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Comparative ontogeny of form and function in developing mallardducks (Anas platyrhynchos)

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COMPARATIVE ONTOGENY OF FORM AND FUNCTION IN
DEVELOPING MALLARD DUCKS (ANAS PLATYRHYNCHOS)
by
Terry Ronald Dial
A thesis submitted to the faculty of
The University of Utah
in partial fulfillment of the requirements for the degree of
Master of Science
Department of Biology
The University of Utah
August 2010
UMI Number: 1476914
All rights reserved
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UMI 1476914
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The
University
of
Utah
Graduate
School
STATEMENT
OF
THESIS
APPROVAL
The
thesis
of
Terry
R.
Dial
has
been
approved
by
the
following
supervisory
committee
members:
David
R.
Carrier
,
Chair
5/11/2010
Date
Approved
Dennis
M.
Bramble
,
Member
5/11/2010
Franz
Goller
,
Member
5/11/2010
Date
Approved
Date
Approved
and
by
Neil
J.
Vickers
the
Department
of
and
by
Charles
A.
Wight,
Dean
of
The
Graduate
School.
,
Chair
of
Biology
ABSTRACT
Two major strategies exist among developing warm-blooded vertebrates to cope
with the vulnerable nature of being diminutive and inexperienced as a juvenile. Precocial
juveniles decrease their vulnerability by entering the world in a relatively mature state of
development – newly born or hatched neonates are capable of independently foraging and
avoiding predators with little influence from the parent. In contrast, altricial juveniles
enter the world in a relatively immature state of development (relying heavily on parental
care), but adopt extremely high rates of growth – thus decreasing the period of time spent
being vulnerable. The contrasting strategies of premature form (precociality) and high
growth rate (altriciality) could set potential limits on the degree to which animal form and
function are capable of changing throughout development. Two discrete investigations
attempt to measure the developmental differences in animal design and utility between
precocial and altricial growth strategies.
Mallards (Anas platyrhynchos), like most Anseriformes (waterfowl), undergo
differential development of the forelimbs (wings) and hindlimbs (legs) – the ability to run
and swim initiates upon hatching, while the ability to fly is delayed into adulthood.
Musculo-skeletal dimensions were tracked throughout the mallard’s 60-day ontogenetic
(post-hatching developmental) period and coupled with whole-body locomotor
performance during maximal running, swimming and flying efforts. The attainment of
mallard locomotor performance parallels the independent morphological maturation of
the forelimbs and the hindlimbs – running and swimming performance (hindlimb
dominated) initiate at relatively high levels but only gradually improve throughout the
first month of development, while flying performance (forelimb only) initiates at
relatively low levels but dramatically improves within the last two weeks of
development.
In a complementary study, aerodynamic forces were measured across a
developmental series of precocial chukar partridge (Alectoris chukar) and altricial
mallard wing development. Lift and drag production improved dramatically over the
course of each species’ ontogeny, but chukar generate lift starting at day eight and
improve only a minor extent, while mallard delay lift production until just prior to
fledging and improve function dramatically. The prevailing theme in each study
indicates precocial strategies offer early functional forms that change very little into
adulthood, while altricial strategies offer rapid and dramatic change in morphology that
can only be utilized in the adult.
iv
TABLE OF CONTENTS
ABSTRACT……………………………………………………………………………...iii
LIST OF FIGURES……………………………………………………………………....vi
LIST OF TABLES……………………………………………………………………...viii
ACKNOWLEDGEMENTS…………………………………………………………..…..ix
Chapter
1. PRECOCIAL HINDLIMBS AND ALTRICIAL FORELIMBS: THE
MODULATION OF ONTOGENETIC STRATEGIES IN MALLARD DUCKS
(ANAS PLATYRHYNCHOS)……………………………. …………………..……..1
Abstract…….……………………………………………………………………...1
Introduction…………………………………………………………………..…....2
Methods…………………………………………………………..………………..6
Results…………………………………………….…….…………………………9
Discussion……………………………………….….……………………………12
2. COMPARATIVE ONTOGENY OF AERODYNAMICS IN TWO AVIAN SPECIES
WITH DIFFERENT LIFE-HISTORY STRATEGIES…..…………………….……26
Abstract………………….………………………………………………….....…26
Introduction…………………………………………………………………..…..27
Methods…………………………………………………………..………………30
Results…………………………………………….…….………………………..33
Discussion……………………………………….….……………………………35
REFERENCES………………………………………………………………………......53
LIST OF FIGURES
Figure
1.1
Body mass, wing loading and surface areas of the foot and wing over ontogenetic
course of mallard, including adult (>365 days)………………………..………...21
1.2
Lengths of limb bones of Anas platyrhynchos over 60-day ontogenetic course
(Adult >365 days old). Elements of the hindlimb and forelimb are aligned from
proximal to distal (top to bottom) and scaled for comparison…………………...22
1.3
Widths of limb bones of Anas platyrhynchos over 60-day ontogenetic course
(Adult >365 days old). Elements of the hindlimb and forelimb are aligned from
proximal to distal (top to bottom) and scaled for comparison…………….……..23
1.4
Masses of major hindlimb and forelimb muscles over 60-day ontogenetic course,
including adult (>365 days) of Anas platyrhynchos……………………………..24
1.5
Running, swimming and flying performance over mallard ontogeny.
Measurements of whole-body velocity during maximum running and swimming
sprint performance and negative acceleration vertically during descending flight
were taken (averages and standard deviations shown)…………………..………25
2.1
Experimental setup of propeller-force plate apparatus. Several motors were
interchanged (see text) to spin a single wing-mount over both chukar and mallard
ontogenetic series at in vivo speeds converted to RPMs (Table 1). Force and
torque were measured about the z-axis and converted into coefficients of lift and
drag respectively. Wings were positioned upside-down and a cowling was placed
over the force sensor to reduce the effect of downwash on the force plate
readouts…………………………………………………………………………..42
2.2
Dorsal views of chukar partridge (Alectoris chukar) and mallard (Anas
platyrhynchos) wings through ontogeny. Wing developmental period initiated at
youngest age force measurements could be resolved on the propeller apparatus.
5-cm scale bar……………………………………………………………………43
2.3
Polar traces of lift coefficient (CL) and drag coefficient (CD) for an ontogenetic
series of wings from (a) chukar partridge (Alectoris chukar) and (b) mallard
(Anas platyrhynchos). CL and CD were measured at angles of attack (α) from -15˚
to 80˚. Symbols refer to α = 0˚ (circles), maximum CL : CD (squares, α indicated)
and maximum CL (triangles, α indicated). Traces are set on the same scale to
emphasize aerodynamic differences between a burst-flight wing (chukar) and a
migratory wing (mallard). Traces are means from N = 2 birds per age class, with
classes beginning at the earliest age force readings could be resolved and ending
with adult wing…………………………………………………………………..47
2.4
Lift-to-drag ratio (CL : CD) over range of angle of attack (α = -15˚ to 80˚) from (a)
chukar partridge (Alectoris chukar) and (b) mallard (Anas platyrhynchos)
ontogenetic series (N = 2 birds per age class). Axes are at same scale for
comparison between wing types…………………………………………………49
2.5
Variability between subjects for coefficients of lift (CL) and drag (CD) as a
function of angle of attack (α) in adult wings of chukar partridge (Alectoris
chukar; a, CL; b, CD) and mallard (Anas platyrhynchos; c, CL; d, CD). Black
traces represent an interpolated average between two wings over a range of α
from -15˚ to 60˚. Error bars = s.d……………………………………………51-52
vii
LIST OF TABLES
Table
1.1
Allometric scaling equations of the form y=amb, where m is body mass in grams,
of skeletal, muscular and structural elements throughout mallard ontogeny.
Expected scaling slopes indicated. Inflection day (i) indicates point at which
exponential growth rate changed. Scaling regressions run before inflection, after
inflection and for entire growth series. Data were log transformed and equations
were fit by reduced major axis regression; parameters are presented as value +
95% confidence interval. Symbols next to slope indicate negative allometry (-),
positive allometry (+) and isometry (=)………………………………………19-20
2.1
Morphometric data from chukar and mallard ontogenetic series (± s.d.). See text
for details……………………………………………………………………..44-45
ACKNOWLEDGEMENTS
I would first like to thank my advisor, Dave, whose genuine enthusiasm for
animal design and life-history biology drew me to his lab and facilitated the development
this thesis. Dave taught me to creatively attack the construction and execution of a
project, while remaining cautious in terms of the interpretation and presentation of
results. He maintained an unreserved confidence in my potential throughout our two
years together, and for that I am most grateful.
To the members of my committee, Dennis and Franz, I thank you for spending
time talking biology, intensively thinking through my proposal, providing thoughtprovoking skepticism and encouraging a high level of professionalism.
Much more than simply a lab mate, Chris Cunningham has acted as my graduate
student mentor, research sounding board, statistical tutor, master R analyzer, presentation
critic and, most importantly, one of my closest friends.
I am also appreciative of the time Jessamyn Markley took out of her life as a
finishing doctorate student in the Carrier lab to discuss ideas and tighten up presentations.
To those at the Field Research Station at Fort Missoula, I would first like to
acknowledge Bret Tobalske, who acted as my adjunct mentor throughout my time in
Montana. From developing the propeller project to executing early morning Sunday spin
trials over coffee and jazz, no one has spent more intensive time educating and training
me on how to conduct rigorous science.
As the third collaborator on the aerodynamics chapter, I am grateful to Ashley
Heers, a graduate student at the University of Montana, who generously provided her
chukar data in order to offer a comparative analysis of wing function throughout
ontogeny.
I am appreciative to Brandon Jackson for his intellectual and physical assistance
with my project; Brandon prompted me to look into using mallards as my model
organism and assisted, along with UM grad student John Sprague, in the design and
construction of a 500 gallon swim tank. Heather Davis oversaw the care and use of my
animals and has been extremely accommodating given my sparse presence around the
Field Station.
My level of productivity during the 2009 summer session of data collection was
enhanced greatly with the involvement of my sister, Natalie; she assisted with filming,
animal motivation, computer analysis and dissections, and instigated frequent and
necessary food breaks. I am also extremely grateful to my Mother, who got me out of the
lab and into the kitchen; her stove-side mentorship offered me an invaluable mental outlet
and has armed me with many killer recipes.
Lastly, a special acknowledgement to the person who has bred in me a love for
the study of life; who constantly promotes creative thinking and an appreciation for the
complexities of nature; who introduced me to Dave’s work and encouraged I look into his
lab; to my Dad, who I have looked up to my entire life for guidance, passion and
imagination.
x
CHAPTER 1
PRECOCIAL HINDLIMBS AND ALTRICIAL FORELIMBS: THE
MODULATION OF ONTOGENETIC STRATEGIES IN
MALLARD DUCKS (ANAS PLATYRHYNCHOS)
Abstract
Developing precocial young often possess relatively longer, more muscular limbs
as compensatory modifications allowing improved juvenile locomotor performance.
Selection for premature tissue/whole-body functional capacity results in an inherent
reduction in rate of growth, allowing altricial species (which spend all of their
development in an immature condition) to experience rapid rates of growth (up to four
times what similar-sized precocial species experience). Anseriformes (waterfowl)
undergo differential developmental trajectories by prematurely initiating hindlimb
capacity for terrestrial and aquatic locomotion, while delaying forelimb flight capability
into adulthood. This study aims to track the growth processes (morphology) and the
functional consequences (performance) of hindlimb precociality and forelimb altriciality
within developing mallard ducks (Anas platyrhynchos). Musculo-skeletal dimensions
were tracked throughout the mallard’s 60-day ontogenetic period and coupled with
whole-body locomotor performance during maximal running, swimming and flying
efforts. Most of hindlimb morphological growth occurs during the first month of mallard
ontogeny, while morphological development of the forelimbs experiences its highest
rates of increase over the latter portion of ontogeny. Mallard forelimb morphology scales
2
with extreme positive allometry, experiencing highest growth rates in a condensed
window at the end of the ontogenetic period. The attainment of mallard locomotor
performance parallels the morphological maturation of the forelimb and hindlimb
modules – hindlimb performance initiates at a relatively high level and gradually
improves throughout the first month of development, while the forelimb experiences
delayed and dramatic improvement in function. By freeing the forelimbs from locomotor
demand early in ontogeny, anseriforms may bypass the potential canalization of juvenile
form present within their precocial hindlimbs, to dramatically depart in forelimb form
and function in the adult.
Introduction
Ontogenetic limits
Juvenile animals are less adept locomotors than their adult counterparts due to
diminutive size, immature musculo-skeletal systems and inexperience with the
environment (Carrier 1996). Although precocial young are relatively mature in terms of
their ability to independently thermoregulate, forage and avoid predators, they are
nevertheless more easily captured by predators and thus suffer increase rates of mortality
(Williams 1966, Wassersug and Sperry 1977). Selective pressures acting on precocial
young promote relatively robust locomotor machinery – longer, more muscular limbs and
greater mechanical advantages around joints – which enhance juvenile escape capacity
(Carrier 1983, 1995; Garland 1985; Trillmich et al. 2003). Although at a relatively
advanced developmental state, precocial endothermic vertebrates experience reduced
rates of growth compared to similar-sized altricial birds/mammals.
3
Growth rate negatively correlates with tissue maturity due to both the inefficient
allocation of energy into growing the body and the inability for developing tissue to both
grow rapidly and function maturely (Case 1978, Ricklefs 1979). If mature tissue is
limited in its capacity to grow or differentiate, it follows that early acquisition of such
tissue may limit the degree to which it can functionally change in mature individuals.
Furthermore, endotherms experience determinate growth, where development persists
only for a discrete period of time; this contrasts with ectothermic vertebrates, which
experience low rates of growth throughout their lifetime. The different selective
demands promoting mature juvenile function or rapid rates of growth could result in
dramatic morphological differences in adult phenotypes when played out over a discrete
developmental window. In an attempt to address how different selective demands on
juvenile form influence adult phenotype, we must first understand what adaptations exist
to circumvent limits on locomotor performance in juveniles (Carrier 1996).
Ontogenetic adaptations
Allometric scaling of morphology during ontogeny is a pervasive adaptation
counteracting the size and physiological handicaps of immature juvenile forms. Growth
of developing Zebrafish (Danio rerio) display a shift from elongated body forms in
juveniles to streamlined forms in adults, which functionally impacts locomotor habit over
the course of ontogeny (McHenry and Lauder 2006). Further, many teleost fish hatch
without caudal fin rays and experience less axial stiffness than their adult counterparts,
reducing juvenile sprint speed, but improving escape acceleration, possibly the most
selectively advantageous locomotor ability regarding survival (Gibb et al. 2006).
Negative allometric scaling of limb length in agamid and Dipsosaurus lizards, where
4
juveniles possess relatively longer limbs than adults, improves juvenile performance to
near-adult levels (Garland 1985; Irschick 2000a). Precocial jackrabbit young have
relatively more muscular limbs and higher mechanical advantages compared to their
adult counterparts (Carrier 1983), resulting in relatively higher jumping accelerations
during escape (Carrier 1995). Due to the inherently weak nature of developing bone,
juvenile jackrabbit, gull and goat limb bones have relatively larger cross sectional areas,
resulting in relatively low bone strain and high safety factors, which reduce the potential
of developing young inducing an irreparable fracture (Carrier 1983; Carrier & Leon
1990; Main & Biewener 2005).
We know much less about the physiological and neurological adaptations
influencing juvenile locomotor performance, but many handicaps appear to be due to
immature muscle physiology and lack of coordinated locomotion in juveniles. Muscle
physiology has been shown to change over the course of the ontogeny of the lizard
Dipsosaurus, where twitch time increases with age, functionally allowing juveniles to
perform escape behaviors as well as adults (Marsh 1988). Neuromuscular control during
chick ontogeny indicates the basic kinematics of running are innate at hatching, while
coordinated control producing economical walking kinematics must be acquired (Muir et
al. 1996). This suggests there exists a developmental bias toward elements of motor
control that impact survival (escape, accelerative responses) rather than those simply
meant to improve economical transport. Lastly, a kinematic comparison between
locomotor capacity in two small mammals found that adult walking patterns were
achieved at one week post birth in the precocial cui, but at 7 weeks post-birth in the
altricial tree shrew (Schilling 2005). This suggests that even within precocial species,
5
functional neuromuscular control requires a period of learning that cannot be innately
programmed within neonates of any species. To further address the impact of
compensatory adaptations on adult phenotype, it is necessary to first understand how
locomotor performance varies ontogenetically and how elements of the locomotor system
change during development.
Anseriform ontogeny
Avian morphology is unique in that the forelimb and hindlimb modules are
capable of functional specialization for different types of locomotion (Dial and Gatesy
2000). Most birds employ the use of their hindlimbs for terrestrial locomotion and their
forelimbs for aerial locomotion, yet both systems have been shown to adaptively
specialize within aquatic environments (e.g., hindlimb swimming in the gull; forelimb
flying in the penguin; Carrier & Leon 1990; Sato et al. 2010). The development of
locomotor function of each module usually occurs simultaneously; for example, when
altricial birds fledge both the hindlimb and forelimb modules acquire functional maturity
upon leaving the nest. In contrast, many precocial galliformes, chukar (Alectoris chukar)
for example, are capable of running the same day they hatch, while they do not possess
functional use of their forelimbs until at least 1 week old (Dial et al. 2006; Dial et al.
2008; Jackson et al. 2009). California gulls (Larus californicus) are an extreme example
of developmental modularity, where hatchlings possess a precocial ability to locomote
terrestrially and aquatically with their hindlimbs, but do not employ the use of their
forelimbs until fully grown (Smith & Diem 1972). This developmental disparity between
forelimb and hindlimb growth is representative of the locomotor demands placed on each
system throughout gull ontogeny (Carrier & Leon 1990).
6
Anseriformes (waterfowl) are considered some of the most precocial species of
birds, possessing thermogenic independence and the ability to forage and avoid predators
upon hatching, and are another example of extreme developmental modularity (Nice
1962; Lilja 1983). Ducks (Anatidae) use their precocial hindlimbs to get to and thrive
within aquatic environments, not relying on flight for predator avoidance during
ontogeny. Flight capacity in mallard ducks (Anas platyrhynchos) initiates at the end of
ontogeny and, though employed in an array of locomotor contexts, appears specialized
for long-distance, high-speed migration. This study aims to track the growth processes
(morphology) and the functional consequences (performance) of precocial and altricial
strategies within developing mallard ducks. By tracking ontogenetic changes in the
musculo-skeletal system in the mallard forelimb and hindlimb, and also obtaining
maximum performance from each module at various stages of growth, we will better
understand the functional consequences of development on locomotor performance.
Methods
Day old mallard chicks (hatchlings) were obtained from a commercial breeder
(Northwest gamebirds, Caldwell, ID, USA) and raised at the Field Research Station at
Fort Missoula, University of Montana. Chicks received food and water ad libitum and
were kept in an indoor climate-controlled room until 2 weeks old, at which point they
were transported to an outdoor aviary for the remainder of development. All the housing
and experimental procedures were approved by the University of Montana Institutional
Animal Care and Use Committee (IACUC: protocol # 029-09BTDBS-060309).
7
Morphometrics
Fifty two mallard ducks composed the entire morphological ontogenetic series
from day 2 to adult (30-1400g). Animals were deeply anesthetized with inhaled
isoflurane (3-5% in 100% oxygen) administered by face mask and given an overdose of a
pentobarbital solution IV in the brachial vein using a 25-27 gauge needle. Three
specimens were obtained every three to five days beginning the day of hatching and
continuing for two months (three birds >365 days old were also incorporated into the
morphometrics). Digital pictures of wing and foot morphology were taken against a
25cm2 grid background and imported into ImageJ v1.42 to determine surface area.
Relevant forelimb and hindlimb muscular elements were excized and weighed. Hindlimb
musculature consisted of the iliotibialis cranialis (ITC) and flexor cruris lateralis (FCL),
which are the major hip extensor and flexor muscles, respectively, as well as the
gastrocnemius (Weinstein et al. 1983). Forelimb musclulature consisted of the pecoralis
and supracorocoideus as the major depressor and elevator of the forelimb, and the triceps
and biceps as elbow extensor and flexor muscles (Weinstein et al. 1983). Specimens
were cleared of excess tissue and skeletonized in dermestid beetle colonies (at U.
Montana and U. Utah). Hindlimb (femur, tibiotarsus and tarsometatarsus) and forelimb
(humerus, ulna and carpometacarpus) bone lengths and widths (mid-shaft diameter) were
measured to the nearest 0.01mm with calipers.
Morphological scaling coefficients were determined across the entire ontogenetic
period, as well as during each period of differential growth rate (before and after
inflection). Scaling coefficients were determined on log-transformed data in R v2.10.1.
Equations were generated from fitting a reduced major axis regression. Inflection points
were determined where the log-transformed morphometric data indicated a shift in
8
constant growth rate (exponential growth displayed a marked decrease in the hindlimbs
and increase in the forelimbs, analyzed in IGOR Pro. v.6.12).
Performance
Whole-body locomotor performance tests were initiated at day 3 and continued
each week for 8 weeks. From a pool of 20 mallards, five individuals were selected at
random for each trial and the three maximal efforts were recorded for each individual.
Maximal running performance was conducted along a 5m long runway, where
individuals were isolated from the group at one end and motivated to rejoin their kin.
Maximum swim speed was conducted in a 5m long, 1m wide and 0.5m deep swim tank
constructed with one transparent plexiglass wall to film through. Individuals were
isolated at one end of the tank and motivated to swim maximally towards the other end.
Maximum forelimb flight performance (no hindlimb involvement) was determined by
isolating one individual on top of an elevated platform (2m above ground) with a padded
landing area of foam and loose straw below. Individuals voluntarily descended to the
group of birds situated on the ground, slowing their descent by flapping their wings.
Performance tests were filmed using high-speed digital video (250 frames s-1, 3x shutter,
Troubleshooter HR, Fastec Imaging) placed orthogonal to the animal’s direction of
travel, filming a 1-2m long calibrated section. The head was marked using reflective tape
and animal displacement was determined using the DLTdv3 program within MatLab
R2010a. Displacement data were smoothed (box algorithm, 5 points) in IGOR Pro v6.12
and velocity (run and swim) and acceleration (fly) were determined from the first and
second derivatives of the smoothed data.
9
Results
Mallard limb function is inherently reliant on the modularity of limb
development. The forelimb and hindlimb locomotor modules of developing mallard
ducks experience temporally independent growth trajectories. Each limb experiences a
dramatic change in rate of growth during the ontogenetic period.
Hindlimb morphometrics
Mallard hindlimb morphology accounts for a greater proportion of hatchling mass
than fledgling mass, scaling with slight negative allometry over the entire ontogenetic
course. From day 0-60, average bone length in the hindlimb scales with isometry
(M0.314). Bone width in the hindlimb scales isometrically over the entire course of
development. Hindlimb musculature does not scale with any distinct trend: the
iliotibialis cranialis (hip extensor) remains isometric while its antagonist, the flexor cruris
lateralis, scales with positive allometry and the gastrocnemius (ankle extensor) scales
with negative allometry. Foot area scales with negative allometry (Table 1.1, Figure 1.1).
Hindlimb morphology accounts for a relatively larger proportion of body mass early in
mallard life history.
Although scaling trends determined over the entire ontogenetic course reveal
proportional changes throughout ontogeny, they discount distinct changes in growth rate
that occur within each morphological element. Bone length and bone width exhibit clear
inflection points at day 34 and 37, respectively. Prior to each inflection point (day 0-34
and 0-37), femur length and width scale with positive allometry, while tibiotarsus and
tarsometatarsus length and width remain isometric (Table 1.1). Scaling relationships
following each inflection point (day 34-60 and 37-60) are not statistically different from
10
zero (Table 1.1), indicating bone growth terminates just past the ontogenetic half way
mark (Figure 1.2, 1.3). Muscle masses of the hindlimb experience pronounced reductions
in growth rate at day 29. Over the first month of ontogeny the iliotibialis cranialis and
flexor cruris lateralis experience positive allometry, while the gastrocnemius scales
isometrically. After day 29, all three hindlimb muscles experience growth rates that are
not different from zero, indicating cessation of muscle growth. The surface area of the
foot experiences negative allometric growth (M0.55) until day 31, at which point growth
rate slows to a slightly lower allometric scaling factor (M0.48; Table 1.1; Figure 1.1).
Most of hindlimb morphological growth occurs over the first half of mallard ontogeny,
which allows the forelimbs to increase relative proportions during the second half.
Forelimb morphometrics
Mallard forelimb morphology scales with extreme positive allometry over entire
ontogenetic period, indicating the forelimb is relatively more robust in the adult birds.
Forelimb morphology scales opposite to that in the hindlimb. Bone length of the
forelimb transitions from slow to rapid growth rate at day 8 in the humerus and ulna and
at day 10 in the carpometacarpus (Table 1.1). Bone width in the forelimb undergoes a
similar shift from slow to rapid growth rate at day 6 in all three elements. From days 610, bone growth rate increases substantially, resulting in extremely high positive
allometry over the remainder of development (Table 1.1, Figure 1.2, 1.3). Forelimb
muscle growth displays slight positive allometry from days 0-29, and severe positive
allometry from days 29-60 (Table 1.1, Figure 1.4). Interestingly, both forelimb and
hindlimb musculature alter their respective growth rates around the same inflection date
(29 days post hatching). Wing area experiences a change in growth rate at 17 days; prior
11
to the inflection area scaled with negative allometry, and following the inflection area
scaled with severe positive allometry (Table 1.1, Figure 1.1). This means wing area
decreases relative to body mass beginning at hatching, but then drastically increases
growth rate from day 17-60. Individual components of the limb initiate in a staggered
manner: bone growth at days 6-10, followed by increases in wing surface area at day 17
and lastly by hypertrophy in muscle mass at day 29.
Performance
Three distinct trends account for mallard performance during ontogeny when
running, swimming and flying. Mallard running performance is a hindlimb-only
locomotor behavior and precocial hatchlings (day 3) are capable of attaining 60% adult
performance (Figure 1.5). Running performance improves with age, but reaches adult
levels around 25 days. Swimming performance begins as a hindlimb-only locomotor
behavior and hatchlings are capable of attaining 40% adult levels in sprint speed (Figure
1.5). Swimming performance improves throughout mallard ontogeny (in contrast to
running) because the birds integrate their developing forelimbs into the swimming
mechanics once the wings are long enough to reach the water – at approx. 30 days, which
is also when hindlimb performance begins to plateau (Figure 1.5). Vertical acceleration
during descent is reduced to a minor degree on account of body drag; mallard hatchlings
descended at approx. 8.0 ms-2 (rather than 9.8 ms-2). The flapping of mallard chicks
during descent does not improve flight performance until the last week of ontogeny
(Figure 1.5). By day 60, mallards can fly indefinitely and are capable of descending at a
near-constant speed (zero acceleration downward).
12
Discussion
Morphological development in the mallard initiates early in the hindlimb, shifting
to the forelimb late in ontogeny. Thus each locomotor module is functionally
implemented at different stages during mallard ontogeny. The hindlimbs experience
selective pressures for mature function throughout the ontogenetic period, and therefore
undergo much less morphological change than do the forelimbs, which experience
delayed and extreme growth for flight performance at fledging. Due to an inherent
tradeoff between tissue maturity and growth rate (Ricklefs 1979), mallard hindlimb
morphology in the adult may be restricted to the degree to which the musculo-skeletal
system can both perform and morph throughout the ontogenetic period. In contrast,
forelimb morphology matures late in development, thus freeing the musculo-skeletal
system of the wing to depart dramatically in form from hatchling to adult.
Hindlimb growth and running performance
Mallard hatchlings at 3 days post-hatching are capable of running at 60%
maximum adult performance due to their prematurely developed hindlimb musculoskeletal system. Through the first half (month) of mallard ontogeny, hindlimb bones and
muscles remain fairly robust relative to the body, scaling isometrically or with slight
positive allometry. At one month post hatching, mallard hindlimb growth begins to
terminate – scaling factors of the musculo-skeletal system through the remainder of
ontogeny are indistinguishable from zero. This is nearly the same point in mallard
ontogeny when running performance plateaus, suggesting developing mallards abandon
improvement of hindlimb growth, and therefore terrestrial locomotor performance, after
one month post-hatching. As mallards age, feeding habits shift from terrestrial
13
insectivory to aquatic herbivory: filter feeding and foraging on duckweed (Collias et al.
1963). A shift to an obligatory aquatic lifestyle may be a product of inefficient terrestrial
locomotion in mallard ducks (Biewener and Corning 2001). Water-bound mallards at 1
month post hatching display a dramatic shift in developmental investment from the
hindlimbs to the forelimbs.
Forelimb growth and flying performance
Developing mallards do not rely on flight performance prior to fledging, yet
forelimb bone growth initiates at approximately 1 week post-hatching and continues at a
constant rate for the remainder of development. Fledging period is highly correlated to
wing length in birds, suggesting linear long-bone growth is rate limiting and must
therefore initiate early in development (Carrier & Auriemma 1992). It is not until
mallard wing bones are 50% of adult size, at 1 month post-hatching, that muscle growth
in the forelimb initiates (Table 1.1, Figure 1.4). For the first month of ontogeny, muscle
mass scales with slight positive allometry (M1.3-1.5), retaining near-similar proportions to
body mass. At ~29 days post hatching and continuing past the 60-day fledging date,
muscle mass of the forelimb scales with severe positive allometry (M2.1-3.7). The onset of
forelimb muscle growth half way through ontogeny coincides with the cessation of
hindlimb muscle growth, suggesting there exists a clear shift of energy allocation within
the body. Muscle growth requires substantial energetic investment, thus it is no surprise
that mallard development partitions fuel deposition into the fore and hindlimb modules
separately – probably based on the ecological utility of each system. Mallard fledging
does not appear to be a product of muscle mass as much as wing maturity. Wing area
increases dramatically from day 17 to 60, at which point growth plateaus and the bird
14
fledges (Figure 1.1). The aerodynamic capacity of the wing in the last 2 weeks of
development improves drastically, which suggests wing shape undergoes major
morphological changes in order to perform maximally in a fledged bird (Dial et al. in
prep). Flying performance improves dramatically the week prior to mallard fledging
owing to the fact that all forelimb elements come into maturity at or around day 60. The
entire developmental process surrounding forelimb development appears to be timed in
preparation for fledging at day 60. The muscles of the forelimb continue to hypertrophy
through fledging, probably due to functional employment of the musculature, similar to
adult birds that begin to fly again following a period of wing molt and muscle atrophy
(Portugal et al. 2009).
Developmental modularity and locomotor integration
Mallard natural history makes use of aquatic environements (rivers, ponds) as
feeding grounds and sanctuaries away from land-based predators, and as a refuge to dive
from arial based threats (Düttmann 1992). The precocial development of mallard
hindlimbs allows chicks to forage and locomote within and around their aquatic habitats,
without the need for functional flight performance. At hatching, mallard swimming
sprint speed is 40% of maximum adult performance. For the first month of mallard
ontogeny, swimming remains a hindlimb-only locomotor behavior and improves in
concert with running performance. At day 30, the point when hindlimb growth plateaus
and development of the musculop-skeletal system shifts to the forelimbs, mallards also
begin to integrate their wings into swim mechanics. At this point in development the
forelimb appendages are long enough to reach the water and provide functional aid to
maximum swimming performance (Figure 1.5). Although mallard hatchlings are capable
15
of producing enough vertical force during swimming to lift their body out of the water,
which reduces body drag along the surface, the recruitment of the wings in older birds
assists in combating the drag developed from a heavier body moving across the water
surface (Aigeldinger & Fish 1995). The integration of the forelimbs into swimming
appears to be a functional intermediary (or rudimentary form) of wing use during takeoff
from the water in adult birds. Unlike diving ducks (Subfamily: Aythyinae), dabbling
ducks (Subfamily: Anatinae) are capable of immediate takeoff from the water and do not
require any horizontal travel over the surface before becoming airborne. The ontogenetic
involvement of the forelimbs in mallard swim mechanics suggests forelimb and hindlimb
integration is central to locomotion throughout mallard life history.
Ontogenetic canalization
Differential growth trajectories between locomotor modules have also been
shown to exist within California gulls (Larus californicus; Carrier & Leon 1990). Similar
to mallard life-history, juvenile gulls use relatively mature hindlimbs to navigate their
terrestrial and aquatic environments, delaying flight capacity to the adult condition.
Development of the gull forelimb is delayed to the last portion of ontogeny, where bone
width and pectoralis muscle mass scale with positive allometry. Since non-functional
tissues are uneconomical to maintain, it is thought that forelimb growth is delayed to
minimize unnecessary energy expenditure during ontogeny (Carrier & Leon 1990).
Interestingly, linear growth of the gull forelimb skeleton initiates at hatching and persists
at a constant rate throughout the entire ontogenetic period. Since linear forelimb bone
growth is thought to be the rate-limiting process in terms of forelimb functionality, gulls
initiate forelimb bone growth at an earlier stage in ontogeny than mallards due to gulls
16
possessing relatively longer adult wings (Carrier & Auriemma 1992). In contrast, gull
hindlimbs scale isometrically in both bone length and gastrocnemius muscle mass, but
experience negative allometric growth in bone width. Relatively wider bones in juveniles
compensate for the weak nature of growing tissue, which experiences an inherent tradeoff
between mature functional utility and rapid rate of growth (Ricklefs 1979).
Across endothermic taxa, growth rate tends to show a strong negative relationship
with neonatal maturity (Case 1978, Ricklefs 1979). The highest growth rates (shortest
ontogenetic periods) are observed in altricial species where juveniles develop in protected
refuges (nests) and are fed and cared for by their parents (experiencing high rates of
energy allocation). Precocial species grow much more slowly than altricial species, in
part because they must locomote in order to forage and evade predation, which means
energy is expended to produce mechanical work rather than physical growth. Precocial
species also exhibit reduced growth rates due to a proposed physiological tradeoff
between tissue maturity and rate of cellular differentiation (Ricklefs 1979). Relatively
mature tissues grow relatively slowly, which means in situations with determinate
growth, selection on the locomotor machinery has the capacity to channel, or canalize,
the juvenile phenotype into adulthood (Frazzetta 1975).
Species exhibiting altricial growth and performance are, in a sense, freed from the
restrictive effects of rapid growth and tissue function. Theoretically this allows altricial
species to adjust their morphology to allow access to novel locomotor habits (e.g.,
dynamic soaring, high-speed aerial predation, aerial insectivory, long-distance
migration), which would otherwise be unattainable in a juvenile condition. Small size
(actually good for flight performance), differentiating tissues and linear bone growth
17
limitations restrict juvenile form and function to a condensed range of precocial
operation. Altriciality, which relinquishes the selective demands placed on developing
locomotor systems, may be an evolutionary requirement for attaining high-performance
locomotor ability.
Mallards, as is the case with the majority of anseriforms, are long-distance, highspeed migratory fliers. Economical flight requires finely tuned aerodynamic structures,
aerobic musculature and sufficient neuro-muscular integration, all of which might
themselves require appropriate investment throughout development. By freeing the
forelimbs from locomotor demands early in ontogeny, anseriforms may bypass the
potential canalization of neonatal form in order to obtain a specialized, high-performance
flight apparatus that would be otherwise non-functional in a diminutive juvenile.
Table 1.1
Allometric scaling equations of the form y=amb, where m is body mass in grams, of
skeletal, muscular and structural elements throughout mallard ontogeny. Expected
scaling slopes indicated. Inflection day (i) indicates point at which exponential growth
rate changed. Scaling regressions run before inflection, after inflection and for entire
growth series. Data were log transformed and equations were fit by reduced major axis
regression; parameters are presented as value + 95% confidence interval. Symbols next
to slope indicate negative allometry (-), positive allometry (+) and isometry (=).
18
19
Day 0-Adult
expected slope r2
Hindlimb
Length (mm)
Day 0
slope
intercept
inflection day (I)
r2
0.33
Femur
0.98
0.329 ± 0.013 (=)
0.716
± 0.035
34
0.99
Tibiotarsus
0.98
0.305 ± 0.013 (-)
1.010
± 0.035
34
0.97
Tarsometatarsus
0.97
0.308 ± 0.017 (-)
0.762
± 0.044
34
0.96
Femur
0.94
0.367 ± 0.028 (=)
-0.361 ± 0.073
37
0.93
Tibiotarsus
0.96
0.335 ± 0.021 (=)
-0.308 ± 0.056
37
0.94
Tarsometatarsus
0.91
0.303 ± 0.027 (=)
-0.181 ± 0.071
37
0.92
Iliotibialis cranialis
0.96
1.008 ± 0.060 (=)
-2.496 ± 0.159
29
0.98
Flexor Cruris Lateralis
0.95
1.241 ± 0.084 (+)
-2.921 ± 0.222
29
0.96
Gastrocnemius
0.97
0.992 ± 0.051 (-)
-2.354 ± 0.133
29
0.97
0.98
0.537 ± 0.022 (-)
-0.195 ± 0.056
31
0.98
Humerus
0.95
0.638 ± 0.044 (+)
-0.022 ± 0.117
8
0.64
Ulna
0.88
0.665 ± 0.070 (+)
-0.213 ± 0.186
8
0.01
Carpometacarpus
0.85
0.664 ± 0.077 (+)
-0.356 ± 0.202
10
0.01
Humerus
0.95
0.595 ± 0.041 (+)
-1.009 ± 0.108
6
0.15
Ulna
0.89
0.676 ± 0.068 (+)
-1.373 ± 0.179
6
0.05
Carpometacarpus
0.91
0.631 ± 0.057 (+)
-1.312 ± 0.149
6
0.11
Pectoralis
0.93
1.762 ± 0.139 (+)
-3.832 ± 0.366
29
0.97
Supracorocoideus
0.95
1.742 ± 0.121 (+)
-4.571 ± 0.318
29
0.97
Triceps
0.93
1.887 ± 0.166 (+)
-5.115 ± 0.457
29
0.90
Biceps
0.95
1.738 ± 0.131 (+)
-4.982 ± 0.360
29
0.92
0.81
1.248 ± 0.167 (+)
-1.573 ± 0.431
17
0.76
Width (mm)
Mass (g)
0.33
1.00
Area (cm2)
0.67
foot
Forelimb
Length (mm)
Width (mm)
Mass (g)
0.33
0.33
1.00
Area (cm2)
wing
0.67
20
Day 0-I
intercept
inflection day (I) r2
I-Adult
slope
intercept
r2
slope
intercept
0.716
± 0.035
34
0.99
0.354
± 0.015 (+)
0.668
± 0.036
0.35
0.286
± 0.118 (=)
0.835
± 0.358
1.010
± 0.035
34
0.97
0.317
± 0.022 (=)
0.987
± 0.051
0.56
0.295
± 0.100 (=)
1.035
± 0.304
0.762
± 0.044
34
0.96
0.328
± 0.027 (=)
0.722
± 0.063
0.32
0.232
± 0.098 (=)
0.983
± 0.296
-0.361 ± 0.073
37
0.93
0.381
± 0.039 (+)
-0.388 ± 0.091
0.00
-0.595 ± 0.327 (=)
2.562
± 0.998
-0.308 ± 0.056
37
0.94
0.342
± 0.032 (=)
-0.321 ± 0.075
0.06
0.435
± 0.232 (=)
-0.616 ± 0.707
-0.181 ± 0.071
37
0.92
0.346
± 0.037 (=)
-0.264 ± 0.088
0.34
0.425
± 0.190 (=)
-0.586 ± 0.579
-2.496 ± 0.159
29
0.98
1.120
± 0.076 (+)
-2.713 ± 0.168
0.03
0.656
± 0.293 (-)
-1.468 ± 0.880
-2.921 ± 0.222
29
0.96
1.432
± 0.133 (+)
-3.290 ± 0.295
0.12
0.704
± 0.299 (-)
-1.361 ± 0.898
-2.354 ± 0.133
29
0.97
1.072
± 0.080 (=)
-2.511 ± 0.178
0.30
0.649
± 0.246 (-)
-1.344 ± 0.737
-0.195 ± 0.056
31
0.98
0.551
± 0.034 (-)
-0.222 ± 0.079
0.68
0.479
± 0.149 (-)
-0.029 ± 0.442
-0.022 ± 0.117
8
0.64
0.200
± 0.097 (-)
0.772
± 0.168
0.97
0.823
± 0.048 (+)
-0.556 ± 0.134
-0.213 ± 0.186
8
0.01
0.258
± 0.230 (=)
0.578
± 0.391
0.95
0.975
± 0.076 (+)
-1.112 ± 0.215
-0.356 ± 0.202
10
0.01
0.274
± 0.206 (=)
0.417
± 0.364
0.93
1.061
± 0.095 (+)
-1.509 ± 0.269
-1.009 ± 0.108
6
0.15
-0.308 ± 0.327 (=)
0.494
± 0.525
0.97
0.694
± 0.041 (+)
-1.293 ± 0.114
-1.373 ± 0.179
6
0.05
-0.880 ± 0.985 (=)
1.218
± 1.583
0.93
0.837
± 0.076 (+)
-1.839 ± 0.211
-1.312 ± 0.149
6
0.11
-0.593 ± 0.644 (=)
0.750
± 1.035
0.96
0.781
± 0.051 (+)
-1.745 ± 0.141
-3.832 ± 0.366
29
0.97
1.287
± 0.104 (+)
-2.857 ± 0.230
0.87
3.707
± 0.611 (+)
-9.600 ± 1.833
-4.571 ± 0.318
29
0.97
1.317
± 0.095 (+)
-3.705 ± 0.211
0.87
3.260
± 0.526 (+)
-9.055 ± 1.578
-5.115 ± 0.457
29
0.90
1.499
± 0.259 (+)
-4.264 ± 0.619
0.80
2.818
± 0.566 (+)
-7.858 ± 1.697
-4.982 ± 0.360
29
0.92
1.387
± 0.211 (+)
-4.229 ± 0.504
0.91
2.050
± 0.283 (+)
-5.864 ± 0.849
-1.573 ± 0.431
17
0.76
0.398
± 0.103 (-)
0.129
0.93
2.882
± 0.309 (+)
-6.282 ± 0.888
± 0.208
21
1600
Body mass
7,('"01%&8#952%
6(**%&12%
1200
800
400
0
800
600
400
200
0
//
500
Foot
25
34$(%&/#52%
34$(%&/#52%
1000
//
30
Wing loading
1200
20
15
10
Wing
400
300
200
100
5
0
0
10
20
30
40
50
60
//
Adult
70
0
0
10
20
30
40
50
60
//
Adult
70
!"#$%&'()*%+,*-%.(-/."012%
Time
(days post-hatching)
Figure 1.1
Body mass, wing loading and surface areas of the foot and wing throughout
mallard ontogeny, including adult (>365 days).
22
100
100
Femur
80
80
60
60
40
40
20
20
0
//
3$01-.%&##2%
100
0
80
80
60
60
40
40
20
20
0
//
Tarsometatarsus
20
20
0
20
30
//
Caropmetacarpus
60
40
10
Ulna
0
40
0
//
100
Tibiotarsus
60
Humerus
40
50
60
//
Adult
70
0
0
10
20
30
40
50
60
//
Adult
70
!"#$%&'()*%+,*-%.(-/."012%
Time
(days post-hatching)
Figure 1.2
Lengths of limb bones of Anas platyrhynchos over 60-day ontogenetic course (Adult
>365 days old). Elements of the hindlimb and forelimb are aligned from proximal to
distal (top to bottom) and scaled for comparison.
23
Femur
8
6
6
4
4
2
2
0
//
Tibiotarsus
3"'-.%&##2%
6
0
5
4
4
3
3
2
2
1
1
0
//
Tarsometatarsus
4
4
3
3
2
2
1
1
0
20
//
6
5
10
Ulna
0
5
0
//
6
5
6
Humerus
8
30
40
50
60
//
Adult
70
Caropmetacarpus
0
0
10
20
30
40
50
60
//
Adult
70
!"#$%&'()*%+,*-%.(-/."012%
Time
(days post-hatching)
Figure 1.3
Widths of limb bones of Anas platyrhynchos over 60-day ontogenetic course
(Adult >365 days old). Elements of the hindlimb and forelimb are aligned from
proximal to distal (top to bottom) and scaled for comparison.
24
4
120
Iliotibialis cranialis
Pectoralis
100
3
80
60
2
40
1
20
0
//
3(**%&12%
8
0
16
Flexor Cruris Lateralis
6
12
4
8
2
4
0
//
5
0
4
8
3
6
2
4
1
2
0
10
20
Supracorocoideus
//
10
Gastrocnemius
0
//
30
40
50
60
//
Adult
70
Triceps
Biceps
0
0
10
20
30
40
50
60
//
Adult
70
!"#$%&'()*%+,*-%.(-/."012%
Time (days post-hatching)
Figure 1.4
Masses of major hindlimb and forelimb muscles over 60-day ontogenetic
course, including adult (>365 days) of Anas platyrhynchos.
25
5.0
Running
-1
Velocity (ms )
4.5
4.0
3.5
3.0
2.5
2.0
Swimming
3.0
-1
Velocity (ms )
3.5
2.5
2.0
0
-2
Vertical acceleration (ms )
1.5
Flying
-2
-4
-6
-8
-10
10
20
30
40
Time (days post hatching)
50
60
Time (days post-hatching)
Figure 1.5
Running, swimming and flying performance over mallard ontogeny.
Measurements of whole-body velocity during maximum running and swimming
sprint performance and negative acceleration vertically during descending flight
were taken (averages and standard deviations shown). 26
CHAPTER 2
COMPARATIVE ONTOGENY OF AERODYNAMICS IN TWO AVIAN
SPECIES WITH DIFFERENT LIFE-HISTORY STRATEGIES
Abstract
The impact of wing development on aerodynamic capacity is not well understood
within the avian clade, yet we know wing morphology is related to flight performance
and ecology in adult birds. To reveal the effects of life-history strategy and ontogeny on
wing function, we used a propeller and force-plate model and studied the aerodynamic
forces across a developmental series of precocial chukar partridge (Galliformes: Alectoris
chukar; Heers 2010) and altricial mallard (Anseriformes: Anas platyrhychos; this study)
wing development. Lift and drag production improved dramatically over the course of
each species’ ontogeny, but chukar capacity to generate lift started at day 8 and
maximum CL improved only a minor extent (80%), while mallard capacity was delayed
until just prior to fledging (day 45) and maximum CL improved dramatically (400%).
Chukar rely on their premature flight capability to rapidly accelerate and escape predation
both as vulnerable juveniles and adults, while mallards seek refuge in a pond or river and
do not fly until fully grown. The restricted ontogenetic change in chukar wing form and
function and the delayed and radical change in mallard wings appear to be a product of
precocial versus altricial life-history strategies affecting ultimate morphological
development, and subsequently adult locomotor performance.
27
Introduction
Morphology and aerodynamics
An empirical understanding has yet to be established for the morphological
impact of wing design on aerodynamic capacity during slow flight in animals. This is due
to, in part, the vast diversity of forms in flying animals and the complexity of
aerodynamic mechanisms during flight at low advance ratios, where wing flapping
velocity exceeds translational velocity of the animal. Unsteady effects during hovering
and slow flight include delayed stall, associated with leading-edge vortices (LEV’s),
wake capture and rotational circulation (Dickinson et al. 1999; Lehmann 2004). The
importance of these unsteady effects was discovered while using robotic models that
were programmed to move a rigid wing through the full wing-stroke trajectory observed
during flapping (Ellington et al. 1996; Dickinson et al. 1999; Lehmann 2004), and, more
recently, using revolving-wing “propeller” models (Usherwood & Ellington, 2002a, b;
Usherwood, 2009) in which a fixed wing is spun to emulate the middle phase of
downstroke. Although such models may have significant limitations, including the lack
of wing flexibility (Venella et al. 2008; Young et al. 2009), new work with live animals
supports, for example, the hypothesis that there is a significant contribution of LEV’s to
the aerodynamics of slow flight (Thomas et al. 2004; Muirjes et al. 2008; Warrick et al.
2009).
Research using propeller and robotic models has produced two surprising results
that merit further study. First, these physical models suggest that morphology has almost
no effect upon wing aerodynamics, particularly at angles of attack (α) that are used by
animals during flight (Usherwood & Ellington, 2002a, b; Usherwood, 2009). Second, the
28
observed lift-to-drag ratios (L:D) at moderate and high angles of attack (α) are quite low
compared with expectations from fixed-wings during translational motion (Withers,
1981; Drovetski, 1996; Videler et al. 2004).
Propeller experiments reveal virtually no change in aerodynamic performance
regardless of dramatic alterations in wing plan-form (leading-edge detail, camber, twist)
or aspect ratio (Usherwood & Ellington 2002a). Further, there is no major difference in
coefficients of lift (CL) and drag (CD) among insects and birds that range in Reynolds
number (Re), from 1100 in mayfly (Ephemera vulgata) to 26000 in blue-breasted quail
(Conturnix chinensis; Usherwood & Ellington 2002b). Astoundingly, wing aerodynamic
capacity is largely unaffected when rock dove (pigeon, Columba livia) wings are
compared with cardboard replicas (same area and outline, no camber and twist). Taken
together, these results suggest something other than morphology drives functional utility
of wings in slow flapping flight (Usherwood 2009). One exception exists: hummingbird
(Trochilidae) wings at low α reportedly produce significantly more lift than flat plate
models (Altshuler et al. 2004).
Secondly, it is surprising that L:D ratios for spinning or robotic wings are
generally less than 2:1, and this has led to a proposed “normal forces” model in which the
net pressure distribution about the wing gives rise to a force that is normal to the wing
chord (Usherwood & Ellington 2002a, b; Usherwood, 2009). Experiments using flow
visualization in the wake of a common swift (Apus apus) in crusing flight indicate total
L:D ratios = 13:1 (Henningsson et al. 2008). In contrast, and consistent with thin-airfoil
theory (Norberg, 1994), fixed bird wings in translation produce relatively high lift-to-
29
drag ratios (e.g. L:D > 7) and resultant lift that is approximately normal to incurrent flow
(Withers 1981; Norberg 1994).
Life-history strategies
The importance of flight to developing ground birds is critical as it provides a
means for predator escape and possibly foraging opportunities (Jackson et al. 2009).
Chukar partridge (Galliformes: Alectoris chukar, hereafter “chukar”) exhibit a precocial
development of flight performance, where juveniles possess the ability to produce useful
aerodynamic forces in vivo at one week post-hatching (Tobalske & Dial 2007). The
short, broad, highly cambered chukar wing is implemented early in ontogeny for burst
(accelerative) flight (Dial et al. 2006). Adult flight style changes very little, although
chukar flight performance improves throughout ontogeny (Dial et al. 2006). In contrast,
mallard ducks (Anseriformes: Anas platyrhychos, hereafter “mallards”), are precocial in
terms of hindlimb-powered locomotion (terrestrial and aquatic), but experience delayed
maturation of their wings until just prior to fledging (Dial 2010). Waterfowl spend their
ontogenetic period exploiting food-rich and predator-free ponds and rivers, using flight
primarily for long-distance seasonal migration rather than burst-escape accelerations.
The onset of bone growth, muscle hypertrophy and feather unfurling during mallard
development is delayed to the last quarter of their ontogenetic period (Dial 2010). This
delay is indicative of altricial developmental timing, where onset of functional maturity
initiates rapidly and at the end of ontogeny, in either forelimb or hindlimb locomotor
modules (Gatesy & Dial 1996).
This study looks to compare the ontogenetic acquisition of aerodynamic capacity
between two bird species exhibiting contrasting life history and locomotor strategies. In
30
quantifying the aerodynamic capacity of chukar and mallard wings through ontogeny, we
will better understand the functional impact morphology has on animal aerodynamics and
the significance life-history strategy has on locomotor design and performance.
Methods
Wing preparation and ontogenetic series
Our sample of ontogenetic series began with day 8 in the chukar and day 30 in the
mallard. These were the earliest stages of wing development for which our propeller and
force-plate apparatus (Figure 2.1) could resolve forces when the wings were spun at in
vivo angular velocities. For the chukar series (day 08, 10, 20, 50 and 70), wing stages
were determined primarily by wing area, which incrementally doubles for the first four
stages and stops once an adult wing is developed (Figure 2.2, Table 2.1). The mallard
series initiated at onset of pin feather growth (day 30), advanced as barbules unfurl (day
45) and ended in 5-day increments proceeding towards the mature, fully developed wing
(day 60). Spin trials were duplicated with a second set of wings for each age-class.
Right wings were removed at the shoulder and pinned and taped to dry using a
backing of rigid foam board. The spread of the wings mimicked in vivo morphology at
mid-down stroke, determined from high-speed video (1000 Hz) of each species during
wing-assisted incline running (WAIR; Dial 2003; Jackson et al. 2009) or flight. A brass
rod, varying from 1.5 to 5 mm in diameter according to wing size, was inserted into a
pre-drilled hole in the head of the humerus of each wing. The attachment was reinforced
using epoxy cement. The rod served to mount the wing on the shaft of our motor and
provided a counterbalance during rotation. The wing was oriented on the shaft of the
motor so that the leading edge was parallel to the horizontal plane.
31
All measures of wing morphology including first, second and third moments of
area were obtained from the dried wings using a digital camera to photograph the dorsal
view of the wing, with analysis accomplished using ImageJ v1.42 and custom m-files in
MatLab R2010a.
Propeller apparatus and force recordings
The general propeller-force plate assembly was the same for all spin trials (Figure
S1), except for the motor used. Mid-experiment, we were compelled to increase the
torque capacity of the motor to accomplish the mallard measurements. Wings were
mounted upside down (Usherwood, 2009) to NEMA 23 stepper or brushless DC motors
(Anaheim Automation, Inc., Model 23W108D-LW8 and BLWR232S-36V-4000) for the
chukar ontogenetic series, and to a NEMA 34 motor (Anaheim Automation, Inc.,
34W214D-LW8) for the mallard series. For the size-23 stepper motor, we used an Arcus
ACE-SDE driver and Arcus software. For the size-23 brushless motor, we used a
Luminary Micro LM3S8971 BLDC Motor controller. Lastly, for the size-34 motor, we
used a driver and power supply from Anaheim Automation, Inc. (DCL 601USB, MBC
12101 and PSA 40V8A) as well as SMC60WIN v. 2.01 software.
We used a custom-built force plate (Bertec Corp.) to measure force along and
torque about the z-axis (Usherwood, 2009) which offered a known conversion of 10000
mN/V for force and 800 mN*m / V for torque. Resonant frequency for the plate,
including the motor assembly (S1) was 220 Hz. Analog (voltage) output from the force
plate were converted and amplified with gain settings from 1 (for adult wings) to 100 (for
juvenile wings) using a Bertec model M6810 amplifier. We imported these data into a
PC computer using an ADInstruments PowerLab 8SP A/D converter sampling at 1000
32
Hz and Chart v5.2 software using a 1 Hz low-pass digital filter. A shield housing
(cowling) isolated the force plate from air velocities induced by upwash from the
spinning wing. For each age-class, in vivo angular velocity, as averaged over the full
down stroke, was calculated using high-speed video, and converted to revolutions per
minute (Table 2.1). The values for angular velocity of the chukar wings were obtained
from bouts of WAIR (Jackson et al. 2009) and, for mallard wings, we used angular
velocity during descending flight.
Because of uncertainty about whether these flight conditions are directly
comparable, we tested intermediate-age chukar and mallard wings at double and half
RPM. We observed effects of absolute values of force but, consistent with Usherwood
(2009), RPM did not affect CL and CD.
Spinning
Spin trials were performed over a range of angles of attack from -20° to 90° in
~10° increments for each wing. Average lift and drag measurements were captured over
10 seconds of steady-speed rotation. We calculated CL and CD following Usherwood &
Ellington (2002a) and assuming a “triangular” induced-velocity distribution based off
raw (vertical and horizontal) force coefficients (CV and CH):
CL = (CV,steadycosε - CH,steadysinε) (U/Ur)2,
(1)
and
CD = (CH,steadycosε - CV,steadysinε) (U/Ur)2
(2)
where ε is downwash angle, U is wing velocity and Ur is local air velocity (see
Usherwood & Ellington 2002a for further details of calculations).
33
We measured α, the geometric angle of attack of the wing relative to the
horizontal plane of rotation, using reflective markers placed on the feathers overlying the
wrist and on the trailing edge of secondary flight feather number 1. As the wings
deformed under aerodynamic loading (Usherwood, 2009), herein we report the “active” α
during spinning. To measure active α, we used a Photron SA-3 camera, with 1024 x
1024 pixel resolution, sampling at 1000 Hz and with a shutter speed of 1/5000 sec.
Angles were measured from recorded video images using Photron PFV v.3.20 software
and a PC Computer.
After completing the wing measurements, we spun brass rods of the same
diameter as the supporting rods, doubled in length for counterbalance, and subtracted half
the drag developed from these trials to eliminate the contribution of the counterbalance
portion of brass rod during wing trials.
Analysis
We used IGOR Pro. v.6.12 software to analyze our data. For each wing, we fitted
a 100-point spline-interpolation curve for CL and CD from -15˚ to 80˚. We then computed
an average and standard deviation between the two wings for each age class. From the
averaged coefficient values we generated polar traces of CL as a function of CD as well
graphs of the of CL : CD ratio as a function of α.
Results
The changes in wing anatomy that occur during ontogeny dramatically influenced
aerodynamic function in chukar and mallard wings (Figure 2.3). Chukar and mallards
undergo similar ontogenetic periods in terms of wing development (70 and 60 days,
respectively) despite a two-fold difference in adult mass (600g and 1200g) (Dial et al.
34
2006, Dial 2010). Standard deviations were generally < 25% of the mean CL and CD
(Figure 2.5).
Chukar
Day 08 is the first stage at which flight feathers emerge in the chukar wing, and is
thus the starting stage of the ontogenetic-aerodynamic series (Figure 2.2). A day 08 wing
at maximum CL : CD is capable of generating nearly as much lift as drag (CL : CD =
0.88, Figure 2.3a). Only two days later, a day 10 wing is capable of generating sufficient
lift to overcome drag (CL : CD = 1.44, Figure 2.3a). Less functional change occurs
between day 10 and 20, but notably, maximum CL : CD increases from 1.44 to 2.45 and α
at these peak values of CL : CD decreases from 38˚ to 28˚ (Figure 2.3a). From day 20 to
50, very little morphological change takes place except that wing area doubles in size
(Table 2.1). This impacts the functional capacity (in terms of CL as a function of CD) of
the wing very little (compare D20 and D50 polar traces, Figure 2.3a). Over the final
stage of chukar wing development (day 50 to 70), morphological elements of wing shape
improve the wing’s lift-generating capacity. At 0˚ α, CL : CD = 1 and maximum CL : CD
= 4 at 15˚ α (Figure 2.4, Table 2.1). The maximum CL improves with each increase in
age and occurs at shallower α (Figure 2.3).
Mallard
The mallard developmental series is rooted at day 30, the ontogenetic halfway
mark, when pin feathers first begin to emerge even though they will not begin to unfurl
until day 45 (Figure 2.2, Table 2.1). The polar curve of a day 30 mallard indicates the
wing is practically incapable of lift generation and entirely non-functional: even at
maximum CL : CD, drag outweighs lift seven-fold (CL : CD = 0.13, Figure 2.4b, Table
35
2.1). From day 30 to day 45, the mallard wing experiences dramatic morphological
change both in terms of size (wing area quadruples; Table 2.1) and shape (Figure 2.2,
Table 2.1). The functional significance of shape change is observed in the ability of a
day 45 wing to generate 1.46 times more lift than drag at 25˚ α (Figure 2.3, 2.4). Five
and ten days later (day 50 and 55), maximum CL : CD increases to 2.26 and 3.43
respectively (Figure 2.3, 2.4). By the adult condition (day 60), a mallard wing can
produce five times the amount of lift for a given amount of drag at 11˚ α (Figure 2.3, 2.4).
The maximum coefficient of lift is 2.12 in the adult mallard wing at 35˚ α (Figure 2.3).
Comparison
Despite similar ontogenetic periods, improvement in mallard aerodynamic
capacity occurs over a much shorter (more condensed) period than in chukars (Figure
2.3). In the final 15 days of wing development, mallard aerodynamic capacity improves
to the same degree as that taking 60 days in the chukar (Figure 2.3). There exists an
ontogenetic tendency in both species for wings to improve lift-generation at 0˚ α with
increasing age (Figure 2.3). As each bird ages, maximum CL : CD increases and occurs at
a lower α, with mallards experiencing lower α than chukars (Figure 2.3). Overall, then, it
appeared that morphology rather than size, per se, improved aerodynamic capacity.
Discussion
Effect of morphology
In contrast to previous findings (Usherwood & Ellington 2002a,b; Usherwood
2009; Altshuler et al. 2004), aerodynamic capacity is significantly influenced by
ontogenetic changes in wing morphology. Both chukar and mallard wings increase in
length and chord through ontogeny, but decrease in aspect ratio with age (chukar AR
36
down by 20% to 2.9; mallard AR down by 40% to 3.6; Table 2.1). Furthermore, camber
increases two-fold in the mallard ontogenetic series, but remains unchanged throughout
chukar development (Table 2.1). These known morphological differences occurring
throughout chukar and mallard ontogeny impart dramatic functional consequences on
wing aerodynamic capacity. Ontogenetically, chukar and mallard improve aerodynamic
capacity in terms of total lift production and lift-to-drag economy (Figure 2.3). Improved
capacity is achieved in concert with lower α, again indicating that aerodynamics in
mature animals rely more on lift-based rather than drag-based mechanisms. Although lift
can be generated by any non-specialized structure (i.e., cardboard cutout, Usherwood,
2009) by angling the plan form to oncoming wind, the ability of a structure to further
improve aerodynamic capacity relies on topographical contortion of the wing (such as
asymmetrical shape, camber and twist).
Effect of life-history strategy
Ontogenetic improvement of aerodynamic capacity in chukar and mallard wings
remains a general trend, yet the temporal unfurling of such capacity contrasts
dramatically between the two species. Chukar are precocial fliers in that diminutive
juveniles rely on the ability to use their forelimbs for aerial locomotion to escape
predatory threats (Dial et al. 2006). Since linear bone growth presents an inherent
limitation to fledging time (Carrier & Auriemma 1992), chukar chicks, which are fledged
a week following hatching, possess relatively short wings for their body size. Short
wings force the chukar to expand chard length in order to provide surface area for the
airfoil to function. By increasing chord length, aspect ratio decreases (Table 2.1) and the
wings produce relatively high amounts of drag, which is uneconomical for distance flight,
37
but highly useful in takeoff. Chukar chicks, which use their wings for escape flight
(takeoff), are capable of generating vortex rings (indicating circulation about the wing)
during each down stroke at 6 days post hatching (Tobalske & Dial 2007). The precocial
ability for chukar chicks to generate useful aerodynamics suggests strong selective
pressures must be acting to promote mature morphology in juveniles. It is known that
tissues (skeletal, muscular, structural) experience tradeoffs between mature function and
rapid growth (Ricklefs 1979). This presents a potential limitation in the degree to which
morphological elements can change in form since endothermic vertebrates experience
determinate periods of ontogenetic growth. Thus, precocial animals, growing under the
confines of tissue limitations, may experience restricted freedom to depart from the
juvenile condition (Frazzetta 1975; Carrier 1996).
In contrast, mallards delay functional implementation of their forelimbs for aerial
locomotion until they are adult size. Although precocial in their early locomotor ability
to run and swim, delayed developmental trajectory of the mallard forelimb reflects a
fundamentally altricial track. No intense selective pressures exist on the forelimb for
premature flight capacity during ontogeny, thus the mallard forelimb experiences rapid
rates of growth and substantial changes in morphology.
Implications for flight style
Aside from developmental trajectory, chukar and mallard ultimately assume
different flight styles based on their different ecological settings. From the first time a
chukar can become air born, flight is used for burst escape; large, anaerobic pectoralis
muscles power an explosive, high wing beat frequency takeoff bout, lasting only a few
seconds before fatigue forces the bird to land and run to safety (Tobalske & Dial 2000).
38
In contrast, mallard flight is an adult-only phenomenon and employed primarily for
migration. Takeoff is less important given the aquatic refuges most mallards inhabit,
although the ability to launch from the water is not trivial in most dabbling ducks
(Family: Anatinae). In this sense, chukar wings are specialized for burst takeoff
performance where acceleration from the ground is essential, while mallard wings are
specialized for high-speed, long-distance, economical flight.
The consequence of contrasting design in chukar and mallard wings is reflected in
the aerodynamic profile of each adult bird. The CL : CD at 0˚ α is 40% higher in the
mallard than the chukar, indicating a more-economical adult wing design. Maximum CL
: CD is 20% higher in the mallard and occurs at a shallower α (11˚ vs. 15˚ for mallard vs.
chukar). A higher lift-to-drag ratio is indicative of a more efficient wing, but not
necessarily one that can generate a large maximum lift coefficient. Paradoxically, the
adult mallard wing generates 20% greater CL than the adult chukar wing, even though
galliforms are thought to possess specialized high lift wings for accelerative takeoff bouts
(Tobalske & Dial, 2000; Askew et al. 2001). Chukar possess lower wing loading and
higher wing beat frequencies than mallards (Table 2.1), which is why they are so
effective at whole-body acceleration from the ground.
Potential limitations and future investigation
Certainly live animals are ideal models for measuring aerodynamic performance
because of natural wing flexibility and neuromuscular control of wing movements that
are far more complex than simple rotation about a fixed shaft; therefore, validating our
results using live animals remains a goal for future work. However, live animals are not
suited for measuring performance outside the envelope they will willingly perform.
39
Within this study, wing shape is representative of standing take-off, vertical flight or very
slow flight with low advance ratio (ratio of flight speed to speed of tip of wing). At best,
the wing posture is relevant to mid-down stroke during flapping flight.
Kinematics of flapping avian flight are complex, with long-axis rotation of the
wings and variation in camber and twist through the wingbeat (Oehme 1971, Tobalske et
al. 2007). It is known from robotic models that unsteady aerodynamics contribute
significantly to the forces produced during hovering and slow flight (Ellington et al.
1996; Dickinson et al. 1999; Lehman, 2004). Recent work using flapping insect wings
(Mountcastle & Daniel, 2009) and computational fluid dynamics (Young et al. 2009)
indicates that wing flexibility also has a significant effect upon aerodynamic function.
Inertial-elastic forces mainly drive insect wing flexibility (the passive deformation of the
wing surface influenced by wing architecture and membrane material properties) from
rapid accelerations during wing reversals rather than aerodynamic forces (Combes &
Daniel 2003). Thus, an important challenge for understanding the effects of morphology
on aerodynamic performance will be to compare our data representing mid-wing
translation with observations of near-field aerodynamics from live animals through the
entire wingbeat cycle (e.g. Warrick et al. 2009).
Avian flight stroke kinematics (α, stroke plane angles, wingbeat frequency and
amplitude) have been observed to change as a function of flight speed in a number of
species (Tobalske & Dial 1997, Tobalske et al. 2007, Dial et al. 2008). Wing dynamics
also change throughout the flight stroke as well as throughout ontogeny (Dial et al. 2008,
Jackson et al. 2009). Juvenile chukar use higher α when performing similar flight
behaviors as adults (Dial et al. 2008), possibly because juvenile chukar wings generate
40
maximum CL at higher α compared to adult wings. Because this study addresses wing
function only at mid down stroke, we are unable to say how wing dynamics influence
aerodynamics throughout the entire flight stroke.
In conclusion, wing morphology imparts a large effect on aerodynamic capacity,
which contrasts to previous findings. Furthermore, development of aerodynamic function
through ontogeny relies on the life history and ecology of juvenile birds. Some birds are
capable of acquiring wing function prematurely to reduce vulnerability during ontogeny
(e.g., chukar). Other developing birds remain safe by inhabiting refuges (nests, ponds)
and do not require wing function prior to fledging (e.g., mallards). Finally, ontogenetic
strategies can alter the selective demands placed on developing tissues and structures –
this may impart inherent limitations to the degree to which developmental processes mold
morphological design.
41
Figure 2.1
Experimental setup of propeller-force plate apparatus. Several motors were
interchanged (see text) to spin a single wing-mount over both chukar and mallard
ontogenetic series at in vivo speeds converted to RPMs (Table 2.1). Force and
torque were measured about the z-axis and converted into coefficients of lift and
drag respectively. Wings were positioned upside-down and a cowling was placed
over the force sensor to reduce the effect of downwash on the force plate readouts.
42
43
Figure 2.2
Dorsal views of chukar partridge (Alectoris chukar) and mallard (Anas
platyrhynchos) wings through ontogeny. Wing developmental period initiated at
youngest age force measurements could be resolved on the propeller apparatus.
5-cm scale bar.
44
Table 2.1
Morphometric data from chukar and mallard ontogenetic series (± s.d.). See text
for details.
Chukar
Wing length (m)
Wing Chord (m)
Aspect Ratio AR
D8
35.3
±
1.1
0.078
±
0.001
0.022
±
0.000
3.57
±
0.07
D10
43.9
±
4.1
0.093
±
0.000
0.034
±
0.003
2.76
±
0.26
D20
88.7
±
3.7
0.143
±
0.003
0.053
±
0.003
2.68
±
0.21
D50
287.0
±
17.0
0.229
±
0.001
0.071
±
0.006
3.24
±
0.27
D70
(Adult)
446.0
±
5.7
0.242
±
0.009
0.083
±
0.002
2.91
±
0.18
Mallard
Mass (g)
Mass (g)
Wing length (m)
Wing Chord (m)
Aspect Ratio AR
D30
636.9
±
70.6
0.169
±
0.012
0.034
±
0.001
5.02
±
0.20
D45
1027.5
±
143.5
0.312
±
0.020
0.073
±
0.017
4.43
±
1.29
D50
1066.4
±
107.6
0.352
±
0.016
0.081
±
0.010
4.38
±
0.33
D55
1093.6
±
3.5
0.359
±
0.033
0.069
±
0.027
5.74
±
2.74
D60
(Adult)
1208.1
±
53.0
0.397
±
0.017
0.112
±
0.003
3.55
±
0.07
45
Area (m2)
2nd Mom Area
Wing loading (Nm-2)
3rd MomArea
Re
0.0017
±
0.0001
3E-06
±
2E-07
1.9E-07
±
1.3E-08
1.0E+05
±
1.3E+03
7170.5
±
0.0030
±
0.0003
1E-05
±
2E-06
7.3E-07
±
1.5E-07
7.2E+04
±
6.2E+01
12892.7
±
0.0076
±
0.0003
4E-05
±
1E-06
4.1E-06
±
1.1E-07
5.7E+04
±
4.5E+03
30865.4
±
0.0163
±
0.0012
2E-04
±
3E-05
3.3E-05
±
5.2E-06
8.7E+04
±
1.3E+03
63043.3
±
0.0202
±
0.0003
3E-04
±
2E-05
5.7E-05
±
5.1E-06
1.1E+05
±
1.3E+02
74313.6
±
Area (m2)
2nd Mom Area
Wing loading (Nm-2)
3rd MomArea
Re
0.0057
±
0.0006
4E-05
±
1E-05
5.0E-06
±
1.9E-06
5.5E+05
±
1.2E+05
10933.3
±
0.0226
±
0.0038
5E-04
±
4E-05
1.1E-04
±
1.8E-05
2.2E+05
±
6.6E+03
36357.6
±
0.0285
±
0.0047
1E-03
±
3E-04
2.4E-04
±
9.3E-05
1.9E+05
±
4.9E+04
47259.9
±
0.0244
±
0.0076
8E-04
±
1E-04
2.0E-04
±
2.1E-05
2.3E+05
±
7.3E+04
40378.2
±
0.0444
±
0.0029
2E-03
±
3E-04
4.7E-04
±
8.5E-05
1.3E+05
±
2.9E+03
100161.3
±
Tip Velocity (ms-1)
Camber
RPM
303.8
0.53
±
0.06
5.37
±
0.04
657
1215.9
0.43
±
0.05
6.42
±
0.00
657
1171.0
0.47
±
0.03
9.45
±
0.19
633
4670.1
0.55
±
0.05
14.70
±
0.07
613
980.2
0.49
±
0.00
14.77
±
0.57
582
Tip Velocity (ms-1)
Camber
RPM
1085.1
0.22
±
0.07
5.49
±
0.38
310
6142.8
0.43
±
0.12
8.49
±
0.53
260
7738.9
0.46
±
0.13
9.87
±
0.44
268
12546.3
0.70
±
0.28
10.07
±
0.91
268
6547.5
0.52
±
0.13
15.16
±
0.65
365
46
Figure 2.3
Polar traces of lift coefficient (CL) and drag coefficient (CD) for an ontogenetic series of
wings from (a) chukar partridge (Alectoris chukar) and (b) mallard (Anas
platyrhynchos). CL and CD were measured at angles of attack (α) from -15˚ to 80˚.
Symbols refer to α = 0˚ (circles), maximum CL : CD (squares, α indicated) and
maximum CL (triangles, α indicated). Traces are set on the same scale to emphasize
aerodynamic differences between a burst-flight wing (chukar) and a migratory wing
(mallard). Traces are means from N = 2 birds per age class, with classes beginning at
the earliest age force readings could be resolved and ending with adult wing.
47
a.
2.5
2.0
42
Coefficient of Lift
1.5
46
57
15
59
24
1.0
28
55
38
30
0.5
day 70 (adult)
day 50
day 20
day 10
day 08
0.0
-0.5
0.0
b.
0.5
1.0
1.5
Coefficient of Drag
2.0
2.5
3.0
2.5
35
2.0
45
1.5
Coefficient of Lift
54
11
44
15
1.0
21
25
0.5
24
42
day 60 (adult)
day 55
day 50
day 45
day 30
0.0
-0.5
0.0
0.5
1.0
1.5
Coefficient of Drag
2.0
2.5
3.0
Figure 2.4
Lift-to-drag ratio (CL : CD) over range of angle of attack (α = -15˚ to 80˚) from (a)
chukar partridge (Alectoris chukar) and (b) mallard (Anas platyrhynchos) ontogenetic
series (N = 2 birds per age class). Axes are at same scale for comparison between
wing types.
48
a.
49
5
4
Lift : Drag
3
day 70 (adult)
day 50
day 20
day 10
day 08
2
1
0
0
b.
20
40
Angle of attack (deg)
60
80
5
4
Lift : Drag
3
day 60 (adult)
day 55
day 50
day 45
day 30
2
1
0
-1
0
20
40
Angle of attack (deg)
60
80
50
Figure 2.5
Variability between subjects for coefficients of lift (CL) and drag (CD) as a
function of angle of attack (α) in adult wings of chukar partridge (Alectoris
chukar; a, CL; b, CD) and mallard (Anas platyrhynchos; c, CL; d, CD). Black
traces represent an interpolated average between two wings over a range of α
from -15˚ to 60˚. Error bars = s.d.
51
a.
1.5
1.0
Cl
0.5
0.0
Bird A
Bird B
-20
0
20
Angle of attack (deg)
40
60
Angle of attack (deg)
b.
2.0
Cd
1.5
1.0
0.5
Bird A
Bird B
-20
0
20
Angle of attack (deg)
Angle of attack (deg)
40
60
52
c.
2.0
Coefficient of Lift
1.5
1.0
Bird A
Bird B
0.5
0.0
-20
0
20
Angle of attack (deg)
40
60
Angle of attack (deg)
d.
3.0
2.5
2.0
Cd
Bird A
Bird B
1.5
1.0
0.5
-20
0
20
Angle of attack (deg)
Angle of attack (deg)
40
60
53
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