|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online August 9, 2007
Journal of Experimental Biology 210, 2851-2858 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001230
Differences in metabolic costs of terrestrial mobility in two closely related species of albatross
1 Centre for Ornithology, School of Biosciences, University of Birmingham,
Edgbaston, Birmingham B15 2TT, UK
2 British Antarctic Survey, Natural Environment Research Council, High
Cross, Madingley Road, Cambridge CB3 0ET, UK
* Author for correspondence (e-mail: Alexander.kabat{at}gmail.com)
Accepted 14 May 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
O2).
Conversely, T. melanophrys were able to move up a significantly
steeper incline than T. chrysostoma while maintaining a similar
maximal O2. Each
species demonstrates stride length, force production (behavioural) and leg
length (morphological) adaptations that minimise the cost of traversing their
chosen colonies, indicating a clear relationship between terrestrial
performance and local topography. However, it is not possible to determine if
the difference in locomotory ability results from differences in colony
topography, or if choice of colony site is dictated by the ability of the
species to traverse different terrain.
Key words: Thalassarche melanophrys, Thalassarche chrysostoma, cost of locomotion, metabolic rate, procellariiform, energetics, gait analysis
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
; Prince et al.,
1994). Breeding site fidelity is high for both species, with
movements of established breeders between adjacent colonies, even those
separated by a few hundred metres, being rare
(Prince et al., 1994). Both
species nest on mounds of soil and vegetation, with BBA tending to favour
steeper slopes than GHA (Tickell and
Pinder, 1975). Although BBA will sometimes nest alongside GHA in
relatively flat colonies, it is atypical to find GHA in the steeper colonies
inhabited by BBA (Carboneras,
1992), thus suggesting one or more factors limit where GHA
nest. Once birds have taken flight, they can clear the topography of the land making the metabolic cost of movement independent of slope, terrain and other terrestrial obstacles. However, when on land albatrosses must cope with variations in topography, which may induce varying metabolic costs. In addition, many birds must walk or run in order to become airborne. Relative colony slope may have an important influence on nest site selection and, given the high degree of nest site fidelity, it could be hypothesized that BBA possess greater locomotory efficiency during locomotion up an incline compared to GHA. Conversely, it could be hypothesized that GHA are better adapted for level terrestrial locomotion, thus minimizing metabolic costs compared to BBA.
In most animals, the rate of oxygen consumption
(O2) is a linear
function of speed during terrestrial locomotion in a horizontal plane (e.g.
Schmidt-Nielsen, 1972;
Taylor, 1985;
Taylor, 1994;
Taylor et al., 1982;
Butler, 1991). The extrapolated
y-intercept of this line is often higher than the
O2 measured when
the animal is naturally at rest (Taylor et
al., 1970). The difference between the y-intercept and
resting O2 has
been termed the `postural' effect
(Schmidt-Nielsen, 1972),
suggesting that it represents the energetic cost of maintaining the body in a
locomotory posture.
The total metabolic cost of locomotion can be calculated as the sum of
maintenance metabolic costs (equal to resting
O2), postural
costs, and the cost of moving an animal's mass for a particular duration and
distance. These costs are increased when the animal is moving on an incline,
as the force of gravity is acting against the mass of the animal as it moves
upwards. Net mechanical efficiency on an incline is defined as the work done
against gravity divided by the additional metabolic energy expended to
accomplish this work. As efficient locomotion could be vital for maintaining
an animal in a positive energy balance, maximising mechanical efficiency can
be a substantial evolutionary pressure.
Interspecific comparisons across a range of animal sizes suggest that the
mass-specific volume of muscle fibres activated to support body mass during
locomotion is independent of body size
(Taylor et al., 1980;
Biewener, 1989;
Kram and Taylor, 1990). It has
also been suggested that there is a relationship between rate of metabolic
energy expenditure and the rate of muscular force generation. The rate of
force generation shows a linear relationship with running speed in both birds
and mammals (Roberts et al.,
1998; Kram and Taylor,
1990). Thus, the rate of energy expenditure during locomotion can
be predicted by knowing an animal's body mass (proportional to the volume of
active muscle used to generate force against the ground) and the
foot–ground contact duration (tc), which is
inversely proportional to the rate of force generation
(1/tc) (Kram and
Taylor, 1990; Roberts et al.,
1998). By using this approach, the rate of energy expenditure
during locomotion can be predicted without including any major complexities of
muscle physiology (Kram and Taylor,
1990).
The present study investigated the metabolic cost, mechanical efficiency on an incline and gait characteristics of terrestrial walking in BBA and GHA in order to determine: (1) if there are any differences in terrestrial locomotory ability and (2) what behavioural or physiological adaptations might account for any observed differences.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Animal handling
The study was carried out on 11 black-browed albatross Thalassarche
melanophrys Nunn 1998 and five grey-headed albatross T.
chrysostoma Brooke 2004 from two colonies on Bird Island, South Georgia
(54°00'S, 38°03'W), in January of the 2005/2006 austral
summer. In order to minimise potential impacts, only non-breeders of either
sex were tested. These birds were mainly failed breeders or GHA in their
`sabbatical' year (Ryan et al.,
2007). The nests that the birds were defending at the time of
capture were used for the collection of topographical data (as below). It was
not possible to obtain higher numbers of GHA, as this species spends little
time at the colony during their `sabbatical' year or following reproductive
failure.
Nest site topography
The slope (
) of the adjacent 1.0 m of ground surrounding each nest
(Fig. 1A) was measured with a
protractor (to 0.5°) in degrees from the horizontal
(Fig. 1B,C), as determined by a
spirit level. The angle facing directly down the slope was defined as the
0° position and the 90°, 180° and 270° measurements were taken
in a clockwise pattern from this position
(Fig. 1B). The mean of
each nest was defined as the `mean nest ' and is the mean of the
absolutes of all angles (Fig.
1B). However, as it is likely that the bird will try to use the
`path of least resistance', the least steep slope for each nest was extracted
(hereafter called the `minimum approach ').
|
O2) of the 11
BBA and five GHA were measured both at rest and during treadmill exercise
using standard open-flow respirometry
(Bevan et al., 1994;
Withers, 2001). A 246 l clear
PerspexTM respirometer enclosed the bird while on a variable-gradient,
variable-speed treadmill (model EG10, Powerjog Sports Engineering Ltd,
Birmingham, West Midlands, UK). The respirometer was placed securely on a
wooden frame that was permanently attached to the treadmill and rubber seals
ensured an airtight fit between the respirometer and the frame. Brush-style
draught excluders ensured a good seal between the wooden frame and the
treadmill belt. Adequate gas mixing within the chamber was assured by the
inclusion of two 12x12 cm, 12 V fans. Three B105 Charles Austen air
pumps (Byfleet, Surrey, UK) pumped ambient air through the chamber at 110 l
min–1, measured using an electronic flow meter (100 Flo-Sen,
McMillan Co., Georgetown, TX, USA), which was calibrated at the beginning,
middle and end of the experiment using a 150 l min–1
mechanical flow meter (KDG, 2000, KDG Instruments, Crawley, Sussex, UK).
Relative humidity, barometric pressure and temperature were recorded using a
Honeywell HIH-3610 sensor (Farnell, UK). Water vapour was mathematically
scrubbed by numerical integration of the product of the gas flow and fractions
of partial pressures (see Fellows and
Macdonald, 1985) to provide a flow rate corrected to standard
temperature (273 K) and pressure (101.3 kPa) dry (STPD). The chamber
temperature was maintained between 12 and 14°C. A sub-sample of excurrent
air was drawn off downstream of the respirometer and passed through a column
of self-indicating DrieriteTM (Hammond Drierite Co., Xenia, OH, USA) and
scrubbed for carbon dioxide before being sent to a Servomex 570A O2
analyser (Crowborough, East Sussex, UK). The system was calibrated with gas
mixtures of atmospheric air and nitrogen
(Fedak et al., 1981)
controlled by a Wösthoff gas mixing pump (2M301/a-F, Bochum, Germany).
Nitrogen dilution tests (Fedak et al.,
1981) showed that the accuracy of the system was within 2%, and
the 99% wash-out time was calculated to be 10.4 min using the formula
described by Lasiewski et al. (Lasiewski
et al., 1966).
The output signals from the O2 analyser, humidity and temperature sensors, and barometer were passed to a purpose-built interface box that amplified the signals to a standard range of –10 V to +10 V. The amplified output voltages were passed to a laptop computer (Dell LT316) fitted with a digital signal acquisition PCMCIA card (DAQCard-500 National Instruments, Newbury, UK). The computer sampled outputs at 1000 Hz, took a running mean and saved these values every 3 s throughout the experiment via a program developed using LabView v5.11 (National Instruments, Austin, TX, USA). Partial pressures of ambient O2 were recorded for 3 min every 20 min, as an automated baseline check via a solenoid valve (SMC EVT307, Radio Spares, Corby, UK) controlled by the interface box and LabView software. Rate of oxygen consumption was calculated as ml min–1 STPD for each animal.
Resting rates of oxygen consumption
Resting O2
was measured from birds sitting quietly within the darkened respirometer while
on the treadmill prior to each exercise session. Standing-at-rest
O2 was recorded
for a minimum of 15 min or until a stable baseline was achieved. Birds of
either species would consistently stand whenever the researchers approached
and remained standing and alert if the researchers were within visual range.
Previous studies have shown that although psychological stressors may cause an
increase in heart rate, they are unlikely to result in a measurable difference
in metabolic rate (Blix et al.,
1974) and thus this is a suitable measure of standing-at-rest
O2.
Exercise protocol
One to two training sessions were conducted at least 24 h prior to
experimentation. Training consisted of placing a bird within the experimental
chamber and walking it at 0.1–0.2 km h–1 for 5–15
min depending on its willingness and ability to adapt to the treadmill. For
experimental testing, birds were placed in the respirometer at least 4 h prior
to the beginning of experimentation to allow acclimation. To determine maximum
speed and rate of oxygen consumption at maximal speed
(O2max.speed),
birds were randomly exercised at seven speeds (0.2–1.27 km
h–1). Each trial began with a 2–3 min warm-up at
0.1–0.2 km h–1. Thereafter, the speed was increased in
0.2 km h–1 increments every 2 min until the designated test
speed was reached. Not all birds would walk at the higher speeds. Each
experimental speed was maintained for a sufficient length of time to enable
acclimation of the animal and equilibration of oxygen levels (minimum 20 min).
A 5 min mean of the rate of oxygen consumption recorded during the prescribed
experimental speed was used as the recorded
O2 for that
trial. At sub-maximal speeds, animals were required to perform for a minimum
of 45 min (including warm up). Experiments were terminated when an animal
could not sustain the prescribed speed or would not walk consistently. At the
completion of an exercise trial, the bird was allowed to recover while
remaining within the respirometer until its
O2 returned to
its resting level, at which point the bird was given at least an additional 30
min recovery time before the next exercise trial commenced.
The speed used in the incline experiments was the minimum speed at which
all animals could sustain horizontal exercise for at least 25 min. At this
speed (0.6 km h–1 and hereafter called the `cruising' speed),
O2 was
40–60% of the maximum recorded. This speed was chosen in order to induce
a large increase in metabolic rate within the birds' aerobic scope
(Ellerby et al., 2003), and at
a speed that is above their walk–run transition speed
(Gatesy, 1991;
Gatesy, 1999). The
walk–run transition speed was defined as the speed at which the body
posture of the albatross changes, with the head, neck and torso becoming more
parallel to the horizontal plane (regardless of treadmill angle). Animals were
exercised at six different inclines (2–12%) in random order at the
cruising speed in order to determine maximum incline and rate of oxygen
consumption at maximal incline
(O2max.incline).
Each trial began with a 2–3 min warm up at 0.1–0.2 km
h–1 at 0% incline and the speed was then increased to 0.6 km
h–1 for an additional 2 min. At the completion of this
warm-up, the incline was increased in 2% increments every 2 min until the
designated test incline was reached. Each experiment was maintained for a
sufficient length of time to enable acclimation of the animal and
equilibration of oxygen levels (minimum 25 min). Longer acclimation and
sampling times were required during the incline experiments, as both species
took longer to settle into a rhythmic walking pattern. A 10 min mean of the
oxygen consumption rate recorded during the prescribed experimental incline
was used as the recorded
O2 for that
trial. At the completion of the exercise, trial birds were allowed to recover
as above.
Mechanical work efficiency
Vertical mechanical work was calculated using the formula corrected for the
angle of the treadmill:
 | (1) |
is the percentage
treadmill incline (as displayed by the treadmill), M is mass in kg,
g is the force of gravity, and U is velocity. The
factor sin[arctan(/100)] is the conversion factor from percentage incline
to degrees incline of the treadmill. The net vertical efficiency (NVE) was
then calculated as the vertical mechanical work rate divided by the vertical
metabolic power (incline metabolic rate – speed-matched level metabolic
rate) multiplied by 100 (Full and Tullis,
1990) using the formula:
 | (2) |
O2incline
is the rate of oxygen consumption during treadmill exercise at 0.6 km
h–1 and at the prescribed incline and
O2cruising is
the rate of oxygen consumption during treadmill exercise at the cruising speed
of 0.6 km h–1 at 0% incline.
Video recording
Recordings were taken of each species while walking on the treadmill during
both the speed and incline exercise trials using a Sony colour digital video
camera (model DCV-HC40E) at 60 interlaced frames s–1. File
footage was downloaded into a Toshiba Tectra laptop computer for
frame-by-frame analysis using Adobe Premiere 6.5 software. The position of the
wooden frame used to secure the respirometer to the treadmill made it
impossible to have a parallel view of the bird's feet, thus the camera
position was elevated to 30° but remained perpendicular to the animal. Ten
strides per speed per trial for each bird were analysed and stride length
(Ls), and foot contact time (tc) were
determined from recorded trials. The inverse of foot–ground contact time
was used to evaluate the rate of force generation as a predictor of
differences in metabolic rate across speed in these two species
(Kram and Taylor, 1990;
Roberts et al., 1998).
To obtain morphological measurements, birds were anaesthetised using 3% isoflurane with O2-enriched air. Leg length (Ll) was measured to the nearest 0.5 mm while in a natural gait orientation. Natural gait was determined by matching limb position to digital photographs of undisturbed animals walking on relatively flat ground within their perspective colonies. Ll was measured from the greater trochanter of the femur to the flexor tuberculum of the tarsometatarsal on both legs of each bird. Measurements were taken in replicates of five, and the means were used in further analysis.
Analysis
All statistical analyses were performed using `R' v 2.3.1. Data are
presented as means ± s.e.m. Slopes and intercepts of fitted
relationships (including total body mass as a covariate when appropriate) were
tested for difference from equality using Welch two-sample t-tests or
analysis of covariance (ANCOVA) (Zar,
1998). For all tests, P was set at 0.05.
Maximum speeds, maximum inclines achieved,
O2max.speed, and
O2max.incline,
were compared between species using nested repeated-measures (RM) ANCOVAs.
Analysis was performed with species as the fixed factors and
individualxspecies as the random factors. Prior to this, homogeneity of
regression of the slopes was checked with a nested repeated-measures (RM)
ANCOVA speciesxspeed interaction and speciesxincline interaction
in a model that included the following fixed factors:
species+speed+speciesxspeed, or species+incline+speciesx incline
and the random factors: individual nested with species.
For exercising birds,
O2 and
1/tc, were compared using nested RM-ANCOVA with the
following fixed factors: species+speed and a random factor: individual nested
with species. Prior to this, homogeneity of regression slopes was checked with
a nested RM ANOVA speciesxspeed interaction, in a model that included
the following fixed factors: species+speed+speciesxspeed or
species+incline+speciesxincline and a random factor: individual nested
with species.
|
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
and
minimum approach (Fig.
2). The mean nest was 55.01±0.89° for the
black-browed albatross and 11.70±0.94° for the grey-headed
albatross, and the minimum approach were 19.40±1.42° and
5.30±0.69°, respectively.
|
Mean maximal speeds differed significantly between the two species (Fig. 3A; Table 2). When performing on the flat, GHA were able to walk approximately 12% faster than BBA. Whereas, BBA could walk at a significantly greater mean maximal incline at 0.6 km h–1 than the GHA (Fig. 3B; Table 2).
|
|
|
|
O2 while
standing between the BBA and the GHA (Table
3, Fig. 6A). Both
BBA and GHA were able to walk at a `cruising' speed of 0.6±0.03 km
h–1 at 0% incline for more than 60 min, including the
3–5 min warm up. No significant difference was seen between species in
mean O2 at the
cruising speed and 0% incline (Fig.
6B; Table 3). There
was also no significant difference between species in mean
O2max.speed on
the flat (Fig. 6C), and between
species in mean
O2max.incline
(Fig. 6D). Intra-species
analysis showed no significant difference between mean
O2max.speed and
mean
O2max.incline
(Fig. 6C/D;
Table 3).
|
|
RM-ANCOVA has shown that there were significant differences (Fig. 7; Table 1) in the rates of force generation (1/tc) between these species during both maximal speed and maximal incline exercise. Intra-species comparisons showed that for both the BBA and GHA, the 1/tc produced were significantly greater at maximal speed than those at minimum speed and at maximal incline compared to those at minimum incline (Fig. 7; Table 1).
|
Inter-species RM-ANCOVA (Fig. 8; Table 1) revealed significant differences between the slopes of mean NVE and between the values of mean NVE recorded at minimum incline (2%). There was no significant difference in mean NVE at the maximum incline at which the BBA and GHA could perform (10% and 8.4%, respectively). Intra-species analysis showed that the mean NVE produced by the GHA at the minimum incline was significantly greater than that at maximal incline (Fig. 8; Table 1); however, no difference was seen in the BBA (Fig. 8; Table 1).
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
O2. In addition,
BBA can sustain a `cruising' speed of 0.6 km h–1 on a
significantly steeper incline than GHA, although both reach similar
O2 maxima. The
question is how are BBA able to perform better on the incline without
incurring significantly higher metabolic costs than those of their
congener?
It has been proposed that Ls should correlate with
Ll (Hoyt et al.,
2000), and that up to 20% of the energetic cost of locomotion is
due to the muscular action used to swing the limb
(Ellerby and Marsh, 2006;
Marsh et al., 2006). Animals
with longer limbs and strides tend to have lower transport costs, as the rate
of vertical force generation decreases with longer stance periods
(Kram and Taylor, 1990).
Therefore, we might speculate that the longer Ll and
Ls found in the GHA accounts for the lower rates of oxygen
consumption recorded in comparison to the BBA when performing at the same
speeds on the flat. Hoyt et al. suggested that, for a given species, longer
limbs may decrease the force necessary to support body mass
(Hoyt et al., 2000). However,
the increased cost of swinging longer heavier limbs may nullify the simple
univariate relationship between limb length and locomotory cost, resulting in
no net gain (Hoyt et al.,
2000; Marsh et al.,
2004). As BBA have shorter Ll and
Ls than GHA at the same speed on the flat, they must be
utilising a greater stride frequency than GHA. Using a mathematical model, Kuo
concluded that stride frequency is a significant determinant of the metabolic
cost of swinging the limbs during walking
(Kuo, 2001). However,
mechanical work must be performed to redirect the centre of mass from the
pendular arc in the transition from one step to the next
(Kuo, 2002). The metabolic
energy needed to perform this work could be minimized by taking short steps
(Donelan et al., 2002).
GHA have a greater mean NVE when exercising below an 8% incline, at which point mean NVE becomes equal to that of BBA, above which they are unable to perform. Conversely, BBA show similar NVE regardless of the incline and are able to perform at a much greater incline than the GHA, suggesting that they have a single gait that it is optimised for steeper inclines. The shorter Ls combined with the greater rate of force production at the steeper inclines could reflect the use of quick, short and vertically powerful strides by the BBA, maximising the force production while minimising the effort of each leg needed to traverse the slope. This suggests that BBA have adopted a gait behaviour that minimises the cost of incline locomotion.
The present study has shown that these two species of albatross have evolved behavioural differences (Ls and 1/tc) and morphological adaptations (Ll) that minimise the cost of moving around their colony sites. It is clear that there is a relationship between terrestrial performance and topography of the colony and it is logical that the species that inhabits the steeper colony site would be the best adapted for moving up an incline. Each species has evolved greater locomotor abilities in their respective environments that are not associated with differences in the metabolic cost of locomotion. The greater maximum speed of GHA on the level is not associated with a decreased rate of force generation, as would be predicted from their greater leg length. At moderate inclines the NVE of the GHA is significantly higher then that of the BBA. Although at the maximum incline at which the GHA can perform their NVE is similar to that of the BBA, the BBA can maintain a similar NVE on significantly steeper inclines, allowing similar rates of oxygen consumption at different maximal inclines.
The results of this study correspond well with the observed behaviour of
both albatross species at the colony; GHA tend to run several steps prior to
take-off whereas BBA walk to the nearest cliff edge or take off directly from
their nest mound. However, it is difficult to determine whether this
relationship is causal, as selection pressures may operate more strongly away
from the colony. During calm or light wind conditions at sea, if an albatross
wants to take off from the water it must run into the wind along the sea
surface while beating its wings to gain sufficient lift, which is thought to
be its most energetically costly activity
(Warham, 1996;
Weimerskirch et al., 2000).
Although there is considerable overlap in feeding areas of BBA and GHA during
the chick-rearing period, during the incubation period BBA females forage
further north than male or female GHA
(Phillips et al., 2004).
Moreover, during the non-breeding periods these species migrate to quite
distinct geographical regions that experience dissimilar prevailing weather
systems (Croxall et al., 2005;
Phillips et al., 2005). It is
possible, therefore, that the differences in terrestrial performance reflect
behavioural and morphological adaptations that minimise energy expenditure
during take-off at sea, and that this influenced site topography preferences
when colonies were established at breeding islands.
|
Acknowledgments |
|---|
|
Footnotes |
|---|
Present address: BirdLife International, Wellbrook Court, Girton Road,
Cambridge CB3 0NA, UK 
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bevan, R. M., Woakes, A. J., Butler, P. J. and Boyd, I. L. (1994). The use of heart rate to estimate oxygen consumption of free-ranging black-browed albatrosses Diomedea melanophrys. J. Exp. Biol. 193,119 -137.[Abstract]
Biewener, A. A. (1989). Scaling body support in
mammals: limb posture and muscle mechanics. Science
245, 45-48.
Blix, A. S., Strømme, S. B. and Ursin, H. (1974). Additional heart rate – an indicator of psychological activation. Aerosp. Med. 45,1219 -1222.[Medline]
Butler, P. J. (1991). Exercise in birds.
J. Exp. Biol. 160,233
-262.
Carboneras, C. (1992). Family Thalassarche. In Handbook of the Birds of the World. Vol. 1 (ed. J. del Hoyo, A. Elliott and J. Sargatal), pp. 312-321. Barcelona: Lynx Edicions.
Croxall, J. P., Silk, J. R. D., Phillips, R. A., Afanasyev, V.
and Briggs, D. R. (2005). Global circumnavigations: tracking
year-round ranges of non-breeding albatrosses. Science
307,249
-250.
Donelan, J. M., Kram, R. and Kuo, A. D. (2002).
Mechanical work for step-to-step transitions is a major determinant of the
metabolic cost of human walking. J. Exp. Biol.
205,3717
-3727.
Ellerby, D. J. and Marsh, R. L. (2006). The
energetic costs of trunk and distal-limb loading during walking and running in
guinea fowl Numida meleagris. II. Muscle energy use as indicated by blood
flow. J. Exp. Biol. 209,2064
-2075.
Ellerby, D. J., Cleary, M., Marsh, R. L. and Buchanan, C. I. (2003). Measurement of maximum oxygen consumption in Guinea fowl Numida meleagris indicates that birds and mammals display a similar diversity of aerobic scopes during running. Physiol. Biochem. Zool. 76,695 -703.[CrossRef][Medline]
Fedak, M. A., Rome, L. and Seeherman, H. J.
(1981). One-step N2-dilution technique for calibrating
open-circuit measuring systems. J. Appl. Physiol.
51,772
-776.
Fellows, I. W. and Macdonald, I. A. (1985). An automated method for the measurement of oxygen consumption and carbon dioxide excretion in man. Clin. Phys. Physiol. Meas. 6, 349-355.[CrossRef][Medline]
Full, R. J. and Tullis, A. (1990). Energetics
of ascent: insects on inclines. J. Exp. Biol.
149,307
-317.
Gatesy, S. M. (1991). Hind limb scaling in birds and other theropods: implications for terrestrial locomotion. J. Morphol. 209,83 -96.[CrossRef]
Gatesy, S. M. (1999). Guineafowl hindlimb function. I. Cineradiographic analysis and speed effects. J. Morphol. 240,115 -125.[CrossRef]
Hoyt, D. F., Wickler, S. J. and Cogger, E. A. (2000). Time of contact and step length: the effect of limb length, running speed, load carrying, and incline. J. Exp. Biol. 201,221 -227.
Kram, R. and Taylor, C. R. (1990). Energetics of running: a new perspective. Nature 346,265 -267.[CrossRef][Medline]
Kuo, A. D. (2001). A simple model of bipedal walking predicts the preferred speed-step length relationship. J. Biomech. Eng. 123,264 -269.[CrossRef][Medline]
Kuo, A. D. (2002). Energetics of actively powered locomotion using the simplest walking model. J. Biomech. Eng. 124,113 -120.[CrossRef][Medline]
Lasiewski, R. C., Acosta, A. L. and Bernstein, M. H. (1966). Evaporative water loss in birds. II. A modified method for determination by direct weighing. Comp. Biochem. Physiol. 19,459 -470.[Medline]
Marsh, R. L., Ellerby, D. J., Carr, J. A., Henry, H. T. and
Buchanan, C. I. (2004). Partitioning the energetics of
walking and running: swinging the limbs is expensive.
Science 303,80
-83.
Marsh, R. L., Ellerby, D. J., Henry, H. T. and Rubenson, J.
(2006). The energetic costs of trunk and distal-limb loading
during walking and running in guinea fowl Numida meleagris. I.
Organismal metabolism and biomechanics. J. Exp. Biol.
209,2050
-2063.
Phillips, R. A., Silk, J. R. D., Phalan, B., Catry, P. and Croxall, J. P. (2004). Seasonal sexual segregation in two Thalassarche albatrosses: competitive exclusion, reproductive role specialization or foraging niche divergence? Proc. R. Soc. Lond. B Biol. Sci. 271,1283 -1291.[Medline]
Phillips, R. A., Silk, J. R. D., Croxall, J. P., Afanasyev, V. and Bennett, V. J. (2005). Summer distribution and migration of nonbreeding albatrosses: individual consistencies and implications for conservation. Ecology 86,2386 -2396.[CrossRef]
Prince, P. A., Rothery, P., Croxall, J. P. and Wood, A. G. (1994). Population dynamics of Black-browed and Grey-headed Albatrosses Diomedea melanophris and D. chrysostoma at Bird Island, South Georgia. Ibis 136, 50-71.
Roberts, T. J., Kram, R., Weyand, P. G. and Taylor, C. R. (1998). Energetics of bipedal running. I. Metabolic cost of generating force. J. Exp. Biol. 201,2745 -2751.[Abstract]
Ryan, P. G. R., Phillips, R. A., Nel, D. C. and Wood, A. G. (2007). Breeding frequency in Grey-headed Albatrosses Thalassarche chrysostoma. Ibis 149, 45-52.[CrossRef]
Schmidt-Nielsen, K. (1972). Locomotion: energy cost of swimming, flying and running. Science 172,222 -228.
Taylor, C. R. (1985). Force development during
sustained locomotion: a determinant of gait, speed and metabolic power.
J. Exp. Biol. 115,253
-262.
Taylor, C. R. (1994). Relating mechanics and energetics during exercise. Comparative vertebrate exercise physiology: unifying physiological principles. Adv. Vet. Sci. Comp. Med. A 38,181 -215.
Taylor, C. R., Schmidt-Nielsen, K. and Raab, J. L.
(1970). Scaling of energetic cost of running to body size in
mammals. Am. J. Physiol.
219,1104
-1107.
Taylor, C. R., Heglund, N. C., Mcmahon, T. A. and Looney, T.
R. (1980). Energetic cost of generating muscular force during
running: a comparison of large and small animals. J. Exp.
Biol. 86,9
-18.
Taylor, C. R., Heglund, N. C. and Maloiy, G. M. O.
(1982). Energetics and mechanics of terrestrial locomotion. I.
Metabolic energy consumption as a function of speed and body size in birds and
mammals. J. Exp. Biol.
97, 1-22.
Tickell, W. L. N. and Pinder, R. (1975). Breeding biology of the Black-browed Albatross Diomedea melanophris and Grey-headed Albatross D. chrysostoma at Bird Island, South Georgia. Ibis 117,433 -451.
Warham, J. (1996). The Behaviour, Population Biology and Physiology of the Petrels. London: Academic Press.
Weimerskirch, H., Jouventin, P. and Mougin, J. (1985). Banding recoveries and the dispersion of seabirds breeding in the French Austral and Antarctic territories. Emu 85,22 -33.
Weimerskirch, H., Guionnet, T., Martin, J., Shaffer, S. A. and Costa, D. P. (2000). Fast and fuel-efficient? Optimal use of wind by flying albatrosses. Proc. R. Soc. Lond. B Biol. Sci. 267,1869 -1874.[Medline]
Withers, P. C. (2001). Design, calibration and calculation for flow-through respirometry systems. Aust. J. Zool. 49,445 -446.[CrossRef]
Zar, J. H. (1998). Biostatistical Analysis (4th edn). Upper Saddle River, NJ: Prentice Hall.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
