Cretaceous Research (1998) 19, 225±235
Article No. cr970102
Bone microstructure of the diving Hesperornis and the volant Ichthyornis from the Niobrara Chalk of western Kansas *A. Chinsamy, {L. D. Martin and {P. Dodson * University of Cape Town, Zoology Department, Rondebosch, 7700, and South African Museum, Post Of®ce Box 61, Cape Town, 8000, South Africa { Natural History Museum, Dyche Hall, University of Kansas, Lawrence, Kansas, 66045, USA { University of Pennsylvania, School of Veterinary Medicine, 3800 Spruce, Philadelphia, PA, 191044065, USA Revised manuscript accepted 27 November 1997
We report on the bone microstructure of the Cretaceous birds Hesperornis regalis and Ichthyornis victor. Thin sections of representative elements of both these ornithurine birds show a rapid, sustained bone deposition without any pauses or interruptions in bone formation. This growth pattern contrasts sharply with the cyclical pattern of bone deposition previously reported for the Cretaceous non-ornithurine birds Patagopteryx and representatives of the enantiornithines. These ®ndings suggest physiological advancement in Cretaceous ornithurine birds. The bone microstructure of the diving Hesperornis shows similarities to the bone structure of modern penguins, and to that of a loon from the Cretaceous of Antarctica. # 1998 Academic Press KEY WORDS: Cretaceous birds; Hesperornis; Ichthyornis; bone histology.
1. Introduction A wealth of new discoveries have signi®cantly advanced our understanding of the diversity and phylogenetic relationships of early birds (e.g., Zhou, 1992; Sereno & Rao, 1992; Perle et al., 1993; Chiappe, 1995). In addition, recent studies have provided insights into the biology (see Feduccia, 1996) and physiology of these early birds (e.g., Ruben, 1991; Chinsamy et al., 1994). However, few studies have been conducted on the bone microstructure of early birds. Until recently, only the bone histology of Hesperornis had been examined (Houde, 1986, 1987). More recently, two studies have examined the bone histology of Patagopteryx and representatives of the enantiornithines (Chinsamy et al., 1994, 1995), which currently represent the most primitive birds to be examined histologically. The presence of lines of arrested growth, which mark pauses in bone formation, indicates that these birds were incapable of sustained rapid growth. In this study we provide a comparative analysis of the bone histology of the ornithurine birds Hesperornis regalis, a hesperornithiform, and Ichthyornis victor, an ichthyornithiform (Figure 1). The hesperornithiforms and ichthyornithiforms are Cretaceous toothed birds, well known from many species (Feduccia, 1996). Although found in the same deposits, Hesperornis and Ichthyornis had drastically different lifestyles. Hesperornis was a highly specialised ¯ightless bird adapted for diving, while Ichthyornis shows de®nite skeletal adaptations for powerful ¯ight. As in extant diving birds, such as loons and grebes, Hesperornis used its laterally compressed feet for generating propulsive forces during swimming. Hesperornithiformes are generally considered to be a diverse group that had a world-wide 0195 ± 6671/98/020225 + 11 $30.00/0
# 1998 Academic Press
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Modern birds, such as Aptenodytes, Spheniscus, Columba, Gavia, Podiceps
Ichthyornis
ORNITHURAE
Hesperornis
Patagopteryx
Enantiornithes
AVES
Archaeopteryx
Figure 1. Cladogram depicting the phylogenetic relationships (see Chiappe, 1995) of the avian taxa cited in the text.
distribution during the Cretaceous (Feduccia, 1996). Most forms are recovered from marine sediments, although specimens are known from a Middle Campanian estuarine deposit in Alberta (Fox, 1974) and from freshwater deposits (Martin, 1983, 1991) of the Upper Cretaceous of South Dakota. The volant piscivore Ichthyornis, is widely distributed in marine deposits of North America. It has strong wing bones and a well-developed keel on the sternum, indicative of powerful ¯ight (Feduccia, 1996). It is generally accepted that Ichthyornis used its long jaws and recurved teeth for scooping ®sh from surface waters (as gulls and terns scoop ®sh from surface waters today). 2. Materials The Hesperornis and Ichthyornis specimens used in this study were recovered from the Niobrara Chalk (Late Cretaceous) of western Kansas. This material includes a humeral fragment (KUVP 2294, Kansas Museum of Natural History) of Ichthyornis, and two femoral fragments of Hesperornis (a midshaft fragment, KUVP 2289, and a distal fragment, KUVP 123108, both in the Kansas Museum of Natural History). The bone fragments used in this study were found associated with other skeletal material that permitted their taxonomic identi®cation (L. D. Martin, pers. obs.). For comparative purposes we also examined the femoral bone microstructure of a Cretaceous loon (TTU P 9265) from the Late Cretaceous, Lopez de Bartodano Formation of Seymour Island, Antarctica (Chatterjee, 1989), and of the extant Emperor and Humboldt penguins, Aptenodytes forsteri and Spheniscus demerus. The Emperor penguin was chosen as these birds have particularly stressful breeding patterns, which may be re¯ected in their bone histology. Other modern bird femora were also studied, including that of Columba livia, the pigeon,
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representing a volant bird, and that of two diving birds (which are also capable of ¯ight), the red throated loon (Gavia stellata) and the black necked grebe (Podiceps nigricollis). The bone samples were prepared for thin sectioning according to the methodology outlined in Chinsamy & Raath (1992). The thin sections were examined using polarised and transmitted light microscopy. Quantitative measurements were made using Sigma Scan image measurement software (Jandel Scienti®c Software). 3. Results 3.1. Hesperornis regalis In transverse section, the femur exhibited a thick compact bone wall and a rather small medullary cavity (Figure 2A). The maximum thickness of the compacta is 5.2 mm. This cannot be re¯ected as a percentage of the diameter because of post-mortem distortion. Accurate measurements of the medullary cavity were also not possible because of compaction. The margin of the medullary cavity is distinctly resorptive in nature. Volkman's canals are clearly present and extend radially from the medullary cavity into the compacta. A number of large erosion cavities are located just internal to the medullary cavity. Neither cancellous tissue, nor compacted coarse cancellous tissue is present. The compacta is richly vascularised and consists of a large number of primary osteons within the woven bone framework of the ®bro-lamellar bone tissue (Figure 2B). The blood vessels tend to be mainly perpendicular to the long axis of the bone, though some radial and reticular arrangements also occur, as well as a number of enlarged vascular cavities. Some of these cavities have a narrow layer of centripetally deposited lamellar bone, which indicates that Haversian reconstruction had already begun. Some completely formed secondary osteons occur nearer the medullary cavity. The histology of the distal femoral fragment (KUVP 123108) is fairly similar to that of the midshaft femoral fragment (KUVP 2289). The orientation of the blood vessels in the sections of distal fragment are, however, predominately reticular. A relatively thick compact bone wall surrounds a small medullary cavity which is devoid of any cancellous tissue. Erosion cavities are present in the perimedullary region and the margin of the medullary cavity is resorptive. Secondary osteons tend to be located near the medullary cavity, but some more peripherally located ones can be seen. In a more distal section of KUVP 123108 some cancellous bone tissue was located around the medullary cavity. 3.2. Ichthyornis victor The humeral fragment in transverse section revealed a thin layer of compact bone surrounding the medullary cavity (Figure 3A). In this specimen, as in the Hesperornis specimens above, distortion prevented detailed measurements of the cross sectional dimensions of the bone. However, the thickness of the bone wall varied between 0.55 mm ÿ1.00 mm. The compacta consists of an uninterrupted ®bro-lamellar bone tissue which has numerous blood vessels embedded in the woven bone matrix (Figure 3B). The vessels are mainly longitudinally arranged primary osteons. Some radial and circumferential anastomoses occur. No secondary osteons were observed. Large erosion spaces are visible around the medullary cavity.
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Figure 2. Cross sections of a femur (KUVP 2289) of Hesperornis regalis. A, shows the relatively thick compact bone wall. The compacta is highly vascularised, consisting of mainly longitudinally orientated vascular canals. Scale bar 500 m. B, higher magni®cation of framed region of A showing a large number of primary osteons, and some secondary osteons. Scale bar 250 m.
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Figure 3. Transverse section of a humerus (KUVP 2294) of Ichthyornis victor. A, shows the relatively thin compact bone wall which has a few large cavities present. The bone is highly vascularised by primary vascular canals. The medullary cavity (M) is lined by a narrow layer of lamellar bone. Scale bar 250 m. B, higher magni®cation of the framed region in A showing the richly vascularised periosteal bone and the narrow band of endosteal lamellar bone which lines the medullary cavity. Scale bar 100 m.
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3.3. Cretaceous loon In transverse section (TTU P 9265; Figure 4), the average bone wall thickness of the loon is 37% of the diameter of the bone. This bone wall is substantially thicker than in the modern loon, Gavia stellata, where the bone wall thickness is only 15% of the cross sectional diameter of the bone. This thick compacta is highly vascularised by both primary and secondary osteons which lie in a woven bone matrix of ®bro-lamellar bone tissue. The secondary osteons are mainly located in the mid-compacta and near the margin of the medullary cavity (Figure 3B). Several large erosion cavities are also present near the margin of the medullary cavity. The medullary margin is lined by lamellated tissue which has a number of Volkman's canals. 3.4. Aptenodytes forsteri (Emperor penguin) and Spheniscus demerus (Humboldt penguin) The bone microstructure of both penguins is fairly similar (Figures 5, 6) and are dealt with simultaneously. In transverse section, both penguins display a relatively thick, dense compact bone wall surrounding a small medullary cavity. The thickest region of the compacta in the Emperor penguin amounted to 5.4 mm, representing 33% of the cross sectional diameter, while in the Humboldt penguin the bone wall measured 2.6 mm, or 31% of the cross sectional diameter. In both penguins the compacta is highly vascularised. Longitudinally oriented primary and secondary osteons are located in the woven bone framework of the ®bro-lamellar bone tissue. The most peripheral part of the compacta, in both species, consists of a layer of lamellar bone with osteocytes arranged in parallel (Figures 5A, 6A). In the Emperor penguin, a number of large cancellous spaces occur around the medullary cavity, while none occur in the Humboldt penguin. Only one large erosion cavity was observed in the Humboldt penguin and this clearly contained secondary centripetal deposits of lamellar bone. In both penguins the medullary cavity was lined by a layer of lamellated bone, containing Volkman's canals that radiated into the compacta. 4. Discussion Hesperornis, the Cretaceous loon, and the penguins show similarities in their bone structure which can be directly attributable to their diving lifestyles. In all of these diving birds, the bone wall is relatively thick (BuffreÂnil & Shoevaert, 1989). It is reasonable to assume that this increase in bone mass allowed the birds to overcome buoyancy during dives. Conversely, Ichthyornis, like other volant birds (such as pigeons), has a relatively thin bone wall. This drastic reduction in the amount of bone compacta may be related to lightening of the skeleton as an adaptation for ¯ight. A number of large erosion spaces are also located within Ichthyornis compacta, which probably further reduce the weight of the limb. It is notable that in the extant red throated loon (Gavia stellata) and black necked grebe (Podiceps nigricollis), which are diving birds that are also capable of ¯ight, the relative bone wall thickness is intermediate between the situation in ¯ightless diving birds and that of birds adapted for both ¯ying and diving. In the modern loon and grebe, the bone wall thickness is respectively 15% and 16% of the cross sectional diameter. The Cretaceous loon has a substantially thickened bone wall as compared to these modern birds that are capable of both ¯ight and diving. It is suggested that
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Figure 4. Transverse section of a femur (TTU P 9265) of the Cretaceous loon. A, shows the thick compact bone wall which is highly vascularised by a reticular type of orientation of blood vessels. Some secondary osteons are visible. A, centripetally deposited lamellar bone tissue lines the medullary cavity. Scale bar ˆ 250 m. B, shows the primary vascular canals embedded in a woven bone matrix. Scale bar ˆ 100 m.
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Figure 5. Cross section of the femur of a Spheniscus demerus (Humboldt penguin). A, shows the thick, highly vascularised bone wall. The peripheral layer of lamellar bone (arrow) has ¯attened, parallel-arranged osteocytes. M indicates the medullary cavity. Scale bar 200 m. B, is a higher magni®cation of the bracketed area in A and shows several primary osteons. Scale bar 80 m.
this extinct loon may have been ¯ightless or, if it ¯ew at all, may not have been a strong ¯ier. The peripheral lamellated bone seen in the penguins, and the extensive development of secondary osteons, indicates that they were adults. Unlike the penguins, both of the Niobrara fossil birds lack peripheral lamellar bone, suggesting that the fossil birds which we examined are subadults. In Ichthyornis, the medullary cavity is lined with lamellated bone suggesting that medullary expansion had occurred.
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Figure 6. Cross sections of the Aptenodytes forsteri (Emperor penguin). A, low magni®cation showing the thick, highly vascularised compact bone wall of the femur, and a thin layer of lamellar bone at the periphery. Scale bar 280 m. B, higher magni®cation of bracketed area in A showing the reticular and longitudinal primary osteons, and also some secondary osteons. Scale bar 200 m.
4.1. Physiological implications When lines of arrested growth were ®rst reported in Patagopteryx and the Enantiornithine birds, it was proposed that these birds were physiologically unlike modern birds since they were incapable of sustained rapid growth (Chinsamy et al., 1994, 1995). Hesperornis and Ichthyornis show no evidence of cyclical growth as in extant ornithurines. Even the Emperor penguin, a bird that is severely
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stressed during the breeding season, shows no observable histological change in its bone. We propose that Hesperornis and Ichthyornis were capable of a rapid sustained growth, as in modern birds, which may have been associated with an endothermic physiology. This is in contrast to the more primitive non-ornithurine birds Patagopteryx and the Enantiornithines. The lack of any continental deposits in the Late Niobrara Chalk suggests that these sediments were deposited far offshore (Feduccia, 1996). This implies that the hesperornithiforms and ichthyornithiforms found in these deposits were capable of venturing into the open seas (Feduccia, 1996). An endothermic physiology would have facilitated such long distance forays. 5. Conclusions We draw the following conclusions from our study of Hesperornis and Ichthyornis: The bone microstructure re¯ects the locomotory capabilities of birds (aquatic vs aerial locomotion). Extinct diving birds, Hesperornis, and the Cretaceous loon exhibit distinct thickening of their bone walls. Ichthyornis has thin, lightweight bones, which may represent an adaptation for ¯ight. The lack of lines of arrested growth in these Cretaceous ornithurine birds (Hesperornis, Ichthyornis, and the Cretaceous loon), implies that they were capable of rapid sustained growth. They were physiologically more advanced than the non-ornithurine Patagopteryx and the Enantiornithines. Acknowledgements We thank Luis Chiappe, American Museum of Natural History, New York, and Phillipa Haarhoff, South African Museum, Cape Town for discussion. Sankar Chatterjee, Texas Technical University is thanked for providing the Cretaceous loon specimen for thin sectioning. The extant bird samples were provided by the South African Museum, Cape Town, and the Ornithology Department, San Diego State University, San Diego, USA. Clive Booth, Kholeka Mvumvu, and Kerwin von Willigh provided technical assistance. Paul Barret and Luis Chiappe reviewed this manuscript and are thanked for their constructive comments. This research was supported by the National Science Foundation (NSF) EAR 95± 06694 and by the Foundation for Research Development (FRD), South Africa. References BuffreÂnil, V. & Shoevaert, D. 1989. DonneÂes quantitatives et observations histologiques sur la pachyostose du squelette Dugong dugon (MuÈller) (Sirenia, Dugongidae). Canadian Journal of Zoology 67, 2107±2119. Chatterjee, A. 1989. The oldest Antarctic bird. Journal of Vertebrate Paleontology 9 (3), 16A. Chiappe, L. M. 1995. The ®rst 85 million years of avian evolution. Nature 378, 349±355. Chinsamy, A. & Raath, M. A. 1992. Preparation of fossil bone for histological examination. Palaeontologia Africana 29, 39±44. Chinsamy, A., Chiappe, L. & Dodson, P. 1994. Growth rings in Mesozoic avian bones: physiological implications for basal birds. Nature 368, 196±197. Chinsamy, A., Chiappe, L. & Dodson, P. 1995. The bone microstructure of Patagopteryx and Enantiornithines. Paleobiology 21, 561±574. Feduccia, A. 1996. The origin and evolution of birds, 420 pp. (Yale University Press, New Haven, CT). Fox, R. C. 1974. A middle Campanian, nonmarine occurrence of the Cretaceous toothed bird Hesperornis Marsh. Canadian Journal of Earth Sciences 11, 1335±1338.
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