Skeletons and bones are the most durable specimens in avian collections. They are nearly maintenance-free in comparison with skins, spirit specimens, or tissues. They are data-rich and, to some, aesthetically striking—yet avian osteological specimens have always been a minor constituent of museum bird collections. Systematic ornithology of the previous centuries focused on plumage and external morphology, and birds collected in the field were perforce transformed into the compact, round skin specimen that forms the bulk of the world's museum collections. These traditional skin specimens were considered of paramount importance and, to the collectors and curators, represented “value—money value and scientific value” (Coues 1874).

The traditional preparation of skin specimens leaves only the cranium and the distal elements in the wings and feet, and early collectors usually discarded the remaining bones and the torso. Sometimes, however, partial osteological specimens comprising the axial skeleton, femur, and humerus or other combinations were prepared from the torso as an ancillary step in the scientific collection process, usually only if there were time available after the higher-priority skins were prepared. Often, single elements were preferred, and some collections specialized in synoptic collections of crania or sterna. Olson (2003) points out that because sterna were easy to obtain from skinned torsos, they were often the element of choice in anatomical collections, even in cabinets of curiosity (Fig. 1). The great French encyclopedist l'Herminier constructed a classification of birds based solely on sterna (l'Herminier 1827), and Coues and other 19th-century ornithologists distinguished several taxa (e.g. Pelecaniformes, Alcidae) on the presence or absence of a perforate nasal (Coues 1872).

Although exceptions exist, avian skeletons of the past were most often prepared as mounted displays and thus, as is often the case even today, data were secondary to the aesthetics of presentation. Consequently, osteological specimens collected before the mid-20th century are often incomplete or data-poor, or comprise mixed proveniences—particularly those used as reference collections for bone identification. Olson (2003) provides a succinct history of avian osteological collections and should be consulted for a more complete background on their development and the nature of early specimens. Here, we explore some possible reasons for the relative unpopularity of avian osteological specimens, examine the value and use of bony specimens in modern ornithological research, and suggest possible directions and solutions for the future.

Current Status of Avian Osteological Collections

Avian osteological specimens come in several different forms, from complete skeletons with all major bones to single isolated elements (Table 1). Complete skeletons are the foundation of most modern osteological research collections: in these, every major bone of the bird is preserved, including left and right elements. The disadvantage of these skeletal specimens is that their preparation precludes nearly any other type of specimen, with the exception of tissue specimens, because the skin and internal anatomy of the collected bird are usually destroyed in the process. Partial skeletons have elements missing; the most common partial skeleton prepared in modern treatments leaves only a left or right set of distal elements (e.g. ulna, radius, carpometacarpus, hallux) in the skin, the distal end of the maxilla, and other bones necessary for a durable skin specimen (Winker 2000). Partial skeletons encompass a broad range of included elements (sometimes only the torso elements, sometimes articulated sterna and clavicles, etc.). Mounted skeletons are nearly always complete (but not entire; see below) and usually were intended for display, but some of the earliest research specimens were mounted with the elements articulated for movement. Mounted specimens are difficult to use for research, because many of the characterrich locations on bones near their articulating surfaces are often obscured by wires or holes, and early preparators would often use bones from several specimens to “part out” missing or pathological elements.

Lots, or bulk collections of bones, are most commonly associated with subfossil or archeological settings. The Museum of Comparative Zoology (Harvard University) and the U.S. National Museum (Smithsonian Institution), for example, have numerous large boxes of many thousands of Great Auk (Alca impennis) bones gathered from slaughter sites on Grand Funk Island, Canada. While nearly every major bone is represented, very few of these specimens are associated; that is, there is no way to determine which bones came from the same bird. Single elements are most commonly associated with fossil specimens or specialized reference collections for comparative studies. As mentioned above, early avian anatomists focused on sterna or crania, for example, to the exclusion of other bones.

Each of these forms of osteological specimens can be characterized by four primary features: whether they are entire, associated, articulated, or vouchered. Entire specimens have every bone preserved from the collected bird. Although most complete specimens are entire, there are many which, as a consequence of collection or preparation mishaps, lack a few very small or delicate bones, such as the hyoid, the cranial xiphoid of pelecaniform birds, the alula, and so on. Entire specimens offer the greatest research value, but are rarest in the early specimens. An associated skeleton originates from a single bird, and nearly every complete or partial specimen with data is associated; mounts may or may not be; and lots and single elements, by definition, are never associated. Articulated elements are what make a prepared mount, but elements can also be articulated by dried ligaments and skins, as in some early complete and partial specimens or in semi-prepared skeletons.

By far the most problematic issue with osteological specimens is vouchering. A vouchered specimen was identified by reference to the actual bird when it was collected or prepared. Partial skeletons often lack easily diagnosable elements, and mistakes in identification or other lapses during preparation can lead to errors very difficult to detect later (see below).

Survey of Major Collections

Overall, skeletal specimens constitute ≈7% of the total specimens held in 10 of the largest ornithological collections (Table 2). There are some notable variations from this general pattern, attributable to the particular history of a museum collection. For example, the number of osteological specimens at Florida State Museum exceeds the number of skin specimens by ≈30%, whereas those at the British Museum represent only ≈1% of the total collections. The Florida collections were, in large part, formed by Pierce Brodkorb, a leading avian paleontologist of the 20th century. The British Museum's collection started out as, and remains, the premier collection of bird skins; skeletons never had a chance there. Similarly, osteological collections represent a large part of the University of Kansas collections, because of the long history of skeletal preparations begun by Charles Bunker in the first decade of the 20th century (Hall 1951, Johnston 1995).

The number of osteological specimens in a collection does not necessarily correlate with the depth of taxonomic coverage. The U.S. National Museum has by far the greatest diversity of specimens, with 5,109 species represented (Table 3), more than half the known species of birds. The Field Museum of Natural History and the Royal Ontario Museum rank at the top of the list for mean number of specimens per species, an index that relates to the collecting effort for series of specimens rather than single examples. The British Museum collection, while ranking about seventh in number of species, has only ≈5 specimens per series. These data reflect several interacting factors. First, the top-ranked institutions have dynamic collecting programs that continue to preserve osteological specimens. By contrast, osteological collections begun in the late 19th and early 20th centuries were usually intended for the study of comparative function and morphology. The modern emphasis on the study of geographic and population variation demands more specimens than the comparative approach. Second, space is always a factor, and some collections are unable to expand beyond their current size. But expansion is needed—more specimens are needed in avian museum collections.

More specimens are needed because many species of birds are still unrepresented by even a single skeletal specimen. For example, 30% of tinamou species have no osteological specimens, and 67% of the genera have unrepresented species (Table 4). In more speciose orders, the pattern is similarly bad. In Apodiformes, for example, 33% of species have no specimens, 46% of genera have species with no skeletal specimens, and 74% of species have ≤10 specimens. For Caprimulgiformes, 40% of species have no specimens, 50% of genera have species without any specimens, and overall, 84% of species have ≤10 specimens.

Clearly, osteological specimens are under-represented in the top museum collections, but the global situation is likely much worse than this. Osteological specimens have migrated from smaller museums and natural history cabinets into the collections of major museums, thus skewing the skeleton:skin ratio higher in those few institutions. The frequency of skeletal collections among all scientific collections may be much lower than 8%. For example, several recent estimates of the total number of bird specimens existing in world collections range from 8 to 10 million (Banks et al. 1973, Goodman and Lanyon 1994, Mearns and Mearns 1998), whereas the total number of skeletons and other osteological specimens probably does not exceed 500,000 (Wood et al. 1982, Wood and Schnell 1986, Mearns and Mearns 1998). In other words, <5% of the world's ornithological collections are represented by osteological material of any kind— single elements to entire complete skeletons.

Shortcomings and Benefits of Osteological Material

There may be many reasons for the discrepancy in specimen preferences, but one aspect unrelated to scientific use of osteological material is the relatively high labor cost and delay associated with preparation. Skilled preparators can make skin specimens very quickly in the field; thus, for example, Elliott Coues and Henry Henshaw, in the 1880s, competed for the quickest preparation on a friendly wager. The winner (Henshaw) completed a study skin of a recently collected House Sparrow in one minute and thirty-five seconds; Coues took five seconds longer (Cutright and Brodhead 1981). Under normal conditions, Coues felt that four specimens an hour was an acceptable rate (Coues 1874); with today's more rigorous requirements, one specimen an hour is fairly typical (Winker 2000). By contrast, the fastest completion of an entire skeleton by D.C. took three-and-a-half days, including about three hours of dedicated technician time in preparation; the rest of the time was taken by beetles cleaning the bones of extraneous tissue. This additional burden of time and personnel costs dissuades most collectors and museums from casually adding osteological material to the collection mix.

The bottlenecks in osteological preparation are bone-cleaning and element-numbering. Most skeletal preparators now use dermestid beetles (Dermestes maculatus) to remove flesh and connective material from the skeleton, a technique first developed at the University of Kansas by Charles Bunker at the turn of the last century (Matthiesen 1989, Johnston 1995). A few specialized applications may require bacterial maceration, chemical treatment, or boiling for cleaning bones; but these techniques are rarely employed, because of undesirable effects on the bones. The consensus is that bone-cleaning with dermestid beetles (or other carnivorous invertebrates, like marine crustaceans) is more efficient (Matthiesen 1989, Winker 2000), but the process is generally held to be noisome and undesirable (Weed 2003).

After the bones are cleaned, the skeleton is usually disarticulated and then soaked in various solutions, depending on its condition—a weak ammonia solution to reduce odor, for example. Most importantly, each element is annotated with the specimen acquisition or register number. An experienced preparator can number (nearly) every element of a robin-sized bird in about an hour; smaller birds and larger birds can take longer, because of small bone size or additional preparation time associated with greasier bones. Numbering of elements is a critical step in the process, because if it is not done there is a great danger of mixing or losing elements in use. Given the more numerous steps in skeletal preparation as compared with skin preparation, there are many opportunities to lose elements, to exchange bones with other specimens of the same species, or to intermix different species under preparation at the same time. Despite this, and because of the high demands on personnel in numbering, many osteological specimens in the world's museums are unnumbered or only partially numbered (perhaps as high as 25% overall; D. Causey pers. obs.).

Nonetheless, osteological material has many positive aspects. In contrast to study skins, which offer few standard morphological measurements and are subject to wear, avian skeletons make possible many more quantitative measurements with a high degree of replication (see Olson 2003 for more details). Osteological specimens are low-maintenance, have high durability, and are much less susceptible to variations in storage regime, insect damage, or post-preparation degradation than other specimen types (Matthiesen 1989, Winker 2000, Olson 2003).

New Directions in Curation

Of the two main impediments in preparation of osteological specimens, element-numbering seems the most tractable for improvement. Several new technological developments offer promising alternatives to numbering each element by hand with pen and ink. Precision laser engraving can be quite quick, about 1 s per element, using numbers, letters, symbols, even barcodes (Fig. 2). One great limitation is that the engraving physically alters the surface of the bone by removing material through carbonization, which may be objectionable for many types of research application.

Precision microfibers (or microtaggants) as small as 5 μm in diameter carrying up to 10⁷ different codes can be applied to the external surface of bony elements through a spray adhesive. The advantage is that an entire skeleton can be marked in a single spray; the grave disadvantage is that the microfibers must be read using a microscope and decoded. Loss of the codebook would make this type of system unintelligible— a shortcoming shared with barcoding and other symbolic marking.

Microprecision inkjet printers offer a close replicate of manual numbering, and as the resolution increases (in 2005, 1,200 dpi [dots per inch]), and with computerized control for printing on curved surfaces like bone shafts, become increasingly more useful for rapid numbering of elements.

All these technological alternatives to manual numbering, and others, have the potential to speed the preparation process of osteological material, but all suffer the same problem of high cost. Even a relatively cheap precision inkjet printer ($40,000 in 2005) is likely beyond the budgets of most museums, so technological solutions may have to await the creation of a centralized, entrepreneurial specimen-processing facility, similar to what has evolved in molecular biology for oligonucleotide synthesis and DNA sequencing. Many institutions now outsource that work, which used to be done in individual laboratories, to central facilities or for-profit enterprises.

Future Research in Osteological Collections

Osteological collections continue as a resource for current avian research (Fig. 3). Traditional uses are focused on the bony morphology, and examples of recent published research include comparative anatomy and morphology (Ponton et al. 2004, de Margerie et al. 2005), paleobiology (Holdaway et al. 2003, Causey et al. 2005), paleontology (Bourdon et al. 2005, Clarke et al. 2005), avian systematics (Mayr 2003, Zhou and Zhang 2003), and zooarcheology (Plug et al. 2003, Fiori et al. 2004).

Recently, avian osteological material has served as a resource for research far removed from the purposes originally assigned to bony material. For example, modern materialanalysis of avian bones, tendons, and other connective tissues has greatly facilitated medical and veterinary treatments, as well as provided new insights into vertebrate evolution (Naldo et al. 2000, Summers and Koob 2002, Tully 2002). Bone has proved to be an excellent source of DNA, and subfossil bone has been used to enable molecular study of extinct populations and species of birds (Terbutt and Simons 2002). It should be pointed out that studies focused on the ancient DNA contained in bone often use specimens collected before DNA was known to science (i.e. 1860). Osteological specimens collected today are just as likely to serve as a resource for presently unknown scientific technologies 150 years in the future.