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The wings before the bird: an evaluation of
flapping-based locomotory hypotheses in
bird antecedents
T. Alexander Dececchi
1
, Hans C.E. Larsson
2
and Michael B. Habib
3,4
1Department of Geological Sciences, Queens University, Kingston, Ontario, Canada
2Redpath Museum, McGill University, Montreal, Quebec, Canada
3Keck School of Medicine of USC, Department of Cell and Neurobiology, University of Southern
California, Los Angeles, California, United States
4Dinosaur Institute, Natural History Museum of Los Angeles, Los Angeles, CA, United States
ABSTRACT
Background: Powered flight is implicated as a major driver for the success of birds.
Here we examine the effectiveness of three hypothesized pathways for the evolution
of the flight stroke, the forelimb motion that powers aerial locomotion, in a
terrestrial setting across a range of stem and basal avians: flap running, Wing
Assisted Incline Running (WAIR), and wing-assisted leaping.
Methods: Using biomechanical mathematical models based on known aerodynamic
principals and in vivo experiments and ground truthed using extant avians we seek
to test if an incipient flight stroke may have contributed sufficient force to permit
flap running, WAIR, or leaping takeoff along the phylogenetic lineage from
Coelurosauria to birds.
Results: None of these behaviours were found to meet the biomechanical threshold
requirements before Paraves. Neither was there a continuous trend of refinement
for any of these biomechanical performances across phylogeny nor a signal of
universal applicability near the origin of birds. None of these flap-based locomotory
models appear to have been a major influence on pre-flight character acquisition
such as pennaceous feathers, suggesting non-locomotory behaviours, and less
stringent locomotory behaviours such as balancing and braking, played a role in
the evolution of the maniraptoran wing and nascent flight stroke. We find no
support for widespread prevalence of WAIR in non-avian theropods, but can’t
reject its presence in large winged, small-bodied taxa like Microraptor and
Archaeopteryx.
Discussion: Using our first principles approach we find that “near flight” locomotor
behaviors are most sensitive to wing area, and that non-locomotory related selection
regimes likely expanded wing area well before WAIR and other such behaviors
were possible in derived avians. These results suggest that investigations of the
drivers for wing expansion and feather elongation in theropods need not be
intrinsically linked to locomotory adaptations, and this separation is critical for our
understanding of the origin of powered flight and avian evolution.
Subjects Evolutionary Studies, Paleontology
Keywords Flight, WAIR, Maniraptora, Macroevolution, Theropoda, Flap running, Flight stroke
How to cite this article Dececchi et al. (2016), The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird
antecedents. PeerJ 4:e2159; DOI 10.7717/peerj.2159
Submitted 23 January 2016
Accepted 27 May 2016
Published 7 July 2016
Corresponding author
T. Alexander Dececchi,
td50@queensu.ca
Academic editor
Andrew Farke
Additional Information and
Declarations can be found on
page 31
DOI 10.7717/peerj.2159
Copyright
2016 Dececchi et al.
Distributed under
Creative Commons CC-BY 4.0
INTRODUCTION
Evolution of powered flight in vertebrates was a key innovation that spurred the
evolutionary success of birds, bats, and pterosaurs (Sears et al., 2006;Butler et al., 2009;
Benson & Choiniere, 2013). Of the three radiations, the theropod to bird transition has
garnered the most interest and scholarship due to the higher quality of the fossil record
documenting the origin and refinement of their flight including: the evolution of feathers,
reduced body size, an avian-like physiology and respiration, elongate forelimbs, and
modifications of the pectoral and forelimb musculoskeletal system (Baier, Gatesy &
Jenkins, 2007;Codd et al., 2008;Dececchi & Larsson, 2009;Dececchi & Larsson, 2013;
Makovicky & Zanno, 2011;Benson & Choiniere, 2013;Brusatte et al., 2014;Xu et al., 2014).
Despite the wealth of fossil evidence documenting this transition deducing the origin and
subsequent evolution of the flight stroke, a biomechanical innovation that permitted
aerial locomotion, remains elusive.
The flight stroke of extant birds traces a complex ellipsoidal path that is controlled by
derived muscle origins and insertions and modified shoulder, elbow, and wrist joints and
ligaments (Gatesy & Baier, 2005). Many antecedent functions of the flight stroke have
been proposed. These include a raptorial function of the forelimbs for fast prey capture
(Ostrom, 1974), behavioural precursors such as courtship, balance, or warning displays
(Fowler et al., 2011;Foth, Tischlinger & Rauhut, 2014), as well as locomotory functions
(Caple, Balda & Willis, 1983;Dial, 2003;Chatterjee & Templin, 2007).
Powered flight differs from gliding flight in that it uses active flapping to generate
thrust. Some models of the origin of avian flight propose antecedents living in trees and
deriving the flight stroke from a parachuting or gliding stage (Chatterjee & Templin, 2004;
Alexander et al., 2010;Dyke et al., 2013) based primarily on the observation that many
modern arboreal tetrapods perform similar behaviors (Dudley et al., 2007;Evangelista
et al., 2014). Yet nearly all stem avians have hindlimb morphologies that compare most
closely to extant cursorial tetrapods (Dececchi & Larsson, 2011) and a multivariate analysis
of limb element lengths recovered the earliest birds as most similar to extant terrestrial
foragers (Bell & Chiappe, 2011;Mitchell & Makovicky, 2014). The only theropod taxa that
may diverge from this are Scansoriopterygidae, a clade known from four small,
fragmentary specimens, but presenting intriguing and radically divergent morphologies
from other maniraptoran theropods. Notably, when preserved, they possess large pedal
and manual phalangeal indices, a reduced crural index, a reduced hindlimb length, and
reduced limb integument not seen in avian antecedents, including paravians (Glen &
Bennett, 2007;Bell & Chiappe, 2011;Dececchi & Larsson, 2011;Dececchi, Larsson & Hone,
2012). One scansoriopterygid may even possess a skin patagium that may have functioned
as an airfoil (Xu et al., 2015). These putative gliding structures are extremely divergent
from other theropods and likely represent a convergent pathway to becoming volant.
Of all the models for the origin of the flight stroke from a terrestrial life history two
major categories exist: those that have locomotory functional aspect are flap running
(Burgers & Chiappe, 1999), wing assisted incline running or WAIR (Dial, 2003), and
vertical leaping (Caple, Balda & Willis, 1983). Behaviors in the second category are
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 2/41
non-locomotory behaviors, such as balancing during prey capture (Fowler et al., 2011)
and braking during high-speed turns (Schaller, 2008). The three stringent locomotory
behaviours (WAIR, flap running and vertical leaping) are variations on a proto-flight
stroke assisting in force generation to increase ground and launch velocities (Burgers &
Chiappe, 1999) or to assist in ascending steep inclines to facilitate escape to elevated
refuges such as into trees or up inclined rock faces (Dial, 2003). All three are present
throughout much of extant bird diversity and have been areas of research into the possible
pathways for the origins of powered flight.
WAIR is a behaviour observed primarily as a means of predator escape, especially in
pre-flight capable juveniles (Tobalske & Dial, 2007;Dial, Jackson & Segre, 2008;Jackson,
Segre & Dial, 2009;Heers & Dial, 2012;Heers, Dial & Tobalske, 2014). This has been
suggested to provide a series of functional and morphological stages using immature age
classes of extant individuals as proxies for transitional evolutionary stages from basal
coelurosaurs to volant birds (Dial, Randall & Dial, 2006;Heers & Dial, 2012). This has
been most thoroughly studied in the Chukar partridge (Alectornis chukar, hereafter
referred to as Chukars), though work has been done in other extant birds such as the
Brush Turkey (Alectura lathami) and Peafowl (Pavo cristatus)(Heers & Dial, 2015). At
the earliest juvenile stages Chukars (0–5 days post hatching [dph] and < 20 g) either crawl
or asymmetrically flap their wings to produce forces of approximately 6–10% of their
body weight (Jackson, Segre & Dial, 2009;Heers, Tobalske & Dial, 2011;Heers, Dial &
Tobalske, 2014) to ascend inclines of less than 65, slightly greater than the level that
they can ascend using their legs alone (55–60)(Bundle & Dial, 2003;Dial, Randall &
Dial, 2006). At these low angles, the primary locomotory forces are generated from the
hindlimbs but this changes when higher angles are attempted (Bundle & Dial, 2003).
To ascend to sub vertical angles, juvenile and older individuals must produce forces
equaling a minimum of 50% of their body weight (Dial & Jackson, 2011). Larger birds
with masses greater than 0.8 kg such as adult Brush Turkeys or Peafowl struggle to WAIR
at this level (Dial & Jackson, 2011;Heers & Dial, 2015). Low angle WAIR has been
hypothesized to be present throughout Coelurosauria and sub vertical WAIR minimally
at Paraves (Dial, 2003;Heers & Dial, 2012;Heers, Dial & Tobalske, 2014).
Vertical leaping (both from the ground and perches) begins as an effectively ballistic
process in flying animals, initiated by the hindlimbs in birds (Heppner & Anderson, 1985;
Bonser & Rayner, 1996;Earls, 2000;Tobalske, Altshuler & Powers, 2004), bats (Schutt et al.,
1997;Gardiner & Nudds, 2011), and insects (Nachtigall & Wilson, 1967;Nachtigall, 1968;
Nachtigall, 1978;Schouest, Anderson & Miller, 1986;Trimarchi & Schneiderman, 1995;
Dudley, 2002). Immediately after the ballistic phase is initiated, the wings are engaged for
the climb out phase of launch. Leaping takeoffs are common among small to medium
sized birds (Provini et al., 2012) but are also present in many larger birds including
Turkeys (Tobalske & Dial, 2000), Peafowl (Askew, 2014), Tinamou (Silveira et al., 2001)as
well as herons, storks, eagles, and vultures) (TA Dececchi and MB Habib, 2015, personal
observations). The largest living flying birds, Kori bustards, are documented to use a
very short run before launch (Prozesky, 1970), though large captive specimens have
demonstrated a true leaping takeoff, as well (MB Habib, 2014, personal observations).
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 3/41
Caple, Balda & Willis (1983) proposed as a model for the origin of flight in birds,
especially in smaller taxa. Flap-running is used in some extant birds, especially semi
aquatic species, to accelerate to takeoff speeds whether starting from a water or land
launch (though mostly associated with compliant surfaces, e.g. water–see Earls, 2000).
Here we present biomechanical models to test when and if a flight stroke may have
contributed to flap running, WAIR, or leaping takeoff along the phylogenetic lineage from
Coelurosauria to birds and if these models coincide with the evolution of pennaceous
feathers and musculoskeletal adaptations for flight. Our goal is to take evolutionary
narratives about pathways to flight origins and evaluate them using quantitative,
mechanical models derived from living birds. Although feathery integument is likely to
have been a synapomorphy for all dinosaurs and perhaps even all ornithodirans (Godefroit
et al., 2014 but see Barrett, Evans & Campione, 2015), the evolution of pennaceous
forelimb and hindlimb feathers has been hypothesized to have been driven by selection
for locomotion (Burgers & Chiappe, 1999;Xu et al., 2003;Dial, Randall & Dial, 2006;Heers,
Tobalske & Dial, 2011). Thus we set up a testing regime to determine if non-avian
theropods could produce biomechanical values that fit within the realms of those measured
in modern animals exhibiting these behaviors, and if is there a decoupling of the timing of
the success in these behaviours from the origin of previous proposed flight related traits.
MATERIALS AND METHODS
Due to uncertainty regarding soft tissues in fossil organisms, some variables were treated
as constants in the taxa modeled and based on values for extant birds. These include
feather material properties, arrangement and muscle power. Using these values provided
conservative estimates in the sense that they would yield more capable performances
for taxa that may lie near biomechanical thresholds. Wing feather arrangements for
some fossils appear to be similar to modern birds (Elz
˙anowski, 2002;Xu et al., 2003;
Foth, Tischlinger & Rauhut, 2014) though for some taxa this has been disputed (Xu,
Zheng & You, 2010;Longrich et al., 2012).
A greater source of uncertainty and debate is fraction of forelimb muscle mass that
is due to the M. pectoralis and its potential power output. Extant birds have extremely
large wing muscles, as a proportion to their bodyweight (Marden, 1987). The mass of
M. pectoralis for birds’ ranges between 10–20% of total body mass (Greenewalt, 1975;
Askew, Marsh & Ellington, 2001), and total flight muscle fractions for birds can reach 40%
(Hartman, 1961;Greenewalt, 1962). This is significantly larger than that estimated in non-
avian theropods or early birds. For example, Archaeopteryx’s pectoral muscles are
estimated at only 0.5% of its body mass (Bock, 2013) with the entire forelimb (including
bone and all other tissues) at 11–14% (Allen et al., 2013). For our analysis, we calculated
values for power available from the forelimb and hindlimb based on the assumption
that non-avian theropods had forelimb muscle mass fractions of 10% their total mass and
that hindlimb muscle mass fractions were 30% of total mass. These values are likely
significant overestimations for non-paravians pectoral regions, but the pelvic region
values are within the range previous estimated for non-avian maniraptorans (Allen et al.,
2013), whose estimates do not include the M. caudofemoralis. The pectoral muscle values
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 4/41
we assigned are similar to estimates of pectoral region mass in Microraptor and
Archaeopteryx, though those estimates are based on the entire pectoral region tissues
(except feathers) and thus the relative mass of the pectoral musculature is likely smaller.
Yet power and muscle mass may not be the main determinant for the use of wings as
locomotory structures. Jackson, Tobalske & Dial (2011) estimated that pigeons, with
approximately 20% of their body mass as pectoralis muscles, only used approximately
10% of their mass-specific power for low angle WAIR. Further, it has been suggested that
power output itself may not determine flight ability, but lift to power ratio (Marden,
1987). For this analysis we have assumed extant bird power productions and metabolic
capacities for short “burst” activities for non-avian theropods and early birds. Although
paravian metabolism was not at the levels seen in extant birds, it was sufficient to perform
short burst activities (Erickson et al., 2009). Regardless, as our methodology uses wing-
beat frequency in conjunction with body size and wing arc measures to generate a lift
production value, we are not dependent on either theory (power or lift force) to produce
meaningful results.
Taxonomic sampling
Forty-five specimens representing twenty-four non-avian theropod taxa and five avian
taxa were examined. Non-avian theropod specimens ranged in mass from approximately
60 g to 18 kg (Tables 1 and S1). Of these, twenty-eight are from specimens accounting for
twelve non-avian theropod taxa with preserved feather material, the rest are from closely
related taxa that are inferred to be feathered and were included to broaden the scope of
the maniraptorans represented. We a priori excluded the tyrannosaurids Yutyrannus,
because of its large size (estimated mass ∼1,400 kg), and Dilong, due to its incompletely
preserved forelimb. Multiple individuals were included for Anchiornis,Similicaudipteryx,
Caudipteryx,Microraptor,Sinosauropteryx,Mei,Archaeopteryx,Jeholornis, and Sapeornis to
represent different size classes and ontogenetic stages as different stages in ontogeny may
have different life history strategies (Parsons & Parsons, 2015). To address the possibility
of WAIR in juvenile but not adult members of Pennaraptora, three late stage embryos:
MOR 246-1 Troodon formosus per Varricchio, Horner & Jackson (2002), MPC-D100/971.
Citipati osmolskea and MPC-D100/1018 Oviraptor incertae sedis per Lu
¨et al. (2013)
were included in this analysis. These specimens are incomplete, but forelimb lengths could
be estimated based on the fact that the humerus/forelimb ratio in non-avian and basal
avian theropods does not change significantly across ontogeny (Table S2). We used the
value of ∼43% MOR 246-1 based on the ratios seen in other Troodontids (range between
39–45%) based on Mei,Jinfengopteryx,Anchiornis,Aurornis,Sinovenator,Sinornithoides
and Xiaotingia. For MPC-D100/971 and MPC-D100/1018 we used 41% based on Citipati.
For all late stage embryos we reconstructed wing area as if they possessed wings with
pennaceous feathering proportional to that seen in adults. This is likely an overestimation,
as hatchling and young juveniles in other non-avian theropods do not show pennaceous
development to the extent of adults (Xu et al., 2009,Zelenitsky et al., 2012).
Mass estimations for non-avian theropods were based on values for femur length
(Christiansen & Farin
˜a, 2004) except for Yixianosaurus, which has no preserved
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 5/41
Table 1 Fossil taxa examined in this study. Taxa in bold were specimens without preserved forelimb remegies for whom feather lengths were
estimated based on closely related taxa or other members of the same genus. For Jianchangosaurus we based our estimate on the longest preserved
body feather traces, this is defensible as this clade is not know to have pennaceous remegies (Foth, Tischlinger & Rauhut, 2014) and in other
maniraptorans without remegies the integument on the distal cervicals are similar in size, if not longer, than those on the forelimbs (Currie & Chen,
2001). CF indicates mass estimated based on Christiansen & Farin
˜a (2004), Liu indicates avian mass estimates based on Liu, Zhou & Zhang (2012),
Fe for avian mass estimates based on Field et al. (2013). See text for discussion of body mass calculations and wing beat frequencies.
Taxa Reference Wing length
(m)
Span
(m)
Mass
(kg) CF
Mass
(kg) Liu
Mass
(kg) FE
Wing Area
(m
^
2)
Wing
loading
N/M
2
Anchiornis Li et al. (2010) 0.16 0.33 0.09 – – 0.01 70
Anchiornis Sullivan et al. (2010) 0.24 0.50 0.38 – – 0.03 146
Archaeopteryx Foth, Tischlinger & Rauhut (2014) 0.31 0.65 –0.24 –0.06 38
Archaeopteryx Foth, Tischlinger & Rauhut (2014) 0.31 0.65 – – 0.36 0.06 57
Archaeopteryx Mayr et al. (2007) 0.29 0.61 –0.23 –0.06 38
Archaeopteryx Mayr et al. (2007) 0.29 0.61 – – 0.32 0.06 55
Archaeopteryx Elz
˙anowski (2002) 0.33 0.69 –0.31 –0.07 45
Archaeopteryx Elz
˙anowski (2002) 0.33 0.69 – – 0.48 0.07 70
Archaeopteryx Mayr et al. (2007),Nudds &
Dyke (2010)
0.26 0.55 –0.18 –0.05 38
Archaeopteryx Mayr et al. (2007),
Nudds & Dyke (2010)
0.26 0.55 – – 0.25 0.05 53
Archaeopteryx Mayr et al. (2007) 0.27 0.57 –0.19 –0.05 36
Archaeopteryx Mayr et al. (2007) 0.27 0.57 – – 0.27 0.05 51
Archaeopteryx
@
Mayr et al. (2007) 0.19 0.39 –0.11 –0.02 47
Archaeopteryx
@
Mayr et al. (2007) 0.19 0.39 – – 0.14 0.02 60
Aurornis
*
Godefroit et al. (2013) 0.22 0.47 0.38 – – 0.02 160
Caudipteryx Zhou & Wang (2000) 0.35 0.72 5.52 – – 0.09 631
Caudipteryx Sullivan et al. (2010) 0.28 0.58 3.77 – – 0.04 863
Changyuraptor
#
Han et al. (2014) 0.68 1.42 5.64 – – 0.43 130
Citipati MPC-D100/971 Lu
¨et al. (2013) 0.11 0.22 0.05 0.00 397
Confuciusornis Chiappe et al. (1999) 0.32 0.67 –0.14 –0.09 15
Confuciusornis Chiappe et al. (1999) 0.32 0.67 – – 0.19 0.09 20
Eoconfuciusornis Sullivan et al. (2010) 0.22 0.46 –0.09 –0.04 24
Eoconfuciusornis Sullivan et al. (2010) 0.22 0.46 – – 0.12 0.04 30
Eosinopteryx Godefroit et al. (2013) 0.16 0.33 0.14 – – 0.01 111
Jeholornis Ji et al. (2002) 0.41 0.86 –0.34 –0.12 29
Jeholornis Ji et al. (2002) 0.41 0.86 – – 0.54 0.12 45
Jeholornis
*
Zhou & Zhang (2002) 0.55 1.15 –0.60 –0.21 28
Jeholornis
*
Zhou & Zhang (2002) 0.55 1.15 – – 1.05 0.21 49
Jianchangosaurus Pu et al. (2013) 0.40 0.83 14.70 – – 0.03 5,018
Jinfengopteryx
*
Ji et al. (2005) 0.17 0.37 0.46 – – 0.01 317
Mahakala
#
Turner, Pol & Norell (2011) 0.20 0.42 0.67 – – 0.03 229
Mei long
*
Gao et al. (2012) 0.12 0.26 0.36 – – 0.01 505
Mei long
*
Xu & Norell (2004) 0.15 0.31 0.73 – – 0.01 714
Microraptor Li et al. (2012) 0.24 0.50 0.17 – – 0.04 46
Microraptor Xu et al. (2003),Sullivan et al. (2010) 0.41 0.86 0.88 – – 0.12 69
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 6/41
hindlimbs, for whom upper and lower mass estimate boundaries were taken from
Dececchi, Larsson & Hone (2012). As non-avian and avian theropods show significant
difference in hindlimb scaling (Dececchi & Larsson, 2013), this method could not be
applied to the avian theropods in our dataset. For birds, two mass estimates were
generated from the regressions derived from humerus length equations of extant birds
(Liu, Zhou & Zhang, 2012;Field et al., 2013), this element was selected as it showed high
correlation values in both source datasets and were easily computable for all specimens.
Nodal values were calculated based on a modified version of the phylogeny in Dececchi &
Larsson (2013) (Data S1).
Table 1 (continued).
Taxa Reference Wing length
(m)
Span
(m)
Mass
(kg) CF
Mass
(kg) Liu
Mass
(kg) FE
Wing Area
(m
^
2)
Wing
loading
N/M
2
Microraptor hanqingi
#
Gong et al. (2012) 0.47 0.98 2.05 – – 0.18 110
Oviraptor incertae sedis
MPC-D100/1018
Lu
¨et al. (2013) 0.09 0.19 0.03 0.00 305
Protarchaeopteryx Ji & Ji (1997) 0.26 0.54 2.58 – – 0.02 1,445
Sapeornis Pu et al. (2013) 0.44 0.92 –0.51 –0.12 43
Sapeornis Pu et al. (2013) 0.44 0.92 – – 0.88 0.12 74
Sapeornis
*
Zhou & Zhang (2003a) and
Zhou & Zhang (2003b)
0.57 1.21 –0.80 –0.20 40
Sapeornis
*
Zhou & Zhang (2003a) and
Zhou & Zhang (2003b)
0.57 1.21 – – 1.49 0.20 74
Similicaudipteryx Xu et al. (2009),
Dececchi & Larsson (2013)
0.40 0.84 4.23 – – 0.12 345
Similicaudipteryx Xu et al. (2009),
Dececchi & Larsson (2013)
0.07 0.15 0.06 – – 0.00 372
Sinocalliopteryx Sullivan et al. (2010) 0.37 0.77 18.43 – – 0.05 3,596
Sinornithoides Russell & Dong (1993) 0.31 0.77 18.4 – – 0.04 1,151
Sinornithosaurus Ji et al. (2001) 0.26 0.54 1.94 – – 0.02 1,032
Sinornithosaurus Sullivan et al. (2010) 0.19 0.41 0.29 – – 0.01 229
Sinosauropteryx Currie & Chen (2001) 0.10 0.20 0.88 – – 0.00 4,755
Sinosauropteryx Currie & Chen (2001) 0.05 0.09 0.19 – – 0.00 11,910
Sinovenator
*
Benson & Choiniere (2013) 0.24 0.50 2.44 – – 0.03 919
Tianyuraptor Chan, Dyke & Benton (2013),
Dececchi & Larsson (2013)
0.39 0.82 13.36 – – 0.06 2,272
Troodon Embryo MOR 246-1 Varricchio, Horner & Jackson (2002) 0.08 0.16 0.05 0.00 214
Xiaotingia
*
Xu et al. (2011) 0.24 0.50 0.82 – – 0.03 305
Yixianosaurus Dececchi, Larsson & Hone (2012) 0.29 0.61 1.30 – – 0.04 323
Yixianosaurus Dececchi, Larsson & Hone (2012) 0.29 0.61 1.89 – – 0.04 470
Yulong%
$
Lu
¨et al. (2013) 0.18 0.38 0.50 – – 0.02 280
Zhenyuanlong Lu
¨& Brusatte (2015) 0.58 1.22 11.99 – – 0.23 515
Notes:
@
Based on other Archaeopteryx specimens.
#
Denotes estimates based on Microraptor gui.
*
Based on Anchiornis.
$
Based on Caudipteryx.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 7/41
Wing dimensions
Wing length was calculated based on the length of the humerus, ulna, metacarpal II, and
the longest primary feather length, arranged in a straight line. Metacarpal length was
used instead of total manus length as the longest primaries attach to the metacarpals
and distal forelimb in paravians (Savile, 1957;Elz
˙anowski, 2002;Xu, Ma & Hu, 2010;
Foth, Tischlinger & Rauhut, 2014). This gives values similar to those previously reported
for maximal straight-line length of the wing in Archaeopteryx, differing by less than
1% (Yalden, 1971). Wing area was estimated using a chord value 65% of maximum
primary length based on the differences between the longest primary feather and the
shortest, distal primary in Archaeopteryx (Elz
˙anowski, 2002;Foth, Tischlinger & Rauhut,
2014)andCaudipteryx (Qiang et al., 1998). This estimate produces a greater wing area,
by 15%, than what was calculated by Yalden (1971) for the Berlin specimen of
Archaeopteryx and produces similar overestimations for other paravian taxa with
published wing areas such as Microraptor (+38% compared to Chatterjee & Templin
(2007) estimate and +9% over that of Alexander et al. (2010) and Zhenyuanlong
(5% greater than calculated by Lu
¨& Brusatte (2015)). Therefore, we treat our values as
upper bound estimates of maximum wing area as they are also overestimates of
functional wing area since they ignore the natural flexed position that the limbs take
during locomotion. We used this value for our primary analysis as it gives highest
possible values for all our force production data and thus the maximum likelihood of
success in achieving the minimum threshold values indicating the possible presence of a
behavior in said taxon. For taxa without primary feathers preserved (Ta bl e 1), we
estimated their length based on either other members of the same genus or closely
related taxa and assuming congruent lengths. We estimated body width using furcular
widths (Tabl e S 3) this represents an addition of between 10–15% to the value of the
non-avian theropod skeletal arm span. In extant bird wings feathers add another 40 + %
to skeletal arm length (Nudds, Dyke & Rayner, 2007) and proportionally more in many
non-avian theropods (Ta ble 1 ). Wingspan was set 2.1 times wing length (feather lengths
included) to assure we did not underestimate the potential wingspan and the influence
of the body on wing area in non-avian taxa.
Model construction
To test WAIR, flap running, and vertical leaping we used equations based on those of
Burgers & Chiappe (1999) and on extant bird flight work in Pennycuick (2008) to estimate
force production in a similar context to what is examined here.
bw ¼0:5ClpfAmp þUðÞ
2S=9:8M
Where bw denotes the proportion of body weight supported by the lift generated by the
wings (see Supplemental Materials Section S4 for more complete description of all
formula and calculations). This relatively simple model was chosen as it is easier to update
with new paleobiological information and allowed us to see directly the result of varying
the input data to see how varying models of theropod functional limitations shape the
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 8/41
results. To test the accuracy of our model, we compared our body weight support results
to published data for Chukar partridges during WAIR across the three ontogenetic stages,
Pigeon data during WAIR, and birds during takeoff (Table 2). Our values are within the
range seen in published data for all three stages of WAIR development and show values
greater than 1.0 for all birds undertaking leaping takeoff. As our simple model accurately
matches real world experimentally derived values of extant taxa, we believe it a suitable
starting point to derive comparative force production data for fossil avian and non-avian
theropods.
Creation of benchmarks
As WAIR ability is not uniform across ontogeny and seems to be linked to force
production (Jackson, Segre & Dial, 2009), we created two-benchmarks of proportion of
body mass supported for taxa to reach. Values between 0.06–0.49 body weight (bw) are
classified as level 1 WAIR, which corresponds to the earliest stages of ontogeny and sub
vertical ascents (late stage I and early stage II per Jackson, Segre & Dial, 2009) with greater
than 50% contribution to external vertical work generated by the hindlimbs (Bundle &
Dial, 2003). 0.5 bw and greater denote level 2 WAIR, equivalent to more mature Stage II
and III individuals (per Jackson, Segre & Dial, 2009) which are capable of high angle
to vertical ascents and whose forelimbs become more prominent in force production
(Bundle & Dial, 2003). Although we understand the transition between stages during
WAIR is semi-artificial, we wished to create a classification scheme that corresponds to the
different levels of WAIR capabilities seen in extant systems (Jackson, Segre & Dial, 2009).
The selection of 0.06 bw for achieving stage I was chosen to represent real world recorded
Table 2 Results of equations for calculating forces produced during WAIR and takeoff using data from extant avians. For Chukars body mass,
wing area and body velocity are based on Tobalske & Dial (2007), Flapping frequency and angle are based on Jackson, Segre & Dial (2009).
Coefficient of lift values (Cl) based on Heers, Tobalske & Dial (2011). For pigeons WAIR all data based on Jackson, Tobalske & Dial (2011) except for
wing area, which is taken from pigeons Crandell & Tobalske (2011) from pigeons with similar mass and wing length. For avian takeoff values are
based on Tobalske & Dial (2000) and Askew, Marsh & Ellington (2001).
Taxon Stage Body
Mass
(kg)
Wing
Area
(m
^
2)
Flap
angle
(rad)
Wing
beat
(Hz)
Velocity
(m/s)
BW BW BW BW
Cl = 1.0 Cl = 1.2 Cl = 1.5 Cl = 1.6
Chukar I 0.024 0.0036 1.57 22 0.60 0.06 0.08 – –
Chukar II 0.222 0.0297 2.5 18.7 1.20 0.85 1.02 – –
Chukar III 0.605 0.0499 2.16 18.7 1.50 0.65 0.78 0.97 1.02
Pigeon WAIR 650.42–0.47 0.067 1.57 6.2–6.7 1.50 0.21–0.26 0.25–0.31 0.31–0.39 0.33–0.41
Pigeon WAIR 850.42–0.47 0.067 1.57 7.3–7.7 1.50 0.28–0.31 0.34–0.37 0.42–0.46 0.45–0.49
Northern bobwhite Take off 0.199 0.0243 2.44 19.9 3.25 – – – 1.25
Chukar Take off 0.4915 0.0483 2.64 16.1 2.87 – – – 1.62
Ring necked
pheasant
Take off 0.9434 0.1002 2.64 11 2.34 – – – 1.37
Turkey Take off 5.275 0.3453 2.79 7.6 2.32 – – – 1.26
Blue breasted quail Take off 0.0436 0.0098 2.44 23.2 4.81 – – – 2.42
Harris hawk Take off 0.92 0.119 2.60 5.8 4.13 – – – 2.07
Pigeon Take off 0.307 0.0352 2.48 9.1 2.62 – – – 1.19
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 9/41
minima for this behavior and thus should be considered minimal levels achieved before
reconstructions of WAIR are accepted.
Coefficient of lift (Specific lift)
We examined potential performance during the wing-driven phase of flap-running,
WAIR, and leaping takeoff in our analyses. As a result, all three of the behaviors are subject
to constraints of lift production efficiency. The production of lift relative to planform area,
speed, and fluid density is summarized as the coefficient of lift.
During WAIR analysis, a coefficient of lift (CL) of 1.0 was used. This corresponds to a
value estimated during WAIR use in juvenile Chukars at early stage II (10 dph) (Heers,
Dial & Tobalske, 2014) but greater than that in the earlier ontogenetic stages (Heers,
Tobalske & Dial, 2011). We selected this value as this age class has been proposed to be
analogous to derived maniraptoran theropod capabilities such as Anchiornis and
Microraptor and this Cl is achievable by all ontogenetic stages beyond 5 dph depending
on the angle of attack (Heers, Dial & Tobalske, 2014). For leaping takeoff we used a Cl of
1.5, which corresponds to the minimal values estimated in adult Chukars during high
angle WAIR (Heers, Tobalske & Dial, 2011) and below the 1.64 calculated for the pigeon
during takeoff (Usherwood, 2009). For flap running, we used the equations of Burgers &
Chiappe (1999) with the following modifications: we ran permutations for all three
downstroke (50, 70 and 90) angles not just 50as per the original analysis and reduced
the Cl to 1.2 from 2. We choose to make the Cl closer to that estimated during late stage
Chukar WAIR attempts (Heers, Tobalske & Dial, 2011) as WAIR is simply a specific use
case of flap running on a highly angled substrate. This value is achievable by Chukars
older than 20 dph (Heers, Dial & Tobalske, 2014). Using the Cl of non-volant and juvenile
Chukar both produces reasonable minimum values for these behaviours and more closely
simulates the expected outputs in non-avian theropods before powered flight.
During low advance ratio wing-driven behaviors (launch, landing, WAIR, etc.), the
coefficient of drag can be quite large. In young Chukars, the coefficient of drag can be near
the coefficient of lift, thereby potentially providing a significant component of weight
support during controlled descent or significantly affecting reaction forces during WAIR
(Heers, Tobalske & Dial, 2011). To confirm that using pure Cl as our specific fluid force
coefficient was an accurate approach (instead of the total fluid resultant with both Cl and
Cd), we compared predicted reaction forces and weight support to values measured in
vivo and reported in the literature (Tobalske & Dial, 2007;Heers, Dial & Tobalske, 2014).
Because a close match was found across multiple size classes, we assume for the remainder
of the calculations that reaction forces during WAIR are not greatly affected by a high
coefficient of drag (though we note that for controlled descent or burst climb out,
behaviors we did not investigate, high Cd is likely a critical component).
Wing beat frequency
Wing beat frequencies scale negatively to body mass in steady flight (Greenewalt, 1975;
Pennycuick, 2008) and takeoff (Askew, Marsh & Ellington, 2001;Jackson, 2009) across
species in extant birds. Wingbeat frequencies during takeoff are similar to those during
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 10/41
WAIR (Tobalske & Dial, 2007). For this study we used the maximum takeoff wingbeat
frequency regressions from Jackson (2009) for all birds in his sample (see all Supplemental
Tables), and for only ground foraging birds (GF), we also added Galliformes takeoff
data from Askew, Marsh & Ellington (2001) to Jackson’s dataset to produce a third
regression equation (MOD). For the MOD dataset we incorporated a phylogenetic
correction using PDAP v 1.15 (Midford, Garland & Maddison, 2010), with branch lengths
based on divergence times derived from the chronograms of Jetz et al. (2012) (Data S2).
Wing range of motion
Abduction of the forelimb beyond the horizontal plane that transects the vertebral column
was not possible in most non-avian theropods resulting in a maximum stroke angle for
forelimb motion to be less than 90(Senter, 2006a;Senter, 2006b;Turner, Makovicky &
Norell, 2012). The glenoid fossa faces ventrolaterally in these taxa and only shifted to a
more lateral configuration at Paraves (Makovicky & Zanno, 2011;Turner, Makovicky &
Norell, 2012). The glenoid continued to translate upward until reaching the dorsolaterally
facing position of most extant birds at the phylogenetic level of Jeholornis and Sapeornis
(Zhou & Zhang, 2003a;Zhou & Zhang, 2003b).
Extant birds have extensive shoulder abductive ranges. For example, during WAIR, the
abductive flap angle of juvenile Chukars ranges from 90at stage I to greater than 143at
stage II (Jackson, Segre & Dial, 2009). Images show that in all cases, the forelimb ascends to
a vertical or slightly beyond position (see Tobalske & Dial, 2007, Figs. 4 and 6; Jackson,
Segre & Dial, 2009, Fig. 1; Heers, Dial & Tobalske, 2014, Fig. 1).
Given the abduction limitations of the non-avian theropod glenoid, we chose flap
angles of 50, 70 and 90to encapsulate the range of values expected across Theropoda and
ran them for all taxa. An angle of 90is likely unattainable for all non-avian theropods due
to the constraints of reducing contact with the substrate on the latter part of the
downstroke and shoulder morphology since the humerus cannot exceed the dorsal rim of
the glenoid which is aligned with the vertebral axis (or vertebral frame of reference per
Dial, Jackson & Segre, 2008). It was included to create an upper bracket on possible
support values.
Velocities for the center of mass used for the different analyses were based on those of
extant birds. For WAIR used as our assigned velocity 1.5 m/s based on the speed of adult
birds (Tobalske & Dial, 2007). This is higher than achieved for the early, pre-flight
capable ontogenetic stages (0.6 m/s in stage I, 1.2 m/s in stage II), and thus acts as a fair
upper velocity bound, though it is likely beyond the capabilities of non-avian theropods
with less developed wings. For leaping we calculated three values: height gain if wing
thrust was added to that generated by the hindlimbs, vertical distance increase given the
increased take off velocity due to flapping and takeoff potential from a standing jump.
Calculating height and distance gain was done through a modification of existing
equations used to model pterosaur launch (Witton & Habib, 2010) to account for the
bipedal nature of non-avian theropods (see Supplementary Information for these
equations). To compensate for the effects of body size, a scalar is introduced to ensure
the pre-loading values would be 2.4, a conservative value well within the range seen in
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 11/41
extant tetrapods (Biewener, 2003). Our pre-loading scalar accounts for the fact that
animals gain significant power amplification from the release of stored elastic energy in
their limbs. Even in non-specialist jumpers this amplification can be greater than twice
the maximum mass specific power derived from the muscles and in specialist can be
10 higher or more (Henery, Ellerby & Marsh, 2005 and references therein). For leaping
takeoff, our starting inputs were two different takeoff speeds recorded in on extant
avians (Earls, 2000;Tobalske & Dial, 2000;Askew, Marsh & Ellington, 2001). Higher
values for leaping have been recorded in some mammals (Gu
¨nther et al., 1991)andafter
several wing beats in birds (Askew, Marsh & Ellington, 2001;Berg & Biewener, 2010),
thus these values may not represent the maximal possible values for small theropods.
For flap running the assigned start value was 2 m/s, which is the same starting velocity
used in Burgers & Chiappe (1999). This speed is well within the range of sprint speeds of
many lizards (Huey, 1982;Christian & Garland, 1996;Irschick & Jayne, 1999)and
small mammals (Iriarte-Dı
´az, 2002), whereas many terrestrial birds can sustain this
speed for over thirty minutes (Gatesy & Biewener, 1991;Gatesy, 1999).Thesevaluesare
likely well below the maximum sprint speed of these taxa (Sellers & Manning, 2007)but
allowed us to determine if there was significant increase in speed using the wing
generated thrust alone.
We excluded the potential drag and damage caused by hindlimb feathers of some
paravians through contact with the substrate. At low hindlimb angles used during the
ascent of inclined surfaces (see the metatarsus during WAIR in Fig. 1 from Jackson, Segre &
Dial, 2009) the distal limb feathers would have contacted the surface and caused frictional
drag, which would have reduced performance and damaged the feathers (Dececchi &
Larsson, 2011). Although these variables may have evolved throughout the transition from
theropods into early birds, treating them as constants provided a “best case scenario” for
non-avian theropods constraining the upper limits for when these behaviours were
possible.
Wing contribution to leaping
Three additional estimates for wing contributions to vertical leaping were made. The
first estimates the percentage increase possible to the maximum leap through the
addition of thrust generated by flapping. This calculation assumed the maximum
wing output occurred at the top of the leap arch, and that the forces generated were
directed vertically. This was done through a modification of the terrestrial launch
methodology of Witton & Habib (2010, see Data S3) to accommodate bipedal
theropod models with and without wing generated thrust. The difference between the
maximum heights gained with wing generated thrust was presented as a percentage
increase (see Datas S3 and S4 for more detailed description of the equations used and
a sample calculation spreadsheet). The second evaluates the horizontal distance
extension to a leap through the addition of flapping generated thrust. This was
calculated by using the speed at takeoff generated by the equations for bipedal launch
(see Datas S3 and S4)atboth30and45
launch angle. The later corresponds to the
theoretical best angle for a projectile while the former more closely resembles the
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 12/41
angle of takeoff measured in human and lizard leapers (Toro, Herrel & Irschick, 2004;
Linthorne, Guzman & Bridgett, 2005;Wakai & Linthorne, 2005). In both cases our
models were treated as if there was no difference in takeoff and landing height, thus
making the calculation of jump distance
Djump ¼v2sin 2
=g
Where v equals the takeoff velocity and Θthe angle of takeoff.
Vertical take offs were deemed possible when body weight (bw) support values were
equal to or greater than 1.0 using the speed and lift parameters mentioned above.
Jinfengopteryx
Microraptor
Anchiornis
Archaeopteryx
Similicaudipteryx
Sinosauropteryx
Sinocalliopteryx
Protoarchaeopteryx
Jianchangosaurus
Caudipteryx
Eosinopteryx
Xiaotingia
Yulong
Mei
Aurornis
Mahakala
Sinoventor
Sinornithosaurus
Changyuraptor
Eoconfuciusornis
Jeholornis
Sapeornis
Tianyuraptor
Confuciusornis
Tyrannosauroidae
Zulong
Bicenternaria
Compsogntahidae
Tugulusaurus
Alvarezsauroidae
Ornithomimosauria
Ornitholestes
Beipiaosaurus
Therizinosauroidae
Falcarius
oviraptorid embryos
Caegnathidae
Avimimus
troodontid embryo
Dromaeosauria
Unenlagiinae
Ornithuromorpha
Enantiornithes
Maniraptoriformes
Maniraptora
Pennaraptora
Paraves
Aves
Coelurosauria
log (wing loading) (N/m^2)
1
2
3
4
fledged 10 dph Chuckar
WAIRing 3 dph Chuckar
WAIRing juvenile Brush turkey
Figure 1 Wing loading values in non-avian theropods. Each open circle denotes the value per spe-
cimen for taxa with multiple specimens included in analysis. Note that only a minority of paravian
specimens are below the lines denoting values pre WAIR quadruped crawling in Chukar (3 dph) and
when fledging occurs (10 dph) as well as WAIR capable Brush Turkeys.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 13/41
RESULTS
Wing loading
Increase in WAIR ability broadly corresponds to decreased wing loading in Chukars
(Heers & Dial, 2015), something noted in other galliform birds (Dial & Jackson, 2011).
Thus wing loading values may offer a rough comparison between non-avian theropod
specimens and Chukars of a similar body mass. Among non-avian theropods, wing
loading values ranged from 46 N/m
2
(Microraptor) to over 11,000 N/m
2
(Sinosauropteryx). Of the thirty-four non-avian specimens included, only eight,
representing five genera (all are deinonychosaurs) showed loading values less than that
seen in 1-day-old Chukars (170 N/m
2
), the highest values recorded across ontogeny. 1-
day-old Chukar chicks do not WAIR, can only surmount inclines of less than 48still
performed asynchronous wing beats and their wings make prolonged contacts with
the substrate in a crawling fashion (Jackson, Segre & Dial, 2009;Heers & Dial, 2015). No
non-paravian showed values less than the 160 N/m
2
measured at 3 dph Chukars, with
most pennaraptorans at values 2–8 times that seen at even the highest Chukar chick
loadings (Table 1;Fig. 1). Focusing on the embryonic and early ontogenetic stage
specimens in our analysis, to test whether WAIR was possible at early ages and lost
through ontogeny, we recovered loading values again significantly higher than the highest
values seen during Chukar ontogeny, with values 126–234% those of 1-day-old chicks
which were also significantly smaller. For comparison, the hatchling size Similicaudipteryx
specimen (STM 4-1) had a body mass estimated at approximately 63 g, similar to a 17 dph
Chukar chick (stage II), but wing loading values of 372 N/m
2
, 5.8 times higher than seen
in the 17 dph chick and over twice that seen in 3 dph Chukars due to Similicaudipteryx
having a wing area only the size of a 6 dph chick which weight approximately 16 g. This
suggests that none of the non-paravian theropods could perform the lowest levels of
WAIR, even disregarding their limited range of motion and flapping frequency compared
to juvenile extant avians. None of the Mesozoic avian taxa, under either mass
reconstruction, showed loading values above 74 N/m
2
, which corresponds to
approximately 11 dph (stage II) Chukar chicks, which is approximately the time where
fledgling begins (Harper, Harry & Bailey, 1958;Christensen, 1996).
WAIR
At a CoM velocity of 1.5 m/s nine of thirty-four specimens of non-avian theropods
reached the minimal benchmark for level 1 WAIR (0.06 bw) under at least one of the three
flapping speed and flap angle permutations (Fig. 2;Tables 3 and S4–S6). When the
velocity was decreased to 0.6 m/s number that succeed decreased to eight as the
Sinornithosaurus specimen based on the measurements of Sullivan et al. (2010) failed to
achieve the 0.06 bw benchmark (Fig. 2;Table 3). All are deinonychosaurs. Three
specimens (the larger Similicaudipteryx specimen, and the smaller mass estimates for
Yixianosaurus and Yulong) approach the WAIR level 1 criteria, but none yield values
higher than 0.05 bw, and this only under the MOD reconstruction at the highest
abduction angle. All specimens of Microraptor and the smaller specimens of Anchiornis
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 14/41
Figure 2 Evolution of WAIR performance. Estimated evolutionary ranges of WAIR stages I and II (Dial, 2003;Heers & Dial, 2012;Heers, Dial &
Tobalske, 2014) are mapped over a phylogeny of selected Maniraptoriformes. Upper lines are for 90flap angles and lower lines for 50flap angles.
Flight-stroke specific characters are mapped onto the phylogeny: 1, forelimb integument; 2, pennaceous feathers on forelimb; 3, L-shaped sca-
pulocoracoid; 4, laterally facing glenoid; 5, asymmetrical remigies; 6, alula; 7, incipient ligament-based shoulder stabilization; 8, dorsolaterally
facing glenoid; 9, full ligament-based shoulder stabilization. The bottom coloured lines denote 50flap angles and upper coloured lines 90.
Silhouettes from PhyloPic images by B. McFeeters, T.M. Keesey, M. Martynuick, and original.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 15/41
Table 3 Table of body wight support values across specimens under 90flap angle. Body weight (bw) support values across non-avian and basal
avian taxa under three different flapping frequency estimators (see text for description). Calculations are based on the 90flap angle permutation at
two velocity of the centre of mass (0.6 and 1.5 m/s). This correspond to recorded velocity of earliest WAIR capable juveniles (0.6 m/s) and adult (1.5
m/s) Chukars (Tobalske & Dial, 2007).
Taxa Specimen M/S bw All bw GF bw MOD M/S bw All bw GF bw MOD
Anchiornis BMNHCPH828 1.5 0.24 0.22 0.22 0.6 0.17 0.15 0.15
Anchiornis LPM B00169 1.5 0.10 0.09 0.12 0.6 0.06 0.06 0.08
Archaeopteryx 11th 1.5 0.70/0.37 0.62/0.33 0.78/0.46 0.6 0.52/0.27 0.45/0.23 0.59/0.34
Archaeopteryx Berlin 1.5 0.67/0.38 0.60/0.34 0.74/0.46 0.6 0.50/0.27 0.43/0.24 0.56/0.34
Archaeopteryx London 1.5 0.57/0.28 0.50/0.25 0.67/0.37 0.6 0.42/0.20 0.37/0.17 0.51/0.27
Archaeopteryx Munich 1.5 0.66/0.39 0.59/0.34 0.68/0.43 0.6 0.48/0.28 0.42/0.24 0.51/0.32
Archaeopteryx Thermopolis 1.5 0.71/0.41 0.63/0.37 0.75/0.47 0.6 0.52/0.29 0.46/0.26 0.56/0.34
Archaeopteryx Eichstatt 1.5 0.42/0.29 0.38/0.26 0.39/0.28 0.6 0.30/0.20 0.26/0.17 0.27/0.19
Aurornis YFGP-T5198 1.5 0.08 0.07 0.10 0.6 0.05 0.05 0.07
Caudipteryx IVPP 12344 1.5 0.01 0.01 0.02 0.6 0.01 0.00 0.01
Caudipteryx IVPP 12430 1.5 0.01 0.01 0.01 0.6 0.00 0.00 0.01
Changyuraptor HG B016 1.5 0.11 0.10 0.25 0.6 0.05 0.05 0.14
Citipati MPC-D100/971 1.5 0.03 0.03 0.03 0.6 0.02 0.02 0.02
Eosinopteryx YFGP-T5197 1.5 0.12 0.11 0.12 0.6 0.08 0.07 0.08
Jianchangosaurus 41HIII-0308A 1.5 0.00 0.00 0.00 0.6 0.00 0.00 0.00
Jinfengopteryx CAGS-IG 04-0801 1.5 0.03 0.02 0.03 0.6 0.02 0.01 0.02
Mahakala IGM 100/1033 1.5 0.04 0.03 0.05 0.6 0.02 0.02 0.03
Mei long DNHM D2154 1.5 0.01 0.01 0.02 0.6 0.01 0.01 0.01
Mei long IVPP V12733 1.5 0.01 0.01 0.01 0.6 0.00 0.00 0.01
Microraptor BMNHC PH 881 1.5 0.49 0.43 0.50 0.6 0.35 0.31 0.36
Microraptor IVPP V 13352 1.5 0.28 0.25 0.42 0.6 0.20 0.17 0.32
Microraptor hanqingi LVH 0026 1.5 0.14 0.12 0.24 0.6 0.08 0.07 0.15
Oviraptor in sedis MPC-D100/1018 1.5 0.05 0.04 0.03 0.6 0.03 0.03 0.02
Protarchaeopteryx GMV2125 1.5 0.00 0.00 0.01 0.6 0.00 0.00 0.00
Similicaudipteryx STM22-6 1.5 0.02 0.02 0.05 0.6 0.01 0.01 0.03
Similicaudipteryx STM4-1 1.5 0.02 0.02 0.02 0.6 0.01 0.01 0.01
Sinocalliopteryx JMP-V-05-8-01 1.5 0.00 0.00 0.00 0.6 0.00 0.00 0.00
Sinornithoides IVPP V9612 1.5 0.01 0.01 0.01 0.6 0.00 0.00 0.01
Sinornithosaurus NGMC-91A 1.5 0.01 0.01 0.01 0.6 0.00 0.00 0.01
Sinornithosaurus Sullivan et al. (2010) 1.5 0.05 0.05 0.06 0.6 0.03 0.03 0.04
Sinosauropteryx NICP 127587 1.5 0.00 0.00 0.00 0.6 0.00 0.00 0.00
Sinosauropteryx NIGP 127586 1.5 0.00 0.00 0.00 0.6 0.00 0.00 0.00
Sinovenator IVPP V11977 1.5 0.01 0.01 0.01 0.6 0.00 0.00 0.01
Tianyuraptor STM1–3 1.5 0.00 0.00 0.00 0.6 0.00 0.00 0.00
Troodon embryo MOR 246-1 1.5 0.04 0.04 0.03 0.6 0.02 0.02 0.02
Xiaotingia STM 27-2 1.5 0.03 0.03 0.05 0.6 0.02 0.02 0.03
Yixianosaurus IVPP 12638 1.5 0.03/0.02 0.03/0.02 0.05/0.03 0.6 0.02/0.01 0.02/0.01 0.03/0.02
Yulong 41HIII-0107 1.5 0.03 0.03 0.04 0.6 0.02 0.02 0.02
Zhenyuanlong JPM-0008 1.5 0.02 0.01 0.04 0.6 0.01 0.01 0.03
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 16/41
and Eosinopteryx yielded bodyweight support values above 0.06 bw across all
permutations at 1.5 m/s whereas at 0.6 m/s only the smaller Anchiornis and Microraptor
gui specimens achieve this. Within non-avian theropods using a 90flap angle at 1.5 m/s,
only a single specimen of Microraptor gui (BMNHC PH881) has body weight support
values reaching the 0.5 bw cutoffs for WAIR level 2, though the larger specimen (IVPP V
13352) comes close under the MOD reconstruction (Tables 3 and S4–S6). At 50only the
smaller Anchiornis,Changyuraptor,Eosinopteryx and all 3 Microraptor specimens, achieve
the 0.06 bw benchmark at 1.5 m/s and this decreases to only the smaller Anchiornis and
Microraptor at 0.6 m/s. No non-avians or Archaeopteryx achieved bw support values
higher than 0.33 under the 50at 1.5 m/s and only Microraptor gui, Archaeopteryx
specimens and the smaller Anchiornis reaching a minimal of 0.1 bw under this
permutation.
Among Mesozoic birds, the different mass estimation methods produced significantly
different body weight support values and are more prominent in the most basal birds in
our analysis Sapeornis and Jeholornis (Fig. 2;Tables S4–S6). All basal avians show the
capability of level 1 WAIR (bw support values of 0.06 or greater) under all flap frequencies
estimates, mass estimates or flap angles used here and no avians showing values below 0.1
bw under any permutation. In Archaeopteryx, there is no clear trend in WAIR capability
and allometry as all specimens besides the Eichstatt individual show a similar range of
body weight support values (Table 3). At the higher flap angle and lower mass, all avians
show the capability for level 2 WAIR (> 0.5 bw). All birds more derived than
Archaeopteryx yield a body weight support values in excess of 1.0 bw at their lower mass
estimate at 1.5 m/s 90flap angle under all 3 flap frequencies, except for Sapeornis where
the smaller specimen exceeds 1.0 bw only under the MOD permutation. Of note, the
values recovered for more derived avians are significantly higher than those observed in
experimental data (Tobalske & Dial, 2007) or calculated using extant measurements
(Tables 2 and S7) and well above the 1.0 threshold for takeoff. This suggests that these taxa
could have performed this behavior at lower wing beat frequencies, body velocities and
flap angles than the values used here, as seen in some extant birds (Jackson, Tobalske &
Dial, 2011), or that physiology and power production differed between extant and basal
birds (Erickson et al., 2009;O’Connor & Zhou, 2015), or a combination of both. If the latter
is correct, it suggests our measurements for non-avian theropods overestimate the power
production potential in these taxa, and thus overestimate their WAIR capabilities.
Flap running
Among non-avian theropods, flap running peaked in effectiveness within small-bodied
paravians (Fig. 3;Table S8). With a 90flap angle, the smaller Anchiornis specimen and
Microraptor gui were the only non-avian taxa to show increases greater than 1.0 m/s under
all permutations (71–79 and 75–208% performance increases, respectively), although only
Microraptor achieved speeds capable of flight. More realistic 50flap angles yielded only a
23–27 and 26–65% performance increase for these taxa. Among non-paravians, even
under the highest flap angle and flap frequency permutations no taxon exceeded an
increase of 17% in running speed with the highest values found in the larger specimen of
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 17/41
Similicaudipteryx. At flap angles below 90only the larger Similicaudipteryx and the
lighter mass estimated Yixianosaurus specimens among non-paravians yielded velocity
increases approaching 10%. Although some paravians had high levels of increased speed,
Figure 3 Evolution of flight stroke enhancements to flap running (orange) and vertical leaping
(blue) performance. Estimated ranges are mapped over a phylogeny of selected Maniraptoriformes.
Averages are presented when multiple specimens are available. Upper lines are for 90flap angles
and lower lines for 50flap angles. Flight-stroke specific characters are mapped onto the phylogeny:
1, forelimb integument; 2, pennaceous feathers on forelimb; L-shaped scapulocoracoid; 4, laterally facing
glenoid; 5, asymmetrical remigies; 6, alula; 7, incipient ligament-based shoulder stabilization; 8, dor-
solaterally facing glenoid; 9, full ligament-based shoulder stabilization. The bottom coloured lines
denote 50flap angles and upper coloured lines 90. Silhouettes from PhyloPic images by B. McFeeters,
T.M. Keesey, M. Martynuick, and original.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 18/41
Mahakala, Mei, Jinfengopteryx, Xiaotingia, Tianyuraptor, and Sinovenator showed
increases of less 17% under all permutations, with many showing values in the single
digits. At 50only Microraptor sp., Changyuraptor,Eosinopteryx and Anchiornis showed a
greater than 10% increase in running velocity. All specimens of Archaeopteryx showed
speed increases similar to or greater than those seen in Microraptor and Anchiornis though
there is no clear pattern relating body size to speed, as the largest (London) and smallest
(Eichstatt) specimens yielded similar values (Table S8). Only Microraptor and all
specimens of Archaeopteryx showed the ability to achieve takeoff velocities by this method
alone (Table S8).
Leaping
The use of forelimbs during jumping was divided into three discrete analyses, one
examining the potential of the wings to increase maximum jump height, one to examine
distance gained horizontally, and finally to see if the wings could generate enough force to
take off from a standing start as seen in most extant birds.
Vertical
No non-paravian gained more than 8% additional height with flapping using the
highest flap angles, and most gained less than 3% (Fig. 3,Table S9). Using more
reasonable flap angles of 50, none exceeded 4%. Within paravians, several taxa generated
greater than 10% height increases, including Anchiornis,Microraptor,Eosinopteryx,
Changyuraptor,Aurornis and all Archaeopteryx specimens (Table S9). Despite this most
troodontids, both the “short armed” Jehol Dromaeosaurs, Mahakala and Sinornithosaurus
showed values more similar to non-paravians, between 1–8.5% increase in height. Of
interest, the “four winged” taxa used here (Anchiornis,Microraptor, and Changyuraptor)
yielded increased height gains on the order of 16–64%, with Microraptor gui specimens
showing values in excess of 50% (Fig. 3,Table S9). Even under the lowest flap angle
settings, both specimens of M. gui showed leaping height increases of greater than 30%,
almost four times the value for the non-paravians under any setting, and Changyuraptor
and Microraptor hanqingi showed values of approximately 20%, which is greater than
twice the highest value seen in any non-paravian. All Archaeopteryx specimens showed
height gains greater than 30% under all mass permutations, with the lighter estimates for
the Berlin, Thermopolis and 11
th
specimen exceeding 190% non-flapping height values.
Interestingly the only specimen that did not reach the 50% height gain under any
permutation is the Eichstatt specimen, the smallest in our analysis, whose range between
34–48% gains is similar to what is seen in the larger microraptorine specimens (excluding
Sinornithosaurus).
Horizontal
Similar to vertical leaping, there was a marked disparity between distance gained in the
“four winged” paravian taxa and all others (Table S10). Only one non-paravian
Similicaudipteryx STM-22, under the highest setting and at a 45takeoff angle, showed
distance increases of 5% or greater. Among paravians Microraptor,Changyuraptor, the
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 19/41
smaller Anchiornis and all species of Archaeopteryx show leaping values greater than 20%
non-flapping horizontal distance at the 45take off, though this drops to 15% at 30.
Vertical takeoff
Among non-avians, only Microraptor gui achieved body weight supports greater than 1
under any flap angle or flapping frequency permutation under the two avian derived take
off speeds assessed. No non-paravian showed values greater than 0.15 bw under these
conditions (Tables S11–S13). Outside of Microraptor, Changyuraptor and the smaller
specimen of Anchiornis, deinonychosaurians did not have values beyond 0.5 bw under
either speed or any flap frequency permutation. In avians at the lower body weight
estimate, all taxa showed values greater than 1.0 bw at the high end of their flapping angle
range. At the higher mass estimates, multiple specimens of Archaeopteryx showed
levels below 1.0 bw, with the lowest values seen in the Eichstatt and London specimens
(Tables S11–S13). Many extant avians use launch speeds between 1.5 m/s and 3.8 m/s
(Earls, 2000;Berg & Biewener, 2010;Heers, Dial & Tobalske, 2014). At these takeoff speeds
avians more derived than Archaeopteryx achieved values in excess of 1.0 bw, with the
exception of the larger mass estimates of Sapeornis under the ALL and GF flapping
estimates (Tables S4–S6 and S11–S13). At the higher speed of 5.1 m/s, achievable by strong
leapers, beyond Microraptor the only other non-avian theropods to achieve greater
than 1.0 bw support was the smaller specimen of Anchiornis under a single flap rate
permutation at 90flap angle.
DISCUSSION
A major challenge of attempting to create models that examine evolutionary transitions is
that of efficiency versus effectiveness. Evolved traits may need to only function at some
basic level, rather than contribute high degrees of functional adaptation. Thus, an
argument against our use of thresholds, such as a 6% body weight support as the
minimum for WAIR, is that smaller values, such as 5% or even 1%, may still provide
selective advantages for individuals. Although this line of thought is defensible, we suggest
a challenge to this. The first is that these low values are not testable in the sense that there
are not physically defined thresholds to demarcate when a behaviour may or may not
function. Without these parameters to test, any discussion becomes a story-telling
scenario. In addition, we have used liberal parameters in reconstructing extinct taxa based
on output values measured in modern, derived avians. This optimistic reconstruction of
the possible ignores that non-avian theropods have additional functional restrictions
based in their musculoskeletal, neuromuscular and integumentary systems not present in
extant birds. The minimal age of origin for powered flight in avian theropods where is 130
million years ago (Wang et al., 2015) and this behavior and all its functional and
morphological components have been under refinement through selection ever since.
Thus, we postulate that the claim that non-avian theropod would be able to perform
functions at output levels below the threshold minimums seen in extant avian taxa
difficult to defend. For example, flapping frequency and flap angle have large effects on the
resulting body weight support values and using avian take off values are likely significant
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 20/41
over estimations for values obtainable in most if not all the taxa sampled here. Our use
of a velocity of 1.5 m/s is based on the speed of adult Chukars, whose WAIR ability is
much greater than proposed of any non-avian taxa examined here. Using juvenile
values (0.6 m/s of stage I) reduces the bw support values by approximately one third.
Additionally, by using coefficient of lift values of 1, which is higher than is seen in a 20 dph
Chukar at 45angle of attack (stage II per Jackson, Segre & Dial, 2009), we are likely highly
positively biasing the results. Thus, we argue that due to our relaxed constraints and the
significantly higher wing loadings to that seen in any stage of Chukar development (even
the asymmetrical crawling stage of 1–3 dph from Jackson, Segre & Dial, 2009), the taxa
sampled here that did not reach the 0.06 bw threshold derived from in vivo experiments or
meet the wing loading values seen in the earliest stages of ontogeny should not be
considered WAIR capable. Although we do not have in vivo derived values to compare
with leaping and flap running estimates, it is not parsimonious to propose that small
incremental increases measured only under unnaturally lenient conditions support a
behavior.
For all behaviours tested here there is a sharp contrast in performance levels between a
small number of paravian taxa (Microraptor, Anchiornis, Changyuraptor, Aurornis and
Eosinopteryx) and all other non-avian taxa. This discrepancy is marked not only because it
does not correlate to the origin of pennaceous feathers at pennaraptora but it also does not
include all members of Paraves within the high performing category. Multiple small
bodied and basal members of both deinonychosaurian subgroups, such as Mahakala,
Xiaotingia, Jinfengopteryx, Mei, Sinovenator and Sinornithosaurus, show little evidence of
benefit from flapping assisted locomotion. As these taxa are similar in size to the paravians
that do show potential benefits, the argument that this loss is a byproduct of allometry is
not possible. Allometric loss of performance is possible though in the larger, feathered
dromaeosaurs like Velociraptor (∼15 kg, Turner et al., 2007)orDakotaraptor (∼350 kg,
Depalma et al., 2015), but our data from embryonic maniraptorans does not support this
postulate. As our measurements for the small paravian wing areas are based either on
preserved feather length (Sinornithosaurus) or on long feathered close relatives (Anchiornis
for Xiaotingia,Jinfengopteryx,Mei,Sinovenator and Microraptor for Mahakala) our values
for them are likely overestimates and suggests that locomotion was not a major driver for
forelimb evolution, even among small sized paravians.
Flap running
There are questions as to whether a flap running model is particularly efficient for any
taxa. One immediate set of constraints relates to performance of the hind limb under a
potential flap-running model. The thrust production model we used assumes the
hindlimb and forelimb propulsion potentials were simply additive. However, in reality the
hindlimb performance must have some maximum output that is likely to be exceeded if
the forelimbs produce significant additional propulsive force. Thus, at high wing-
produced thrust production, the hindlimbs likely cannot move fast enough to
accommodate the faster speeds. Under such conditions, an animal would pitch forward
and fall.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 21/41
We also assume that most of the lift produced by the wings during flap-running could
be oriented as thrust. The proportion of force that can be oriented as thrust is, however,
constrained by wing kinematics, particularly the amount of spanwise twist that the wing
can undergo during the flight stroke (Iosilevskii, 2014). Thus, our thrust proportions
for theropods may be unrealistically high, overestimating the speed generated.
Additionally, downstroke lift production not reoriented as thrust would act to displace
some weight. Although this is important and necessary in flight, it would reduce hindlimb
performance during flap-running by reducing the normal force acting through the feet.
A similar phenomena occurs during high angled WAIR (Bundle & Dial, 2003). Finally,
the production of lift during flap-running, regardless of orientation relative to travel,
would generate significant amounts of drag (including profile drag, pressure drag, and
induced drag). Given these potential performance constraints, it is questionable whether
flap-running would be as effective a locomotion mode as our data suggests, even for
taxa like Microraptor.
WAIR
The finding that not a single non-paravian reaches the 6% bodyweight threshold for level
1 WAIR challenges the proposal that WAIR offers a behavioural pathway for basal
maniraptorans (Dial, Randall & Dial, 2006;Heers, Tobalske & Dial, 2011;Heers, Dial &
Tobalske, 2014). The few cases that approach these values (Similicaudipteryx,Yulong, and
Yixianosaurus) are only achieved under wing angle and wing beat permutations that are
unrealistic given their pectoral musculoskeletal structures (Baier, Gatesy & Jenkins, 2007;
Turner, Makovicky & Norell, 2012). MOD derived wing beat values in beats per second for
the larger Similicaudipteryx (6 Hz), Yixianosaurus (7–8 Hz), Yulong (10 Hz) are greater
than or equal to those of smaller extant birds such as the Magpie (Pica pica) (9.2 Hz),
Crow (Corvus brachyrhynchos) (6.6 Hz) and Raven (Corvus corvax) (6.1 Hz) (Jackson,
2009) and are so elevated due to the inclusion in that dataset of galliform birds, which are
short burst specialists with shortened wings, large pectoralis and supracoracoideus muscle
masses and muscle fiber adaptations to maximize their flight style (Askew & Marsh, 2001;
Tobalske et al., 2003). These specialized muscles are adapted to allow wing beat frequencies
beyond those of other birds at a similar body mass (Tobalske & Dial, 2000;Tobalske &
Dial, 2007;Jackson, 2009;Jackson, Segre & Dial, 2009) thus inflating our wing beat
frequency estimates. Wing beat frequencies were likely much lower in non-avian
theropods than in modern birds during takeoff, which is higher than during level flight
(Dial, 1992;Berg & Biewener, 2010), given the relatively small size of their wing
musculature and plesiomorphic musculoskeletal anatomy (Jasinoski, Russell & Currie,
2006;Allen et al., 2013;Baier, Gatesy & Jenkins, 2007;Bock, 2013;Burch, 2014).
In none of our nine permutations did values indicating level 1 WAIR performances
become unambiguously optimized at Paraves (Data S1). This is despite our conservative
application of constraints such as use of a 90flap angle, flap frequencies comparable of
greater than many extant avians, WAIR velocity comparable to adult Chukars and
generous wing area estimates. In paravians that do shown positive scores, these are no
more than 0.12 bw under 90flap angle at a velocity of 1.5 m/s and any flapping frequency
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 22/41
reconstruction for the larger Anchiornis,Aurornis,Eosinopteryx or Sinornithosaurus and
Changyuraptor under all but the MOD flapping rate estimate (Table 3). This suggests
that tightening these constraints either singularly or combination would likely exclude
marginally performing taxa from even this threshold. For example, using the body
velocity of 6–8 dph Chukars (0.6 m/s) at 70flap angle, excludes Aurornis, the larger
Anchiornis,Eosinopteryx under all permutations and Changyuraptor except under the
MOD flapping frequency.
Given the low values seen Aurornis and reduced flapping ability in Eosinopteryx
(Godefroit et al., 2013) it is likely that only the juvenile Anchiornis specimen, Microraptor
and Changyuraptor among non-avian theropods would even have the potential to use this
behavior. When we introduce other factors in addition to those listed above such as the
symmetrical feathers or the plesiomorphic pectoral girdle would likely have limited the
prevalence of WAIR further, if present at all, to only the microraptorines as they would
have further reduce the effectiveness of the wings in force generation. Feather asymmetry
aids in resisting out of plane forces and is crucial for their bending and twisting during the
flight stroke (Ennos, Hickson & Roberts, 1995;Norberg, 2002). While the pectoral girdle
morphology of Anchiornis which show non-elongated and convex coracoid and lack of
ossified sternum or fused gastralia, denote reduced pectoral muscle mass compared to
microraptorines (Zheng et al., 2014). This does not make a strong case that this behavior
was present ancestrally in Paravians, yet alone that it coincided with pennaceous feather
evolution and elongation (present at Pennaraptora) or other flight related adaptations.
Our findings suggest that if present at all, there is a minimum of two origins for the use of
flap-based locomotion with the presently accepted phylogenetic hypotheses; once within
microraptorines, and once in Aves. This is not completely surprising, as other traits related
to flight, such as an alula, elongated coracoid, and a broad, ossified single sternum plate,
are also independently derived in Microraptor and basal avians that are more derived than
Sapeornis, suggesting convergent evolution in early powered flight (Zheng et al., 2014).
To compare the results of our body mass and wing area estimates to others in the
literature we ran the WAIR and leaping takeoff analyses using previously published mass
and wing area values for Archaeopteryx (Yalden, 1984), Microraptor (Chatterjee & Templin,
2007;Alexander et al., 2010), Caudipteryx and Protarchaeopteryx (Nudds & Dyke, 2009). In
all cases, WAIR values were similar, often below, values calculated in our analysis
(Table S14). Non-paravians yielded WAIR values near 0 bw and take off speeds were
required to be greater than 46 m/s. Microraptor specimens showed takeoff velocities
between 4.1–6.6 m/s, values achievable either by running or leaping methods and similar
to those estimated in our original analysis.
Locomotory pathways to flight: necessity or red herring?
Our first principles modeling approach, which accurately predicts WAIR values for
Chukar chicks, supports the postulate that for these “near flight” behaviors, wing area is
the major determinant of function rather than power. One potential argument for why a
locomotory pathway is required for the evolution of flight related characters is that the
muscle hypertrophy in the pectoral girdle present in extant flying birds would be unlikely
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 23/41
to have evolved passively if display or stability flapping methods drove the origin of large
wings. Although it is undeniable that extant avians have proportionally and significantly
more wing musculature than non-avian theropods, the minimum level needed to achieve
a ground-based takeoff is unknown. There are several volant birds with flight muscle
ratios (flight muscle mass proportion of total mass) below 16% (Marden, 1987). Juvenile
Chukars that fledge less than two weeks after hatching (Harper, Harry & Bailey, 1958;
Christensen, 1970;Christensen, 1996) and young peafowl (which fledge after one to two
weeks Fowler, 2011) also have ratios below this value. Recent estimates for Microraptor
yield values within this range (Allen et al., 2013).
Fledging aged Chukars and Peafowl have a reduced flight muscle fraction compared to
adult birds. In Chukar’s, at 14–15 dph, the pectoral mass is only 48–62% the relative size
(as a proportion of total mass) compared to adult birds, while in Peafowl (12 dph) this
range is between 38–45% (Heers & Dial, 2015). Yet at this age the wing loading values
are significantly less than in adults, with 15 dph Chukars showing values only 38% of
adults and 11–14 dph Peafowl showing values ranging from 22–25% of those seen in
adults. Among non-avian theropods only Microraptor (specimens BMNHC PH 881, IVPP
V 13352, LVH 0026 under Alexander et al., 2010’s mass estimate) and the juvenile
Anchiornis (BMNHCPH828) have similar wing loading values to fledging aged Chukar
(10–17 dph) (Heers & Dial, 2015). Of these, only Microraptor and early avians have
previously been suggested to have similar pectoral muscle mass fractions (pectoral limbs
region 13–15% of total mass per Allen et al., 2013) combined with similar wing loading
values as seen in volant juvenile Chukars (minimum forelimb muscle mass of 14% of
body mass, wing loading values below 80 N/m
2
). Thus, we contend that these taxa
may have had a power output that would be capable of ground based take off, as the
reduced pectoral musculature was compensated for by their large wing size.
Even at slight lower estimates of flight muscle, mass percentage take off may be possible
in Microraptor and basal avians. Early fledgling aged Chukar chicks show forelimb muscle
mass fractions (Heers & Dial, 2015) below the 16% suggested as the minimum for
takeoff by Marden (1987). This is due to their proportionally large wings. With such a
proportionally large wing area, even at low forelimb mass fledging aged Chukars can that
generate lift values estimated at between 10.4–12.2 N/kg of body mass (using the muscle-
specific power output value of 360 W/kg per Askew, Marsh & Ellington, 2001) which
exceeds the minimum needed for takeoff (9.8 N/kg) (Marden, 1994). Therefore, if wing
area can partially overcome the need for significant muscle mass fractions arguments on
the need for a selective pathway to muscle hypertrophy need not be invoked when
discussing the origins of flight. This would also help explain the lack of features indicating
significant hypertrophy in pectoral musculature, such as a lack of a sternal plate, in
the earliest fliers (Zheng et al., 2014) and the delayed presence of a keel until
Ornithothoraces (O’Connor & Zhou, 2015). These findings suggest that powered flight
originated before pronounced muscle hypertrophy and likely depended more on wing
loading and shoulder mobility. Thus, the pathway to large pectoral muscles is one that
occurred within Aves, not before and likely is linked to the refinement and extension
of level flight capabilities.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 24/41
For WAIR, a similar tradeoff between muscle mass and wing area likely exists. In
juvenile galliforms, flight muscle mass increases logistically throughout ontogeny. In
Chukars this goes from about 2% in crawling, non-WAIR capable 3 dph juveniles to
26–29% in 100 + dph adults (Heers & Dial, 2015). Individuals capable of stage I WAIR
(8 dph, maximum WAIR angle 65) have proportional muscle masses between 7.5–9.9%
of body mass, which represents 25–40% of adult proportional pectoral mass values
(Heers & Dial, 2015). They also show wing loading values only 55–60% those of an adult,
which should be noted can achieve much larger maximum WAIR angles (> 90). A similar
pattern is seen in both late Stage II WAIR Chukars and in juvenile Peafowl. The former
can ascend up to 85despite showing reduced pectoral muscle mass relative to body mass
(48–62% adult values) but have wing loading values only 40% those of adult birds.
Juvenile peafowl, which at 12 dph can achieve higher WAIR angles than adults, display less
than half the relative pectoral muscle mass fraction of adults, but have wing loading value
of only 1/4 to 1/3 that seen in adults (Heers & Dial, 2015). This suggests that reducing
wing loading could partially compensate for the lower proportional muscle mass, an
idea that is also supported by findings in Brush Turkeys where low wing loaded juveniles
can WAIR whereas adults cannot (Dial & Jackson, 2011).
We generated a model for Chukar WAIR ontogeny that predicts wing loading, pectoral
mass, maximum WAIR angle, and age using data from Heers & Dial (2015) (Fig. 4).
Most relationships are nonlinear and multimodal, suggesting complex interactions between
these factors. The original and modeled data show an inflection point between 20–30 dph.
Up to this age, maximum WAIR angle asymptotes at less than 90(Jackson, Segre & Dial,
2009;Heers & Dial, 2015). This corresponds to when the pectoral muscles reaches ∼20%
total body mass and the beginning of Stage III where both extended level flight and vertical
flight is possible (Jackson, Segre & Dial, 2009). Here is also when we begin to see, through in
vivo measurements, the steady increase in wing loading values from their minimum of
55 N/m
2
at day 22 continuing upwards to the full term (100 + dph) score of 161 N/m
2
.
Early stage Chukar chicks have forelimb masses within the range suspected for non-
avian theropods (up to 15 dph) and we see a correlation among these chicks between
maximum WAIR angle and lower wing loading (Figs. 4 and 5). WAIR capable Chukar
chicks during this period, which corresponds to late Stage I through Stage II of Jackson,
Segre & Dial (2009), show relatively constant wing beat frequencies (22–26 Hz) and flap
angles (∼140) further supporting the idea that wing loading is a major factor influencing
maximum WAIR angle. Wing loading values in WAIR capable galliforms are significantly
below that seen in much of our dataset and only eight specimens, pertaining to five
paravian taxa show wing loading values below 200 N/m
2
(Table 1;Fig. 5). Of these, only
Microraptor, a juvenile Anchiornis, and Eosinopteryx show wing loadings that, according to
this model, suggest WAIR is even possible. Given that the flapping frequencies and stoke
angles under those seen in the extant Chukars for which this relationship between this
compensatory mechanism for low muscle mass occurs, the levels they achieve are likely
beyond non-avian theropods. This suggests that this compensatory pathway would likely
be less efficient or even unavailable to most non-avian theropods, again likely restricting
WAIR potential to only the microraptorines.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 25/41
(N / sq m)
Figure 4 3D scatterplot of values for Chukars modeled for the first 70 days of growth. 2D projections
of the values are shown on each axis-pair plane with grey circles. Age, pectoral limb muscle mass, wing
loading, and WAIR performance data are from Heers & Dial (2015). Maximum WAIR angle was limited
to 100. Regressions were neither linear nor unimodal suggesting a complex interaction between
musculoskeleletal and aerofoil ontogeny and performance. Mass (g) was estimated from age by the
quadratic equation 5.730818 + 3.472647 x+-0.011605 x
2
+ 0.000661 x
3
(R
2
= 0.9902); only ages
less than 100 days were used. Percent pectoral mass was estimated from mass by the quadratic equation
0.858022 + 0.231592 x-0.000658 x
2
5.9340
-7
x
3
(R
2
= 0.92). Wing loading was estimated
from mass by the quadratic equation 1.692164 + -0.018717 x + 8.756264
-5
x
2
+-9.483335
-8
x
3
(R
2
= 0.69). Maximum WAIR angle was estimated from mass by the quadratic equation 38.119489 +
1.137820 x+-0.007969 x
2
+ 1.925223e -05 x
3
(R
2
= 0.9575).
Figure 5 Regression of measured wing loading versus maximum. WAIR angle in Chukar chicks aged
3–15 day post hatching and estimates for selected non-avian theropods. Chuckar data are from Heers &
Dial (2015). Large circles denote Chukar values with their age given as the number inside. Regression for
Chuckar data is 100.17 -20.824x, R2 = 0.848. Small circles denote estimated paravian theropods. Only
specimens with wing loading values comparable to those seen in Chukars (< 2.0 g/cm
2
= 196 N/m
2
) were
included. Demarcation of quadrupedal crawling to WAIR at 65was based on Jackson, Segre & Dial
(2009). Non-avian theropods are: f1, Anchiornis huxleyi BMNHCPH828; f2, Anchiornis huxleyi LPM
B00169; f3, Aurornis xui YFGP-T5198; f4, Changyuanraptor yangi HG B016; f5, Eosinopteryx brevipenna
YFGP-T5197; f6, Microraptor gui BMNHC PH 881; f7, M. gui IVPP V 13352; f8, M. hanqingi LVH 0026
(light mass estimate); f9, M. hanqingi LVH 0026 (heavy mass estimate).
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 26/41
Our first principles modeling approach, which accurately predicts WAIR values for
Chukar chicks, supports the postulate that for these “near flight” behaviors, wing area is
the major determinant of function rather than power. Many possible selective regimes can
be put forward for driving the expansion of wing area before it would provide any
locomotory benefit. These include display (Hopp & Orsen, 2004;Zelenitsky et al., 2012), egg
shielding (Carey & Adams, 2001), braking, or balance (Fowler et al., 2011), and our results
suggest that they need to be investigated in greater detail in order to understand the drivers
for major pre-requisites for the flight stroke and reduced wing loading. The flight stroke
itself, once we have divorced it from the early expansion of the wing and the origin of
pennaceous feathers, likely occurred after expansion into the wing-loading region where
wing based locomotory regimes are possible. Thereafter, multiple possible scenarios can be
sought to explain the origin of flight stroke and flight itself, with potentially different
scenarios occurring in different lineages. Our data indicates that, whichever scenario,
WAIR would be restricted in its functional presence to, at the earliest, small-bodied Paraves
or more likely the base of Aves; well after previous suggestions (Heers & Dial, 2012).
Ontogenetic versus phylogenetic signals
The findings of our model that all non-paravian theropods and most deinonychosaurians
were incapable of using WAIR, raises the question of when along the lineage could WAIR
have evolved and under what selective context? As our data shows there is no evidence of
WAIR in non-paravian theropods, this challenges the hypothesis that modern bird
ontogeny recapitulates the pathway to the origin of flight. Although it is tempting to
suppose that behaviours young, non-volant extant birds undertake can offer some insight
into the origins of flight, modern bird chicks do not present plesiomorphic morphologies.
Although extant birds hatch with somewhat reduced forelimb muscle masses and
feathering, the musculoskeletal morphology is still generally comparable with adult extant
fliers. For example, near-hatchling quail embryos do not have an ossified sternal keel, but
instead have a cartilaginous or connective tissue based on (Meneely & Wyttenbach, 1989;
Tahara & Larsson, 2013;Fig. 5). Some birds, such as chickens, which are bred for greatly
enlarged pectoral muscles, do develop a broad sternum with a robust midline keel in
ovo (Hall & Herring, 1990). In most non-avian theropods, including many small
paravians, the sternum is either composed of a pair of unfused plates or completely absent
(Xu, Wang & Wu, 1999;Hwang et al., 2002;Gong et al., 2012;Godefroit et al., 2013;Zheng
et al., 2014;Lu
¨& Brusatte, 2015) with the notable exception of Microraptor gui (Xu et al.,
2003), thus it is unlikely to have even a cartilaginous or rudimentary keel seen in juvenile
birds. Beyond this the oblique acrocoracohumeral ligament orientation and triosseal
canal and a dorsally oriented glenoid fossa are also present in extant avian embryos, even
in poor fliers like Chukars, but not in non-avian theropods. These differences combined
with those in muscle mass and neuromuscular pathways differentiate the ontogentic
transitions of juvenile birds from evolutionary ones regarding avian origins. This is
especially true as the exemplar non-avian theropod taxa (Dial, Randall & Dial, 2006;
Heers & Dial, 2012;Heers & Dial, 2015) do not represent an anagenic sequence but
are instead derived members of lineages separated by tens of millions of years.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 27/41
Modified flapping behaviors are present in other birds that can’t fly, such as steaming in
pre-fledgling ducklings (Aigeldinger & Fish, 1995), begging and signaling in altricial chicks
(Ryde
´n & Bengtsson, 1980;Glassey & Forbes, 2002;Ngoenjun & Sitasuwan, 2009), and
social displays and thermoregulation in Ostriches (Bolwig, 1973;Mushi, Binta & Lumba,
2008). This indicates that even in the most basal lineage of extant avians, the ancestral
flight stroke has been modified by juvenile and non-volant individuals to perform other
tasks. Even late stage avian embryos and wingless hatchlings perform coordinated
flapping motions on their own and when stimulated (Hamburger & Oppenheim, 1967;
Provine, 1979;Provine, 1981a;Provine, 1981b;Provine, 1982) showing that the
neurological pathway for flapping motion is active and functioning before hatching in
precocial birds (Provine, 1979). These embryonically established neural controls are thus
available to the earliest hatchlings of modern birds (volant or not) but non-avian
theropods may not have had neuromuscular control or the coordinated flapping
behaviours even extant chicks do.
Although ontogenetic trajectories are relatively linear, with regards to a species,
phylogenetic trajectories are not. The WAIR capabilities of extant birds may be a direct
result of their advanced powered flight adaptations rather than a precursor for it. Because
the factors that facilitate WAIR are the same as those that permit flight (increased wing
area, muscle resources, and flapping arc), WAIR may be more of a spandrel that extant
birds have capitalized on rather than a selective pathway. Thus, we propose instead that
juvenile birds exapted the flight stroke for use as an escape technique before they were
capable of takeoff and flight, and this derived escape response was only possible once the
complex flight adaptations of derived birds evolved.
Ground takeoff
Although no thrust based locomotory method succeeded in providing an adequate
evolutionary pathway with an obvious evolutionary trend that surpassed biophysical
thresholds, some individual specimens did succeed at crossing these thresholds under
certain parameters. Notably, Microraptor gui and Archaeopteryx showed significant results
in all three methods. Interestingly, both taxa were estimated to have had the potential for
ground based takeoff at both sprint speeds and leaping takeoff values (Tables S8 and S11–
S13). Given the effects of flap running’s thrust generation (though see potential
limitations below), takeoff speeds can be achieved with a starting velocity well within the
range of similar sized extant tetrapods. Even a sprint speed, without wing assistance, of 7
m/s is not unrealistic given greater speeds are obtained by the Roadrunner (Lockwood,
2010), Red legged Seriemas (Abourachid, Ho
¨fling & Renous, 2005), multiple small
mammals (Iriarte-Dı
´az, 2002), and some lizards (Huey, 1982;Clemente, Thompson &
Withers, 2009).
Living birds that launch by running are overwhelmingly aquatic or semi-aquatic taxa,
suggesting that running takeoff is mostly an adaptation to compliant surfaces (as
referenced in Earls (2000)). Other birds utilize a leaping takeoff to initiate flight with high
instantaneous speeds during leaping (Biewener, 2003), easily matching the values used
here. The required speed values for takeoff we calculated could be lowered if we assumed a
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 28/41
coefficient of lift above 1.5, similar to those seen during takeoff in extant birds
(Usherwood, 2009) or if we reduced our mass estimates. Microraptor has an elongated
hindlimb, especially when compared to basal birds of similar snout-vent length (Dececchi
& Larsson, 2013). These proportionately longer hindlimbs may have not only increased
top running speed, as leg length is related to stride length and speed (Garland & Janis,
1993;Hoyt, Wickler & Cogger, 2000), but also leads to an overestimation of body mass
because body masses for theropods are generally derived from femur length (Dececchi &
Larsson, 2013). If we reduce the mass of Microraptor gui (IVPP V 13352) to that of a
similar sized Archaeopteryx specimen (Solnhofen) we get a mass estimate of between 0.4–
0.6 kg, or between 42–67% of the value used here for IVPP V 13352. This is similar to
differences we see between mass estimates of femur length and 3D models for LVH 0026
(Tables S1 and S14). Using 0.6 kg for Microraptor, values greater than 1.0 bw are achieved
at speeds of only 3.8 m/s, and even less if Cl values closer to extant birds of 1.64 are used.
This suggests that at reasonable speeds, even with a coefficient of lift below that of extant
birds, Microraptor was likely capable of ground based take off. Also during leaping take off,
the horizontal velocity of birds increases rapidly after the first few strokes (Berg &
Biewener, 2010). Therefore, effective flight strokes coupled with a strong ability to jump
would supply ample velocity to help achieve vertical takeoff.
Although no single locomotory behaviour tested here surpasses minimal thresholds for
high incline running or powered flight, a flight stroke in stem avians may have had
performance benefits to biomechanical scenarios that are more difficult to test.
Specifically, feathered forelimbs, coupled with a nascent flight stroke, may have
contributed subtle, but evolutionarily advantageous performance benefits to high speed
maneuvering and braking and balancing during prey capture. Even slight performance
enhancements to vertical and horizontal leaping may have had highly positive adaptive
effects. Enhancements of even a few percent may had tremendous advantages to these
animals, particularly if we compare the small margins of performance differences of extant
predator-prey interactions. Unlike leaping, WAIR is a behavior with minimal thresholds
that must be overcome. As such incremental gains cannot be achieved until that threshold
is reached, something that we find, despite our relaxed conditions, is not present in the
majority of non-avian theropods and may have been restricted solely to the
microraptorines and avians. Thus, the hypothesis that incremental gains in WAIR would
have adaptive benefits and drove forelimb and pectoral evolution in non-avian theropods
is not supported as no non-paravian maniraptoran show any capability to perform this
behavior.
CONCLUSION
All models tested here suggest that the feathered forelimbs of all non-paravian theropods
and most non-avian theropods were not capable of surpassing the minimal physical
thresholds of powered flight and WAIR. The origin of pennaceous feathers was not tied to
a dramatic locomotory shift in these early non-avian theropods. Non-paravian taxa
such as Caudipteryx,Similicaudipteryx, and Yixianosaurus have forelimb feathers greater
than 100 mm in length, and similar sized feathers are suspected on other oviraptorosaurs
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 29/41
(Paul, 2002;Hopp & Orsen, 2004), large dromaeosaurs (Depalma et al. 2015) and even
ornithomimids (Zelenitsky et al., 2012;van der Reest, Wolfe & Currie, 2016). These
structures represent a significant energetic investment for structures that we estimate to
have had minimal locomotory benefits. Moreover, the symmetry of the vanes of the
pennaceous feathers in these taxa would make the feathers aeroelastically unstable, further
constraining their use in a locomotor context (even the pennaceous feathers of
microraptorines may have been somewhat unstable during aerial locomotion, with vane
asymmetries below the critical values for functional aeroelastic flutter reduction see
Feo, Field & Prum (2015)). These taxa also possessed large tail feathers that were likely
used for display (Pittman et al., 2013;Persons, Currie & Norell, 2014) and feather melanin
based pigmentation likely coincides with the origin of pennaceous feathers (Li et al., 2010;
Li et al., 2014). This suggests other non-locomotory functions such as display or brooding
were likely significant evolutionary driver for pennaceous feather growth (Hopp &
Orsen, 2004;Zelenitsky et al., 2012).
The mosaic evolution of flight related characters suggests the evolution of the flight
stroke was not continuous in this clade, nor driven by a single overall driver. If different
behavioural traits or selective regimes and not a single locomotory function were driving
the evolution of feather elongation, one may not expect the concordance of “pre-flight”
characters in different coelurosaur clades or even in all members of a single clade. This
would explain the non-uniform distribution of traits such as the elongated forelimbs with
well-developed feathers (Dececchi & Larsson, 2013;Godefroit et al., 2013;Foth, Tischlinger
& Rauhut, 2014), laterally facing glenoid (Gao et al., 2012), and an ossified sternum for
muscle attachment (Zheng et al., 2014).
Although it is beyond the scope of this paper to speculate on which driver or
combination of drivers led to feather elongation and forelimb musculoskeletal
evolution for powered flight, we suggest that future research not focus on any single
event or “pathway” to attempt to explain pre-avian evolution of characters later
exapted into the flight apparatus. Given the time between the Paravian-avian split and
the appearance of the Jehol microraptorines is approximately 40 million years,
estimated from the oldest known paravian Anchiornis (161 Ma) and Microraptor
(120 Ma) (Xu, Zhou & Wang, 2000;Xu et al., 2009) a single continuous locomotory
based evolutionary driver is unlikely. Moreover, it seems unparsimonious to argue that
refining flapping based locomotion was central to the evolution of maniraptorans
when the lineages show marked difference in their ecology, body size, limb usage and
feather extent.
Although the selective pressures for each of these traits is unknown, what is apparent is
it that pennaceous feathers and other critical characters related to the evolution of
powered flight were not originally adapted for significantly different locomotion. It is also
clear that WAIR was not a major driver for the evolution for much of Maniraptora or even
Paraves. These findings reshape how we view the origins of birds and the evolution of
different maniraptoran clades and refocus our investigations to look at taxa not as steps of
a ladder towards the origin of flight, but as organisms adapting to the unique demands of
their immediate behavioural and ecological surroundings.
Dececchi et al. (2016), PeerJ, DOI 10.7717/peerj.2159 30/41
ADDITIONAL INFORMATION AND DECLARATIONS
Funding
The authors received no funding for this work.
Competing Interests
The authors declare that they have no competing interests.
Author Contributions
T. Alexander Dececchi conceived and designed the experiments, performed the
experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the
paper, prepared figures and/or tables, reviewed drafts of the paper.
Hans C.E. Larsson contributed reagents/materials/analysis tools, wrote the paper,
prepared figures and/or tables, reviewed drafts of the paper.
Michael B. Habib conceived and designed the experiments, performed the experiments,
contributed reagents/materials/analysis tools, wrote the paper, reviewed drafts of
the paper.
Data Deposition
The following information was supplied regarding data availability:
Dryad: 10.5061/dryad.1f5h4.
Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/
10.7717/peerj.2159#supplemental-information.
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