The ecological and evolutionary interface of hummingbird flight physiology
1 Section of Integrative Biology, University of Texas at Austin, Austin, TX
78712, USA
2 Smithsonian Tropical Research Institute, PO Box 2072, Balboa, Republic of
Panama
* Present address and address for correspondence: Department of Integrative Biology, University of California, Berkeley, CA 94720, USA (e-mail: colibri{at}socrates.berkeley.edu )
Accepted 25 May 2002
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Summary |
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Relationships among flight-related morphology, competitive ability and foraging behavior have been the focus of numerous studies on tropical and temperate hummingbirds. Ecologists have hypothesized that the primary selective agents on hummingbird flight-related morphology are the behaviors involved in floral nectar consumption. However, flight behaviors involved in foraging for insects may also influence the evolution of wing size and shape. Several comparisons of hummingbird communities across elevational gradients suggest that foraging strategies and competitive interactions within and among species vary systematically across elevations as the costs of flight change with body size and wing shape.
Key words: aerodynamics, biomechanics, evolutionary physiology, flight, hovering, hummingbird
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Introduction |
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The earliest fossil trochilids date from the Pleistocene, and estimates for
the origination of hummingbirds are strongly dependent on assumptions for the
molecular clock (Bleiweiss et al.,
1994; Bleiweiss,
1998
; Gerwin and Zink,
1998
). It is nonetheless clear that hummingbirds split from the
swifts, their sister taxon, some time in the early Tertiary and probably in
the Paleocene. Today's major lineages of hummingbirds all date to the Miocene
and reflect a vigorous expansion of lowland taxa into mid and high elevations
(see Bleiweiss, 1998
;
Dudley, 2001
). Adaptation to
hypobaric hypoxia has thus been an essential underpinning to hummingbird
diversification and represents a physiological feat all the more impressive
given the aerobically demanding flight behaviors, including hovering and
vertical ascent, characteristic of this taxon. Hummingbirds are found only in
the New World and, with the exception of transient hovering in sunbirds and
other flower-visiting birds (see
Westerkamp, 1990
), have no
behavioral counterpart in the Old World avifauna.
For hummingbirds, the evolution of hovering required integration of
morphological (e.g. the fusion of radial wing bones) and physiological (e.g.
elevated wingbeat frequencies, increased aerobic capacity) traits within the
ecological context of dedicated nectarivory. Nonetheless, evolutionary
pathways for the acquisition of this unique avian flight behavior remain
unclear. The eponymous swifts, for example, virtually never hover, and no
transitional forms are evident within the most basal yet adeptly hovering
hummingbird lineage, the hermits (subfamily Phaethornithinae). Miniaturization
relative to apodiform ancestors has been a predominant morphological theme of
hummingbird evolution, and upregulation of metabolic capacity necessarily
occurred in concert with a reduction in body size
(Cotton, 1996). The allometry
of flight performance among trochilid taxa is, accordingly, of substantial
physiological interest, particularly given the extremes of endothermic design
represented by the smallest hummingbirds.
Hovering, and, more generally, the ability to generate vertical forces,
represents only one component of flight performance. Other axial forces (e.g.
thrust generation during forward flight) and the torques underlying changes in
body orientation are much less studied in hummingbirds, but are equally
important components of flight performance in this extraordinary avian
lineage. Extended maneuvers and chases, for example, involve the production of
either linked or temporally decoupled rotations about orthogonal body axes,
together with the modulation of vertical forces, thrust and sideslip (see
Dudley, 2000,
2002
). On much longer time
scales, many hummingbirds engage in migratory flight across both elevational
and latititudinal gradients. Here, we emphasize current understanding of
hovering aerodynamics and energetics, but emphasize that many other aspects of
the hummingbird flight envelope probably derive from as yet unrecognized
physiological novelties.
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Mechanistic underpinnings to hummingbird flight performance |
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Miniaturization, in fact, underlies many of the physiological and
biomechanical extremes for which hummingbirds are so notorious. Increased
heart rates, high wingbeat frequencies and extraordinary mass-specific rates
of oxygen consumption are often attributed to the demands of hovering flight.
Very fast forward flight in hummingbirds, however, requires oxygen uptake at
rates substantially higher than those during hovering or at intermediate
flight speeds (Berger, 1985).
Rapid accelerations and vertical ascent also require the expenditure of
aerodynamic and metabolic power well in excess of that for normal hovering
(see Dudley, 2000
). The
morphological and biochemical specializations of hummingbird flight muscle are
well known (e.g. Suarez et al.,
1991
; Mathieu-Costello et al.,
1992
; Suarez,
1992
), but those features of the circulatory and respiratory
systems required to sustain aerobic performance are similarly impressive. In
common with other birds, trochilids exhibit an enhanced pulmonary diffusion
capacity relative to that of bats (Dubach,
1981
; Duncker and
Güntert, 1985
; Maina,
2000
). Cardiovascular performance may, however, ultimately limit
hummingbird flight energetics. Maximum cardiac output is a strong predictor of
aerobic capacity in many birds and mammals
(Bishop, 1999
), whereas the
relative heart mass of hummingbirds is substantially higher than that
predicted by allometric regressions of heart mass for all other birds (see
Hartman, 1961
;
Bishop, 1997
). Heart mass
increases isometrically in hummingbirds when phylogenetic relatedness among
species is accounted for (Table
1; Fig. 1), but the
relevant cardiac and respiratory variables are not known for hummingbirds
under conditions of either maximal hovering or fast forward flight. Given that
the muscle-mass-specific metabolic rates of flying hummingbirds represent the
highest known values for vertebrate striated muscle (Lasiewski,
1963
;
1964a
;
Epting, 1980
;
Suarez et al., 1991
), any
hypothesis that cardiovascular supply of oxygen limits overall aerobic
performance must be shown to pertain specifically to hummingbirds for general
validation.
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During hovering flight, hummingbirds exhibit approximate kinematic and
aerodynamic symmetry between the down- and upstrokes
(Weis-Fogh, 1972), although
precise data are lacking. Kinematic features such as the frequency and
amplitude of wing motions are well described for hovering, but we know little
about more detailed kinematic features that influence aerodynamic force
production. A partial list of variables includes angle of attack, pronational
and supinational velocities, the deviation of wing motions from simple
harmonic motion and the elevation of the wing relative to the stroke plane
broadly defined by wingtip motions. These static variables and the dynamic
time courses are known to influence the magnitude and direction of steady and
unsteady forces generated on flapping wings at comparable Reynolds numbers
(see Ellington et al., 1996
;
Van den Berg and Ellington,
1997a
,b
;
Dickinson et al., 1999
; Sane
and Dickinson, 2001
,
2002
). Relative to hovering
insects, hummingbirds exhibit a much stronger negative allometry of wingbeat
frequency and a correspondingly greater positive allometry of wing area
relative to body mass (Dudley,
2000
). The aerodynamic implications of these allometries are
unclear, although a reduction in wingbeat frequency may mitigate inertial
power requirements that increase in proportion to the cube of oscillation
frequency. The relative wing mass of hummingbirds substantially exceeds that
of most insects, and the overall inertial costs of wing oscillation may
therefore be substantial. Elastic energy storage of wing inertial energy may
reduce or even eliminate such costs (see Weis-Fogh,
1972
,
1973
;
Wells, 1993
), but this
possibility has yet to be demonstrated experimentally.
In addition to their obligate hovering at flowers, hummingbirds are exposed
to forces of natural and sexual selection that require forward flight, linear
accelerations, quick directional changes and evasive responses. The modulation
of aerodynamic output is best termed agility, a term that specifically refers
to changes in the speed and direction of flight
(Dudley, 2002). Axial agility
involves the capacity to accelerate in the forward, lateral and vertical
dimensions, whereas torsional agility indicates rotational accelerations about
each of the three mutually orthogonal body axes (i.e. speed of initiation of
roll, pitch and yaw). In hummingbirds, axial agility has been studied
predominantly in the context of vertical force production. Wing motions are
bilaterally symmetrical in this case, and an increase in stroke amplitude is
the predominant means of increasing total aerodynamic force output. Anatomical
limits to stroke amplitude ultimately limit force production for flight both
in hypodense gas mixtures and during maximal vertical load-lifting
(Chai and Dudley, 1995
;
Chai et al., 1997
;
Chai and Millard, 1997
).
Excess capacity in lift and power exhibited under such conditions is
presumably used in nature for the purposes of vertical ascent, climbing
flight, translational accelerations and fast forward flight. Maximal flight
performance can also be strongly context-dependent. For example, ruby-throated
hummingbirds (Archilochus colubris) engaged in vertical load-lifting
exhibit short-duration, but high-intensity, power outputs that exceed maxima
exhibited in hypodense air (Chai et al.,
1997
). Interspecific comparisons of hummingbirds also suggest a
trade-off between maximum power and flight duration
(Chai and Millard, 1997
; see
below), although phylogenetically controlled studies are lacking.
Intraspecific morphological variability among hummingbirds can also be
correlated with variation in axial agility. Transient weight reduction imposed
on individual ruby-throated hummingbirds decreases wing loading (given an
invariant wing area) and increases hovering performance in hypodense gas media
(Chai and Dudley, 1999).
Sexual dimorphism in the same species is pronounced, with the heavier females
being less capable of sustaining hovering flight
(Chai et al., 1996
;
Chai and Dudley, 1999
). In
common with other birds, molting in ruby-throated hummingbirds results in a
substantial increase in the metabolic costs of flight and a reduction in
maneuverability (see Chai,
1997
; Rayner and Swaddle,
2000
). Similar effects are presumably associated with the
extensive lipid loading exhibited by premigratory hummingbirds. The
extraordinary energetic consequences of non-stop flight in those neotropical
trochilid taxa that migrate to and from the North American continent were
modeled by Lasiewski (1964b
),
but we know little empirically about fuel use, water balance and nectaring
strategies during sustained flights. The only available estimate of mechanical
power requirements for hummingbird in forward flight
(Pennycuick, 1968
) suggests a
power curve that the parallels aforementioned metabolic requirements, namely
relatively constant power expenditure up to airspeeds of approximately 10 m
s-1, followed by a steep increase. Airspeeds during migration might
be expected to occur near this rise in the curve if energetic expenditure per
unit distance traveled is to be minimized.
Most present-day hummingbirds are mid-montane specialists, whereas
phylogenetic relationships among major trochilid lineages suggest progressive
colonization of higher elevations (see
Bleiweiss, 1998;
Dudley, 2001
;
Schuchmann, 1999
). An increase
in altitude involves parallel reductions in air density, oxygen partial
pressure and air temperature. Each of these physical features potentially
influences hummingbird flight performance. Also, mechanical power expenditure
during hovering increases with greater body mass and with decreased air
density (Ellington, 1984b
),
but heavier hummingbird species tend, somewhat paradoxically, to occur at
higher elevations (Fig. 2).
Compared with hovering under normobaric conditions, substantial excess lift
and power capacity are exhibited by hummingbirds hovering in hypobaria
(Berger,
1974a
,b
).
Concomitant increases in stroke amplitude but relative constancy in wingbeat
frequency parallel those kinematic changes seen under conditions of hypodense
challenge (Chai and Dudley,
1995
). Even when aerodynamic and energetic demands remain constant
under normodense conditions, hummingbirds display considerable resistance to
hypoxia (Chai and Dudley,
1996
). Hypobaric conditions are thus well met by hummingbirds
through a combination of substantial lift power reserves and relative
insensitivity to hypoxia, the latter extending in hovering ruby-throats to
conditions of oxygen availability equal to those found at 4000 m
(Chai and Dudley, 1996
).
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Natural hypobaria is also associated with reductions in mean air
temperature. The flight metabolic rate of hovering hummingbirds varies only
slightly with ambient temperature (Chai et
al., 1998; Berger and Hart,
1972
), but the physiological effects of convective heat loss
during forward flight, as yet unstudied, may be substantial. Variation in air
temperature may also influence maximal lift and power production. For example,
the wingbeat frequency and stroke amplitude of ruby-throated hummingbirds
engaged in maximal load-lifting vary inversely as air temperature increases,
possibly in response to thermoregulatory demand
(Chai et al., 1997
). One
pronounced physiological feature of hummingbirds that probably evolved in
parallel with the occupation of higher elevations is torpor. Daily torpor is
pronounced in montane hummingbirds and also well suits those taxa that migrate
into temperate-zone regions for survival in colder climates (see
Carpenter, 1974
;
Hiebert, 1993
;
Calder, 1994
;
Bicudo, 1996
). Phylogenetic
variation in hummingbird hypometabolism has not been systematically studied,
and the phylogenetically basal and generally lowland phaethornithines would be
particularly interesting in this regard. We finally note that hyperoxia fails
to enhance maximal hovering ability (Chai
et al., 1996
; Altshuler et al.,
2001
), a finding consistent with the convective (and particularly
cardiovascular) limits on metabolic capacity mentioned above.
Forward flight requires the generation of thrust to overcome body drag in
addition to the body weight support that characterizes hovering. Particularly
at higher airspeeds, some mitigation of vertical force production may be
attained via lift generation on the body. Modulation of forward
thrust derives primarily from the reorientation of an otherwise vertically
directed aerodynamic force vector. In hummingbirds, as in other flying
animals, variable partitioning of this output vector between vertical and
horizontal components is correlated with changes in body pitching moments,
which may derive from torques generated actively by the wing and passively by
the body (see Greenewalt,
1960; Dudley,
2000
). During forward flight, wing flapping velocities are
augmented by the translational airspeed, an effect that substantially
mitigates aerodynamic demand. For example, ruby-throated hummingbirds in fast
forward flight exhibit stroke amplitudes well below limiting values
characteristic of hovering flight
(Greenewalt, 1960
). In wind
tunnels, the maximum airspeeds of hummingbirds range from 13 to 15 m
s-1 (Greenewalt,
1960
; Berger, 1985
;
Chai and Dudley, 1999
;
Chai et al., 1999
). Maximum
forward flight speeds do not differ substantially either between the genders
of ruby-throated hummingbirds or between molting and non-molting individuals
(Chai et al., 1999
;
Chai and Dudley, 1999
). For
obvious logistical reasons, little is know about the forward flight of
hummingbirds in nature. Groundspeed measurements of hummingbirds commuting
between flowers or escaping from experimenters suggest flight speeds of
between 5 and 11 m s-1
(Pearson, 1961
;
Gill, 1985
), whereas
short-distance flights between flowers occur at speeds no greater than 1.2 m
s-1 (Wolf et al.,
1976
). By contrast, display dives using gravitational accleration
may exceed 20 m s-1 (see
Stiles, 1982
;
Tamm et al., 1989
).
Changes in the body roll, pitch and yaw of flying hummingbirds derive from
aerodynamic and inertial torques applied about the body axis in question; the
rapidity of body rotation is termed torsional agility. Alteration of body
pitch can derive from bilaterally symmetrical changes in a variety of wingbeat
kinematic features or from dorsoventral tail motions
(Dudley, 2002). Bilaterally
asymmetric motions of the wings, the tail or the body itself yield the
rotational moments underlying body roll and yaw. Although famously
maneuverable, hummingbirds have never been the subject of relevant
three-dimensional studies. Both the magnitude of applied aerodynamic torque
and the moment of inertia about the rotational axis in question influence
instantaneous rotational acceleration. The wings of volant vertebrates
represent substantial contributions to body rotational inertia
(Thollesson and Norberg, 1991
;
Van den Berg and Rayner, 1995
;
Dudley, 2002
), and
instantaneous wing position may therefore affect the inertial responsiveness
of the wing/body system. The often greatly exaggerated tails of many
hummingbirds may impose a similar inertial constraint on rotational
acclerations. Although remarkably diverse in morphology and size, the
potential aerodynamic roles of hummingbird tails have never been investigated,
but contributions to roll, pitch and yaw are all likely possibilities.
Unsteady forces on the tail, as well as aeroelastic twisting of individual
tail feathers, may also enhance force and moment production during maneuvers
(see Norberg, 1994
).
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Ecological implications |
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Accurate calculation of induced power requirements requires knowledge of
the region in space through which the wings beat and apply a downward pressure
impulse (Ellington, 1984a).
The average pressure thus applied to the surrounding air is indicated by the
aerodynamic parameter of disc loading, the ratio of the body weight
(mg, where m is mass and g is gravitational
accleration) to the disc area swept by the wings A and across which
body weight is supported. Disc loading varies in inverse proportion to the
wing length R, but must also incorporate effects of variation in the
stroke plane angle ß and the stroke amplitude
. During hovering
flight, disc loading is given by
mg/
R2cosß, where
is given in
radians (see Ellington,
1984a
). Induced power costs are directly proportional to the
square root of disc loading, but also vary in inverse proportion to the square
root of air density (Ellington,
1984b
; Norberg,
1990
).
Specifically with reference to hovering hummingbirds, Epting and Casey
(1973) defined wing disc
loading as the ratio of mg to A, but estimated A as
(b/2)2, where b is the wing span (i.e. the
distance between the outstretched wing tips;
Norberg, 1990
). Subsequent
estimates of wing disc loading for hummingbirds estimated b using the
more easily measured chord distance from the wrist joint to the wingtip
(Carpenter et al., 1993
;
Feinsinger and Chaplin, 1975
;
Feinsinger and Colwell, 1978
;
Feinsinger et al., 1979
;
Kodric-Brown and Brown, 1978
).
Note that, in these and other ornithological studies, this distance is termed
the `wing chord', whereas aerodynamic usage designates the wing chord as
orthogonal to such radial measures. In any case, the estimated relationship
between wrist joint to wingtip distance and wing span (see Greenewalt,
1960
,
1975
) contains considerable
scatter in part because wing proportions vary among species.
Relative to contemporary understanding of hovering mechanics, estimates of
hummingbird disc loading contain many assumptions potentially subject to
error. Particularly noteworthy are (i) that wing length equals half the wing
span, and (ii) that stroke amplitude equals 180°. Both these assumptions
will tend to overestimate disc loading and thus systematically to
underestimate induced power expenditure. Nonetheless, mass-specific metabolic
power input during hovering is correlated with this estimate of disc loading
in a comparison of seven hummingbird species
(Epting, 1980).
A variety of studies have sought to associate Epting and Casey's
(1973) estimate of hummingbird
disc loading with competitive ability
(Feinsinger and Chaplin, 1975
;
Feinsinger and Colwell, 1978
;
Kodric-Brown and Brown, 1978
;
Kuban and Neill, 1980
). In the
sexually dimorphic species examined so far, male dominance is correlated with
greater disc loading in males (Carpenter
et al., 1993
). It is worth noting, however, that the North
American species (mostly rufous hummingbirds, Selasphorus rufus) tend
to be smaller and show reversed sexual dimorphism compared with the majority
of larger hummingbirds (see Colwell,
2000
). In addition, the wingtips of males in the genus
Selasphorus are modified for sound production, which tends to reduce
wing length and to yield higher wing disc loading. One notable exception to
this trend is in broad-tailed hummingbirds (S. platycercus), in which
the outer primary is slightly lengthened and attenuated. The effects of sexual
dimorphism in body mass and wing area on competitive behavior have not been
examined across the full range of body sizes in hummingbirds. Gender-specific
evaluation of the aerodynamic and metabolic costs of flight is clearly
required if biomechanical underpinnings to behavior are to be inferred.
Estimates of disc loading have also been broadly correlated with
hummingbird foraging strategies, species being categorized either as
territorial and defending floral aggregations or as trapliners that forage
among dispersed flowers and that do not engage in resource defense.
Territorial hummingbirds were predicted to have high values of wing disc
loading because effective aerial defense was presumed to require shorter wings
and greater aerial maneuverability. In contrast, the wing disc loading of
trapliners was predicted to be lower than that of territorial hummingbirds
(Feinsinger and Chaplin,
1975). Using data from the cloudforests of Monteverde, Costa Rica,
and the eastern Rockies of Colorado, Feinsinger and Chaplin
(1975
) found support for the
prediction that territorialists had higher wing loading than trapliners,
although their data did not control for the effects of phylogeny or
elevation.
Further associations between disc loading and hummingbird ecology were
proposed by Feinsinger and Colwell
(1978), who observed trochilid
species from the Caribbean and Central and South America. From these
observations, they proposed six foraging guilds, each defined by body size,
bill length, foot size and wing disc loading. The aforementioned hummingbirds
from Monteverde were recategorized into these six foraging guilds, and data
for competitive interactions between two species from the Lesser Antilles were
presented in support of this hypothesis. However, evidence from other authors
indicates that the division among guilds may be less clear, with one notable
example being the competitive interactions between a `high-reward' trapliner,
the long-tailed hermit (Phaethornis superciliosus), and hummingbirds
from other `guilds' (Stiles and Wolf,
1979
).
How tightly do qualitative categorizations of foraging strategy correspond
to quantitative features of flight physiology? Thus far, the relationship
between competitive ability and flight-related morphology has been addressed
through analyses of relatively small species assemblages in North America and
on Caribbean islands (Kodric-Brown and
Brown, 1978; Kodric-Brown et
al., 1984
). Competitively dominant hummingbird species exhibit
higher wing disc loadings (sensu
Epting and Casey, 1973
), but
are also heavier, thereby precluding causal association of competitive ability
and the relative magnitude of induced power expenditure. Existing
interspecific comparisons of hummingbird competitive ability are also
confounded by potentially non-random phylogenetic relatedness among the
species in question. More generally, flight performance during competitive
interactions probably derives from a variety of behaviors supplemental to
hovering. Differing components of both axial and torsional agility can
potentially influence the outcome of aerial interactions (Dudley,
2000
,
2002
), and a comparison of
wing disc loading alone captures but a limited subset of the relevant flight
mechanics. Context-specificity may also be critical to the interpretation of
behavioral dominance. Other factors that potentially influence the foraging
strategies of most species included (i) age, (ii) gender, (iii) the abundance
and distribution of resources, (iv) the presence and relative dominance of
competitors, and even (v) the time of day
(Wolf et al., 1976
;
Feinsinger and Colwell, 1978
;
Feinsinger et al., 1979
;
Pimm et al., 1985
;
Sandlin, 2000
). In addition,
foraging strategies may vary latitudinally. Selasphorus rufus, for
example, is a dominant territorialist during breeding in North America, but is
mostly a subordinate, non-territorial species on its wintering grounds.
Experimental tests of the influence of hummingbird flight morphology on
competitive outcomes have relied upon manipulations of feeder density. In
staged encounters between heterospecific hummingbird pairs, a larger species
maintained positive energy balance whereas a smaller competitor species always
lost mass (Tiebout, 1993).
However, the smaller species was able to the feed more often when the feeders
were more dispersed (Tiebout,
1992
).
Most ecomorphological studies of hummingbirds have examined links between
characters thought to influence flight performance and foraging for flower
nectar or feeder solutions. The consumption of arthropods by hummingbirds has
largely been ignored in these considerations despite the prevalence of
arthropods in the diet of many hummingbirds
(Remsen et al., 1986). One
exception is an analysis of arthropod feeding flight behavior of the
hummingbirds of La Selva, Costa Rica
(Stiles, 1995
). Four types of
insect feeding flight behavior were described, and the tactics used for
arthropod foraging were constant across habitats and seasons, whereas the
tactics of nectar-foraging varied systematically. In addition, several wing
variables (including wing disc loading and aspect ratio) correlated much more
closely with arthropod-foraging than with nectar-foraging tactics. From these
results, Stiles (1995
)
proposed an alternative hypothesis, namely that the primary direct selective
force on wing morphology has been arthropod-foraging, whereas selection
via nectar-foraging may have been indirectly imposed via
constraints on arthropod-foraging imposed by bill morphology. In any case, it
appears likely that arthropod-foraging, as well as other behaviors such as
predator avoidance and mating displays, must have influenced the evolution of
hummingbird flight performance and related morphology.
Several lines of evidence suggest that hummingbirds actively regulate body
mass and that such variation influences flight behavior. During the breeding
season, male ruby-throated hummingbirds maintain a low body mass, but they
gain weight following the cessation of reproductive activity
(Mulvihill et al., 1992).
Daily measurements of the mass of breeding broad-tailed hummingbirds indicate
that males actively regulate low body mass during the day and then engorge
themselves immediately before sunset
(Calder et al., 1990
).
The influence of wing morphology and body mass on flight performance has
also been investigated within sexually dimorphic species. As part of their
larger studies of montane hummingbirds, Feinsinger and colleagues
(Feinsinger and Chaplin, 1975;
Feinsinger and Colwell, 1978
)
made guild classifications for seven species in which the sexes differed in
body mass and/or wing disc loading. The males and females of two of these
species, purple-throated mountain-gems (Lampornis calolaema) and
broad-tailed hummingbirds, were classified in different guilds. In both cases,
males were heavier, had higher wing loadings and were placed in a more
competitive guild (i.e. territorialist or facultative trapliner, respectively)
compared with females (classified as generalists and trapliners,
respectively). Male violet sabrewings (Campylopterus hemileucurus)
were also substantially heavier and had higher wing disc loadings than
females, but both were classified as generalists. Two of the remaining species
had heavier males but equivalent values for wing disc loading, and both sexes
were classified in the same guild. The final two species exhibited slight
differences between the sexes, but the sexes were again classified into the
same guild. Addressing this question further will require a more refined
measurement of competitive ability (sensu
Pimm et al., 1985
;
Sandlin, 2000
) and a much
broader sample of species than is presently available.
Mechanistically, the implications of variable body mass for flight
performance and indirectly for competitive ability are unclear. Calder et al.
(1990) predicted that reduced
body mass would facilitate acceleration for courtship displays and aerial
encounters with competitors (see also
Dudley, 2002
). In
ruby-throated hummingbirds, maximum flight speeds, both among individuals and
for the same individual in differing molt condition, are unchanged in spite of
changes in body mass of up to 27% (Chai et
al., 1999
; Chai and Dudley,
1999
). Neither translational nor rotational accelerations have
been determined, however, for any hummingbird species. Moreover, rufous
hummingbirds vigorously maintain territories while concurrently increasing
body mass by up to 33% (Carpenter et al.,
1983
). The potential influences of body mass on competitive
ability and foraging behavior are multifarious in nature and, to date, have
not been causally associated with effects on flight performance per
se.
Hummingbird body mass appears to undergo substantial variation during
migration. Carpenter et al.
(1983) created perches on
scales to measure instantaneous mass in rufous hummingbirds during their
migratory stopover. These highly territorial birds adjusted territory size to
gain mass as quickly as possible during stopovers and departed after reaching
a body mass threshold (Carpenter et al.,
1983
). Resident Costa's hummingbirds (Calypte costae) at
the same site maintain a relatively steady moderate body mass and adopt a
strategy that minimizes foraging time
(Hixon and Carpenter, 1988
).
Some populations of ruby-throated hummingbirds cross the Gulf of Mexico for
the spring migration. Before departing, these birds often double their mass
(Robinson et al., 1996
) and
thus fly with extra weight relative to non-migratory periods. In these
examples, the fattened hummingbirds engage primarily in forward flight during
migration, and maximum forward velocity is probably unaffected by changes in
body mass (see Chai et al.,
1999
). Actual flight speeds during migration are unknown for any
hummingbird.
In summary, our understanding of the ecological implications of intra- and
interspecific variation in hummingbird morphology and flight performance is at
a rudimentary stage. Most measures of hummingbird competitive ability and
foraging behavior have relied upon qualitative assessments. A quantitative
method for assessing competitive ability has been introduced by Pimm et al.
(1985), in which species
dominance is assessed through observations of feeding activity at
microhabitats that differ in quality. A high-quality site with a feeder of
high-concentration sucrose solution is defended by the most aggressive birds,
whereas feeders with low-concentration sucrose solutions are used by
subordinate individuals. A comparison of the time spent feeding at the
preferred habitat with overall time spent at the feeder thus provides a
numerical index of competitive ability that can be compared with other
variables such as population densities. These methods have also been used to
assess the influence of learning on behavior
(Mitchell, 1989
;
Sandlin, 2000
). Applying the
methods of Pimm et al. (1985
)
to several species complexes and combining behavioral data with morphological
and biomechanical variables may greatly enhance our ecological understanding
of hummingbird flight performance. An important caveat is that behavioral
studies in artificial settings (i.e. feeders in the field or in laboratory
contexts) may not adequately capture natural foraging performance.
![]() |
Elevational variation in flight performance |
---|
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---|
Comparisons in a phylogenetic context will also be necessary to determine
why hummingbird species might have diversified under environmental conditions
that exacerbate the costs of flight in general and, specifically, of hovering.
A historical perspective may also aid in our understanding of how hummingbirds
expanded into high-elevation niches and whether such an invasion was a unique
event or one of several radiations
(Bleiweiss, 1998). The largest
phylogeny currently available for trochilids contains 73 taxa, including many
high-elevation species (J. A. McGuire and D. L. Altshuler, unpublished data).
Consideration of the elevational ranges of the taxa included in this analysis
suggests that hummingbirds may have evolved at mid elevations and subsequently
invaded both low and high elevations in several lineages
(Fig. 3). An alternative
explanation is that hummingbirds originated in moist, lowland forests and
subsequently invaded mid- and high-elevation habitats (see
Bleiweiss, 1998
;
Dudley, 2001
).
|
Allometric considerations potentially confound the interpretation of
elevational effects on hovering performance and body size evolution of
hummingbirds. Larger body size presents a double mechanical/metabolic
challenge to hovering flight in that the mass-specific induced power
requirements increase with (body mass)1.17
(Norberg, 1995), whereas the
maximum aerobic capacity of volant animals tends to scale negatively with body
mass (Bishop, 1997
;
Norberg, 1990
). Flight is thus
relatively more costly and metabolically challenging for heavier animals.
Somewhat surprisingly, then, mean body mass among over 325 described
hummingbird species increases significantly at higher elevations, whereas
species diversity decreases (Fig.
2). One possible evolutionary response to the increased relative
cost of flight with body mass is a positive allometry in the flight muscle
mass of hummingbirds (Table 1;
Fig. 4). Also, greater body
mass at higher elevations probably enhances thermoregulatory ability, storage
capacity and feeding rate, the last variable being an important determinant of
the outcome of competitive interactions
(Wolf and Gill, 1986
). Our
analysis of Peruvian hummingbirds from the eastern slopes of the Andes
indicates that hummingbirds above 3000 m have a greater mean body mass [8.3 g;
N=7 species; mean of 6.0 g excluding the giant hummingbird
(Patagona gigas)] relative to species below this elevation (5.4 g;
N=32 species; D. L. Altshuler and R. Dudley, unpublished data). Most
revealingly, the giant hummingbird weighs over 20 g but occurs not in the
lowlands but rather at mid and high elevations (see also
Schuchmann, 1999
). What
biomechanical and physiological adaptations are characteristic of
high-elevation hummingbirds?
|
Feinsinger et al. (1979)
predicted that wing disc loading of hummingbirds (sensu
Epting and Casey, 1973
) would
decrease with increasing elevation if hovering costs and competitive ability
were positively linked and if other selective forces on body size and wing
length were relatively unimportant. For 38 hummingbird species in southeast
Peru, Feinsinger et al. (1979
)
determined an inverse relationship between wing disc loading and the midpoint
of elevational range. Feinsinger et al.
(1979
) also calculated that
induced power expenditure during hovering was independent of elevation, a
surprising result given the dependence of this variable on the square root of
air density.
We have expanded upon the work of Feinsinger and Colwell and their
collaborators by investigating the load-lifting performance of hummingbirds
along the eastern slopes of the Peruvian Andes. Hummingbirds were filmed
during free hovering flight and also when hovering with maximum weight imposed
via an asymptotically increasing load-lifting assay (see
Chai et al., 1997;
Chai and Millard, 1997
). We
currently have data from 43 species spanning an elevation gradient from 400 to
4300 m, and we are using the aforementioned phylogeny to aid in the
interpretation of the results. A comparison of wing loading and mean elevation
for a species' range using phylogenetically independent contrasts has revealed
a significantly negative relationship between these variables
(Fig. 5), in agreement with the
results of Feinsinger et al.
(1979
). Estimated power output
was also found to be unrelated to changes in elevation for both normal
hovering and hovering during maximal load-lifting, further supporting earlier
findings. However, a comparison of power requirements during free flight with
the maximum power produced during load-lifting revealed that the power margin
(the ratio of maximum power produced during load-lifting to the power required
during free hovering) decreased significantly with increasing elevation. Thus,
high-elevation hummingbirds are operating with a narrow capacity for flight
during competitive or other behaviors that require burst activity.
|
In addition to the flight costs imposed by low air pressure, flight
metabolic rate is affected by the decreased ambient temperature at high
elevations. As air temperature decreases, resting hummingbirds increase their
metabolic rate, heart rate and breathing rate (Lasiewski,
1963,
1964a
;
Lasiewski et al., 1967
).
Hummingbirds can compensate for these increased physiological costs by falling
into torpor and drastically reducing metabolic functions
(Carpenter, 1974
;
Hainsworth and Wolf, 1970
;
Lasiewski, 1963
;
Wolf and Hainsworth, 1972
).
Changes in wingbeat kinematics during hovering at low ambient temperatures are
apparently associated with decreased muscle efficiency and thus increased heat
production (see Berger and Hart,
1972
; Chai et al.,
1998
).
Little is known about the flight performance of hummingbirds at high
elevations. Although wingbeat kinematics and mechanical power output have been
the subject of numerous laboratory manipulations in low-density and
low-temperature air (Chai et al.,
1996,
1998
,
1999
; Chai and Dudley,
1995
,
1996
;
Dudley and Chai, 1996
;
Altshuler et al., 2001
), no
study has yet to incorporate the full variety of environmental features
characteristic of high elevation to assess whole-animal flight capacity.
Interesting areas of research will include measurements of wingbeat kinematics
and power margins at high elevations to determine how hummingbirds compensate
for the increased costs of flight. In addition, it has been suggested that
hummingbirds at high elevations often perch or land on the ground to feed. It
would be worthwhile to obtain time budgets for flight behaviors across
elevations to determine whether hummingbirds adjust their flight modalities
accordingly. Casual observations of large species in the high Andes also
suggest that these taxa may use bounding and undulating flight, in contrast to
low-elevation taxa, which engage in continuous flapping flight.
![]() |
Directions for future research |
---|
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---|
Adaptation to montane conditions has been a major feature of hummingbird evolution, yet most information about hummingbird flight derives, for anthropogenic reasons, from studies within laboratories at or near sea level. Parallel reductions in air density, oxygen partial pressure and air temperature represent important abiotic challenges that can be decoupled in laboratory contexts, but that also may be correlated with biotic features of the environment and that influence flight behavior. For example, are there systematic changes with elevation in the quantity and composition of floral rewards obtained by hummingbirds? Are hovering duration and territoriality adjusted accordingly? Can variable floral geometry influence wingbeat kinematics and associated power expenditure? Does specificity of co-evolutionary mutualism between hummingbirds and flowers vary across elevational gradients? Does latitudinal migration in a minority of trochilid taxa derive evolutionarily from the capacity to engage in altitudinal migration? Seasonal movements up and down mountains are well-known in many South American hummingbird taxa and present an excellent opportunity to assess behavioral and biomechanical responses to natural hypobaria.
Finally, we wish to draw attention to the other, lesser known lineage of
hovering vertebrates. Glossophagine phyllostomids, also known as flower bats,
are important neotropical pollinators that regularly engage in hovering,
albeit for relatively short periods
(Winter and von Helversen,
2001). The 32 described glossophagine species range in mass from 7
to 32 g and thus easily exceed in body size the largest hummingbirds (see von
Helverson, 1993). In bats generally, the anatomical connection of the wings to
the hindlegs yields a relative increase in wing surface area, but also limits
rotational capacity about the longitudinal wing axis. The kinematic symmetry
between down- and upstrokes characteristic of hovering hummingbirds is thereby
precluded, yet glossophagines nectaring at flowers are remarkably stationary.
Instead of half-stroke symmetry, glossophagines rotate only the distal regions
of the wing during the upstroke (von
Helversen, 1986
), but apparently use faster tip velocities to
generate the requisite weight support. Also, the much lower wing loadings of
glossophagines relative to hummingbirds yield substantially lower
mass-specific costs of hovering mediated via a reduction in induced
power requirements (see Winter,
1998
; Voigt and Winter,
1999
).
Hovering is extremely rare among volant vertebrates, yet size limits to hovering performance, be they aerodynamic or energetic in character, remain poorly understood. Why is sustained hovering of such restricted taxonomic occurrence, and why did it evolve only in the New World? How exactly did hummingbirds evolve from a fast-flying, swift-like ancestor? Armed with a well-resolved phylogeny and the apparatus of modern flight biomechanics, students of hummingbird biology are now well equipped to answer these interesting questions.
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Acknowledgments |
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