iBet uBet web content aggregator. Adding the entire web to your favor.
iBet uBet web content aggregator. Adding the entire web to your favor.



Link to original content: http://www.ncbi.nlm.nih.gov/pubmed/19816582
Was dinosaurian physiology inherited by birds? Reconciling slow growth in archaeopteryx - PubMed Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2009 Oct 9;4(10):e7390.
doi: 10.1371/journal.pone.0007390.

Was dinosaurian physiology inherited by birds? Reconciling slow growth in archaeopteryx

Gregory M Erickson  1 , Oliver W M Rauhut, Zhonghe Zhou, Alan H Turner, Brian D Inouye, Dongyu Hu, Mark A Norell
Affiliations

Was dinosaurian physiology inherited by birds? Reconciling slow growth in archaeopteryx

Gregory M Erickson et al. PLoS One. .

Abstract

Background: Archaeopteryx is the oldest and most primitive known bird (Avialae). It is believed that the growth and energetic physiology of basalmost birds such as Archaeopteryx were inherited in their entirety from non-avialan dinosaurs. This hypothesis predicts that the long bones in these birds formed using rapidly growing, well-vascularized woven tissue typical of non-avialan dinosaurs.

Methodology/principal findings: We report that Archaeopteryx long bones are composed of nearly avascular parallel-fibered bone. This is among the slowest growing osseous tissues and is common in ectothermic reptiles. These findings dispute the hypothesis that non-avialan dinosaur growth and physiology were inherited in totality by the first birds. Examining these findings in a phylogenetic context required intensive sampling of outgroup dinosaurs and basalmost birds. Our results demonstrate the presence of a scale-dependent maniraptoran histological continuum that Archaeopteryx and other basalmost birds follow. Growth analysis for Archaeopteryx suggests that these animals showed exponential growth rates like non-avialan dinosaurs, three times slower than living precocial birds, but still within the lowermost range for all endothermic vertebrates.

Conclusions/significance: The unexpected histology of Archaeopteryx and other basalmost birds is actually consistent with retention of the phylogenetically earlier paravian dinosaur condition when size is considered. The first birds were simply feathered dinosaurs with respect to growth and energetic physiology. The evolution of the novel pattern in modern forms occurred later in the group's history.

PubMed Disclaimer

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Long bone histology of a non-avialan dinosaur and a Mesozoic bird viewed with polarized microscopy.
(A) The femoral microstructure of the small alvarezsaurrid, Shuvuuia deserti (IGM 100–99) is compared to the tibial histology (B) of the Early Cretaceous avialan, Confuciusornis sanctus (IVPP V11521). Both show well-vascularized bone owing to the presence of numerous primary vascular canals (large black structures), and woven fibered matrix characterized by oblong, randomly oriented osteocyte lacunae (numerous small black structures). Arrows point to growth lines in the form of a line of arrested growth (left) and an annulus (right). Scale bars  = 0.5 mm (A) and 0.1 mm (B).
Figure 2
Figure 2. Skeletal elements from the largest known Archaeopteryx specimen showing cortical delamination.
Femora, tibiae, fibulae, pubes, and gastralia from the Solnhofen specimen (BMMS 500), are shown. The brown cortical layer of the left femur (inset box) is superior to the light gray underlying bone layer that is exposed where the former flaked-off. This is consistent with a growth line interface. These thin, hypermineralized osseous layers partition the more fibrous zonal tissues and act as planes of weakness where exfoliation can occur.
Figure 3
Figure 3. Fibrous surface texture and longitudinal vascular canals visible within the cortices of Archaeopteryx long bones.
(A) Tibial diaphysis from the smallest known Archaeopteryx, the Eichstät specimen (JM 2257) showing sparse longitudinal vascularization in the form of parallel striae. Comparable immature texture and patterning is found in the major long bones throughout the Archaeopteryx growth series. For example, it is seen in the tibiae of the moderately larger Munich specimen (BSPG 1999 I 50) shown in (B), and in the largest known individual (The Solnhofen specimen, BMMS 500) shown in (C). Scale bars  = 1.5 mm.
Figure 4
Figure 4. Slab and counterslab of the Munich Archaeopteryx (BSPG 1999 I 50).
Cortical samples were extracted from the fracture faces of broken elements. (A) Main slab with arrows showing where femoral samples were extracted. (B) Counterslab showing where the fibula was sampled. Scale bar  = 5 cm.
Figure 5
Figure 5. Cladogram for the Maniraptora showing character mapping of primary femoral histological types with respect to scale.
The specimens are viewed with polarized microscopy. Each is oriented with the periosteal surface towards the top of the figure. Five histological character suites (I.–V.) are present. The attributes composing each suite appear below the figure and are denoted by (black and/or gray horizontal bars). For example: Maniraptoran Type I shows longitudinal vascularizaton, parallel-fibered matrix, and low porosity. Lines stemming from the bottom the histological images trace to the representative histological suites for each taxon. The character suites show intracladal scale dependence with respect to femoral length. The basal avialans conform to expectations of same-sized non-avialan maniraptoran outgroups. Phylogenetic hypothesis based on ref. 22.
Figure 6
Figure 6. Maniraptoran femoral porosity shown with respect to scale.
Intracortical transverse plane porosity from the histological sections was quantified (See Materials and Methods). These data are plotted with respect to femoral length. Data for non-avialan taxa are denoted by black diamonds. The regression equation describes only their distribution. The blue lines bound the 95% confidence interval. The red diamonds represent the basalmost avialans studied here. Note: their data are encompassed by the maniraptoran confidence interval and that for sister taxon Deinonychosauria (not shown).
Figure 7
Figure 7. Histological section of an Archaeopteryx femur (BSPG 1999 I 50) viewed with polarized microscopy.
(A) Parallel-fibered bone is found throughout the cortex as shown by the flattened, circumferentially oriented, lenticular osteocyte lacunae (tiny black structures) and matted bone fabric (lower left). (B) Primary longitudinal vascular canals are few (large black circular structures). These are occasionally found incompletely formed at the periosteal surface (arrow) and are responsible for the fibrous surface texture of the elements and long striae seen deep within the bones of all known individuals. Scale bar  = 0.75 mm.
Figure 8
Figure 8. Femoral histology of the basal birds Jeholornis and Sapeornis viewed with polarized microscopy.
(A) In Jeholornis (IVPP 13353), parallel-fibered bone matrix similar to that of Archaeopteryx makes up the cortex. However porosity is greater as in Mahakala. A growth line that locally varies between a line of arrested growth and an annulus is shown (arrow). (B) In the larger Sapeornis (LPM B00166), the matrix is primarily woven-fibered and shows a mix of longitudinal and reticular vascularization. Avascular parallel-fibered bone brackets a line of arrested growth (arrow) in this sub-adult specimen. Scale bar  = 0.15 mm
Figure 9
Figure 9. Growth depictions for Archaeopteryx.
(Left) The size and estimated age for all ten specimens are depicted. The growth curves are based upon age and size estimates (diamonds) for the eight specimens where femoral length is known. The dashed line represents the best fit for the unconstrained statistical analysis with hatchling and adult size undefined. The solid line represents the best fit when hatchling and adult size are constrained. (Right) The maximal growth rates from these analyses (1.87–2.2 g/day; hollow diamond) fit expectations (1.83–1.87 g/day; [31]) for same-sized non-avialan dinosaurs (solid line) – animals that grew like slow growing endotherms, here compared to marsupials (M). The Archaeopteryx estimates are three times lower than typical rates for extant precocial land birds (5.7 g/day; P], 15 times lower than alticial land birds (28.6 g/day; A), and four times higher than typical rates for extant reptiles (0.46 g/day; R) . Specimens designations: Ei  =  Eichstäat, Mu  =  Munich, 8th  =  8th Exemplar, Te  =  Teyler, Th  =  Thermopolis, Be  =  Berlin, Ma  =  Maxberg, O&S  =  Exemplar der Familien Ottmann & Steil, Lo  =  London, So  =  Solnhofen.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Gill FB. New York: WH Freeman; 2007. Ornithology, 3rd ed.758
    1. Chiappe LM. Sydney: University of New South Wales Press; 2007. Glorified Dinosaurs: The Origin and Early Evolution of Birds.263
    1. Chiappe LM, Witmer LM, editors. Berkeley: University of California Press; 2002. Mesozoic Birds: Above the Heads of Dinosaurs.520
    1. Gauthier J, Gall LF, editors. New Haven: Peabody Museum of Natural History; 2001. New Perspectives on the Origin and Early Evolution of Birds.613
    1. Chinsamy A. Baltimore: Johns Hopkins Press; 2005. The Microstructure of Dinosaur Bone: Deciphering Biology with Fine-Scale Techniques.195

Publication types