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First published online January 27, 2004
Journal of Experimental Biology 207, 869-879 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00841

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Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus)

E. de Margerie^1,*, J.-P. Robin², D. Verrier², J. Cubo¹, R. Groscolas² and J. Castanet¹

¹ Adaptation et Evolution des Systèmes Ostéo-Musculaires, FRE CNRS 2696, 2 place Jussieu, 75251 Paris Cedex 05, France
² Centre d'Ecologie et Physiologie Energétiques, UPR CNRS 9010, 23 rue Becquerel, 67087 Strasbourg Cedex 2, France

View larger version (95K): [in a new window]   Fig. 1. Undemineralized diaphyseal thin-sections of the four bones studied (a single chick shown). Ordinary transmitted light. Anterior (A), posterior (P), dorsal (D), ventral (V), medial (M) and lateral (L) sides of bone sections are indicated. Scale bar, 1 mm.

View larger version (163K): [in a new window]   Fig. 2. The four fibro-lamellar bone types observed in the long bones of the king penguin chick. Undemineralized diaphyseal thin-sections, observed under ultraviolet light, bone periphery at the top. Two periosteal labels are shown: (1) alizarin injection 3 weeks after hatching; (2) fluorescein injection at 4 weeks. The outer (top) border of the two labels and the sides of the field delineate a tissue `patch', the thickness of which was measured to yield growth rates. (A) longitudinal bone; the asterisks indicate labelling of the primary osteon filling; (B) radial bone; (C) reticular bone; (D) laminar bone. Scale bar, 200 µm.

View larger version (40K): [in a new window]   Fig. 3. Regressions of body mass (A), bill length (B), flipper length (C) and foot length (D) on time from hatching in 30 non-labelled chicks (open circles) and in the four labelled chicks studied in the present paper (filled circles). Overlapping confidence intervals (CI) of regression slopes (except for bill length) indicate a normal growth of labelled chicks.

View larger version (20K): [in a new window]   Fig. 4. Scatterplot of growth rates within tissue types and long bones. Associated detailed statistics are given in Table 2.

View larger version (101K): [in a new window]   Fig. 5. Spongiosa (femur). The core of the trabeculae is constituted by remnants of primary periosteal bone, labelled at the time of its original apposition: label 1 (fluorescein injection at 2 weeks) and label 2 (alizarin injection at 3 weeks) can be seen in partly resorbed primary osteons. Locally, resorption has stopped and some endosteal bone has been apposited (label 3; fluorescein injection at 4 weeks). Scale bar, 100 µm.

View larger version (29K): [in a new window]   Fig. 6. A putative explanation of faster growth in radial bone. Schematic cross sections of tissues. (A) Laminar bone. Circumferential alignment of woven bone struts results from a saltatory and discontinuous activity of the periosteum (profiles expressed on the right of each section). Repeated onset and arrest of production are suspected to be time-consuming. (B) Longitudinal bone. Same phenomenon as in laminar bone (although less pronounced). (C) Radial bone. Radially aligned bone struts are produced continuously by the periosteum. Efficiency of growth is increased. This holds independent of bone porosity.

View larger version (37K): [in a new window]   Fig. 7. Interaction between osteonal orientation and shear flow, under torsional load. Schematic diagrams of tissues. (A) In laminar bone, shear flow is continuous in the circumferencial `sheets' of bone. (B) In radial bone, radial cavities interrupt the shear flow, because they go through circumferential planes. Bone tissue near cavities undergoes highly concentrated stresses and will yield prematurely. Longitudinal bone would have intermediate characteristics.