The youngest individuals in our sample appear to be late stage juveniles. A large proportion of their compacta comprises fibrolamellar bone, which suggests that during early ontogeny bone deposition occurred at a rapid rate13, 21. Such rapid rates of growth during the early growth stages is typical for modern birds; it has also been described in other species such as the secretary bird (Sagittarius serpentarius)14, Japanese quail (Coturnix japonica) 22, king penguin (Aptenodytes patagonicus)23 and ostrich (Struthio camelus)14, as well as in Mesozoic ornithurine birds13, 24, 25. The well-developed ICL in the youngest dodo specimens suggests that medullary expansion had already been completed in these individuals13.

During later stages of ontogeny, the fibrolamellar bone, which formed during early ontogeny, is reconstructed and remodeled13, 14. The compacta of adult individuals show a well-developed ICL and OCL, both consisting of more slowly formed lamellar bone tissue. The formation of the OCL tends to occur after the development of the ICL, and only once sexual maturity has been attained14, 22. This three-layer arrangement of the tissue in the bone wall in the dodo is similar to that described by Enlow and Brown26 for a modern hawk (Buteo), chicken (Gallus), turkey (Meleagris), guinea fowl (Numida) and crow (Corvus), and has been shown for other birds such as secretary bird S. serpentarius 14 and albatross Diomedea 13.

Like large modern flightless birds, e.g. cassowary (Casuarius)27, ostrich (Struthio)14 and rhea (Rhea)28, the dodo also has rapidly formed fibrolamellar bone tissue. However, unlike these birds in which this is the predominant tissue of the bone wall, in the dodo this tissue makes up only one third of it. Slower, more protracted rates of growth during ontogeny have been documented for moas (Dinornithiformes)27, the kiwi (Apteryx)29, and the Late Cretaceous Gargantuavis 30. The slower growth to adult size appears to be related to the lack of predators and to environmental resource stress22, 27, 29, 30. Interestingly, although the dodo does not exhibit the slow protracted growth of these large island birds, it does appear to have had an extended growth period when reaching skeletal maturity, which is confirmed by the presence of several LAGs in the OCL. Thus, the dodo experienced rapid growth rates until the attainment of sexual maturity, but thereafter it took several years to attain skeletal maturity. Such an extended, slow growth after sexual maturity might have been possible on a small island like Mauritius24 where until the arrival of humans, adult birds lacked any natural predators.

Among modern birds, when lines of arrested of growth are present, they tend to be restricted to the OCL13. However, terrestrial birds on islands, like the kiwi29 or Dinornithiformes27, have several LAGs throughout the cortex. Turvey et al.27 proposed that the LAGs in the slow growing Dinornithiformes, and in particular Megalapteryx didinus are the result of severe environmental fluctuations27. Likewise, Köhler et al.31 suggested that the frequent observation of LAGs in wild ruminants were the result of seasonality. In addition, the growth lines evident in the insular Myotragus is considered to be the result of resource limitation32. Experimental studies on birds that were given restricted access to food have demonstrated that although such limitations did not necessarily produce LAGs, they resulted in a decrease in bone depositional rates22. However, if access to food was more severely limited, LAGs may have resulted; this has been suggested for another insular flightless columbiform, the solitaire Pezophaps solitaria 32. In the case of the dodo, harsh seasonal conditions on Mauritius exist during the summer months, between November and March. During this period, cyclones can occur, during which heavy rain and strong winds can strip trees of leaves, flowers and fruit, causing severe food shortages and starvation for the island fauna, and it can take a few months for normal environmental conditions to return3, 33, 34. These events may explain the variations in body mass, as reported by mariners for the dodo8. As these seasonal events and consequent long food shortages could result in nutritional stress, we suggest that the LAGs observed in the OCL in the dodo bones were produced in the summer months, between November and March.

The presence of medullary bone in two specimens proves unequivocally that part of the sample were ovulating females35. The tibiotarsus (ddtbt08) shows a large area of medullary bone in comparison to the femur (ddfem04). This could be a result of histological variability between these skeletal elements13, although they could also suggest differences in their reproductive cycles, i.e. one bird (represented by ddtbt08) had not yet utilized the medullary bone for eggshell production, while the other bird (represented by ddfem04) had already shelled its eggs13, 21, 36. Livezey37 had previously used the K-means statistical method to deduce sexual dimorphism in the dodo; however he did not statistically check the validity of the clusters obtained using the K-means methodology, which therefore invalidates them. Apart from this work, the dodo is not considered to be overly sexually dimorphic, and in the current study we found that the circumferences of the bones of the females were similar to other adult bones in the sample (Supplementary Tables S2–S3). Thus, as for the extinct birds Confuciusornis 35 and Dromornis 38, bone histology has proved to be an important tool in sex determination of the dodo.

The adult dodo specimens generally show a large amount of secondary reconstruction, with many secondary osteons present in the cortex, as well as evidence of extensive resorption around the medullary cavity13. However, five specimens (ddfem03, ddtbt02, ddtbt05, ddtbt06, ddtbt09), have much enlarged cavities in the cortex suggesting that the demand for calcium surpassed the normal requirements. Such significant bone remobilization has been reported in penguins during molting when the demand for calcium is increased39, 40, as well as, for 15 species of modern birds including the domestic pigeon40. Periodic molting is common among modern birds34, 41, 42, which allows time for the replacement of old damaged feathers, and commonly occurs after breeding3, 33, 34, 41, 42. Molting periods have been previously proposed for the dodo43,44,45,46,47, but these are generally unsupported48. On the basis of earlier osteohistological observations made on several other birds species39, 40, we suggest that the presence of extensive resorption in the bones of the dodo could be interpreted as evidence of molting.

We further propose that since molt can generate significant changes in the appearance of birds in terms of color and feather type3, this may explain the many discrepancies in the descriptions of the dodo in historical accounts8, 49. The dodo was variably described as having “three or four black quills” in the place of their wings, and a tail with “four or five small curled plumes of a greyish color”49. Some other descriptions of the dodo mention a “clothing of downy feathers” or even “no feathers on their body, which is covered in black down”49. Thus, we propose that mariners may have been describing the dodo at different stages of molt. Dodos described as having a downy plumage49 were probably observed and described just after molt, as seen in modern birds in a similar condition3, 34, 41, 42, whilst the grey or black plumage49 could correspond to dodo specimens between two molting periods50.

Our study of bone microstructure has given insight into the molting and reproductive behavior of the dodo, but the timing of these events needs further clarification. Since Mauritius has a seasonal cycle of cyclonic events, which occurs between November and March (austral summer), Staub44 suggested that the dodo bred in the austral winter, between March and September, when food was abundant, with a post-breeding molting period between September and December. He based this hypothesis on a description by Captain van Westzanen in 1602, who described the meat of the dodo as a very tasty food. Staub44 considered that this culinary aspect was a result of the birds eating a profusion of fruits from the endemic palm trees (Latania sp., Dictyosperma sp., Hyophorbe sp.), which produced fruits during the winter. Thus, he suggested, that the dodo evolved its reproduction period to coincide with food abundance, following the same reproductive strategy of the solitaire on neighboring Rodrigues Island. However, if we compare this annual molting pattern proposed by Staub44 with information known about modern surviving birds on Mauritius, his hypothesis is improbable. On Mauritius, (contra Staub), all birds breed during the austral summer (between August and January, which sometimes extends into March), and start the post-breeding molt between November and March3, 33, 34, 41. Moreover, the Pink Pigeon (Nesoenas mayeri), which has the longest molting period of any bird on Mauritius, does not molt during the months towards the end of the austral winter (June to October) when food resources are limited33.

Thus, bone histology provides significant information about the timing of breeding and molting periods in the dodo. We can now consider that as LAGs form during the cyclone period between November and March, the breeding and the molting periods can be accurately determined using the amount of bone deposited after the LAG (Fig. 6.1). Assuming that the bone deposition rate is constant between consecutive LAGs, we propose that the thicker the bone deposition between two LAGs, the more time has lapsed since the LAG formed, thereby giving an indication of when the breeding or molting event occurred. Furthermore, if we examine the external cortex of the two specimens that have formed medullary bone (ddtbt08 and ddfem04), it is evident that a relatively large amount of bone had formed after the last LAG. This new bone in the OCL, corresponds to around 50% of the bone deposited between the two previous LAGs (Fig. 2b). Considering that LAGs are formed annually, we can estimate that ovulation happens approximately six months after the last LAG, i.e. about six months after the last austral summer, at the beginning of August (Fig. 6.5). We hypothesize that after egg laying and hatching (Fig. 6.6), the chicks grew rapidly to reach a relatively large size so that they were better able to withstand the environmental stress of the next austral summer (Fig. 6.7), which usually corresponds to the cyclone period, and hence resource limitations.

Figure 6 Diagram summarizing the main conclusions of this research. Blue area: indicates the summer period when storms occur between November and March. Yellow line (----): indicates when the LAGs could be formed due to the storms during the Austral Summer; Red line (−): indicates the possible molting period, after summer; Green line (-.-.-): indicates the probable breeding period. 1 – LAG formation; 2 – Beginning of molting; 3 – Mix between downy plumage and new feathers as described in the historical documents; 4 – End of the molting period, when all the feathers are renewed, as described in the historical literature; 5 – In the case of females, the breeding period start with ovulation; 6 – The eggs are laid, hatching later occurs; 7 – The chicks grow rapidly before the next cyclone season. Full size image

The external cortex of specimens that exhibit evidence of molting in their bone (i.e., several large resorption cavities) have thin lamellar deposits after the last LAG in the OCL (Figs 4 and 5), which further suggests that molting starts just after the last austral summer (Fig. 6.2). Therefore, molting occurred after the breeding and cyclone season, allowing for the renewal of plumage before the next breeding period. This is congruous with the variable descriptions of the plumage of the dodo by mariners in which they described dodos with a downy body and some feathers in the wings and the tail49 during June and July. These descriptions likely correspond to the middle of the molting period, when all old feathers have already been lost and replaced by temporary downy plumage (Fig. 6.3). The new feathers then appear, starting with the wings and the tail, as seen in modern birds3. Mariners further described a plumage composed of real feathers in the documents written in July and September49. This means that at the end of July the molt is completed and the breeding season begins with a new plumage (Fig. 6.4). On the basis of this evidence we propose that the dodo molt occurred between March and the end of July, after the austral summer and cyclone period, and before the next breeding season, which is consistent with the breeding and molting periods described for all surviving birds on Mauritius3, 33, 34, 41.