S02.1: Modelling the avian cervical vertebral system: Structure, function, and phylogeny

Northwest Center for Medical Education and Department of Anatomy, Indiana University School of Medicine, Gary, IN 4608, USA, Fax 219 980-6566 e-mail jvanden@meded.iun.indiana.edu

The cervical and cervicothoracic elements of the avian vertebral column form a series of musculoskeletal units that can serve as a model system for a study of form, shape, change in morphological shape, all of which may be integrated into studies in functional morphology. Patterns of structural and functional variation in these units, such as patterns of intratendinous ossification, and their significance, can be analysed by using (1) techniques of formal descriptive morphology at all levels (i.e., developmental, cellular/subcellular, histological, gross anatomical); (2) light and radiographic imaging studies, and (3) computer simulation of movement patterns. These analyses, in turn, can then be used to answer questions arising from the study of various biological mechanisms, such as pecking, and drinking, and their accompanying behavioural patterns. The cervical portion of the avian vertebral musculoskeletal system may then offer potentially new insights for interdisciplinary studies that integrate data with that derived from various fields of ornithological investigation to answer current questions not only in dynamic morphology, but also in neurobiology, ecomorphology, palaeontology, phylogeny, and systematics, and perhaps clinical anatomical features in avian veterinary medicine.

According to Burton (1984), ‘... despite the wide range of feeding apparatus modifications shown by the head of coraciiform and piciform birds, the cervical column is relatively uniform in major features...’, although Kuroda (1962) had commented that the cervical system in birds ‘... differs greatly in length and in use... [as a] substitute for hands in feeding, preening, fighting [social interactions?], etc. ...’. For at least the past 150 years, various investigators have studied elements of the cervical vertebral system with respect to their biochemical composition, in terms of principles in molecular biology, development, anatomical structure (gross anatomy as well as histology), functional roles, and functional morphology, and, to some extent, also to their value as character-states for studies in avian evolutionary biology, avian evolution, and avian systematics.

Somitogenesis may be defined as the ontogeny and differentiation of paired developmental units known as somites, from the paraxial mesoderm. Tam & Trainor (1994: 275) have characterized this as ‘... a fundamental process of vertebrate embryogenesis, ... [a] constriction of serially repeated [morphological?] modules in head and trunk ... [resulting in the]... formation of reiterating and distinct blocks [of segmental or metameric units] of tissues along the rostral [or cranio-]-caudal body axis, ... a pre-pattern of segmentation that defines the physical boundary and bilateral symmetry of the mesodermal segments in the body axis....’. This segmental patterning within the body wall is later transferred to skeletal elements, muscles, spinal nerves, and blood vessels as the structural elements of the vertebral column.

One of the classic studies on the ontogeny and evolution of the avian vertebral column is that of Piiper (1928), who based his study on species of the genera Larus and Struthio. This study, however, has been difficult to interpret, according to some later investigators, because Piiper (1928) based his model on the classic theory of resegmentation of the somites [Neugliederung], which was first developed by Remak (1855) , then extended by von Ebner (1888), and others. The original Remak theory has been debated for the past 150 years, and was most recently reviewed by Verbout (1976).

There are essentially two fundamental interpretations of the underlying developmental mechanism for the formation of a vertebra. One of these is the hypothesis of the classic resegmentation of a single somite into two unit structures, which are known as sclerotomes. Each sclerotome is then reunited with that from an adjacent somite, and this new unit structure becomes the definitive vertebra. The other hypothesis postulates a temporal, developmental realignment of the position of the sclerotome units, relative to those of the developing muscle units, which are known as myotomes. In either hypothesis, the functional unit for movement will consist of two adjacent vertebrae, the intervertebral disc between them, ligaments and muscles attaching to the vertebrae, and an associated neurovascular bundle. Each vertebra, then, participates in two adjacent motion segments.

Among the significant molecular biology techniques applied to the problem of somitogenesis are those of Kieny et al. (1972) and Kieny & Chevallier (1979), who introduced the quail-chick chimera preparation.. In this experimental preparation, the nucleus of a chick cell, as host, is replaced by that of the same-stage cell nucleus from a Coturnix quail, acting as donor. In other experimental procedures, homotopic as well as heterotopic, stage-matched single somite transplantations have also been successfully carried out. The quail cell nucleus in both techniques serves then as a permanent cell marker [nuclear domain] to permit later identification of descendent cell lineages, including those of the (1) paraxial mesoderm, (2) cartilaginous vertebrae, (3) musculature, (4) general connective tissue of the vertebral column, (5) dermis, and (6) spinal cord meninges from heterospecific, single - somite transplants. Noden (1983a, b, 1991) adopted still other techniques to study the embryonic origins of avian cephalic and cervical muscles and their associated connective tissues, the role of the neural crest in patterning of avian cranial skeletal, connective , and muscle tissues, and the relationships between ontogenetic processes and morphological outcome in the avian head and neck., the latter specifically in terms of general vertebrate craniofacial development. The above studies are well summarised by Christ & Ordahl (1995) and Huang et al. (1996, 1997).

Even before the onset of somitogenesis, there appear developmental units which are known as somitomeres. These structural units are spherical cluster of mesenchymal cells, with an attendant expression of genetic factors, in presomitic mesoderm. These somitomeres occur in all vertebrates and presage the segmentation of the paraxial mesoderm into somites (Tam & Trainor, 1994). An important organisational principle in this developmental process is the expression of the Homeobox (Hox) genes, a highly conserved sequence of nucleotides within the DNA, and which encode proteins that regulate the expression of other genes. These Hox genes are correlated with a strictly regulated spatiotemporal pattern of development along the vertebral column.

In addition to these genetic factors, there are at least two axial planes or ‘orthogonal polarities of cell differentiation’ endowed in each mesodermal segment: a rostro-caudal axis which is established prior to segmentation of the axial mesoderm into somites, and (2) a dorso-ventral axis or polarity which appears after the segmentation. At least six different ‘compartments’ can be demonstrated as a result of these axial polarities:

Compartment 1: A dorsal half or dermomyotome, which in turn differentiates into (1) dermatome, from which will differentiate integumentary features as well as myoblasts, and (2) the myotome, from which arises all skeletal muscle postcranially

Compartment 2: A ventral half, or sclerotome, which unites with the corresponding ventral half of the somite opposite it, to form an unpaired mesenchyme along the rostro-caudal axis. From this mesenchyme will develop the intervertebral disc, specifically from the somitocoele cells of a single somite (as mentioned earlier). The body and arch of a vertebra also arises from this mesenchyme, but in this case, perhaps from sclerotomal cells of adjoining pairs of somites rather than from only a single pair (compare the studies of Bagnall et al. 1988, and Huang et al. 1996, 1997).

Compartment 3: the cranial half of a single sclerotome which remains more loosely structured and which interacts/organises/provides framework for a highly vascularized perineural connective tissue for the migration of neural elements [neural crest cells; motor axons] and ontogeny of segmental vessels.

Compartment 4: A caudal [actually caudolateral] half of the same sclerotome is densely packed with cells, and it gives rise to osteological elements, such as the vertebral arch, the pedicle, and at least some a part of the costal process (the future rib). The pedicle itself unites with the extreme cranialmost portion of the vertebral body (see Schinz & Zangerl 1937).

Compartment 5 and Compartment 6 are both associated with the ontogeny of the muscles (specifically, the contractile muscle fibers) from the dermomytome. The lateral half (Compartment 5) becomes the domain of the hypaxial muscles, and the medial half (Compartment 6) becomes the domain of the epaxial muscles.

In this section, we have seen how an old question from developmental morphology, namely somitogenesis and the transformation of the somites, has been answered at least in part from the avian model using contemporary innovative techniques and technology. As Huang et al. (1996: 238) have clearly demonstrated, the somite is, indeed, the source of the vertebrae, the muscles positioned between them and attaching to them, and the elements of the intervertebral joints, and therefore ‘... the somite ... represents the ancestor of the vertebral motion segment ...’. However, ontogeny represents but one element of an analysis of the patterns of structural variation, or phenotypic plasticity, in the musculoskeletal morphology of the cervical column. We will next consider structural variation and functional morphology in the fully developed cervical vertebral column.

Analysis of structural variation in the adult avian cervical system has had a long history in avian morphology. One of the principal studies is that of Boas (1929), but several others can also be mentioned (Joeger 1858; Donitz 1873; Forbes 1882; Virchow , in a series of papers from 1914- 1931; von Sivers 1934; Böker 1937; Palmgren 1949; Watanabe 1961; Kuroda 1962; Zusi 1962; Baumel 1964; Zusi & Storer 1969; Komarek 1970; Jenni 1981, and Johnson 1984). As indicated earlier, I joined the Leiden group in studies of the functional morphology of the avian cervical system within a broader program of the functional morphology of avian trophic and drinking mechanisms; I will refer to several of these studies in the remaining portion of this section.

Attempts to understand the relationships of the structural elements in terms of their functional morphology have been the basis of ‘old’ questions for which answers have been sought for many years with varying success. Boas (1929) illustrated the functional head/bill-neck system of birds as analogous to the actions of a person who serves as a ‘rag-picker’ (Lumpensammler). In this analogy, the head [craniocervical apparatus] serves as the pick or nail used by rag-pickers to secure the object, and the neck system is the shaft on which the nail is fixed. The analogy is continued in two different ‘functional’ forms. In one form, the straightened nail on the shaft is analogous to a head/bill-neck system that obtains a food item by a direct ‘stabbing’ action, for example, a ‘pecking mechanism with full visual control’. In a second form, the nail is hooklike and the head/bill-neck system, by analogy, might obtain a food item by a type of ‘probing mechanism with partial visual control (even a non-visual tactile control?)’ (see Zweers et al.1994, for further analysis).

Von Sivers (1934), on the other hand, described musculoskeletal variations in a model of a short-necked bird, such as the crow, and of a long-necked bird, such as a representative of the Anseriformes. He also described grebes, herons, and bitterns as ‘halsschnellende Formen’, which, in English, means ‘birds that move their neck quickly’, e.g., with the rapidity of a projectile towards a particular point. Boeker (1937), as well as Kral (1965), extended this concept to an analysis of the cervical movement patterns of the neck in ardeids and ciconiids, in particular, with additional comments as well as on other ‘darting’ or ‘quick-necked’ models (such as anhingas, sunbitterns, grebes, etc.). Boeker (1937), in fact, described the variations in the cervical ligaments of the neck of storks in the context of a ‘pecking’ trophic feeding mechanism, and suggested that this morphology is not permitted within the highly derived ‘fast-peck’ or ‘darting’ mechanism of herons and egrets. See also Bennett & McN. Alexander (1987) and Jiang et al. (1996) for recent discussions of this morphological patterning of spinal ligaments in birds.

Kral (1965) also presented an analysis of the differences in variation in cervical motion patterns of the neck between in ardeids and ciconiids in the form of a ‘workspace’ by analysing the possible cervical motion patterns of the neck. This analytical approach was developed further by Bout et al. (1992, 1997) who digitized morphological parameters that were derived from radiographic imaging studies and then utilised a computer-based program to simulate [test] craniocervical movement patterns during pecking and drinking in selected avian model systems. In an earlier study, v.d. Leeuw & Zweers (1992) characterised the change in motility patterns of the head-neck movements between young Mallard ducklings Anas platyrhynchous and adult birds with respect to the rotation forces and maximisation or minimisation of the rotation efficiency occurring in these movement patterns. Elshoud & Zweers (1987) have described the cervical system as a kinematically under-determined and mechanically open multi-bar system. In all three studies, the underlying morphology of these avian model systems had been earlier described so that there could be a necessary integration of morphology with current innovative techniques to provide additional characterisations of the pecking and drinking mechanisms in birds.

Structural and functional aspects of the cervical system, based on the positioning of the head and on head movements, in addition to the movements of the head/bill, and /hyolingual apparatus movements, are clearly involved in generating behavioural patterns. In his study of the feeding ecology of wading birds, Kushlan (1978) has described in very clear fashion thirty-eight feeding behaviours presently distinguished in wading birds. In his descriptions, he clearly distinguishes several foraging behavioural repertoires, which include various elements of the craniocervical + axial /truncal postures, such as (1) ‘peering over’, in which the cranial axis is positioned [ pointing down ] relative to the cervical axis; (2) ‘head tilting’, in which both the cranial and cervical axes are oriented in the same direction; (3) ‘head cocking’, in which only the head is positioned; and (4) ‘facing down’, in which both the head and bill are pointed downward and submerged in the water during feeding. He discussed each of these behavioural element in their possible ecological significance, correlated with variables of the habitat and prey variables. In addition, he recognizes different trophic mechanisms for different groups of birds, such as (1) the ‘visual foraging + pecking’ trophic mechanism in herons; (2) the ‘visual foraging + pecking’ (perhaps tactile - foraging?) trophic mechanism in adjutant storks; (3) the presumably derived ‘non-visual tactile foraging + probing’ trophic mechanism in the mycterine storks; and (4) the the fully developed ‘non-visual tactile foraging + probing’ trophic mechanism in ibises and spoonbills. A detailed descriptive craniocervical morphology of these avian groups is a necessary first-step to test this hypothesis of functional morphology.

More recently, Heidweiller et al. (1989,1992a-e; see also Weisgram & Zweers 1987) have noted the important basic biological observations that (1) head motion occurs in almost all animal behaviours; (2) the cervical column is indispensable for any behavioural pattern, in which head motion is involved, but that (3) this coupling of the head and neck in any effective avian head motion has received only scattered attention from scientists. They correctly state that the formal description of the [cervical] muscle-bone apparatus does not serve for functional explanation of that apparatus, but rather for gathering anatomical evidence that [cervical] elements may serve as ‘---proper integration of structural and kinematic modifications in the developing cervical column [as a] prerequisite to insure adequate pecking, drinking, preening, and locomotion ---’. They addressed several additional parameters in their studies, such (1) what changes occur in muscles, bones, and tendons of cervical column during post-hatching development, and (2) whether such changes in dimensions can be understood from a mechanical point of view by means of current theories of scaling.

These, and other questions, may have both a descriptive as well as functional morphological basis, and the development of highly similar morphology, for different behavioural patterns, for the same biological role, may have a specific causal basis which is as yet unknown.

Morphological character-states are an important element in the data base for avian phylogenetic systematics [cladistics], a significant methodology today in studies of avian evolution and avian ancestry. Livezey (1997: 399), in fact, in his recent phylogenetic analysis of basal anseriforms, the fossil Presbyornis, and interordinal relationships of waterfowl [essentially, a confirmation of galloanserimorph phylogeny and systematics] states that ‘... phylogenetic [cladistic] analysis of morphological and molecular data remains the only rigorous and philosophically grounded tool available for the reconstruction of higher-order relationships of birds. Phylogenetic techniques apply to fossils as well as modern taxa, and successful applications do not hinge on fossil ‘mosaics’ and can provide empirically detailed, testable alternatives to intuitive evolutionary scenarios ....’.

A data base consisting of more than 90 avian morphological character-states has been derived from the significant advances in recovery of the avian palaeontological record (see Sanz & Bonaparte 1992; Chiappe & Calvo 1994; Sanz et al..1995; Chiappe 1996; Chiappe, Norell, & Clark 1996; Sanz et al.1997 for details). As a result of unavoidable limitations in the available morphological data base, unknown patterns of structural variation, and essentially very little information on functional morphology, these 90 avian morphological character-states have not yet been fully integrated with data derived from other studies. However, some of these character-states for the head and neck system do seem applicable to current studies of trophic mechanisms in living birds, while others seem to be only incompletely described. One of these ‘unanswered’ questions will be reviewed in this final section.

In an earlier section, I discussed a possible integration of data from morphology with that from behavioural biology, derived in the context of an analysis of avian trophic mechanisms. In a recent publication, we (see Vanden Berge and Storer 1995) had published a general review of intratendinous ossification patterns in birds, in which an ‘old’ picture that Boas had included in his 1929 paper was reproduced. This was an illustration of the long tendons of insertion of the longus colli dorsalis muscle in the neck system, which have an intratendinous ossification pattern, in the Paradise or Stanley's Crane, Anthropoides paradisea. Since that publication, and in part from an ongoing interest in cervical patterns in birds, we have initiated a new study of the intratendinous ossification pattern in the cervical system of the Western Grebe, Aecmophilus occidentalis. The initial data base consists of special museum preparations of the osteology of the cervical column which are part of the collection in the Bird Division at the Museum of Zoology of the University of Michigan. Preserved specimens for the study of the musculature are also available and will also be described. The pattern of intratendinous ossification in this cervical system may also be characteristic of several other avian taxa (see Boas 1929; Rydzewski 1935; Owre 1967), although this has not been adequately documented yet in the literature. Not only has the morphological pattern not been fully described as yet, but a functional component for this morphological pattern is equally also unknown.

Komarek (1970, Table 27, Figs. 3 and 4) illustrated the costal process on a cervical vertebra as if it were retained as an element of the cervical osteology although the term costal process is more frequently considered as a developmental term for a sclerotomal derivative that initiates the formation of an independent cervical rib element. The articular head of the cervical rib is then united [ankylosed] with the body of the a vertebra, and the additional structure known as the tuberculum of a cervical rib unites with the transverse process which is derived as a feature from the vertebral arch of the vertebra. Boas (1929), in one of his illustrations (Table 6, Fig. 18, in Rhea), identified a non-ankylosed rib element that clearly formed the ventral floor of a bony canal which transmits the ascending vertebral artery and its accompanying veins, as well as a neural network. The lateral wall of this canal is identified as the transverse process of a vertebra, and the dorsal wall is the base of the cranial articular process, or cranial zygapophysis, thus, both walls are features derived from the vertebral arch. The medial wall of the canal is the lateral face of the vertebral body. The bony ringlike structure which encloses the canal is, in fact, termed Ansa costotransversaria (see Boas 1929, Table 3, Fig. 13, Alca: lateral ‘arm’ = costal tubercle; medial ‘arm’= ‘neck’ of the rib). The caudal ‘entrance’ (Boas 1929: Eingang zum Vertebrarterienkanal) is equivalent to a structure that is known as the transverse foramen, although that term is commonly associated with the entire passage (Boas 1929: Wirbelarterienkanal), with or without length.The first cervical vertebra or atlas ordinarily lacks the foramen; however, the foramen does occur in the atlas of alcids and anseriforms (Boas 1929).

The canal itself may be of varying length over a given vertebra, usually with additional length through formation of two bony shelves or laminae. One of these, the Lamina arcocostalis, extends from the arch of the vertebra to the costal process/rib; the other, the Lamina corporocostalis, extends from the body of the vertebra to the costal process/rib. Although a rib element on a typical cervical vertebra is not readily identified, even in development, the presence of a costal process is still assumed as a structural feature in studies of the cervical column in a variety of bird, as is the ‘free’ caudal end of the rib which has the form of an attentuated style or ‘spine’ of variable length. These new terms for the bony laminae were first proposed as a structural form-feature in Anas by discussions of the present author with Landolt & Zweers (1985), subsequently adopted in a similar a study of Gallus (Zweers, Vanden Berge, & Koppendraier 1987), and then formally adopted by the International Committee for Avian Anatomical Nomenclature in the newest revision of the standardized avian anatomical nomenclature (see Baumel et al. 1992, Handbook of Avian Anatomy: Nomina Anatomica Avium, Second Edition.).

As mentioned by Boas (1929), the head of the incorporated rib is also set off from another bony feature on the body of the vertebra, namely the carotid process, which is associated with another vascular canal in which the carotid artery ascends. A smooth sulcus or groove is also present and is associated with the musculotendinous complex of the M. longus colli ventralis. A line projected dorsoventrally across the caudal end of the ventralmost crest of the Ansa costotransversaria separates the ‘head’ from the ‘spine’ of the rib. Attaching to this skeletal element structure are elements of the lateral cervical musculature as well as the terminal tendons of the M. longus colli ventralis. Ascending in the space below [ventral to] the rib is a neurovascular bundle leading to that particular unit of the cervical system. These structural relationships are particularly evident on the middle series of the cervical vertebrae. In the above descriptive statements, the costal process [rib] is considered to be more than a developmental element in the avian system, i.e., that it has some additional (but essentially unknown) role other than to organise mesenchymal tissue to differentiate as a cervical rib which then ‘disappears’ as an element in the cervical column.

If we now consider the structural pattern of the cervical musculature, then we notice a topographic arrangement of 3 three principal [topographic] [positional] subsystems of cervical musculature - namely dorsal [extensor], ventral [flexor], and lateral - which seem to correspond to the principal elements in osteology. This musculoskeletal pattern is assumed to be linked to functional musculoskeletal units that generate movement patterns in the cervical system associated with basic biological functions such as trophic pecking and drinking.

In particular, the attachments of the lateral cervical muscle system, namely, the Mm. intertransversarii and Mm. inclusi, although very difficult to describe anatomically, seem to have a primary relationship (1) to the vertebral arch, dorsally; (2) to the costal process, laterally; and (3) to the body of the vertebra, ventrally.These muscles are attached dorsally to a flattened aponeurosis (‘Aponeurosis. transversa’, see Landolt and & Zweers 1985), which divides the dorsal and lateral cervical musculature along a horizontal plane, often marked by a linear crest running from the transverse process to the caudal zygapophysis of a vertebra. Ventrally, some of the medial muscle fibers also attach on to the head and spine of the costal process that is adjacent to the attachments of the M. longus colli ventralis. The probable common ‘fixed’ attachment of this subset of muscle would seem to be the array of aponeuroses which attach to the various small crests and tubercles on the series of transverse processes, or ansae, between the most dorsal tubercle (Tuberculum dorsale), and the ventralmost crest opposite the head of the ankylosed rib on each side of a cervical vertebra.

The developmental relationships and detailed anatomy of these musculoskeletal structural features, and the vertebral artery and neural network which lies within the bony canal, is not yet fully described in many birds, including the Western Grebe, but there is at least some evidence that the laminae just described may be derived from ossified aponeuroses (see Rydzewski 1935; Owre 1967, and Storer 1982.) The hypothesis of a functional role for this set of musculoskeletal elements, integrating kinematic forces over the vertebral arch, body of the vertebra, and the costal process/rib, in the avian cervical vertebral system, has not yet been tested. If that hypothesis is accepted, then the bony laminae should be recognised as definitive elements in cervical osteology, especially if they are derived in part also as an ossification of the aponeuroses of the muscle system.

The concept of a set of musculoskeletal elements uniting the vertebral arch with the costal process, and the costal process with the vertebral body of the vertebra, in the avian cervical vertebral system, may have an as yet unknown important bearing on our understanding of the kinematics within the cervical system of birds since it suggests that there may be kinematic forces which must be integrated over all three elements of a given vertebra. If that hypothesis is accepted, then the bony laminae should be recognised as a definitive actual structures, especially if they were derived in part also from an ossification of the aponeuroses of the muscle system. Furthermore, the lateral cervical muscle system may then serve as a ‘functional link’ between the dorsal functional extensor/ dorsiflexor muscle system and the vertebral arch of the vertebra, on the one hand, and the functional ventral cervical muscle system and body of the vertebra. on the other hand.

As a further observation related to this musculoskeletal morphology, there are two studies that describe elements of the trophic mechanism in grebes, although both deal primarily with the head system. Fjeldsa (1981) analysed some morphological aspects of the jaw mechanism among grebes as a part of his analysis of comparative ecology of Peruvian grebes in a study in mechanisms for evolution of ecological isolation. In a much earlier study, and one in which the principal emphasis was not directed toward feeding mechanisms, as such,, Lawrence (1956) suggested that the Western Grebe has an annual shift in foraging strategy from feeding primarily on invertebrates in the spring to adopting a highly piscivorous diet during the breeding season, extending into the postbreeding season. He also suggested that the Western Grebe has a trophic spearing mechanism although he did not describe the anatomy or the functional morphology of the mechanism.

If a spearing mechanism were fully developed in the Western Grebe, then at least one hypothesis may be formulated: the head and neck can be extended in a linear manner as a single functional unit in a similar manner as the throwing of a javelin. If so, then the following questions might be asked: (1) What is the morphology of a spearing mechanism in this bird? (2) What functional roles (s) might be served by the extensive pattern of intratendinous ossification at the anatomical base of the neck, which is part of the craniocervical delivery system of this trophic mechanism in the Western Grebe? (3) Can a mechanical model be developed that explains the morphological system in grebes and which can itself be tested? (4) Is the system unique to the Western Grebe or is a similar system present in other birds that are said to have a spearing trophic mechanism? See Zweers et al. (1994) for further discussion.

One additional question that might be asked for all of the studies reviewed above is a more general one: What additional information may this have in terms of avian phylogenetic systematics? In particular, I would call attention to a morphological feature of the cervical vertebrae, which was described as a ‘vertebral strut’ in Vanellus and other vanelline plovers, in Burhinus (Zusi and Jehl 1970) and was fully accepted as a systematics feature by other investigators (Strauch 1978). There is most certainly a very strong suggestion that this ‘strut’ is indeed a form of an arcocostal lamina which was described above. This structural feature is similar to an ossified aponeurosis which we have seen in grebes. However, this skeletal feature may actually be a character-state whose developmental and/or complete morphology is not yet fully known, and a functional morphological role is only surmised. Furthermore, as a skeletal feature, it may not have been fully realised in current phylogenetic analyses. Feduccia (1996) has postulated a Burhinus-like charadriomorph as a ‘transitional’ shorebird that may have passed through the geological KT boundary, and, therefore, one might assume that this character-state may have a long phylogenetic history. Furthermore, structures similar to the arcocostal and corporocostal laminae are also known from maniraptoran theropods (see, e.g., Deinonychus, Ostrom 1969; see also Barsbold & Osmolska 1990). Many current investigators believe that birds are phylogenetically (cladistically) rooted among maniraptoran theropods (see also Zweers &Vanden Berge 1997, 1998).

A major theme in this symposium is the integration of morphology with data from other scientific disciplines in ornithology. Research projects continue in which the functional morphology of the head and neck systems is studied among selected, testable model systems including galliform, columbiform, and charadriiform systems, and continues with additional studies in progress on palaeognathiform, anseriform, and passeriform systems, in the functional morphology group in Leiden. These continuing studies include elements of (1) developmental morphology; (2) formal descriptive morphology; (3) electromyographic, cinematographic, and radiographic imaging studies; and (4) applications of computer- modelling to answer questions in functional morphology among birds. In conclusion, then, investigators with a specific interest in avian morphology should aim for an integration of morphological data from a wide variety of sources. If so, then their future studies will continue to make a significant contribution to further progress in both morphology as well as ornithology.

I wish to acknowledge my colleagues, Dominique Homberger and Gart Zweers, for their invitation to contribute to this symposium, for our active discussions for several years on the general subject of avian morphology, and for sharing in numerous publications in this subject area. My acknowledgements also extend to students (S. Gussekloo, A. V. D. Leeuw; and F. Nuijens) at Leiden University who have contributed their own data in functional avian morphology to the preparation of this review paper.

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