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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

^* Author for correspondence (e-mail: margerie.e.de{at}club-internet.fr)

Accepted 15 December 2003

Microstructure–function relationships remain poorly understood in primary bone tissues. The relationship between bone growth rate and bone tissue type, although documented in some species by previous works, remains somewhat unclear and controversial. We assessed this relationship in a species with extreme adaptations, the king penguin (Aptenodytes patagonicus). These birds have a peculiar growth, interrupted 3 months after hatching by the austral winter. Before this interruption, chicks undergo extremely rapid statural and ponderal growth. We recorded experimentally (by means of fluorescent labelling) the growth rate of bone tissue in four long bones (humerus, radius, femur and tibiotarsus) of four king penguin chicks during their fastest phase of growth (3–5 weeks after hatching) and identified the associated bone tissue types (`laminar', `longitudinal', `reticular' or `radial' fibro-lamellar bone tissue). We found the highest bone tissue growth rate known to date, up to 171 µm day^–1 (mean 55 µm day^–1). There was a highly significant relationship between bone tissue type and growth rate (P<10^–6). Highest rates were obtained with the radial microarchitecture of fibro-lamellar bone, where cavities in the woven network are aligned radially. This result supports the heuristic value of a relationship between growth rate and bone primary microstructure. However, we also found that growth rates of bone tissue types vary according to the long bone considered (P<10^–5) (e.g. growth rates were 38% lower in the radius than in the other long bones), a result that puts some restriction on the applicability of absolute growth rate values (e.g. to fossil species). The biomechanical disadvantages of accelerated bone growth are discussed in relation to the locomotor behaviour of the chicks during their first month of life.

Key words: fibro-lamellar bone tissue, biomechanical properties, bone microstructure, growth rate, long bone, structure–function