Chinsamy, Martin & Dodson, 1998

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®ceBox 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, 19104-4065, 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 bonedeposition without any pauses or interruptions in bone formation. This growth pattern contrasts shar-ply with the cyclical pattern of bone deposition previously reported for the Cretaceous non-ornithur-ine birds Patagopteryx and representatives of the enantiornithines. These ®ndings suggest physiologicaladvancement in Cretaceous ornithurine birds. The bone microstructure of the diving Hesperornisshows similarities to the bone structure of modern penguins, and to that of a loon from the Cretac-eous 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 repre-

sentatives 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 com-

pressed feet for generating propulsive forces during swimming. Hesperornithi-

formes are generally considered to be a diverse group that had a world-wide

Cretaceous Research (1998) 19, 225±235 Article No. cr970102

0195±6671/98/020225 + 11 $30.00/0 # 1998 Academic Press

distribution during the Cretaceous (Feduccia, 1996). Most forms are recovered

from marine sediments, although specimens are known from a Middle Campa-

nian estuarine deposit in Alberta (Fox, 1974) and from freshwater deposits (Mar-

tin, 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 ster-

num, 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 Barto-

dano Formation of Seymour Island, Antarctica (Chatterjee, 1989), and of the

extant Emperor and Humboldt penguins, Aptenodytes forsteri and Spheniscusdemerus. The Emperor penguin was chosen as these birds have particularly stress-

ful breeding patterns, which may be re¯ected in their bone histology. Other mod-

ern bird femora were also studied, including that of Columba livia, the pigeon,

Ichthyornis

Hesperornis

Patagopteryx

Enantiornithes

Archaeopteryx

ORNITHURAE

AVES

Modern birds, such asAptenodytes, Spheniscus,Columba, Gavia, Podiceps

Figure 1. Cladogram depicting the phylogenetic relationships (see Chiappe, 1995) of the aviantaxa cited in the text.

226 A. Chinsamy et al.

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 (Podicepsnigricollis).

The bone samples were prepared for thin sectioning according to the method-

ology 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 Soft-

ware).

3. Results

3.1. Hesperornis regalisIn 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 tis-

sue 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 Haver-

sian 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 reti-

cular. A relatively thick compact bone wall surrounds a small medullary cavity

which is devoid of any cancellous tissue. Erosion cavities are present in the peri-

medullary 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 cancel-

lous bone tissue was located around the medullary cavity.

3.2. Ichthyornis victorThe 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 cir-

cumferential anastomoses occur. No secondary osteons were observed. Large ero-

sion spaces are visible around the medullary cavity.

Bone microstructure of Hesperornis and Ichthyornis 227

Figure 2. Cross sections of a femur (KUVP 2289) of Hesperornis regalis. A, shows the relatively thickcompact bone wall. The compacta is highly vascularised, consisting of mainly longitudinallyorientated vascular canals. Scale bar � 500 �m. B, higher magni®cation of framed region of Ashowing a large number of primary osteons, and some secondary osteons. Scale bar � 250 �m.


Figure 3. Transverse section of a humerus (KUVP 2294) of Ichthyornis victor. A, shows the relativelythin compact bone wall which has a few large cavities present. The bone is highly vascularised byprimary 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 vascu-larised periosteal bone and the narrow band of endosteal lamellar bone which lines the medullarycavity. Scale bar � 100 �m.


3.3. Cretaceous loonIn 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-lamel-

lar 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 (Humboldtpenguin)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 thick-

est region of the compacta in the Emperor penguin amounted to 5.4 mm, repre-

senting 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 ero-

sion cavity was observed in the Humboldt penguin and this clearly contained sec-

ondary 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 over-

come 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 Ichthyorniscompacta, 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 (Podicepsnigricollis), 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 diam-

eter. 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


Figure 4. Transverse section of a femur (TTU P 9265) of the Cretaceous loon. A, shows the thickcompact bone wall which is highly vascularised by a reticular type of orientation of bloodvessels. Some secondary osteons are visible. A, centripetally deposited lamellar bone tissue linesthe medullary cavity. Scale bar � 250 �m. B, shows the primary vascular canals embedded in awoven bone matrix. Scale bar � 100 �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 devel-

opment 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.

Figure 5. Cross section of the femur of a Spheniscus demerus (Humboldt penguin). A, shows thethick, 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 highermagni®cation of the bracketed area in A and shows several primary osteons. Scale bar � 80 �m.


4.1. Physiological implicationsWhen lines of arrested growth were ®rst reported in Patagopteryx and the Enan-

tiornithine 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

Figure 6. Cross sections of the Aptenodytes forsteri (Emperor penguin). A, low magni®cation showingthe thick, highly vascularised compact bone wall of the femur, and a thin layer of lamellar boneat the periphery. Scale bar � 280 �m. B, higher magni®cation of bracketed area in A showing thereticular and longitudinal primary osteons, and also some secondary osteons. Scalebar � 200 �m.


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 Pata-gopteryx 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 ichthyornithi-

forms 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.

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