Thermal stability and muscle efficiency in hovering orchid bees (Apidae: Euglossini)
Section of Integrative Biology, University of Texas, Austin, TX 78712, USA
Author for correspondence at present address (e-mail:
bborrell{at}berkeley.edu)
Accepted 2 June 2004
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Summary |
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Key words: flight energetics, thermoregulation, muscle, power, efficiency, bee, Euglossa imperialis, Euglossini
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Introduction |
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Because numerous flying insects activate their thoracic muscles at high
frequency, they produce a substantial amount of heat during flight
(Dudley, 2000). For the past 25
years, the prevailing view has been that flying insects are capable of
regulating heat dissipation but not heat production
(Casey, 1989
;
Heinrich, 1980
). However, this
perspective has been called into question by recent studies with honeybees
(Harrison et al., 1996
),
centridine bees (Roberts et al.,
1998
) and dragonflies (May,
1995a
,b
)
that suggest control of heat production via modulation of wingbeat
kinematics. More specifically, these authors have hypothesized that insects
increase wingbeat frequency to elevate body temperatures at low air
temperatures.
Although support for in-flight regulation of heat production is growing, a
number of issues remain unresolved
(Harrison and Fewell, 2002).
To draw closure to this controversy, researchers have identified three lines
for future investigation: complete analyses of wingbeat kinematics and heat
production during flight (Roberts and
Harrison, 1999
), comparative investigations demonstrating the
generality of the phenomenon (May,
1995a
,b
)
and field-based tests representative of natural flight behavior
(May, 1995a
;
Stevenson and Woods, 1997
).
Accordingly, we incorporated these suggestions in determining whether orchid
bees (Apidae: Euglossini) regulate metabolic heat production during
flight.
The flight energetics of orchid bees have been studied extensively in the
past (Casey and May, 1985;
May and Casey, 1983
), and a
recent re-analysis of data from these studies suggested that they regulate
heat production during flight (May,
1995a
). As a neotropical group, orchid bees may not encounter as
great a range of air temperatures as do temperate-zone species but they are an
ideal organism for flight studies because they will readily hover over floral
fragrances located in the field of view of a video camera
(Evoy and Jones, 1971
). In the
present study, we recorded wingbeat kinematics, carbon dioxide production and
heat loss for Euglossa imperialis hovering in a screened insectary
and wingbeat frequency alone for Eg. imperialis and five other orchid
bee species hovering in the field. These data support the hypothesis that
orchid bees regulate metabolic heat production during flight via
changes in wingbeat frequency and muscle efficiency.
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Materials and methods |
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Wingbeat kinematics and mechanical power output
Bees hovering at fragrance baits in the Laboratory Clearing were lured into
a screened insectary and induced to hover in front of a handheld digital
camcorder (Canon ZR10; 60 fields s-1; shutter speed 1/60 s), which
was positioned to record wingbeat amplitude from the dorsal view of the
animal. Bees hovered over a translucent plastic sheet, lit from behind to
enhance contrast of images. A front surface mirror oriented at 45° with
respect to the field of view provided a simultaneous image of stroke plane
angle and body angle. After transferring suitable sequences to NIH Image,
projected amplitude, stroke plane angle (ß) and body angle () were
measured at five frames during the sequence. Wingbeat amplitude (
) was
obtained by dividing projected amplitude by the cosine of the stroke plane
angle to correct for foreshortening. Wingbeat frequency (WBF) was
recorded on the camcorder's audio track using an optical tachometer
(Unwin and Ellington, 1979
). A
virtual instrument programmed in LabView (National Instruments, Austin, TX,
USA) was used to filter out noise and estimate the fundamental frequency from
0.5 s determinations, which were then averaged over the duration of the flight
sequence.
Following measurements of heat loss (see below), standard morphological
parameters were determined for all insects
(Ellington, 1984). Body mass
(mb) and wing mass (mw) were measured
to the nearest 0.0001 g using an analytical balance. Wing length (r)
was measured to the nearest 0.01 mm using digital calipers. Wing area
(S), wing loading (pw), wing aspect ratio
(AR) and non-dimensional radii for moments of wing area and virtual
mass were determined from digital photos of wings. Non-dimensional moments of
wing mass were taken from Dudley
(1995
).
Mass-specific mechanical power output was estimated from inertial
(P*acc), induced
(P*ind) and profile powers
(P*pro) using the hovering aerodynamic model of
Ellington (1984) for the cases
of perfect elastic energy storage (P*per) and
zero elastic energy storage (P*zero). The mean
lift coefficient (CL) was calculated using the mean force
balance during hovering (Ellington,
1984
), and the profile drag coefficient (CD)
was estimated assuming a lift-to-drag ratio of 0.55
(Feuerbacher et al., 2003
;
Sane and Dickinson, 2001
).
We used least-squares regressions to test if flight kinematics or mechanical power or both changed with temperature.
Metabolic power
Following the filming of wingbeat kinematics, metabolic power was estimated
using closed-system respirometry. Bees were placed in a 1 or 2 liter glass
bottle equipped with an infrared carbon dioxide sensor (Vernier Software and
Technology, Beaverton, OR, USA) accurate to 10% of the reading between 0 and
5000 p.p.m. CO2. Carbon dioxide concentration was sampled at a rate
of 1 Hz using a Vernier LabPro 12-bit A-D converter connected via USB
cable to an Apple Macintosh G3 Powerbook running Vernier LoggerPro software.
Mass-specific metabolic rate (P*met) was
calculated from the slope of carbon dioxide concentration as a function of
time, assuming a respiratory quotient of one and an energy equivalent of 21.4
J ml-1 O2.
In spite of hovering abilities exhibited during kinematic trials, bees were
reluctant to engage in continuous flight in the respirometry chamber. We
categorize flight behavior during these experiments as `agitated' because it
was necessary to shake the chamber periodically to prolong flight periods
(Harrison et al., 1996;
Suarez et al., 1996
). Only
respirometry trials in which bees flew continuously for at least 2 min were
included in our final data set. The purpose of these measurements was not to
replicate the comprehensive gas-exchange studies of Roberts et al.
(1998
) or Roberts and Harrison
(1999
) but to complement our
measurements of heat loss and wingbeat kinematics from freely hovering bees.
Consequently, we derived independent estimates of heat production by
subtracting mechanical power output from metabolic power input.
Power for heat production
At equilibrium, metabolic heat production will equal the sum of radiative,
convective and evaporative heat loss. Radiative and convective heat loss can
be inferred from body segment temperatures following flight and the Newtonian
cooling constants of freshly killed specimens
(Heath and Adams, 1969;
May, 1976
;
May and Casey, 1983
). After at
least 1 min of hovering, bees were captured in a hand net. An Omega
mini-hypodermic copper-constantan thermocouple probe (outer diameter 0.2 mm)
was sequentially inserted into the thorax, abdomen and head of the insect
within 10 sfollowing capture. Temperatures were recorded using an Omega 450
ATT temperature meter (Stamford, CT, USA) with 0.1°C resolution. The
insect was killed in acetone fumes and brought to the lab for morphological
measurements and determinations of cooling constants.
Body segment temperatures and WBF were also recorded from an
additional 20 bees at the Central Tower and Laboratory clearings on BCI.
Variation in heat transfer between the thorax and the head or abdomen was
investigated using the head temperature excess ratio:
![]() | (1) |
where Th is head temperature, Ta is
air temperature and Tth is thoracic temperature, and the
abdominal temperature excess ratio:
![]() | (2) |
where Tab is the abdominal temperature. According to
the three-compartment model outlined by Stavenga et al.
(1993), Rh
or Rab will be independent of Ta if
heat transfer does not vary between the thorax and the respective segment. If
insects actively dissipate heat from their thoraces at high
Ta, then Rh or Rab
will increase with Ta. Conversely, if insects regulate
their heads or abdomens above Ta at low
Ta then Rh or Rab
should decrease with Ta.
The induced flow field around a hovering insect provides convective cooling
in the absence of winds or forward flight speed. The magnitude of this
downwash was calculated using the aerodynamic model of Ellington
(1984), assuming uniform flow
across all body segments. The primary orientation of flow with respect to the
body was approximated as the sum of the body angle and the stroke plane angle.
Preliminary experiments with two individuals oriented at 0, 30, 60 and 90°
indicated that flow orientation exhibits the greatest influence on head and
abdominal conductance measurements. Thoracic conductance did not appear to be
sensitive to flow orientation. Based on kinematic analyses of 16 individuals,
the angle between the body and the stroke plane was 31.24±2.16°
(mean ± 95% C.I.). Insects filmed in flight were thus mounted on a thin
metal rod and placed in the test section of a desktop wind tunnel (TSI Model
8392 Certifier; TSI Incorporated, St Paul, MN, USA; turbulence intensity
0.25%) at an angle of 30° with respect to oncoming flow. A mini-hypodermic
thermocouple probe was inserted into the thorax, abdomen or head of the
insect, and a fiber optic microscope lamp was used to warm the insect to
50°C. After cooling at least 5°C, temperatures were logged by hand
every 20 s until segment temperature was within 1°C of air temperature.
This procedure was repeated on each body segment at air speeds of 0, 1 and 2 m
s-1. Air speed was measured using a calibrated hot-wire anemometer
(TSI Incorporated). Following trials, head, abdomen and thorax (without wings
or legs) were weighed using an analytical balance (±1 mg). Body segment
masses were multiplied by a correction factor based on the ratio of total mass
before cooling trials to the sum of the segment masses. The cooling constant,
k, for each segment was calculated from the natural logarithm of the
slope of the linear regression of temperature elevation versus time.
Using data specific to each individual, we employed a regression model to
estimate the cooling constants at the appropriate induced velocity.
Non-evaporative heat loss was calculated as:
![]() | (3) |
where h is the specific heat of insect tissue (3.48),
mth is the thoracic mass, mab is the
abdominal mass and mh is the head mass
(May and Casey, 1983). This
simple model is useful as a first approximation but it disregards internal
conductance due to hemolymph flow and assumes that heat is generated
independently in the head, thorax and abdomen. More detailed approaches can be
found in May (1995b
) and
Stavenga et al. (1993
).
Mass-specific evaporative heat loss (P*evap)
was estimated using regression equations for another member of the family
Apidae, Apis mellifera (Roberts
and Harrison, 1999). Although A. mellifera is known to
modulate evaporative cooling at extremely high temperatures
(Heinrich, 1979
;
Roberts and Harrison, 1999
),
at temperatures below 35°C evaporative heat loss is consistent with data
reported for the anthophorid bees Centris pallida
(Roberts et al., 1998
) and
Xylocopa capitata (Nicolson and
Louw, 1982
). Based on our estimates, evaporative heat loss
accounts for 6-7% of the total heat loss from a hovering Eg.
imperialis, and errors in our extrapolations are unlikely to influence
our major results.
We used a least-squares regression to test whether metabolic heat production declined with Ta.
Muscle efficiency
Muscle efficiency () is the ratio of mechanical power output
(P*mech) divided by metabolic power input
(Josephson et al., 2001
):
![]() | (4) |
Alternatively, efficiency can be calculated using
P*mech in conjunction with heat loss
measurements (Wakeling and Ellington,
1997):
![]() | (5) |
We calculated using equations 2 and 3 for the cases of perfect and
zero elastic energy storage and used these values to test whether
changes with Ta.
In the above calculations of muscle efficiency, we have assumed elastic
energy storage to be constant but we will also consider the possibility of
variable elastic energy storage in our Discussion. It is possible to calculate
efficiency via subtraction using only respirometric and heat loss
data:
![]() | (6) |
This efficiency estimate will be largely independent of Ellington's
(1984) model and assumptions
regarding both elastic energy storage and the lift-to-drag ratio. In effect,
wingbeat kinematics are only used in estimating the induced flow velocity.
Theoretically, the numerator of equation 6 should fall between
P*per and
P*zero, providing an indication of the degree
of elastic energy storage. Unfortunately, because variance in the numerator
was over two orders of magnitude greater than variance in
P*per or P*zero,
low statistical power compromised our ability to estimate elastic energy
storage or test temperature trends using this efficiency estimate.
Field measurement of wingbeat frequency
Wingbeat frequencies for six species of orchid bees hovering at fragrance
baits were recorded at field sites throughout Costa Rica (October 2002-January
2003) and at the Central Tower on Barro Colorado Island (June 2002):
Euglossa championi Cheesman, Euglossa imperialis, Euglossa
purpurea Friese, Euglossa sapphirina Moure, Eulaema
meriana Olivier and Eulaema cingulata Fabricius. The genus
Euglossa consists of smaller (<300 mg) glabrous bees whereas
Eulaema tend to be larger (400-1000 mg), pubescent bees. An optical
tachometer was used to record WBF on a portable cassette recorder
(Sony TCM-20DV). Air temperature was measured using a handheld thermocouple
shielded from the sun and, when bees were hovering in direct sunlight,
operative temperature (Top) was also obtained from a
thermocouple implanted in the corpse of a freshly killed bee
(Armbruster and Berg, 1994).
Operative temperature provides a rough metric for the convective and radiative
heat environment experienced by a hovering bee although it does not take into
account the contribution of air movements produced by the flapping wings. In
addition, evaporative heat loss from our bee corpses may have led to an
underestimate of Top, but we feel these measurements are
more useful than Ta because of variability in solar
radiation at our field sites. After netting bees, body mass was measured using
a portable microbalance (±1 mg).
Audio clips were transferred to a Macintosh G3 Powerbook with 16-bit resolution at a sampling rate of 44.1 kHz. A custom virtual instrument in LabView was used to electronically filter out noise and determine the fundamental frequency from a distribution of 0.1 s determinations (Fig. 1A,B). Least-squares regression was used to test whether WBF declined with Ta and Top.
|
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Results |
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Mean body mass for Eg. imperialis on BCI was 160.8±6.2 mg (mean ± 95% C.I.). Mean wing loading was 21.7±1.3 N m-2. Neither body mass nor wing loading were significantly correlated with Ta (P>0.1). Cooling constants for all body segments increased with airspeed (Table 1).
|
Kinematics and mechanical power output
Out of 28 trials, complete respirometric, thermal and kinematic
measurements were obtained for 13 Eg. imperialis individuals. For
these 13 individuals filmed in the insectary, WBF declined with
Ta, but this trend was not statistically significant
(Fig. 4;
Table 2). Further investigation
using data from 33 individuals from BCI and 126 individuals from Costa Rica
provided statistical support for this trend
(Fig. 4; BCI alone,
P=0.0024; Costa Rica alone, P<0.0001). WBF
declined from approximately 180 Hz at 20°C to 170 Hz at 34°C. A
quadratic regression provided the best fit to the pooled data
(Table 3).
Tth was not significantly correlated with WBF
(F1,32=2.380, P=0.1331). However, the elevation
of Tth over Ta did increase
significantly with WBF (Fig.
5). No other kinematic parameters were significantly correlated
with Ta (Table
3).
|
|
|
|
Mean induced velocity was 1.85±0.08 m s-1. Mean mechanical power output was 152 W kg-1 assuming perfect elastic energy storage or 197 W kg-1 assuming zero elastic energy storage (Table 2). Neither estimate was correlated with Ta (Fig. 6; Table 2).
|
Flight metabolic rate, heat production and muscle efficiency
Mass-specific metabolic rate, P*met, and
non-evaporative heat loss, P*heat, declined
linearly with Ta (Fig.
6; Table 2).
Metabolic heat production declined by 33% as Ta increased
from 24 to 34°C. Subtracting mechanical power output from
P*met, we calculated metabolic heat production
to be 705±85.5 W kg-1 assuming zero elastic energy storage
or 751±85.7 W kg-1 with perfect elastic energy storage.
Neither of these values was significantly different from 677±80.3 W
kg-1, calculated by adding P*evap to
P*heat (P>0.1). All three of these
estimates declined significantly with Ta
(P<0.05). We note that P*heat for
individual #5 was greater than P*met,
indicating an error in either one or both measurements. However, removal of
this data point does not alter our primary conclusions. Mechanical power
output estimated by subtraction
(P*met-P*heat-P*evap)
was 225±98.5 W kg-1, which was not significantly greater
than either P*per or
P*zero (P>0.1).
Muscle efficiency increased linearly with Ta (Fig. 7; Table 2). Mean muscle efficiency was 18% assuming perfect elastic energy storage and 22% assuming zero elastic energy storage (Table 2). Individual values for efficiency estimated by subtraction (equation 6) varied widely (-17 to 47%), but the mean value, 24% (28% without the negative value calculated for individual #5), was only slightly higher than our other efficiency estimates (Table 2).
|
Comparative wingbeat frequency
In the six species of orchid bees studied, WBF scaled as
mb-0.29 (r2=0.959). In all
six species, WBF declined significantly with Top
(Table 3; Figs
4,
8,
9) and Ta
(results not shown). In the two species with the greatest sample size, Eg.
imperialis and Eg. purpurea, a quadratic fit provided the best
fit to the observed data (Figs
4,
9), with WBF remaining
relatively constant at Top between 20 and 25°C and
declining above 25°C.
|
|
WBF declined between 4 and 9% (mean 6%) as Top increased from 24 to 34°C. Percent change in WBF was not correlated with body mass (P>0.1).
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Discussion |
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In comparison with pubescent bees (e.g. Bombus, Eulaema),
Euglossa is a relatively poor thermoregulator
(Roberts and Harrison, 1998).
The slope of Tth on Ta for Eg.
imperialis is closer to 1 than to 0, which led previous authors to
classify tropical bees as thermoconformers rather than thermoregulators
(Heinrich, 1993
). The present
findings demonstrate that Eg. imperialis regulates heat production at
low air temperatures, and we suggest that its poor thermoregulatory ability is
largely a consequence of its small size and lack of pubescent insulation. In
Bombus and Eulaema, pubescence substantially lowers the
convective cooling constant (Heinrich,
1993
; May and Casey,
1983
), but when these bees encounter high temperatures their thick
pile becomes a liability and they must shunt excess heat to their abdomens
(Roberts and Harrison, 1998
).
By contrast, Apis, Centris and Euglossa all possess a
countercurrent exchange mechanism limiting the dissipation of thoracic heat to
the abdomen (Wille, 1958
).
This anatomical constraint suggests that the modulation of heat production
will play a critical role in thoracic temperature regulation by these bees.
Curiously, our data indicated that the abdominal excess ratio declined with
ambient temperature, but this appears to be a rather anomalous finding in
light of previous research on orchid bees
(May and Casey, 1983
) and
other bees (Roberts et al.,
1998
; Roberts and Harrison
1999
).
An additional reason why the slope of Tth on
Ta may be so steep in Euglossa is that these bees
warm their heads at the expense of their flight muscles. We found that Eg.
imperialis regulates Th by augmenting heat transfer
to the head at low Ta. Modulation of heat transfer between
the head and thorax has also been demonstrated in the bee Centris
pallida and the dragonfly Anax junius, but the hypothesized
function of this ability is not to dissipate excess heat from the thorax but
to optimize cephalic neural functioning
(Roberts et al., 1998;
May, 1995b
). We conclude from
our measurements of body segment temperatures that the stability of both
Th and Tth during flight at low
Ta is achieved by variation in heat production not heat
dissipation.
Wingbeat frequency in orchid bees declines with air temperature while
muscle efficiency increases with air temperature. Unfortunately, kinematic
data from our 13 experimental bees proved inadequate for identifying
compensatory mechanisms by which bees maintain constant body weight support
across a range of wingbeat frequencies. Ruby-throated hummingbirds compensate
for declining frequency at high temperatures by increasing the amplitude of
wing motions (Chai et al.,
1998). In the present study, we found no evidence for compensatory
changes in wingbeat amplitude, which is not surprising given the variety of
lift-generating mechanisms available to flying insects
(Dickinson et al., 1999
;
Srygley and Thomas, 2002
).
The modulation of wingbeat frequency observed in orchid bees was consistent
with recent data from other insects that regulate heat production during
flight. For Eg. imperialis, an increase of 10°C results in a 6%
decline in wingbeat frequency. A. mellifera shows an 8% drop over the
same temperature range, and C. pallida declines by almost 14%
(Harrison et al., 1996;
Roberts and Harrison, 1998
).
Wingbeat frequency of two species of dragonflies declined by an average of 18%
as heat production dropped by almost 60%
(May, 1995a
). Interestingly,
in many of the bees examined to date (Euglossa, Centris and
Apis), wingbeat frequency appears to exhibit a two-phase relationship
with air temperature, suggesting that wingbeat frequency may be maximized at
air temperatures below 25°C.
In contrast to flying bees and dragonflies, most insects show a positive
relationship between wingbeat frequency and air temperature
(Oertli, 1989). In beetles,
this phenomenon is manifested as a positive relationship between frequency and
thoracic temperature (Oertli,
1989
). Oertli
(1989
) argues convincingly
that the temperature sensitivity of wingbeat frequency is a consequence of the
resonant properties of the thorax. The present data demonstrate that thoracic
temperature does not influence wingbeat frequency in orchid bees, rather
modulation of frequency influences thoracic temperature elevation.
Indeed, work loop experiments with asynchronous flight muscle indicate that
heat production increases when muscles are activated above their usual
contraction frequencies (Josephson et al.,
2001
). With our experimental methods, we were unable to
distinguish whether changes in muscle efficiency represent a shift in the
biochemical efficiency of muscle contraction
(Baker and Thomas, 2000
;
Maughan and Vigoreaux, 1999
)
or in the amount of elastic energy stored by the thorax during the
deceleration phase of the wing stroke
(Dickinson and Lighton, 1995
;
Ettema, 2001
;
Roberts et al., 1998
).
Metabolic heat production increased by over 200 W kg-1 as
temperature decreased by 10°C. Assuming a constant efficiency of 20%, a
complete shift from perfect elastic energy storage to zero elastic energy
storage would result in a 45 W kg-1 increase in mechanical power
requirements and a >200 W kg-1 increase in metabolic power.
Alternatively, if elastic energy storage remains constant, then efficiency
must decrease by approximately 6% to account for this 200 W kg-1
increase. Further work is needed to identify the physiological and biochemical
mechanisms by which heat production may be decoupled from useful aerodynamic
work.
Because enzyme function is highly temperature dependent, physiological and
biochemical processes may be optimized through temperature specialization
(Hochachka and Somero, 1984).
One hypothesis for specializing at high temperatures is that it may reduce the
threat of overheating during strenuous activities such as locomotion
(Heinrich, 1977
). Animals that
are adapted to operate at high body temperatures must possess a mechanism to
warm themselves at cooler temperatures. Flying bees accomplish this task by
beating their wings at elevated frequencies.
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List of symbols |
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Acknowledgments |
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Footnotes |
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References |
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