Nocturnal giants: evolution of the sensory ecology in elephant birds and other palaeognaths inferred from digital brain reconstructions
Abstract
The
recently extinct Malagasy elephant birds (Palaeognathae,
Aepyornithiformes) included the largest birds that ever lived. Elephant
bird neuroanatomy is understudied but can shed light on the lifestyle of
these enigmatic birds. Palaeoneurological studies can provide clues to
the ecologies and behaviours of extinct birds because avian brain shape
is correlated with neurological function. We digitally reconstruct
endocasts of two elephant bird species, Aepyornis maximus and A. hildebrandti,
and compare them with representatives of all major extant and recently
extinct palaeognath lineages. Among palaeognaths, we find large
olfactory bulbs in taxa generally occupying forested environments where
visual cues used in foraging are likely to be limited. We detected
variation in olfactory bulb size among elephant bird species, possibly
indicating interspecific variation in habitat. Elephant birds exhibited
extremely reduced optic lobes, a condition also observed in the
nocturnal kiwi. Kiwi, the sister taxon of elephant birds, have
effectively replaced their visual systems with hyperdeveloped olfactory,
somatosensory and auditory systems useful for foraging. We interpret
these results as evidence for nocturnality among elephant birds. Vision
was likely deemphasized in the ancestor of elephant birds and kiwi.
These results show a previously unreported trend towards decreased
visual capacity apparently exclusive to flightless, nocturnal taxa
endemic to predator-depauperate islands.
1. Introduction
The
recently extinct Malagasy elephant birds (Palaeognathae,
Aepyornithiformes) included the largest birds ever discovered. Seven
species are recognized across two genera, including the larger,
graviportal Aepyornis and the smaller, gracile Mullerornis [1].
The earliest elephant bird fossils are known from the Pleistocene,
although recent phylogenetic studies using ancient DNA have estimated
that the lineage diverged from its sister taxon, the kiwi, in the
mid-Palaeocene [2,3].
Elephant birds have been proposed to be among the dominant terrestrial
vertebrates on Madagascar prior to the arrival of humans approximately
2000 years ago and had no known predators [4].
No direct data exist regarding elephant bird foraging or activity
patterns but they have generally been considered diurnal herbivores like
the New Zealand moa [4–6].
Little else is known about elephant bird biology, representing a
crucial gap in our understanding of both the evolutionary history of
Palaeognathae and the prehistoric Malagasy ecosystem.
Palaeoneurological
investigation can shed light on elephant bird ecology. Relative
development of external features of the brain correlates with complexity
of associated sensory or cognitive processes, a form–function
relationship useful for reconstructing life-history traits of birds
(e.g. [7–10]).
Palaeognath evolution has been marked by repeated gains of gigantism,
flightlessness, island endemism and crepuscularity/nocturnality. Because
this group is the sister taxon to all other living birds (Neognathae),
investigations of neuroanatomical evolution concomitant with these
repeated patterns hold potential to provide insight to early avian brain
evolution. Accordingly, the palaeognaths are one of the best-studied
bird groups regarding neuroanatomical evolution [6,11–14].
Most attention has been paid to the kiwi, which show extreme
neuroanatomical adaptations to nocturnality, including a highly
developed olfactory bulb and extremely reduced optic lobes [14–17]. By contrast, little attention has been paid to the sister taxon of kiwi, the highly enigmatic elephant birds.
Wiman & Edinger [18]
provided the earliest and only published study of elephant bird brain
shape. They described variation in endocranial anatomy across four
species, including Aepyornis maximus, A. medius, A. hildebrandti and Mullerornis agilis.
The authors noted that the elephant bird olfactory bulbs were large and
the optic lobes were greatly reduced relative to overall brain size
compared to other ratites. Based on these observations, Wiman &
Edinger [18]
predicted that vision was deemphasized in elephant birds in favour of
enhanced olfactory capacity. The authors further noted that optic lobe
development is inversely proportional to body size in elephant birds,
with the largest species (A. maximus) exhibiting the smallest lobes relative to overall brain size; Ohashi et al. [19] confirmed this observation. Although Wiman & Edinger [18]
provided crucial insights into elephant bird brain morphology, the
fidelity of their plaster reconstructions to true brain shape
(especially of the olfactory bulbs) likely suffered when the skulls were
cut during the construction of their endocranial moulds. Also, recent
analyses, some including ancient DNA, provide a new phylogenetic
framework within which to compare palaeognath neuroanatomy. Among these
new insights is the surprising recovery of elephant birds and kiwi as
sister taxa [2,3].
Here, we reinvestigate the neuroanatomy of two elephant bird species, Aepyornis maximus and A. hildebrandti,
using high-resolution X-ray computed tomography (CT). CT is a
non-destructive source of data useful for digitally constructing casts
of the endocranium and associated neurological spaces [8]. First, we redescribe and reinterpret the Aepyornis
brain in an evolutionary framework with emphasis on their closest
living relatives, the kiwi. We then use phylogenetic comparative methods
to investigate the evolution of relative olfactory bulb and optic lobe
size across palaeognaths. Finally, we discuss the new insights these
data provide to the lifestyle of elephant birds on Madagascar and to
palaeognath evolution in general.
2. Methods
(a) Endocast reconstruction and phylogenetic hypothesis
We
used high-resolution X-ray computed tomographic data to reconstruct
digital endocasts for at least one representative of all major extant
and recently extinct palaeognath lineages, including two elephant bird
braincases from the National Museum of Natural History, Paris, France,
(MNHN F 1910-12 and an uncatalogued MNHN specimen). We also
reconstructed the endocasts of a tanager (Passeriformes) and a shorebird
(Charadriiformes) as outgroups of analyses of relative optic lobe size.
Endocasts were reconstructed in Avizo 9 (FEI) following best practices
suggested by Balanoff et al. [20]. Scanning parameters and links to scan data are provided in electronic supplementary material, table S1.
Phylogenetic comparative analyses used the tree and branch lengths from Yonezawa et al. [2] for palaeognaths and from Burleigh et al. [21]
for the rest of Aves. Because the latter study did not include elephant
birds, we grafted the elephant bird–kiwi–cassowary–emu clade, including
branch lengths, from the tree of Yonezawa et al. [2] onto the Burleigh et al. [21]
tree. For each analysis, this tree was then pruned of taxa not included
in our dataset. All tree files used in this study are provided in
electronic supplementary material, tree files 1–4.
(b) Investigating olfactory bulb and optic lobe size among Palaeognathae
To investigate olfactory bulb size evolution across palaeognaths, we compared Bang & Cobb's [22]
olfactory ratio (olfactory bulb length relative to cerebral hemisphere
length, each measured along the longest axis, regardless of orientation)
among our palaeognath sample as well as 88 neognaths taken from Bang
& Cobb [22] and the stem palaeognath Lithornis plebius from Zelenitsky et al. [10]
using phylogenetic generalized least-squares (GLS) regression and by
reconstructing ancestral olfactory ratios. To investigate the
relationships between habitat type and olfactory bulb size among
palaeognaths, we used one-way ANOVA to test for significant differences
in olfactory ratio between open- and forest-dwelling taxa. To
investigate optic lobe size evolution, we reconstructed ancestral ratios
of surface area of a single optic lobe to total brain surface area
among our palaeognath sample with the black-faced grassquit (Tiaris bicolor) and killdeer (Charadrius vociferus, from Smith & Clarke [23]) as neognath outgroups. Measurement data are provided in table 1 and electronic supplementary material, table S2.
Table 1.
Optic lobe, olfactory bulb and brain measurement data for palaeognaths. OLA, optic lobe surface area (cm2); TBA, total brain area (cm2);
OptR, ratio of optic lobe surface area to total brain surface area;
OBL, olfactory bulb length (longest axis regardless of orientation, cm);
CHL, cerebral hemisphere length (longest axis regardless of
orientation, cm); OR, olfactory ratio.
Detailed methods are provided in the electronic supplementary material.
3. Results
(a) Endocast description, comparison and species assignment
Virtual endocasts of two elephant bird specimens revealed interspecific variation in Aepyornis
neuroanatomy. Relative to overall brain size, the larger MNHN F 1910-12
exhibits larger olfactory bulbs, cerebellum and pituitary fossa, as
well as smaller optic lobes; they also differ with respect to
telencephalon shape, most obviously in dorsal and ventral views (figure 1;
electronic supplementary material, figure S1). Taphonomic damage to the
skull roof of the uncatalogued MNHN specimen prevents reconstruction of
the dorsal part of the endocast and hinders volumetric comparison. The
optic lobes in both elephant birds are extremely reduced compared to
most other birds (figure 1);
in MNHN F 1910-12, they are obsolete as in kiwi, and in the
uncatalogued MNHN specimen, they are barely present as in heavy-footed
moa (figure 1;
electronic supplementary material, figures S1 and S2). MNHN F 1910-12
and the uncatalogued MNHN specimen most resemble Wiman and Edinger's [18] cerebrotypes for A. maximus and A. hildebrandti,
respectively, with respect to shape and relative size of the olfactory
bulb, cerebral hemispheres, pituitary and optic lobes. These species
assignments are used for all subsequent interpretations and discussion.
Figure 1.
Digital endocranial reconstructions of (a,b) elephant bird Aepyornis maximus (MNHN F 1910-12), (c,d) elephant bird Aepyornis hildebrandti, (e,f) kiwi, (g,h) greater rhea, (i,j) the open-dwelling Chilean tinamou and (k,l) the forest-dwelling brown tinamou in (a,c,e,g,i,k) ventral and (b,d,f,h,j,l)
left lateral views. Optic lobes are highlighted by dashed lines.
Colours: blue, brain; green, inner ear; red, vasculature; yellow,
cranial nerves. Abbreviations: I, olfactory nerve; II, optic nerve; III,
oculomotor nerve; IV, trochlear nerve; V, trigeminal nerve; VI,
abducens nerve; VII–VIII, facial and vestibulocochlear nerves; IX–XI,
glossopharyngeal, vagus and accessory nerves; XII, hypoglossal nerve;
ca, carotid artery; ce, cerebellum; ff, floccular fossa; ioa, internal
ophthalmic artery; ob, olfactory bulb; ol, optic lobe (red dashed
outline); pf, pituitary fossa; te, telencephalon; va, vallecula; ve,
vestibular organs; w, wulst. Scale bars = 1 cm.
(b) Olfactory bulb size and habitat
Phylogenetic
GLS of olfactory bulb length versus cerebral hemisphere length
recovered a positive relationship among both palaeognaths and neognaths,
as well as all birds combined (figure 2;
electronic supplementary material, results and figure S4).
Reconstruction of ancestral olfactory bulb ratios revealed that small
olfactory bulbs relative to the cerebral hemispheres are typical among
birds and are ancestral for Palaeognathae (figure 3;
electronic supplementary material, figures S5–S6 and tables S3–S4).
Large olfactory bulbs originated independently in the clade containing
elephant birds, kiwi, southern cassowary and emu, as well as among
tinamous (figure 3; electronic supplementary material, figures S5–S6). Reconstruction with elephant birds represented by A. maximus rather than A. hildebrandti indicated that the former species retained the large olfactory ratio exhibited by the ancestor it shared with kiwi (figure 3; electronic supplementary material, figure S5). However, reconstruction including A. hildebrandti rather than A. maximus
indicated that the former species exhibited a secondarily small
olfactory ratio (electronic supplementary material, figure S6). Both
phylogenetic and non-phylogenetic ANOVA revealed a significant
difference in olfactory ratio between open- and forest-dwelling
palaeognaths, regardless of whether A. hildebrandti was treated
as occupying grasslands or forests (electronic supplementary material,
table S5). Specifically, taxa with large olfactory bulbs occupy forested
habitat while those with small bulbs occupy open habitat, except for
the emu (figure 2).
Emus are diurnal omnivores and occupy open Australian grasslands,
despite exhibiting large olfactory bulbs more consistent with a forested
habitat. However, large bulbs are exhibited by the closest relatives of
emus and are estimated here as ancestral for this group (figure 2;
electronic supplementary material, figure S7), suggesting that emus
evolved under different foraging conditions than they experience today.
The emu lineage is estimated to have first arisen in the Oligocene when
Australia was more densely forested than at present [2,24–26]. The most basal divergence within tinamous separates the extant species into generally forest-dwelling and open-area clades [27].
Correspondingly, our sample of tinamous with large bulbs primarily
occupies forested habitat and tinamous with small bulbs primarily occupy
open habitat (figures 1 and 2).
The earliest fossil tinamous are nested within extant clades but
occurred at a time when subtropical forests that then characterized
southern South America were transitioning into more modern, open
environments [27–30]. Thus, it is likely the ancestor of extant tinamous occupied forested rather than open habitat [27]. The heavy-footed moa (Pachyornis elephantopus)
exhibits a relatively small olfactory bulb, consistent with an open
habitat. Indeed, investigation of DNA recovered from plants in
coprolites of four moa species including heavy-footed moa predicted that
this species had a diet comprising herbaceous rather than woody plants [31,32].
However, habitat varied across moa species with some occupying
primarily forested environments and so it is uncertain which habitat
type was ancestral for moa [31–33].
Figure 2.
GLS
regressions of olfactory ratio (olfactory bulb size versus cerebrum
size) for palaeognaths (solid) and neognaths (dashed). Neognath data
from Bang and Cobb [22]. Lithornis plebius data from Zelenitsky et al. [10].
Colour legend: orange, elephant birds; red, kiwi; yellow, cassowary;
pink, emu; purple, moa; cyan, tinamous; green, rhea; tan, ostrich; blue,
lithornithid; white, neognaths.
Figure 3.
Evolution
of the sensory ecology of elephant birds and other palaeognaths showing
transitions in daily activity patterns (inferred from reconstructions
of ancestral relative optic lobe size) and foraging habitat (inferred
from reconstructions of ancestral relative olfactory bulb size). Diurnal
activity patterns were ancestral for palaeognaths, followed by
transition to crepuscularity independently in elephant birds/kiwi, in
cassowaries and possibly in some moa. Within the elephant bird–kiwi
clade, nocturnality arose independently in the largest elephant birds (Aepyornis)
and in kiwi. Open habitat (e.g. grass- and shrubland) was likely
ancestral for palaeognaths, followed by transition to forested habitat
in the clade including elephant birds, kiwi, cassowaries and emus. Emus
likely subsequently transitioned back to open habitat as Australia
became deforested leading up to the present. Forested habitat was likely
ancestral for tinamous followed by transition back to open habitat in
the clade containing the Chilean and red-winged tinamous. Although the
heavy-footed moa likely occupied open habitat, other moa taxa occupied
forested habitat and it is unclear if open or forested habitat was
ancestral for moa. Optic lobe size ancestral state reconstruction (upper
tree) is based on electronic supplementary material, figure S7.
Olfactory bulb size ancestral state reconstruction (lower tree) is based
on electronic supplementary material, figure S5.
(c) Optic lobe size
Reconstruction
of ancestral optic lobe/total brain surface area ratios for
palaeognaths and two neognath outgroups recovered moderately sized (i.e.
emu-sized) optic lobes as ancestral for both the avian crown clade and
Palaeognathae (figure 3;
electronic supplementary material, figure S7 and table S6). Marked
shifts in relative optic lobe size include an increase within tinamous
and extreme reduction independently in the elephant bird-kiwi clade
(followed by further reduction in each lineage) and in the heavy-footed
moa. Because our study sampled only a single moa taxon, it is unclear
when reduction occurred among moa.
4. Discussion
Reconstruction of the neuroanatomy of two elephant bird species, Aepyornis maximus and A. hildebrandti, using high-resolution CT, reveals these birds possessed extremely reduced (and apparently obsolete) optic lobes (figure 1), consistent with previous observations based on both physical and digital endocasts [18,19]. Optic lobes are an external feature of the brain corresponding to the optic tectum [9],
which is an internal brain region with many sensory and cognitive
functions including its role in the tectofugal visual pathway, the
dominant of the two major visual pathways in birds (e.g. [34,35]).
Among extant birds, extreme reduction of the optic lobes is observed
only in nocturnal flightless birds like the parrot kakapo and especially
kiwi (figure 1) [14,36].
In kiwi, reduction of the optic lobes corresponds to reduction of the
component layers of the tectum and thus reduction of the tectofugal
visual pathway [14]. This correlation is consistent with Jerison's [7]
principle of proper mass, which predicts that relative development of a
brain region corresponds to complexity of associated behaviours. If
this correspondence of structural and neurological reduction is also
true for elephant birds, the sister taxon to kiwi, then they likely also
possessed markedly reduced visual systems and were nocturnal. If
additional investigation further supports this hypothesis, it would
represent an ironic twist in the evolutionary story of a bird referred
to in local Malagasy folklore as vorombazoho, or ‘the bird with keen vision’ [37].
The
elephant bird–kiwi clade shows ancestral reduction of the visual
system, with extreme reduction of the optic lobes occurring
independently in a single clade of elephant birds (Aepyornis) and in kiwi (figure 3). Mullerornis was the other, more gracile clade of elephant birds and also exhibited reduced optic lobes (figure 1) [18], though they were relatively larger than in Aepyornis and kiwi, and closer in size to the kakapo [36]. Although the optic lobes of Aepyornis
and kiwi are of similar relative size, kiwi exhibit a suite of
additional neuroanatomical and cranial correlates to reduced vision that
are not observed in elephant birds, including reduced orbits (and
correspondingly reduced eyes) and a wulst that is virtually absent [14].
The wulst is a uniquely avian dorsal projection of the telencephalon
and serves as the endpoint of the thalamofugal visual pathway, the
lesser of the two major visual pathways in birds [38]. The kiwi visual system has been effectively replaced by sophisticated olfactory [14], somatosensory [39] and auditory [15] systems so completely that blindness has been observed in wild populations of kiwi with no apparent impact on fitness [40].
Elephant birds possessed orbits and wulsts like other palaeognaths,
indicating that they may not have been as specialized to nocturnality as
kiwi. Despite almost complete loss of their visual systems, the eyes of
kiwi are rod-dominated [41],
optimizing visual ability in low light, a condition suggested to be
remnant of a crepuscular or nocturnal ancestor that relied more heavily
on vision [40]; we propose that this crepuscular/nocturnal ancestor was that ancestor shared with elephant birds.
Reduction
of vision among birds is an adaptation likely available only to
flightless species on predator-depauperate islands. The avian visual
system has been proposed to respond to transition to a nocturnal
lifestyle either by increased sensitivity or by reduction in favour of
other senses [14].
Increased sensitivity characterizes flighted nocturnal birds (e.g.
owls, oilbirds, nightjars), which exhibit specializations to manoeuvring
and foraging in low-light conditions including rod-dominated retinae,
large eyes and hyperdeveloped wulsts [42].
Only flightless nocturnal birds on islands are known to reduce the
visual system in favour of other senses, including the elephant birds of
Madagascar and the kiwi, kakapo and possibly moa of New Zealand [14,18,36] (figure 3;
electronic supplementary material, figures S1–2, S7–8). Reduced visual
capacity or blindness has evolved within many non-avian terrestrial
vertebrate groups [43–48];
however, only among birds is reduced vision linked to changes in
locomotor strategy (i.e. loss of flight). Because birds must navigate a
three-dimensional environment when flying, flying ability should greatly
influence whether a lineage of nocturnal birds optimizes sensitivity or
forgoes vision. It is thus likely that deemphasis of the visual system
is an evolutionary pathway available only to flightless taxa, like
elephant birds and kiwi. Indeed, the recently extinct Hawaiian waterfowl
Talpanas lippa is hypothesized to have been both flightless
and nocturnal based on its extremely reduced visual system as well as
hindlimb proportions, possibly further supporting this pattern [49]. The rod-dominated eyes of kiwi suggest that reduction of vision followed an initial stage of increased sensitivity [44].
Thus, increased sensitivity to low light and reduced visual capacity
may represent an evolutionary sequence rather than alternative nocturnal
strategies.
Though sister taxa, the tinamous and moa
included in our study show markedly different trajectories with respect
to relative optic lobe size (figure 3). The heavy-footed moa exhibited reduced optic lobes, on par with the kakapo and Mullerornis and consistent with nocturnal or crepuscular activity. Ashwell & Scofield [6]
investigated the palaeoneuroanatomy of eight moa species, including the
heavy-footed moa, and predicted a diurnal activity pattern based on
relatively small olfactory bulbs and a well-developed wulst. However,
the nocturnal kakapo exhibits a well-developed wulst [36].
Our findings suggest that small olfactory bulbs may be more related to
foraging in an open habitat than with activity pattern (figures 2 and 3).
Whether optic lobe reduction is unique to the heavy-footed moa or if it
is indicative of an ancestral condition is unclear. Ashwell &
Scofield [6]
reported that moa optic lobes are generally relatively smaller than in
other ratites, and so it is possible that reduced visual capacity, and
possibly nocturnality, is ancestral for the moa total group or arises
within moa. Robust taxonomic sampling within moa is needed to further
test this hypothesis. Tinamous, in contrast with moas, exhibit large
optic lobes compared with total brain size reconstructed as an increase
within the clade relative to outgroups. The biological significance of
this apparent increase in relative optic lobe size is unclear, though it
is not directly related to habitat type, as both open- and
forest-dwelling tinamous exhibit relatively large lobes. Though
comparatively little attention has been paid to the sensory systems in
tinamous, our results suggest that such investigation may uncover
previously unrecognized specialization in the tinamou visual system.
Palaeognaths exhibit a relationship between habitat and relative olfactory bulb size (figures 2 and 3).
Like the optic lobes, the olfactory bulbs are known to follow the
principle of proper mass, with relative size corresponding to olfactory
ability in birds [50,51].
Large olfactory bulbs are observed in birds that forage under
conditions where visual cues are limited (e.g. in low light or at sea) [14,52,53].
Except for emus, extant palaeognaths with large olfactory bulbs occupy
forested habitats, where visual cues are expected to be limited and
emphasis on olfaction would be favoured. Lithornithidae, an extinct
clade of flighted stem palaeognaths [54,55], also show markedly well-developed olfactory bulbs [10], consistent with the forested habitats inferred for them in the Palaeocene–Eocene of Europe and North America [56].
Palaeognaths with relatively small olfactory bulbs generally occupy
open habitats (e.g. grass- or shrubland). Palaeognaths also exhibit
larger olfactory bulbs relative to cerebral hemisphere than neognaths,
although neognaths show a similar relationship (figure 2; electronic supplementary material, figures S5 and S6). Zelenitsky et al. [10]
observed that olfactory ratios increase relative to body size
throughout the early evolution of both palaeognaths and neognaths. Our
results suggest that the rate of this increase was higher at the base of
palaeognaths than of neognaths, followed by smaller-scale increases in
olfactory ratio in those lineages that shifted to forested habitats.
Our study identified species-level variation in olfactory bulb size among elephant birds (figures 1 and 3; electronic supplementary material, figures S1, S5 and S6). Aepyornis maximus
retained relatively large olfactory bulbs ancestral of the larger
elephant bird–kiwi–cassowary–emu clade, consistent with previous
inferences of a forested habitat for elephant birds based on proposed
foraging strategy and diet [57,58].
Also, much of the known elephant bird range has been proposed to be
densely wooded, with the grasslands replacing woodlands only recently
due to human activity [37,59].
The current paucity of elephant bird remains from the forested eastern
coast of Madagascar may represent a lack of conditions suitable to
subfossil preservation rather than a restriction of elephant bird range.
Aepyornis hildebrandti, in contrast with A. maximus,
exhibited secondarily reduced olfactory bulbs, more consistent with an
open than a forested habitat (electronic supplementary material, figure
S6). These species-level differences in olfactory bulb size, combined
with differences in optic lobe size observed between species and genera
(i.e. Aepyornis versus Mullerornis), may be due to resource/niche partitioning among elephant bird species, with some (e.g. A. maximus) retaining the ancestral nocturnal, forest-dwelling life history while others (e.g. A. hildebrandti, Mullerornis)
possibly became better adapted to a grasslands habitat and more
crepuscular than nocturnal activity patterns. These results suggest that
elephant bird ecology was more complex than previously recognized.
Currently, elephant bird species diversity is poorly understood, with
many species definitions relying solely on differences in size. Finer
understanding of variation in elephant bird ecology will largely depend
on reassessment of these species differences.
Data accessibility
Digital data used in this study are available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.7519042 [60]. All other data are available in the electronic supplementary material.
Authors' contributions
C.R.T.
participated in design of the study, processed digital data, carried
out statistical analyses and drafted the manuscript. J.A.C. conceived
of, participated in design of and funded the study. Both authors gave
final approval for publication.
Competing interests
We have no competing interests.
Funding
Funding from the US National Science Foundation supported this research (NSF EAR 1355282 to J.A.C.).
Acknowledgements
We
thank R. Allain (MNHN) for specimen access and help; R. David (Max
Planck Institute for Evolutionary Anthropology) for assistance CT
scanning MNHN F 1910-12 and MNHN 1875-602; M. Colbert and J. Maisano
(UTCT) for assistance with CT scanning the uncatalogued Aepyornis specimen, Crypturellus, Tinamus and Rhynchotus;
and Z. Li (Institute of Vertebrate Paleontology and Paleoanthropology,
China) for access to all remaining CT scans. We thank D. Cannatella
(University of Texas at Austin [UT]), N. Crouch (UT), S. Davis (UT), C.
Early (University of Ohio), S. English (UT), D. Hillis (UT), S. Hood
(UT), D. Ksepka (Bruce Museum), R. MacPhee (American Museum of Natural
History), G. Musser (UT), J. Proffitt (UT), T. Worthy (Flinders
University) and H. Zakon (UT) for comments and discussion and K.
Rosenbach (University of Michigan) for inspiration for the title. We
thank two anonymous referees for comments that proved invaluable to
improving this report.
Footnotes
- Electronic supplementary material is available online at http://dx.doi.org/10.6084/m9.figshare.c.4274219.
- Received July 20, 2018.
- Accepted October 10, 2018.
- © 2018 The Author(s)
http://royalsocietypublishing.org/licence
Published by the Royal Society. All rights reserved.
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