Medullary bone in an Early Cretaceous enantiornithine bird and discussion regarding its identification in fossils

Abstract

Medullary bone is an ephemeral type of bone tissue, today found only in sexually mature female birds, that provides a calcium reservoir for eggshell formation. The presence of medullary bone-like tissues in extant birds, pterosaurs, and dinosaurs distantly related to birds shows that caution must be exercised before concluding that fossils bear medullary bone. Here we describe a new specimen of pengornithid enantiornithine from the Lower Cretaceous Jiufotang Formation. Consisting of an isolated left hindlimb, the three-dimensional preservation contrasts with the crushed preservation characteristic of most Jehol specimens. Histological examinations suggest this resulted from the presence of a thick layer of highly vascular bone spanning the medullary cavities of the femur and tibiotarsus, consistent with expectations for medullary bone in extant birds. Micro-computed tomographic scans reveal small amounts of the same tissue extending into the pedal phalanges. We consider the tissue to be homologous to the medullary bone of Neornithines.

Osteohistology and Life History of the Basal Pygostylian, Confuciusornis sanctus

“…Specimen DNHM-D1874 is the one in which the identification of probable medullary bone tissue led us to identify it as a female that was ovulating at the time of death (Chinsamy et al, 2013). Contrary to a recent interpretation (O'Connor et al, 2018), the tissues ascribed as "medullary bone tissues" are clearly endosteally formed and are directly attached to the ICL, that is, not free within the medullary cavity (Chinsamy et al, 2013). Based on this specimen, we work under the assumption that the well-ossified individuals without tail feathers are most likely females of the species, and we note that immatures will also not have tail feathers (Table 1).…”

Dinosaur paleohistology: review, trends and new avenues of investigation

“…Since this first identification, MB has also been reported in several other non-avian dinosaurs, including taxa outside the theropod lineage (Lee & Werning, 2008; Hübner, 2012), as well as pterosaurs (Prondvai & Stein, 2014; Prondvai, 2017). It has also been reported in two Mesozoic bird lineages recovered from the Jehol biota: in Confuciusornis (Chinsamy et al, 2013) and in two enantiornithines (an enantiornithine indet., O’Connor et al, 2018 and in Avimaia schweitzerae , Bailleul et al, 2019). Definitive evidence in support of this identification in Avimaia is provided through the preservation of an intra-abdominal egg, indicating this adaptation evolved outside the crown clade (Bailleul et al, 2019).…”

“…Similar results were also found in the non-ornithurine ornithuromorph Yanornis (Wang et al, 2019). Several studies also indicate that most stem birds, like their non-avian dinosaurian relatives, achieved reproductive maturity prior to skeletal maturity (O’Connor et al, 2014, 2018).…”

“…Much of what is known about the transition from dinosaur to avian-style growth comes from specimens found either in the middle to Upper Jurassic Yanliao Biota or the Lower Cretaceous Jehol Biota, both known from northeastern China (Zhou, Barrett & Hilton, 2003). The oviraptorosaur Caudipteryx (Erickson et al, 2009), paravians including Anchiornis (Zheng et al, 2014; Prondvai et al, 2018), basal birds including Sapeornis (Gao et al, 2012), Jeholornis (Erickson et al, 2009; O’Connor et al, 2014; Prondvai et al, 2018), Confuciusornis (Zhang, Hou & Ouyang, 1998; De Ricqlès et al, 2003; Chinsamy et al, 2013), the ornithuromophs Archaeorhynchus (Wang & Zhou, 2017) and Iteravis (O’Connor et al, 2015), and several enantiornithines (O’Connor et al, 2014, 2018) together with Late Cretaceous ornithothoracines from Argentina (Chinsamy, Chiappe & Dodson, 1995) have contributed greatly to our overall understanding of the evolution of avian growth strategies. Despite this work, the study of stem avian histology is still at a relatively early stage compared to that of non-avian dinosaurs.…”

“…Derived from the endosteum, MB can line the medullary cavities and cancellous spaces of the entire avian skeleton in some taxa (Canoville, Schweitzer & Zanno, 2019). In living birds, MB is estrogen dependent, forms extremely fast (although this might not have always been the case in stem taxa; see O’Connor et al, 2018; Bailleul et al, 2019), is high in calcium relative to other types of bone tissue, and is highly vascular, all which facilitate its function as an easily mobilized calcium reservoir (Bloom, Bloom & McLean, 1941; Taylor & Moore, 1953; Yamamoto et al, 2001).…”