applied sciences

Article from Cursorial Running to Aerial for Avian

Farzeen Shahid 1, Jingshan Zhao 1,* and Pascal Godefroit 2

1 State Key Laboratory of Tribology, Department of Mechanical Engineering, Tsinghua University, 100084, .; [email protected] 2 Royal Belgian Institute of Natural Sciences, Vautier street 29, 1000 Brussels, Belgium; [email protected] * Correspondence: [email protected]

 Received: 31 December 2018; Accepted: 5 February 2019; Published: 14 February 2019 

Abstract: Among the different models that have been proposed to explain the origin of avian flight from terrestrial predators, the cursorial and arboreal hypotheses remain the most discussed. However, the data at hand show that, taken separately, both theories have significant limitations in explaining the origin of flight in lineage. Here, we describe an aerodynamics principle that fills in the gaps between those apparently contradictory models. The upslope wind in mountain areas and strong wind in plains provided the meteorological conditions allowing feathered paravians to glide. The results suggest that smaller, feathered paravians could be lifted to glide down to trees on mountain slopes or even to glide up to high trees in plain areas when meeting a strong airflow as they were pursuing a prey or escaping from a predator. The development of more aerodynamical was a key factor for gliding down the trees because of the dependency of the resultant force on the surface area of a paravian’s body. Later in the evolution process, paravians learned to change the orientation of their to gain higher lifts. The proposed principle and the results obtained in the present research help to better estimate the aerodynamic behavior of extinct and will also help to design an efficient and beneficial system for future flying robots.

Keywords: avian flight; cursorial running; arboreal gliding; aerodynamics; huxleyi; evolution

1. Introduction In modern science, researchers take inspiration from living organisms, such as , , , fishes, etc., and incorporate their behavior into artificial yet useful products. Bio-inspired Micro Aerial Vehicle (MAV) and bionic robots open up a vast and boundless area of research, which is beneficial for industries, commercial companies, and academic institutions. It is a difficult task to mimic the extraordinary amount of maneuverability of flying , but by doing so, we can also have an estimate of their aerodynamic performances and biological [1]. In flying animals, wings are one of the most important anatomical features, because control, power, and flight forces are generated by their motion [2]. In modern birds, layers of feathers over the [3] provide different functions during flight, but these feathers passed through an evolutionary process to reach their current structured stage [4]. Recent discoveries of feathered and winged [5] have shed new light on the evolution and origin of flight in bird lineage. Since the discovery of in Germany in 1861, the origin of flight in birds has caused fierce debate among paleontologists [6–10]. It is now widely accepted that birds are closely related to paravian theropods, a of small, carnivorous dinosaurs that also include and [10]. Since the discovery of in 1998 [11], Late and Early

Appl. Sci. 2019, 9, 649; doi:10.3390/app9040649 www.mdpi.com/journal/applsci Appl. Sci. 2019, 9, 649 2 of 14

Cretaceous formations in northeastern China have yielded numerous exquisitely preserved of feathered dinosaurs that document the cumulative evolution of avian characters along the theropod lineage [12–16]. It has also been shown that the theropod lineage, which is directly ancestral to birds, underwent sustained miniaturization over 50 million and evolved skeletal adaptations four times faster than other dinosaurs. After two decades of discoveries, feathers and -related structures are known to be widespread among dinosaurs, with more than 50 non-avialan paravian taxa, known from a series of fossils with great ranges of size, osteology, limb proportions, and integumentary covering [4,10]. Although the was not developed for flight initially [5,10,17–20], the feather subsequently provided aerodynamic capabilities for gliding and flapping flights [12,16]. Nevertheless, there is still an intriguing question about how paravian dinosaurs learned to fly [5,8,9]. Traditionally, paleontologists have advanced two theories for explaining the origin of avian flight. The arboreal model, proposed by Marsh in 1880 [7], holds that flight developed in a climbing, tree-dwelling ancestor that was built for gliding but started flapping to extend its aerial time [7,12,20,21]. Archaeopteryx possessed the same claw curvature of the foot as that of perching birds, suggesting arboreal habits for this ancestral bird [22–24]. However, evidence for trunk-climbing in Archaeopteryx and basal birds is still weak, and the arboreal model is far from being unanimously accepted [6,15] According to the competing cursorial model, originally outlined by Williston in 1879, flight arose in small, bipedal, terrestrial theropod dinosaurs that sped along the ground with arms outstretched and leapt into the air while pursuing prey or evading predators. Feathers on their enhanced the , thereby allowing the creatures to take flight [6,7,12]. However, long leg feathers were developed in a series of basal paravians and birds and were obviously an obstacle for speeding up to glide or fly [16,21,25]. In addition, the flight muscles of Archaeopteryx only represented 9% of the body mass [26], which is far less than the average 25% of the body mass found in modern birds [27]; hence, Archaeopteryx likely had a particularly short and ineffective flapping flight, and, because of its higher mass, Archaeopteryx would have to run much faster than modern birds to achieve lift-off. The wing-assisted incline running (WAIR) hypothesis is a derived version of the cursorial model prompted by observations of chukar chicks; it proposes that wings developed their aerodynamic functions as a result of the need to run quickly up very steep slopes, such as tree trunks, to escape from predators. The progression from wing-assisted incline running to flight can be seen in the growth of birds, from when they are hatchlings to fully grown adults [18]. This article is divided into the following sections: Section2 describes the environmental conditions that prevailed in northeastern China during the and Early period, along with the mechanisms of upslope and downslope winds. A vector diagram depicting the instantaneous and relative velocities of airflow and basic aerodynamics in Anchiornis is introduced in Section3. In Section4, calculations for lift and coefficients and the mass and size of ancestral bird are presented. The results of the trajectories of Anchiornis, arboreal gliding evolution, and stability control during gliding are discussed in Section5. Finally, the article is concluded in Section6.

2. Paleoenvironment of the Earliest Feathered Paravian Dinosaurs The Jurassic and era was a period of intense tectonic movements in eastern Asia. The most important event, known as the “Yanshan movement”, affected the northern margin of the North China Craton and was characterized by intensive tectonic deformation and extensive magmatism. The initial Yanshan movement began during the (), and its main phase took place in the Late Jurassic; the initiation point of this main phase is, for example, recorded in unconformities below the volcanic rocks of the in northern Hebei Province [28]. Volcanic activity was also intense in the area, as revealed by the abundance of intermediate-basic volcanic deposits, such as andesite, andesitic basal, basaltic andesite, and trachyandesite throughout the sequence. The Tiaojishan flora was dominated by , , and Nilssoniales, followed by ginkgophytes; the floristic signature indicates a subtropical-to-temperate warm and humid climate, Appl. Sci. 2019, 9, 649 3 of 14 with a consistent and distinct seasonal pattern [29]. In general, the vertebrate fauna of the Tiaojishan Formation are typically preserved in fine-grain lacustrine beds [30]. Chinese Anchiornithids, therefore, lived in a particularly rugged environment, including mountains and volcanos,Appl. Sci. under 2019, 9 FOR a warm, PEER REVIEW humid climate. Such mountain environments are characterized3 by frequent upslopeChinese winds, Anchiornithids from valleys, therefore, to the lived top ofin thea particularly mountains rugged along environment, the mountainside including (Figure 1a), in the daytimemountains and downslopeand volcanos, windsunder (Figurea warm,1 b)humid at night climate. [ 31 Such–33]. mountain The natural environments upslope are wind in the daytime allowedcharacterizedAppl. Sci. 2019 the, 9 theropods byFOR frequent PEER REVIEW upslope to move winds, from from the valleys ground to tothe the top tall of the trees mountains on the mountainside.along the 3 In normal conditions,mountainside the (Figure maximum 1a), in speed the daytime of the and upslope downslope wind winds varies (Figure between 1b) at 1 night and 12[31–33]. m/s The [31 ,32], with naturalChinese upslope Anchiornithids wind in the daytime, therefore, allowed lived the inther aopods particularly to move ruggedfrom the environment, ground to the tallincluding trees significanton seasonalmountains the mountainside. variationsand volcanos, In normal [33 ].under Whenconditions, a warm, a strong the mahumidximum wind climate. speed occurs ofSuch the in summer,upslopemountain wind theenvironments varies speed between of are the airflow frequently1 reachescharacterizedand 12 m/s 45 [31,32], m/sby frequent with [34]. significant Thereupslope isseasonal winds, no reason variationsfrom valleys to believe[33]. to When the that atop strong theof the wind natural mountains occurs meteorological in summer,along the rules observed inthemountainside today’s speed of worldthe (Figureairflow are 1a),frequently not in applicable the daytimereaches to45 and m/s the down [3 Jurassic4]. slopeThere winds world.is no reason (Figure to 1b) believe at night that [31–33].the natural The meteorologicalnatural upslope rules wind observed in the daytime in today’s allowed world the are ther notopods applicable to move to the from Jurassic the ground world. to the tall trees on the mountainside. In normal conditions, the maximum speed of the upslope wind varies between 1 and 12 m/s [31,32], with significant seasonal variations [33]. When a strong wind occurs in summer, the speed of the airflow frequently reaches 45 m/s [34]. There is no reason to believe that the natural meteorological rules observed in today’s world are not applicable to the Jurassic world.

FigureFigure 1. Mechanism 1. Mechanism of of wind: wind: ( a)) upslope; upslope; (b) (downslope.b) downslope.

3. Gliding3. Aerodynamics Gliding Aerodynamics in Basal in Basal Paravian Paravian Dinosaurs Dinosaurs

A terrestrialA terrestrial basal paravian basal paravian theropod, theropod,Anchiornis Anchiornis,, running running to capture to capture a prey a or prey to escape or to from escape a from a Figure 1. Mechanism of wind: (a) upslope; (b) downslope. predator on the top of a mountain, had an initial absolute velocity 𝒗𝒕, which was high enough to be predator on the top of a mountain, had an initial absolute velocity vt, which was high enough to be its capacity of running when it encountered an upslope airflow, the velocity of which was 𝒗𝟐 at the 3. Gliding Aerodynamics in Basal Paravian Dinosaurs its capacitybrim of runningof the summit when of the it mountain. encountered The relative an upslope velocity airflow,of the upslope the velocityairflow with of respect which to was the v2 at the brim of theAnchiornis summitA terrestrial 𝒗 ofshould the basal mountain.be the paravian resultant Thetheropod, velocity relative Anchiornisof 𝒗𝒕 velocityand 𝒗, 𝟐running, mathematically of the to capture upslope written a prey airflow asor follows:to escape with from respect a to the Anchiornis vpredator on the top of a mountain, had an initialv absolutev velocity 𝒗𝒕, which was high enough to be should be the resultant velocity of𝑣=𝑣t and −𝑣 2, mathematically written as follows:(1) its capacity of running when it encountered an upslope airflow, the velocity of which was 𝒗𝟐 at the brimA ofbalance the summit of projected of the liftmountain. and drag The on relative an Anchiornis velocity body of the is shown upslope in airflow Figure 2a,with and respect its weight to the v = v2 − vt (1) isAnchiornis determined 𝒗 should by the be effective the resultant projection velocity area of of 𝒗 𝒕its and body 𝒗𝟐, mathematicallyin the equivalent written cord asEF. follows: The velocity diagram is separately shown in Figure 2b, where the initial absolute velocity 𝒗𝒕 is divided into the 𝑣=𝑣 −𝑣 (1) A balancehorizontal of projected and vertical lift andcomponents, drag on 𝒗𝒙 an andAnchiornis 𝒗𝒚 , respectively,body isand shown 𝜽 is the in Figureslope angle2a, and of itsthe weight is determinedmountainside. by theA balance effective of projected projection lift and area drag of on its an body Anchiornis in the body equivalent is shown in cord Figure EF. 2a, The and velocityits weight diagram is determined by the effective projection area of its body in the equivalent cord EF. The velocity is separately shown in Figure2b, where the initial absolute velocity vt is divided into the horizontal diagram is separately shown in Figure 2b, where the initial absolute velocity 𝒗𝒕 is divided into the and vertical components, vx and vy, respectively, and θ is the slope angle of the mountainside. horizontal and vertical components, 𝒗𝒙 and 𝒗𝒚 , respectively, and 𝜽 is the slope angle of the mountainside. y

D FL v y B F v2 α y ϕ vt FD A B o x v2 D θ F E FL v v y α B F θ vy ϕ A v2 α ϕ vt C vt FD mg A B o x v2 x θ o vx E F (a) E (b)v α θ vy ϕ A C vt Figure 2. An Anchiornismg body with (a) a balance of projected lift and drag; (b) velocity diagram x containing the relative airflow. o vx (a) E (b)

Figure 2. AnFigureAnchiornis 2. An Anchiornisbody withbody with (a) a(a) balance a balance of of projectedprojected lift lift and and drag; drag; (b) velocity (b) velocity diagram diagram containing the relative airflow. containing the relative airflow. Appl. Sci. 2019, 9, 649 4 of 14

The magnitude of the relative velocity can be obtained in line with the cosine law of triangle, q 2 2 v = (vx + v2cosθ) + v2sinθ − vy . (2)

According to the sine law of triangle,   v2sinθ − vy ∠BAC = arctan . (3) v2cosθ − vx

The (α) between the equivalent EF and the relative velocity v is given below,   v2sinθ − vy α = ϕ + ∠BAC = ϕ + arctan . (4) v2cosθ − vx

In accordance with the aerodynamics theory, we obtain the following:   1 2 1 h 2 2i  FL = 2 CLρsv = 2 CLρs (vx + v2cosθ) + (v2sinθ − vy)  (5) 1 2 1 h 2 2i  FD = 2 CDρsv = 2 CDρs (vx + v2cosθ) + (v2sinθ − vy)  where FL represents the magnitude of lift, which is perpendicular to the relative velocity v, and FD represents the magnitude of drag, which is along the relative velocity v, as illustrated in Figure2b. Both FL and FD result from the aerodynamics of airflow; CL and CD are the lift and drag coefficients of Anchiornis, which are all the functions of the angle of attack as expressed in Equation (4); ρ is the density of airflow; and s is the effective area of Anchiornis. Therefore, the resultant force exerted on Anchiornis of mass m is given by Equation (6), and the trajectory of Anchiornis is determined by the resultant forces in vertical and horizontal directions when it leaves the ground. The dynamics differential equations for Anchiornis can be obtained from Equation (6) and are presented by Equation (7):

"  #  Rx vx, vy, v2  R =   Ry vx, vy, v2   " #  FLsin∠BAC − FDcos∠BAC  R =  FLcos∠BAC + FDsin∠BAC − mg  q ! (6)  1 2 2  ρs (vx + v2cosθ) + (v2sinθ − vy)  2   − − −     v2CLsinθ CLvy CDvx CDv2cosθ   R =  q !    1 ρs (v + v cosθ)2 + (v sinθ − v )2    2 x 2 2 y     CLvx + CLv2cosθ + v2CDcosθ − CDvy − mg q d2x ρs 2 2  m − (vx + v2cosθ) + (v2sinθ − vy)  dt2 2  v C sinθ − C v − C v − C v cosθ = 0  2 L L y D x D 2 (7) d2 q m y − ρs (v + v cos θ)2 + (v sin θ − v )2  dt2 2 x 2 2 y    CLvx + CLv2cosθ + v2CDcos θ − CDvy − mg = 0

2 2 d x d y where dt2 and dt2 represent the accelerations of Anchiornis in the horizontal and vertical directions, dx dy respectively, and vx = dt = v1, vy = dt = 0 when t = 0. The vertical and horizontal components of the resultant forces are affected by the relative velocity v, the inclined angle of the mountain’s slope θ, and the coefficient of lift and drag CL and CD . The displacements of Anchiornis in the horizontal and vertical directions at any moment are the functions of the ’s initial speed vt, the airflow speed v2, and the inclined angle of the mountain slope θ. If Anchiornis is gliding towards a perching point at the top of a tree, h is the height from the perching point to the root of the tree. We can analyze its Appl. Sci. 2019, 9, 649 5 of 14

minimum speed distribution with respect to the airflow speed v2 and the tilt angle θ of the slope of the mountain by the numerical solutions for Equation (7). When the inclined angle of the mountain slope θ is specified, the accelerations of Anchiornis in the horizontal and vertical directions have determinate distributions with respect to v2 and v2, as the lift coefficient CL and drag coefficient CD of the wing could be adjusted to have the best ratio of lift over drag, the formulas of which were interpolated from the simulation for the thin flat plate through the fluent software (more detail is presented in the Section4).

4. Materials and Methods

4.1. Lift and Drag Coefficients Any shaped object with an angle of attack moving through a fluid will generate an aerodynamic force, the perpendicular component to the motion is called lift, while the parallel component to the moving direction is called drag. Both the lift and drag on the moving body are the primary results of its angle of attack and shape. As the feathers of Anchiornis were still primitive, slender and weak [35,36], therefore, its wings might not have the most efficient lifting shapes, as shown in Figure S1(a). We used the most primitive , a thin flat plate, illustrated in Figure S1(b), with an angle of attack to replace its stretched wing. For the specified thin flat plate, the lift coefficient and drag coefficient are all the functions of the angle of attack. So, we supposed that the relationship between the angle of attack and the lift and drag coefficients are as follows:

( 2 n CL = x0 + x1α + x2α + ... + xnα 2 n (8) CD = y0 + y1α + y2α + ... + ynα where CL is the lift coefficient, CD is the drag coefficient, α is the angle of attack in radian, and x1 and y1 (i = 0, 1, 2, . . . , n) are the coefficients of the angle of attack to be determined via simulations. To get the coefficients of lift and drag of the thin flat plate, we ran the simulation program in fluent software with different angles of attack. The simulation started from 0◦ to 88◦, with an increment of 2◦ for each step. Substituting the simulation results into Equation (4), we obtained the relationship between the lift coefficient, drag coefficient, and ratio and angle of attack.

2 CL = 0.053564912 + 1.6115306α − 1.0790198α 2 3 CD = −1.0077079 + 2.1219473α − 0.20780579α + 0.077390225α C (9) L = 0.070129975 + 46.01297α − 246.18671α2 + 579.0272α3 − 733.19925α4+ CD 518.02613α5 − 192.46611α6 + 29.323193α7.

With the simulation data, we drew C , C and CL through MATLAB, as represented in Figure S2. L D CD Using the least square method, we gained their individual interpolated curves to fit these 3 groups of points.

4.2. Mass and Size Parameters of the Ancestors of the Bird The acceleration of gravity and density were selected from the engineering toolbox. The mass of different dinosaurs were obtained from published paleontological data. The calculation of the areas of the equivalent plate wings were performed as follows. First, we set up the three-dimensional (3D) models of the dinosaurs according to the parameters of the fossils in SolidWorks. Then, we measured the areas of the wings and legs, respectively. The surface area, A, is the sum of the 2 wings and hind limb wings. Taking as an example (Microraptor gui (IVPP V13352)) [21], the length of the scale bar is 5 cm, which is the reconstruction of M. gui showing the morphology and distribution Appl. Sci. 2019, 9, 649 6 of 14 of the pennaceous feathers. The length of the scale bar is 6 cm. Then, we constructed the 3D model of the dinosaurs according to these materials. We drew the sketch of the wing and the leg and then stretched the sketch in SolidWorks. Finally, we utilized the measuring tools of SolidWorks to get the areas of the wing and leg. The areas of the wings and the legs are 44035.122 mm2 and 33632.919 mm2, respectively. As the surface area mainly consists of 2 wings and 2 legs, the total area of the equivalent plate wing equals: A = 2 × (44035.122 + 33632.919) = 155336.082 mm2.

Appl.For Sci. the 2019 point, 9 FOR particlePEER REVIEW model of Anchiornis huxleyi, the differential equations for the gliding6 motion were solved using the𝐴=2× well-known(44035.122 Runge–Kutta + 33632.919 method.) = 155336.082 According 𝑚𝑚 to. the physical theory of momentum, the lift, the drag of the airflow, and the self-weight in gliding were taken into the balance For the point particle model of Anchiornis huxleyi, the differential equations for the gliding equation of flight in the air. For a multi-point particle system, we use the Newton–Euler method to motion were solved using the well-known Runge–Kutta method. According to the physical theory of establish their dynamics equations. Both the forward and inverse solutions could be discussed for the momentum, the lift, the drag of the airflow, and the self-weight in gliding were taken into the balance trajectoryequation control of flight of in the the ancestors air. For a of multi-point the bird in particle agile gliding.system, we use the Newton–Euler method to establish their dynamics equations. Both the forward and inverse solutions could be discussed for 5. Resultsthe trajectory and Discussion control of the ancestors of the bird in agile gliding.

5.1.5. Trajectories Results and of Discussion a Basal Paravian from Cursorial Running to Aerial Gliding By substituting the mass and size parameters of Anchiornis [36] into Equation (7), we can analyze 5.1. Trajectories of a Basal Paravian Dinosaur from Cursorial Running to Aerial Gliding its displacement and trajectory. Assuming that the initial velocity in the horizontal direction was 5 m/s and the inclinedBy substituting angle the of themass mountainside and size parameters was θ of= Anchiornis 30◦, we obtained [36] into Equation the trajectories (7), we can of Anchiornisanalyze , as its displacement and trajectory. Assuming that the initial velocity in the horizontal direction was 5 shown in Figure3a, as v2 changed from 0 to 12 m/s. When the speed of the upslope wind changed fromm/s 0 m/sand the to inclined 6 m/s withinangle of thisthe mountainside velocity range was of𝜽 = airflow, 30°, we obtained there was the almost trajectories no possibilityof Anchiornis for, the as shown in Figure 3a, as 𝒗 changed from 0 to 12 m/s. When the speed of the upslope wind changed creature to glide up to a tree𝟐 on the mountain slope, as shown in Figure3b. When the speed of the from 0 m/s to 6 m/s within this velocity range of airflow, there was almost no possibility for the upslope wind changed from 8 to 12 m/s within this velocity range of airflow, the creature could glide creature to glide up to a tree on the mountain slope, as shown in Figure 3b. When the speed of the up toupslope the branch wind changed of a tree from of 8 6-m to 12 height m/s within when this its velocity horizontal range displacement of airflow, the creature was about could 15 glide m on the mountainside,up to the branch as shown of a tree in Figureof 6-m3 heightc. The when detailed its horizontal calculation displacement for different was velocities about 15 is m illustrated on the in Figuresmountainside, S3–S5. as shown in Figure 3c. The detailed calculation for different velocities is illustrated in Figures S3–S5.

(a) (b) (c) ◦ FigureFigure 3. Trajectories 3. Trajectories of ofAnchiornis Anchiornis runningrunning at at a a speed speed of of 5 5m/s m/s and and 𝜽 = θ30°:= 30(a) 𝒗:(𝟐a changes) v2 changes from 0 from to 0 to 12 m/s; (b) 𝒗 changes from 0 to 6 m/s; (c) 𝒗 changed from 8 to 12 m/s. 12 m/s; (b) v2 𝟐changes from 0 to 6 m/s; (c)𝟐v 2 changed from 8 to 12 m/s.

Now,Now, assuming assuming that that the the initial initial velocityvelocity in in the the horizontal horizontal direction direction was was 5 m/s 5 m/sand the and inclined the inclined angle was 𝜽 = 10°,◦ we obtained the trajectories of Anchiornis, as shown in Figure 4a, as 𝒗𝟐 changed angle was θ = 10 , we obtained the trajectories of Anchiornis, as shown in Figure4a, as v2 changed from 0 to 12 m/s. When the speed of the upslope wind changed from 0 to 6 m/s within the velocity from 0 to 12 m/s. When the speed of the upslope wind changed from 0 to 6 m/s within the velocity range of airflow, the creature could barely glide on the mountainside, as shown in Figure 4b. When range of airflow, the creature could barely glide on the mountainside, as shown in Figure4b. When the speed of the upslope wind changed from 8 to 12 m/s within this velocity range of airflow, the thecreature speed of could the upslopeglide up windto a tree changed branch fromhigher 8 than to 12 1.2 m/s m when within its this horizontal velocity displacement range of airflow, was the creatureabout could 8–9 meters glide upon tothe a mountainside, tree branch higher as repres thanented 1.2 m by when Figure its 4c. horizontal The detailed displacement calculation was for about 8–9different meters onvelocities the mountainside, is illustrated in as Figures represented S6–S8. by Figure4c. The detailed calculation for different velocities is illustrated in Figures S6–S8. Appl. Sci. 2019, 9, 649 7 of 14 Appl. Sci. 2019, 9 FOR PEER REVIEW 7 Appl. Sci. 2019, 9 FOR PEER REVIEW 7

(a) (b) (c) (a) (b) ◦ (c) FigureFigure 4. Trajectories 4. Trajectories of ofAnchiornis Anchiornisrunning running at a speed speed of of 5 5m/s m/s and and 𝜽 =θ 10°:= 10 (a) :(𝒗𝟐a changes) v2 changes from 0 from to 0 to 𝒗 𝒗 𝜽 𝒗 12 m/s;12Figure m/s; (b) (v4.b2) Trajectorieschanges𝟐 changes from fromof Anchiornis 00 to 6 m/s; m/s; running (c ()c)𝟐v changes2at changesa speed from of from 85 tom/s 12 8 and to m/s. 12 m/s.= 10°: (a) 𝟐 changes from 0 to 12 m/s; (b) 𝒗𝟐 changes from 0 to 6 m/s; (c) 𝒗𝟐 changes from 8 to 12 m/s. Now,Now, assuming assuming that that the the initial initial velocity velocity in the horizontal horizontal direction direction was was 5 m/s 5 m/s and the and inclined the inclined angleangle was Now,wasθ = 𝜽 0 assuming=◦ ,0°, which which that corresponded corresponded the initial velocity to to the the case in case theon on thehorizontal the plain plain ground, direction ground, we wasobtained we 5 obtainedm/s the and trajectories the the inclined trajectories of Anchiornisangle was, 𝜽as = shown0°, which in correspondedFigure 5a, as 𝑣to thechanged case on from the pl0 ainto 12 ground, m/s. When we obtained the speed the trajectoriesof the wind of of Anchiornis, as shown in Figure5a, as v2 changed from 0 to 12 m/s. When the speed of the wind changedAnchiornis from, as 0 shownto 12 m/s in within Figure this 5a, velocity as 𝑣 changed range of from airflow, 0 to there 12 m/s. was Whenno possibility the speed for theof thecreature wind changed from 0 to 12 m/s within this velocity range of airflow, there was no possibility for the creature tochanged glide up from to 0any to 12tree, m/s as within shown this in velocity Figure range5b. The of airflow,detailed there calculation was no forpossibility different for velocities the creature is to glideillustratedto glide up toup in any toFigures any tree, tree, S9–S10. as as shown shown in in Figure Figure5 b.5b. TheThe detaileddetailed calculation calculation for for different different velocities velocities is is illustratedillustrated in Figures in Figures S9–S10. S9–S10.

(a) (b) (a) (b) Figure 5. Trajectories of Anchiornis running at a speed of 5 m/s and 𝜽 = 0°: (a) 𝒗𝟐 changes from 0 to 12 ◦ Figurem/s;Figure 5. (bTrajectories) 5.𝒗𝟐 Trajectories changes from of ofAnchiornis 0Anchiornis to 12 m/s.running running at a a speed speed of of 5 m/s 5 m/s and and 𝜽 = 0θ°:= (a 0) 𝒗:(𝟐 changesa) v2 changes from 0 to from 12 0 to 𝒗 12 m/s;m/s; ( b(b))v2𝟐 changes from from 0 0to to 12 12 m/s. m/s. Assuming that the initial velocity in the horizontal direction was 8 m/s and the inclined angle wasAssuming 𝜽Assuming = 0°, which that that the corresponded the initial initial velocity velocity to the in incase the the on horizontalhorizontal the plain direction directionground, waswe was obtained8 m/s 8 m/s and andthe the trajectories, theinclined inclined angle as angle was shownθwas= 0 𝜽◦, =in which 0°, Figure which corresponded 6a corresponded for Anchiornis to the to, as casethe 𝑣 casechanged on theon plainthe from plain ground,0 to ground, 12 m/s. we we obtained When obtained the the speed the trajectories, trajectories, of the wind as as shown changedshown in from Figure 0 to 6a6 m/s for withinAnchiornis this ,velocity as 𝑣 changed range of from airflow, 0 to there12 m/s. was When no possibility the speed for of Anchiornis the wind in Figure6a for Anchiornis, as v2 changed from 0 to 12 m/s. When the speed of the wind changed from tochanged glide up from to any 0 to tree, 6 m/s as withinshown thisin Figure velocity 6b. rangeWhen of the airflow, speed ofthere the waswind no changed possibility from for 8 Anchiornisto 12 m/s 0 to 6 m/s within this velocity range of airflow, there was no possibility for Anchiornis to glide up to withinto glide this up velocity to any tree, range as ofshown airflow, in Figure there was 6b. Whenthe possibility the speed for of Anchiornis the wind changedto glide upfrom to 83 tom. 12 m/s any tree,withinThe as this shownabove velocity analysis in Figure range is based of6b. airflow, When on Anchiornis there the speedwas; therefore, the of possibility the windsimilar for changed conclusi Anchiornisons from canto glide 8 be to drawn 12up m/sto when3 m. within we this velocityconsider rangeThe the above of mass airflow, analysis parameters there is based was of otheron the Anchiornis possibilityparavian; therefore, dinosaurs, for Anchiornis similar including conclusito glide Epidexipteryxons up can to be 3 [37], m.drawn Microraptor when we [38],Theconsider Archaeopteryx above the analysis mass [39], parameters is and based of on otherAnchiornis paravian [40], ;as therefore, summarizeddinosaurs, similar including in Table conclusions 1. These dinosaurs can [37], be drawn Microraptorare within when we considerthe[38], range theArchaeopteryx mass from parameters0.11 [39], kg to and 1.5 of Confuciusornis kg, other and paravian the effective [40], dinosaurs, as summarizedarea parameters including in Table areEpidexipteryx within 1. These the dinosaurs range[37], fromMicroraptor are 0.0132within [38], Archaeopteryxmthe2 to range 0.0496 [from39 m],2. and0.11Substituting Confuciusorniskg to 1.5 thekg, possibleand[ 40the], effectivemass as summarized and area size parameters parameters in Table are 1of. Thesewithindinosaurs dinosaursthe fromrange Table from are 1 within0.0132 into the rangeEquationm from2 to 0.0496 0.11 (7), we kgm2. tocanSubstituting 1.5 draw kg, the and theconclusions the possible effective thatmass areawh anden parameters sizethe runningparameters arespeed withinof dinosaursof a cursorial the range from dinosaur Table from 1 0.0132was into m2 to 0.0496fromEquation 5 m to2. 8(7), Substitutingm/s we and can thedraw tilt the the angle possibleconclusions of the mass mountainside that and when size the 𝜽parameters runningwas larger speed than of of dinosaurs0° a cursorialbut less fromthandinosaur 30°, Table wasthe1 into from 5 to 8 m/s and the tilt angle of the mountainside 𝜽 was larger than 0° but less than 30°, the Equation (7), we can draw the conclusions that when the running speed of a cursorial dinosaur was from 5 to 8 m/s and the tilt angle of the mountainside θ was larger than 0◦ but less than 30◦, the dinosaur could be lifted to follow a certain trajectory, falling into an interval that covered a tree on the mountainside. Appl. Sci. 2019, 9 FOR PEER REVIEW 8 Appl. Sci. 2019, 9, 649 8 of 14 dinosaur could be lifted to follow a certain trajectory, falling into an interval that covered a tree on the mountainside.

(a) (b) (c) ◦ FigureFigure 6. Trajectories 6. Trajectories of ofAnchiornis Anchiornis running at at a aspeed speed of 8 of m/s 8 m/s and 𝜽 and = 0°:θ (=a)0 𝒗𝟐:( changesa) v2 changes from 0 to from 12 0 to 𝒗 𝒗 12 m/s;m/s; ((b) v𝟐2 changeschanges from from 0 to 0 6 to m/s; 6 m/s; (b) (𝟐b changes) v2 changes from 8 fromto 12 m/s. 8 to 12 m/s.

Theoretical analysis indicates that the meteorological conditions in the mountain and plain areas

allowedTable 1. theLiving theropods era, mass, to effectivemoveAppl. Sci. 2019 from, 9 FOR area, PEER ground REVIEW and fossil to tr picturesees. From of Epidexipteryxthe viewpoint, Anchiornis of taking, offArchaeopteryx from the , 9 Microraptor ConfuciusornisAppl. Sci. 2019, 9 FOR PEER REVIEW 9 ground, the ,velocity and thresholdTable is. much1. Living era ,lower mass, effective than area, and those fossil pictures predicted of Epidexipteryx , earlierAnchiornis, Archaeopteryx [22]. Equation, Microraptor, and Confuciusornis (6) indicates. Table 1. Living era, mass, effective area, and fossil pictures of Epidexipteryx, Anchiornis, Archaeopteryx, Microraptor, and Confuciusornis. that the vertical component of the resultant forcDatee exertedMass, m onArea, the A dinosaur was dependent on the Species 2 Figure of Fossil Species Date (m. years) Mass, m (Kg)(m.Date years) Mass,(Kg)Area, m Area, A(m A2) ) Figure of Fossil Species Figure of Fossil surface area of the body plane. Therefore, the (m.longer years) and(Kg) stronger(m2) the feather, the larger the area and the vertical component of the resultant force. So, glide activity propelled the development of the feathers of the bird’s ancestors. The early ancestors of the bird could develop longer and longer

feathers to adapt to the need for glidingEpidexipteryx activities. 152–168 [37] Therefore, 0.164 [37] 0.0132 the [37] terrestrial theropods could easily benefitEpidexipteryx from the action 152–168of upslope [37] windsEpidexipteryx 0.164in mounta152–168 [37] [37] in0.164 areas [37] 0.0132 0.0132 or [ 37[37]strong] winds in plain grounds to get to the trees from the ground and again glide back to the ground.

[37] [37] [37]

Anchiornis 155 [36] 0.110 [37] 0.04212 [36] Anchiornis 155 [36] 0.110 [37] 0.04212 [36] Anchiornis 155 [36] 0.110 [37] 0.04212 [36]

[36]

Appl. Sci. 2019, 9 FOR PEER REVIEW 10 Appl. Sci. 2019, 9 FOR PEER REVIEW [36] 10

Archaeopteryx 150 [38] 0.276 [40] 0.0496 [41] Archaeopteryx 150 [38]Archaeopteryx 0.276 150 [40 [38]] 0.276 [40] 0.0496 0.0496 [ 41[41]]

[41]

Microraptor 110–120 [42] 1.50 [43] 0.155 [21] Microraptor 110–120 [42] 1.50 [43] 0.155 [21] Microraptor 110–120 [42] 1.50 [43] 0.155 [21]

Appl. Sci. 2019, 9 FOR PEER REVIEW 11 [21]

Confuciusornis 120 [40] 0.500 [40] 0.0402 [40] Confuciusornis 120 [40] 0.500 [40] 0.0402 [40]

[40] Appl. Sci. 2019, 9, 649 9 of 14

Theoretical analysis indicates that the meteorological conditions in the mountain and plain areas allowed the theropods to move from ground to trees. From the viewpoint of taking off from the ground, the velocity threshold is much lower than those predicted earlier [22]. Equation (6) indicates that the vertical component of the resultant force exerted on the dinosaur was dependent on the surface area of the body plane. Therefore, the longer and stronger the feather, the larger the area and the vertical component of the resultant force. So, glide activity propelled the development of the feathers of the bird’s ancestors. The early ancestors of the bird could develop longer and longer feathers to adapt to the need for gliding activities. Therefore, the terrestrial theropods could easily benefit from the action of upslope winds in mountain areas or strong winds in plain grounds to get to the trees from the ground and again glide back to the ground. AfterAppl. calculating Sci. 2019, 9 FOR the PEER speed REVIEW of the upslope wind for different cases when the dinosaur was running12 at a speed from 5 to 8 m/s and the inclined angle θ varied from 30◦ to 0◦ (Table2), we obtained all the After calculating the speed of the upslope wind for different cases when the dinosaur was possible trajectoriesrunning at a ofspeedEpidexipteryx from 5 to 8 m/sand andAnchiornis the inclinedfrom angle ground 𝜽 varied to from air. 30° The to trajectories0°, we obtained of allAnchiornis the were obtainedpossible for trajectories three cases of Epidexipteryx when Anchiornis and Anchiorniswas running from ground at a speed to air. ofThe 5 trajectories m/s. Assuming of Anchiornis that there is a tree atwere a distance obtained offor 10three m cases along whenx-direction, Anchiornis thewas valuerunning of atv a2 speedchanges of 5 m/s. from Assuming 0 to 7.75 that m/s, there 7.75 to 9.35 m/s,is and a tree 9.35 at a todistance 11.20 of m/s, 10 m along for case x-direction, 1, case the 2, andvaluecase of 𝒗𝟐 3,changes respectively, from 0 to as7.75 shown m/s, 7.75 in to Figure 9.35 7a. m/s, and 9.35 to 11.20 m/s, for case 1, case 2, and case 3, respectively, as shown in Figure 7a. Similarly, Similarly, the trajectories at a speed of 8 m/s can be obtained for Anchiornis when v2 changes from 0 the trajectories at a speed of 8 m/s can be obtained for Anchiornis when 𝒗𝟐 changes from 0 to 2.71 m/s, to 2.71 m/s,2.71 2.71 to 5.85 to 5.85m/s, m/s,and 5.85 and to 5.859.83 m/s, to 9.83 respectively, m/s, respectively, for case 1, case for case2, and 1, case case 3, 2,as and shown case in 3,Figure as shown in Figure77b.b. The The same same analysis analysis is performed is performed on Epidexipteryx on Epidexipteryx for all threefor cases all threeat the speeds cases at5 m/s the and speeds 8 m/s, 5 m/s and 8 m/s,as asshown shown in Figure in Figure 7c and7c,d, Figure respectively. 7d, respectively.

Table 2. TheTable speed 2. The of speed the upslope of the upslope wind wind in different in different cases cases when when the the speciesspecies ran ran at at the the speeds speeds of 5m/s of 5 m/s 𝜃 and 8 m/sand and 8m/s the and inclined the inclined angle angle was wasθ =30 =30°.◦. 𝒎 Case 1 Case 2 Case 3 Speciesm 𝒗𝟏( )Case 1𝒎 𝒎 Case 2 𝒎 Case 3 Species v1( s ) 𝒔 𝒗m𝟐( ) 𝒗𝟐( ) m 𝒗𝟐( ) m v2( s )𝒔 𝒔 v2( s ) 𝒔 v2( s ) Epidexipteryx 5 0–7.75 7.75–9.35 9.35–11.20 Epidexipteryx 5 0–7.75 7.75–9.35 9.35–11.20 Anchiornis 5 0–7.75 7.75–9.35 9.35–11.20 Anchiornis 5 0–7.75 7.75–9.35 9.35–11.20 Epidexipteryx 8 0–2.71 2.71–5.85 5.85–9.83 Epidexipteryx 8 0–2.71 2.71–5.85 5.85–9.83 Anchiornis Anchiornis8 8 0–2.710–2.71 2.71–5.85 2.71–5.85 5.85–9.83 5.85–9.83

(a) (b)

(c) (d)

FigureFigure 7. Trajectories 7. Trajectories of Anchiornisof Anchiornisrunning running atat a speedspeed of: of: (a (a) )5 5m/s; m/s; and and (b) (b8 )m/s; 8 m/s; Trajectories Trajectories of of EpidexipteryxEpidexipteryxrunning running at at a a speed speed of:of: ( cc)) 5 5 m/s; m/s; and and (d) (8d m/s.) 8 m/s.

5.2. Evolution of Arboreal Gliding In the course of their evolution, paravian dinosaurs and early birds progressively developed longer, stiffer, and more aerodynamic fore- and hind-limb feathers, so that the lift–drag ratio of these animals progressively became higher, allowing for more efficient gliding. The earliest birds, as exemplified by Archaeopteryx and Confuciusornis, already possessed fully developed asymmetrical flight feathers [23,40], allowing for longer distance glides, compared with the more basal paravian Anchiornis.

Appl. Sci. 2019, 9, 649 10 of 14

5.2. Evolution of Arboreal Gliding In the course of their evolution, paravian dinosaurs and early birds progressively developed longer, stiffer, and more aerodynamic fore- and hind-limb feathers, so that the lift–drag ratio of these animals progressively became higher, allowing for more efficient gliding. The earliest birds, as exemplified by Archaeopteryx and Confuciusornis, already possessed fully developed asymmetrical flightAppl. Sci. feathers 2019, 9 FOR [23 ,PEER40], allowingREVIEW for longer distance glides, compared with the more basal paravian13 Anchiornis.

Plain Ground Plain Ground

(a) (b)

Plain Ground

(c)

Plain Ground

(d)

Figure 8.8. Process of arboreal gliding: ( a)a) A theropod parachuting from the branch of a tree to thethe ground; (bb)) Trying toto glideglide fromfrom oneone treetree toto another;another; ((cc)) TheThe theropodtheropod couldcould glideglide fromfrom thethe higherhigher position of one tree toto thethe lowerlower positionposition of another;another; (dd)) TheThe theropodtheropod couldcould change its trajectory by adjusting itsits orientationorientation duringduring glidinggliding soso thatthat thethe resultantresultant forceforce couldcould liftlift itit toto aa position.position.

Those early birds could easily parachute from the branch of a tree to the ground or any lower position. Then, later, it could also try to glide from the top branch of one tree to another (Figures 8a and 8b). Under the action of the potential energy of gravity, the early bird obtained an increasing speed to glide to the lower branch of another tree or changed its trajectory by adjusting its orientation during gliding so that the resultant force could lift it into a position with different heights that were lower than its initial one (Figure 8c). For steady flight conditions in descent when the velocity stays constant, the reciprocal lift–drag ratio should equal the slope of the trajectory. The pes might be used for grasping the branches of the tree when the theropods jumped or walked with the assistance of flapping wings between branches. In this way, they changed their positions in a tree with different Appl. Sci. 2019, 9, 649 11 of 14

Those early birds could easily parachute from the branch of a tree to the ground or any lower position. Then, later, it could also try to glide from the top branch of one tree to another (Figure8a,b). Under the action of the potential energy of gravity, the early bird obtained an increasing speed to glide to the lower branch of another tree or changed its trajectory by adjusting its orientation during gliding so that the resultant force could lift it into a position with different heights that were lower than its initial one (Figure8c). For steady flight conditions in descent when the velocity stays constant, the reciprocal lift–drag ratio should equal the slope of the trajectory. The pes might be used for grasping the branches of the tree when the theropods jumped or walked with the assistance of flapping wings between branches. In this way, they changed their positions in a tree with different heights (Figure8d). Thus, the early bird could get high enough potential energy before the next glide. It would parachute from the branch of a tree to the ground, as it failed to grasp the branch when it jumped from one branch to another. Practice allowed it to reach another tree by gliding a long enough distance. In this stage, the early birds learned to control their trajectory in gliding [22].

5.3. Stability Control During Gliding After numerous cycles of gliding with the help of the upslope wind or strong winds in the plains by accident, terrestrial paravians became progressively adapted to a semi-arboreal life, gliding to the trees and then back to the ground. The terrestrial paravians, such as Anchiornis huxleyi, could climb the mountain slope from the mountainside after they glided down (Figure S11). Their wings gradually developed ideal shapes and aspect ratios to increase the lift in glide as their feathers became longer and stronger. Because the aerodynamic coefficients are common numerical approximations of complex aerodynamic conditions, which change in flight (e.g., when the angle of attack or effective area of the wings changes), theoretically the non-avian dinosaur could take a continuous glide when the lift, drag, and its self-weight formed a closed vector polygon (Figures S12 (a) and (b)). As the lift and drag forces are proportional to the aerodynamic coefficients CL and CD, the resultant force of lift, drag, and weight should equal zero when the velocity stays constant. The trajectory direction can be therefore expressed by the following:

F 1 = D = tanθ C (10) FL L CD where θ is the subtended angle between the horizontal direction and the airflow and FL and FD represent the lift and drag forces resulting from the aerodynamics in gliding. Equation (10) shows that the slope of the tangent line of any point on the trajectory represents the lift–drag ratio of the aerodynamic coefficients CL over CD. The larger the ratio, the more advanced the wings were evolved during the millions of years of the avian ancestors’ evolution. During later evolution, early birds learned to change the orientation of their wings to gain higher lifts (Figure S12 (c)). This took place over no more than 15 million years [45,46], which is a very short period relative to the whole history of evolution from the non-avian theropods to the early birds. We used six rigid bodies of Anchiornis huxleyi (Figure S12), including the main body, the four wings, and the , to discuss orientation control during gliding. The system dynamics of Anchiornis huxleyi can be expressed with Newton–Euler equations. The simplified six-rigid-body dynamics show that the ancestor of the bird could control its pose during gliding. As a matter of fact, the creature could use its flexible body parts to control its pose arbitrarily.

6. Conclusions Both the cursorial and arboreal hypotheses are insufficient for explaining flight evolution in bird lineage. Here, we presented a biophysical principle to connect both theories and explained how cursorial paravians could reach the top of the trees. Either the upslope winds in the mountain areas in daytime or the strong winds in the plain grounds provided the natural meteorological conditions Appl. Sci. 2019, 9, 649 12 of 14 for the gliding of avian ancestors from the ground to the trees. In this regard, the gliding between the trees and the ground of paravian theropods might have started long before flight feathers were perfectly aerodynamical. The results indicate that smaller, feathered paravians were able to generate enough lift to glide down to the trees from the mountain slopes and even perhaps to glide up to high trees in the plain areas in strong air flow. The upslope wind plays an important role in this regard, as can be seen in the plotted figures (provided in this article and the Supplementary Materials), in that as the speed of the wind increases, more lift is produced, and the animal could glide up to a higher position. When the winged paravian parachuted from a high enough position or reached a sufficiently high velocity, it could just use the potential or kinetic energy to travel over a long distance by gliding. Early birds gradually learned to use the meteorological conditions in the mountain and plain areas to get to the trees from the ground and again glide back to the ground. In this stage, the early birds became semi-arboreal. Trajectories obtained through differential equations can be useful in designing the parameters and control systems for flying robots. The understanding of the origin of flight and its evolution can be beneficial for the design and development of micro air vehicles. The biomimetic mechanism inspired by the evolution of flight can be useful to evaluate an animal’s flying apparatus, flying capabilities, control strategy, and stability. The aerodynamic behavior of different extinct animals can be studied in a similar manner in order to fill in the research gaps.

Supplementary Materials: The following are available online at http://www.mdpi.com/2076-3417/9/4/649/s1: Figure S1. Reconstruction of airfoil of Anchiornis huxleyi; Figure S2. Interpolated lift coefficient, drag coefficient, and the ratio of lift to drag; Figure S3. Trajectories of Anchiornis running at a speed of 6 m/s and θ = 30◦; Figure S4. Trajectories of Anchiornis running at a speed of 7 m/s and θ = 30◦; Figure S5. Trajectories of Anchiornis running at a speed of 8 m/s and θ = 30◦; Figure S6. Trajectories of Anchiornis running at a speed of 6 m/s and θ = 10◦; Figure S7. Trajectories of Anchiornis running at a speed of 7 m/s and θ = 10◦; Figure S8. Trajectories of Anchiornis running at a speed of 8 m/s and θ = 10◦; Figure S9. Trajectories of Anchiornis running at a speed of 6 m/s and θ = 0◦; Figure S10. Trajectories of Anchiornis running at a speed of 7 m/s and θ = 0◦; Figure S11. Wing-assisted incline running helped Anchiornis huxleyi climb the mountain; Figure S12. Forces acting upon a winged theropod during stable gliding flight; and Table S1. Simulation results of the lift and drag coefficients for the thin plate reconstructed in the scale of 1:1 according to the fossil using the ANSYS software. Author Contributions: All authors have contributed equally to the paper. Funding: This research was supported by the National Natural Science Foundation of China (grant no. 51175277) and the Scientific Research Foundation of State Key Laboratory of Tribology of China. Conflicts of Interest: The authors declare no conflicts of interest.

References

1. Sreetharan, P.S.; Wood, R.J. Passive Aerodynamic Drag Balancing in a Flapping-Wing Robotic . J. Mech. Des. 2010, 132, 051006. [CrossRef] 2. Marden, J.H. Maximum Lift Production During Takeoff in Flying Animals. J. Exp. Btol. 1987, 130, 235–258. 3. Chin, D.D.; Matloff, L.Y.; Stowers, A.K.; Tucci, E.R.; Lentink, D. Inspiration for wing design: How forelimb specialization enables active flight in modern vertebrates. J. R. Soc. Interface 2017, 14, 20170240. [CrossRef] [PubMed] 4. McKellar, R.C.; Chatterton, B.D.E.; Wolfe, A.P.; Currie, P.J. A diverse assemblage of late cretaceous dinosaur and bird feathers from Canadian Amber. Science 2011, 333, 1619–1622. [CrossRef][PubMed] 5. Clarke, J. Feathers before flight. Science 2013, 340, 690–692. [CrossRef][PubMed] 6. Ostrom, J.H. Archaeopteryx: Notice of a “New” Specimen. Science 1970, 170, 537–538. [CrossRef][PubMed] 7. Ostrom, J.H. Bird flight: How did it begin? Did birds begin to fly “from the trees down” or “from the ground up”? Reexamination of Archaeopteryx adds plausibility to an “up from the ground” origin of flight. Am. Sci. 1979, 67, 46–56. [CrossRef] 8. Forster, C.A.; Sampson, S.D.; Chiappe, L.M.; Krause, D.W. The theropod ancestry of birds: New evidence from the Late Cretaceous of Madagascar. Science 1998, 279, 1915–1919. [CrossRef] 9. Garner, J.P.; Taylor, G.K.; Thomas, A.L.R. On the origins of birds: The sequence of character acquisition in the evolution of avian flight. Proc. R. Soc. B Biol. Sci. 1999, 266, 1259–1266. [CrossRef] Appl. Sci. 2019, 9, 649 13 of 14

10. Sereno, P.C. The evolution of dinosaurs. Science 1999, 284, 2137–2147. [CrossRef] 11. Xu, X.; Zhou, Z.; Wang, X. The smallest known non-avian theropod dinosaur. 2000, 408, 705–708. [CrossRef][PubMed] 12. Prum, R.O. Dinosaurs take to the air. Nature 2003, 421, 323–324. [CrossRef][PubMed] 13. Paul, G.S. Comment on “Narrow Primary Feather Rachises in Confuciusornis and Archaeopteryx Suggest Poor Flight Ability”. Science 2010, 328, 887–889. [CrossRef][PubMed] 14. Zheng, X.; Xu, X.; Zhou, Z.; Miao Desui, Z.F. Comment on “Narrow Primary Feather Rachises in Confuciusornis and Archaeopteryx Suggest Poor Flight Ability”. Science 2010, 330, 320. [CrossRef][PubMed] 15. Nudds, R.L.; Dyke, G.J. Response to Comments on “‘Narrow Primary Feather Rachises inConfuciusornis and Archaeopteryx Suggest Poor Flight Ability’”. Science 2010, 330, 320. [CrossRef] 16. Zhang, F.; Zhou, Z. Leg feathers in an early cretaceous bird. Nature 2004, 431, 925. [CrossRef][PubMed] 17. Gibbons, A. New Feathered and Dinosaurs Fossil Birds Brings Closer. Am. Assoc. Adv. Sci. 1996, 274, 720–721. [CrossRef] 18. Dial, K.P. Wing-assisted incline running and the evolution of flight. Science 2003, 299, 402–404. [CrossRef] 19. Zhang, F.; Zhou, Z. A primitive enantiornithine bird and the origin of feathers. Science 2000, 290, 1955–1959. [CrossRef] 20. Zelenitsky, D.K.; Therrien, F.; Erickson, G.M.; DeBuhr, C.L.; Kobayashi, Y.; Eberth, D.A.; Hadfield, F. Feathered non-avian dinosaurs from North America provide insight into wing origins. Science 2012, 338, 510–514. [CrossRef] 21. Xu, X.; Zhou, Z.; Wang, X.; Kuang, X.; Zhang, F.; Du, X. Four-winged dinosaurs from China. Nature 2003, 421, 335–340. [CrossRef][PubMed] 22. Chatterjee, S.; Templin, R.J. The flight of Archaeopteryx. Naturwissenschaften 2003, 90, 27–32. [CrossRef] [PubMed] 23. Zhou, Z. The origin and early : Discoveries, disputes, and perspectives from fossil evidence. Naturwissenschaften 2004, 91, 455–471. [CrossRef][PubMed] 24. Feduccia, A. Evidence from Claw Geometry Indicating Arboreal Habits of Archaeopteryx. Science 1993, 259, 790–793. [CrossRef][PubMed] 25. Zheng, X.; Zhou, Z.; Wang, X.; Zhang, F.; Zhang, X.; Wang, Y.; Wei, G.; Wang, S.; Xu, X. Hind wings in basal birds and the evolution of leg feathers. Science 2013, 339, 1309–1312. [CrossRef][PubMed] 26. Ruben, J.A. Reptilian physiology and the flight capacity of Archaeopteryx. Evolution 1991, 45, 1–17. [CrossRef][PubMed] 27. Speakman, J. Flight capabilities of Archaeopteryx. Int. J. Org. Evol. 1993, 47, 336–340. [CrossRef] 28. Dong, S.W.; Zhang, Y.Q.; Long, C.X.; Yang, Z.Y.; Ji, Q.; Wang, T.; Hu, J.M.; Chen, X.H. Jurassic tectonic revolution in China and new interpretation of the “Yanshan Movement.”. Acta Geol. Sin. Ed. 2008.[CrossRef] 29. Yongdong, W.; Ken’ ichi, S.; Wu, Z.; Shaolin, Z. Biodiversity and palaeoclimate of the Middle Jurassic floras from the Tiaojishan Formation in western , China. Prog. Nat. Sci. 2006, 16, 222–230. [CrossRef] 30. Sullivan, C.; Wang, Y.; Hone, D.W.E.; Wang, Y.; Xu, X.; Zhang, F. The vertebrates of the Jurassic Daohugou Biota of northeastern China. J. Vertebr. Paleontol. 2014.[CrossRef] 31. Vergeiner, I.; Dreiseitl, E. Valley winds and slope winds—Observations and elementary thoughts. Meteorol. Atmos. Phys. 1987, 36, 264–286. [CrossRef] 32. Kleissl, J.; Honrath, R.E.; Dziobak, M.P.; Tanner, D.; Val Martín, M.; Owen, R.C.; Helmig, D. Occurrence of upslope flows at the Pico mountaintop observatory: A case study of orographic flows on a small, volcanic island. J. Geophys. Res. Atmos. 2007, 112, 1–16. [CrossRef] 33. Whiteman, C.D.; Doran, J.C. The relationship between overlying synopic-scale flows and winds within a valley. J. Appl. Meteorol. 1993, 32, 1669–1682. [CrossRef] 34. Whiteman, C.D. Mountain Meteorology: Fundamentals and Applications; Oxford University Press: Oxford, UK, 2000; ISBN 0-19-513271-8. 35. Longrich, N.R.; Vinther, J.; Meng, Q.; Li, Q.; Russell, A.P. Primitive wing feather arrangement in Archaeopteryx lithographica and Anchiornis huxleyi. Curr. Biol. 2012, 22, 2262–2267. [CrossRef][PubMed] 36. Hu, D.; Hou, L.; Zhang, L.; Xu, X. A pre-Archaeopteryx troodontid theropod from China with long feathers on the metatarsus. Nature 2009, 461, 640–643. [CrossRef][PubMed] 37. Zhang, F.; Zhou, Z.; Xu, X.; Wang, X.; Sullivan, C. A bizarre Jurassic maniraptoran from China with elongate ribbon-like feathers. Nature 2008, 455, 1105–1108. [CrossRef][PubMed] Appl. Sci. 2019, 9, 649 14 of 14

38. Kurochkin, E.N.; Dyke, G.J.; Saveliev, S.V.; Pervushov, E.M.; Popov, E.V. A fossil brain from the Cretaceous of European Russia and avian sensory evolution. Biol. Lett. 2007, 3, 309–313. [CrossRef] 39. Xu, X.; Zhao, Q.; Norell, M.; Sullivan, C.; Hone, D.; Erickson, G.; Wang, X.; Han, F.; Guo, Y. A new feathered maniraptoran dinosaur fossil that fills a morphological gap in avian origin. Chin. Sci. Bull. 2009, 54, 430–435. [CrossRef] 40. Nudds, R.L.; Dyke, G.J. Narrow primary feather rachises in Confuciusornis and Archaeopteryx suggest poor flight ability. Science 2010, 328, 887–889. [CrossRef] 41. Carney, R.M.; Vinther, J.; Shawkey, M.D.; D’Alba, L.; Ackermann, J. New evidence on the colour and nature of the isolated Archaeopteryx feather. Nature Commun. 2012, 3, 637. [CrossRef] 42. Xu, X.; Norell, M.A. Non-avian dinosaur fossils from the Lower Cretaceous Jehol Group of western Liaoning, China. Geol. J. 2006, 41, 419–437. [CrossRef] 43. O’Connor, J.; Zhou, Z.; Xu, X. Additional specimen of Microraptor provides unique evidence of dinosaurs preying on birds. Proc. Natl. Acad. Sci. USA 2011, 108, 19662–19665. [CrossRef][PubMed] 44. Li, Q.; Gao, K.; Vinther, J.; Shawkey, M.D.; Clarke, J.; D’alba, L.; Meng, Q.; Briggps, D.E.G.; Prum, R.O. Plumage Color Patterns of an. Science 2010, 327, 1369–1372. [CrossRef][PubMed] 45. Sereno, P.C.; Chenggang, R. Early Evolution of Avian Flight and Perching: New Evidence from the Lower Cretaceous of China. Science 2014, 255, 845–848. [CrossRef][PubMed] 46. Padian, K.; Chiappe, L.M. The origin and early evolution of birds. Biol. Rev. 1998.[CrossRef]

© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).