such as long bones and the vertebral column
(movies S1 to S3).
Although the current available material cannot provide a complete view of the ontogenetic
development of Hamipterus, and despite some
uncertainty in regarding these embryos as representing late embryonic stages, some general
observations can be made that considerably expand our knowledge about the embryology and
ontogeny of pterosaurs (14). The skull roof was
not well ossified before the animal hatched, albeit more than in birds (15) but less than in
lepidosaurs (16) and crocodiles (17). Prior to
hatching, the lower jaw already shows an anterior
expansion that gets more developed during ontogeny. The symphyseal region increased from
around 23% in embryos to 43 to 45% of the total
lower jaw length in juveniles and subadults. No
teeth were found in any of the embryos. Because
teeth tend to be very resistant and embryos of
dinosaurs (11), birds (18), and one pterosaur (3)
show them, there seems to be no taphonomic
explanation for their absence. Therefore, this
embryo might be at a stage of development in
ovo prior to teeth eruption, or dental eruption
is delayed in this pterosaur, contrary to the
condition found in lizards and crocodiles (19),
the latter favored here.
Overall, wing elements show ossified shafts
but still unformed articulations, such as the
humerus and the wing metacarpal (Fig. 3, H
and K). In two embryos, other metacarpals are
also ossified despite being very thin, with metacarpal I reaching the carpus. No extensor tendon process was identified, suggesting that it
ossifies only slightly before or after hatching.
The deltopectoral crest is warped in juveniles
but not in the embryos, indicating that its distal
end was still cartilaginous. This suggests that the
most powerful wing depressor, m. pectoralis (20),
which is attached to the deltopectoral crest, was
not well developed in neonates. The embryonic
scapula lacks a processus scapularis (Fig. 3G),
which is the origin of m. teres major, a muscle
involved in the elevation of the wing (20). This
structure is observed in the smallest nonembryonic individual recovered, in which the scapula is slightly more than four times as longer
than in the embryos. The femur, on the contrary, is well developed, showing the typical
pterosaurian femoral head, with a constricted
neck and complete distal articulation (Fig. 3I).
This suggests that the hind limbs have developed
more rapidly compared to the forelimbs and
might have been functional right after the animal hatched. Thus, newborns were likely to move
around but were not able to fly, leading to the
hypothesis that Hamipterus might have been
less precocious than advocated for flying reptiles in general (6) and probably needed some
Osteohistological sections of some postcranial
elements from embryos and larger-sized indi-
viduals were made (Fig. 4 and figs. S8 to S10).
None showed plywood-like bone, which is re-
garded as unique for pterosaurs (21). Secondary
osteons, which are rare in these flying reptiles
(22), are also lacking. In the embryo, the cortex
of all three sectioned bones (radius, ulna, and
one wing phalanx) is composed of woven bone,
with large vascular canals, which indicates fast
growth (23). Regarding nonembryonic elements
found scattered in the matrix, osteohistological
sections of three ulnae were made. The smallest
shows fibrolamellar bone without any growth
mark, suggesting that it belonged to a young
individual. The second (~140 mm) also shows
fibrolamellar bone, but presents internal circum-
ferential layers (ICLs) with one line of arrested
growth (LAG) and an annulus, suggesting that
growth of the medullary cavity had ceased (23).
Another LAG can be found in the outermost part
of the periosteal bone matrix, but no external
fundamental system (EFS) (1) was developed.
This configuration has been interpreted as an
indicator of sexual maturity (24). In the largest
ulna (~190 mm), the ICLs are also present, and
one LAG and an annulus are placed in the out-
ermost part of cortex, but no EFS is formed yet.
Based on the presence of growth marks (LAG
and annulus) and the absence of any sign of
bone remodeling or secondary structures (23)
that could erase those marks, this bone might
represent an individual at least 2 years old, still
growing at the time of its death.
The main locality where eggs have been col-
lected is characterized by a succession of white
to gray, middle- to fine-grained sandstones that
were deposited in a fluvio-lacustrine environ-
ment (fig. S12). Localized lenses of mudstone are
present (fig. S13). Egg- and bone-carrying layers
have a thickness between 10 to 30 cm and show
extensive mudstone pellets. In a 2.2-m section,
eight layers with pterosaur bones have been
identified, four of which show egg concentra-
tions in a vertical distance of 1.4 m. This sedi-
mentological data, associated with the exceptional
quantity of eggs and bones, indicate that events of
high energy such as storms have passed over a
nesting site, causing the eggs to be moved inside
the lake where they floated for a short period
of time, becoming concentrated and eventually
buried along with disarticulated skeletons. Our
findings further demonstrate the exceptional con-
ditions necessary for the preservation of such
fragile material and can explain the notable pau-
city of pterosaur eggs and embryos in the pale-
ontological record compared to other reptiles
(25), because the preservation potential of soft-
shelled specimens is regarded as very poor (26).
Furthermore, this occurrence implies colonial
breeding for Hamipterus tianshanensis, as dem-
onstrated by the osteohistological identification
of individuals in different growth stages, a hy-
pothesis speculated for pterosaurs before on the
basis of very limited evidence (7). The large quan-
tities of specimens, and now eggs, indicate that
gregarious behavior might have been widespread
among derived pterosaurs.
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We thank L. Xiang, H.-J. Zhou, and R.-J. Wang [Institute of
Vertebrate Paleontology and Paleoanthropology, Chinese
Academy of Sciences (CAS)] for the preparation of the specimens,
W. Gao for photography, A.-J. Shi for line drawings, and
Y.-M. Hou and P.-F. Yin for help with the CT scan and
reconstruction (IVPP). We are also indebted to Y. Li, L. Xiang,
Q.-G. Liu, R.-J. Wang, H.-J. Zhou, W. Gao, H.-Q. Shou (IVPP),
and G.-L. Wu, B.-L. Guan, H.-M. Wu, Q.-J. Li, H.-Y. Chen,
F. Yan, Y.-L. Tian, Z.-J. Yin, H.-P. Dai, and J. Tong (Hami) for
assistance in the field work. This study was supported by the
National Natural Science Foundation of China (41572020,
41688103, 41602011, 91514302, and 40825005),
the Strategic Priority Research Program (B) of CAS
(XDB18000000), the Hundred Talents Project of CAS, the
Excavation Funding and Emphatic Deployed Project of IVPP,
CAS. T.R. acknowledges funding from the Fundação de
Amparo à Pesquisa e Inovação do Espírito Santo (FAPES no.
67678254) and the Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq no. 460784/2014-5); and
A. W.A.K. from the Fundação Carlos Chagas Filho de Amparo à
Pesquisa do Rio de Janeiro (FAPERJ no. E-26/202.893/2015) and
the Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq no. 304780/2013-8). All specimens
are housed at the Institute of Vertebrate Paleontology and
Paleoanthropology in Beijing, China.
Figs. S1 to S13
Tables S1 to S5
Movies S1 to S3
References (27, 28)
14 March 2017; resubmitted 15 July 2017
Accepted 26 October 2017