a swollen ventral edge of the septum nasi and probably represents the original anterior part of the trabecula communis. As in Nyctisirigmus pectoralis pectoralis (Fourie, 1955), in the young nestlings of Merops there is a total continuity between the processus prenasalis and the trabecular bar, so that they form a single functional unit. Engelbrecht (1958) claims that the proc. prenasalis serves as substratum around which the membrane bones in that region are formed, as was suggested by W. K. Parker (1869) and Romanoff (I960). In the nestling of Nyctisirigmus pectoralis pectoralis the proc. prenasalis and the trabecular bar are partially resorbed (Fourie, 1955). The condition of Merops is indeed different from that of most other birds, because the proc. prenasalis together with the solum nasi ossifies as an interpalatine and fuses with the maxillo-palatines, forming an indirect desmognatism. The anterior part of the proc. prenasalis is totally resorbed in the adult, but the part placed ventrally to the nasal capsules remains and ossifies. So the proc. prenasalis is not totally resorbed, but its posterior region is part of the structure of the adult palate. Thus the well-developed central ridge in the anterior region of the upper beak (Rawal, 1970; Rawal & Bhatt, 1974) in the adult Merops is formed totally by the solum nasi and by the proc. prenasalis (Fig. 9). Anteriorly the central ridge shows a pair of small fenestrae that may be due to the absence of the solum nasi in this region. According to Burton (1984), desmognathy may be important for the evolution of the Musculus pterygoidaeus dorsalis that in most Coraciiformes has its insertion on the maxillo-palatine. Such an attachment requires a strong maxillo-palatine and a strong contraction of the M. pterygoidaeus dorsalis may impose a severe stress on the maxillo-palatine. The presence of the mediopalatine in Merops may be an adaptative response to the particular feeding habits of this bird. The Meropidae catch their prey in flight, but, as they feed on comparatively large preys they do not swallow them immediatelely; after the catch, they perch on some branch and kill the prey by battering it on the branch with strong lateral movements of the head. Therefore, significant forces would act across the bill

11 258 A. BRUSAFERRO, A. M. SIMONETTA MA PL Fig. 9 - The indirect desmognatism in the Merops adult skull. MA, maxillary; MP, maxillopalatine; PL, palatine; SN, solum nasi; V, vomer. Bar, 1 mm. axis and they include upward forces and lateral ones. Simple upward forces meet a resistance from the welldeveloped maxillo-palatines, but these will not necessarily require fusion. The technique of beating the prey against the perch may well, instead, have been an important selective factor: the lateral forces involved are necessarily large and they may well require a solid bridge across the middle part of the beak (Burton, 1984). Burton' claim (1984) is corroborated by the fact that the subadult skull of Merops shows a delayed development of the entire nasal region, while the cartilages of the braincase display a good state of pericordal and endocordal ossification. 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