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Evolutionary physiology

A bone for all seasons

Because mammals have such high metabolic rates, it has long been thought that their growth is invulnerable to seasonal variation. But their bones turn out to contain annual lines, just as those of cold-blooded animals do. See Letter p.358

The bones of at least some animals contain a record of yearly growth, akin to the rings of tree trunks. But what causes this, and does it occur in all animals? These questions arise from our knowledge that corals and molluscs lay down regular growth lines in their skeletons, and that annual growth lines have also been recorded in fishes, amphibians and some reptiles. Because these are slow-growing, cold-blooded animals, the lines were widely assumed1 to represent pauses in growth resulting from the animals' inability to withstand cyclical environmental stresses such as cold or lack of nutrients. The discovery of these growth lines in dinosaurs2 fostered the hypothesis that they, too, were slow-growing and had 'typical reptilian' metabolic patterns. But reports2 of growth lines in some large fossilized birds, as well as in some fossilized and living mammals, considerably weakened this hypothesis.

On page 358 of this issue, Köhler et al.3 survey the bones of ruminant mammals hailing from the poles to the tropics, in wet to dry climates, and consistently find growth lines (Fig. 1a)Footnote 1. Their study contributes to a growing body of literature that undermines the idea that depositing growth lines is a sign of metabolic inferiority.

Figure 1: Marking time.

a, Köhler et al.3 show that the bones of ruminants contain lines that reflect annual growth patterns, as seen in this cross-section of a long bone from a red deer (Cervus elaphus). The arrows point to annual lines that indicate periods during which growth effectively ceased temporarily. The maze-like network of blood vessels appears rather chaotic in the earlier growth stages (lower part of figure), and settles into a more layered pattern later on (upper part of figure). The completion of growth is indicated by a layer of tissue, called the external fundamental system (EFS) that lacks bone cells or blood vessels. Scale: 500 μm. Picture from ref. 3. b, Identical features are seen in typical dinosaur fossil bones2,3,10, such as that of the ornithopod dinosaur Tenontosaurus tillettii, shown here. Scale: 1,000 μm. Picture provided by Sarah Werning (modified from ref. 11).

Because experimental studies of physiology can be performed only on living animals, the metabolic patterns of extinct species are impossible to assess directly. As a result, we tend to think of animals' physiological features in terms of dichotomies — 'cold'- versus 'warm'-blooded, for example — rather than as continua. Furthermore, we often, for convenience, allot extinct forms to one or other of these alternatives on the basis of a single or a few features that seem to correlate well with what we see in the living world4. The presence of what are presumed to be annual growth lines in dinosaurs (Fig. 1b) and other extinct reptiles seemed to match the pattern in living cold-blooded forms. Therefore, dinosaurs were for many decades widely considered to have been cold-blooded.

The problem with this perfunctory generalization was that the bones of warm-blooded extant animals, such as birds and mammals, had never been properly assessed. The bone characteristics of small birds and mammals, which predominate among living forms, were well known. But these species complete skeletal growth in a few weeks or months, so their bones contain no annual growth lines. It was thus presumed that, being warm-blooded, they were unaffected by seasonal vicissitudes, whereas cold-blooded animals always showed annual lines2.

To the contrary, Köhler et al.3 found that all of the 41 ruminant species they studied — including antelopes, deer and giraffes — deposit growth lines. They show that these are formed annually during the unfavourable season, when the animals lower their body temperatures and metabolic rates, presumably as a way to conserve energy. When the favourable season begins, body temperatures and metabolic rates increase again, and so do growth rates. So it seems that mammals are no different from other vertebrates in this respect.

Do annual growth lines always reflect environmental stress? To explore this question, one group of researchers kept a colony of pygmy lemurs under constant conditions of food and temperature, but varied the light regime to reflect annual periodicity5. They then took a subset of the animals and changed the light regime to a 10-month cycle. The bones of both groups deposited growth lines, but the subset did so every 10 instead of every 12 months, falsifying the hypothesis that stress was involved, and instead suggesting the influence of an internal response to light cues, perhaps mediated by the pineal gland in the brain. So, whereas the rhythms of annual growth cycles in vertebrates may originally have reflected environmental stress, it seems that these rhythms have become ingrained in the genes, even in the absence of stress.

What do these findings mean for dinosaurs, and for the interpretation of vertebrate growth in general? In recent years, several studies have chipped away at the cold-blooded dinosaur model. For one thing, the density of blood vessels (vascular canals) in their bones was very high, more comparable to that seen in mammals (Fig. 1) and birds than in reptiles and amphibians6. High vascular density implies high blood flow and rapid growth, which can be sustained only by high metabolic rates2. The larger dinosaurs and their relatives grew faster than smaller species, a pattern consistent with other vertebrate groups7. But young dinosaurs of larger species may sometimes have grown too quickly to leave annual lines in their first year, and other very large ones (such as sauropod dinosaurs) mostly grew too fast to deposit annual lines at all. It seems that these were anything but typical reptiles, and Köhler and colleagues' findings remove another false correlation from this picture.

Another part of this puzzle is the conundrum of determinate versus indeterminate growth. Most warm-blooded animals grow to a typical adult size, at which point growth ceases or radically slows until death; this is called determinate growth. As growth slows, the annual lines appear much closer together, because less bone tissue is deposited between them. Such animals tend to finish long-bone deposition with a layer of tissue that lacks blood vessels and bone cells, in contrast to tissue that is deposited earlier in the growth process. This finishing layer is called the external fundamental system (EFS; Fig. 1), and has not been found in most studies of cold-blooded animals. However, an EFS has been identified in both extant crocodylians8 and some of their extinct Triassic relatives9, both of which were previously thought to grow in an indeterminate manner — that is, slowly but continually throughout life. Furthermore, dinosaurs also deposited an EFS when fully grown10. Thus, it now seems likely that all vertebrates, living and extinct, have determinate growth, and that we don't see an EFS in slow-growing creatures because most individuals die before they reach full size.

There is still much to learn about the distribution of growth lines in living and extinct vertebrates, as well as what they mean physiologically and how different metabolic regimes of growth and deposition have evolved. But Köhler and colleagues have provided a crucial piece of this puzzle, by conclusively demonstrating that growth lines are typical of large mammals, and thereby discounting the idea that this feature is a characteristic of cold-blooded animals.


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    *This article and the paper under discussion3 were published online on 27 June 2012.


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Correspondence to Kevin Padian.

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Padian, K. A bone for all seasons. Nature 487, 310–311 (2012).

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