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First published online January 3, 2006
Journal of Experimental Biology 209, 364-371 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.01999
Drosophila melanogaster locomotion in cold thin air
Department of Biology, Box 351800, University of Washington, Seattle, WA 98195-1800, USA
* Author for correspondence (e-mail: dillonm{at}u.washington.edu)
Accepted 16 November 2005
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Summary |
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Key words: Drosophila melanogaster, high altitude, mountain, flight, walking speed, temperature, physiology, interaction, air density, air pressure, oxygen
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Accompanying this rapid temperature change, at 4000 m the partial pressure of
oxygen (PO2) falls to half its sea level value, and air
density decreases by 40%. These physical changes should, both individually and
in concert, compromise the physiology of ectothermic insects
(Mani, 1968; Sømme,
1989,
1995). Despite these
challenges, however, many ectothermic insects maintain robust populations on
mountains (e.g. Mani, 1968;
Brehm et al., 2003;
Romero-Alcaraz and Avila,
2000). Fruit flies in the genus Drosophila (family
Drosophilidae) are found from less than 100 m to over 3000 m in the
Californian Sierra Nevada (Dobzhansky,
1948) and above 5000 m in the Indian Himalayas
(Khare et al., 2002). To
maintain robust populations on high mountains, these small ectothermic insects
must locate food and mates, and evade predators, despite the combined
physiological challenges of low temperature, low PO2 and
low air density. Here we ask whether these factors, independently and in
concert, compromise insect locomotory performance.
Decreased temperatures at high altitude affect insect performance because
physiological reaction rates are strongly determined by temperature
(Huey and Kingsolver, 1989).
Low temperatures reduce metabolic rates and change the dynamics of muscle
contraction (Josephson, 1981),
impairing muscle physiology (Scaraffia and
De Burgos, 2000; Hosler et
al., 2000) and therefore locomotory performance of fruit flies.
Walking speed of D. melanogaster is slower in colder temperatures
(Gibert et al., 2001;
Crill et al., 1996). Similarly,
in tethered flies, less power is produced for flight at low temperatures
(Curtsinger and Laurie-Ahlberg,
1981; Lehmann,
1999).
Reduced PO2 may compromise fruit fly locomotion by
reducing metabolic rate. The dramatic altitudinal reduction in
PO2 may challenge tissue oxygen delivery because insects
depend on diffusion (at least through the terminal tracheoles) for which
PO2 is the driving force
(Denny, 1993). However, oxygen
delivery may not limit insects at high altitude because insects are generally
very resistant to low oxygen levels
(Krishnan et al., 1997;
Hoback and Stanley, 2001; but
see below for potential interactions between PO2 and
temperature and their effects on oxygen delivery).
Reduced air density should make it difficult to fly at high altitude
because aerodynamic forces produced by wing flapping increase linearly with
air density (Dudley, 2000).
Despite this theoretical limitation, many insects fly on high mountains
(Mani, 1968). Furthermore, in
the laboratory, orchid bees fly in pure heliox (21% O2, balance
helium), despite the 64% reduction in air density (approximately equivalent to
the top of Mount Everest; Dudley,
1995). To do so, orchid bees increase mechanical power output by
40-50%, suggesting that flight in low air densities, though possible, may be
energetically expensive.
Some research exists on the independent effects of temperature,
PO2, and air density on insect locomotory performance.
However, high altitude ecosystems are uniquely characterized by the
combination of these factors, yet no study has investigated the interactions
among these factors and their potential synergistic effects on insect
locomotion. Recent work documenting large interactive effects of temperature
and oxygen on insect development (Frazier
et al., 2001; Woods and Hill,
2004) strongly suggests that such interactions should be
considered in studies of insect physiology.
Here we measure the direct and interactive effects of temperature and
barometric pressure on walking and flight performance of wild-caught
Drosophila melanogaster. We use a standard technique to measure
walking speed (Crill et al.,
1996; Gilchrist,
1996) and introduce a novel method to measure whole animal flight
ability and flight motivation. We find strong negative effects of reduced
temperature and reduced air pressure on flight ability and walking speed. Low
temperatures and low air pressures interact to reduce flight performance more
than predicted by the additive effects of these variables. Our results suggest
that future studies on high altitude physiology incorporate the suite of
physical factors that characterize high altitude ecosystems.
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Materials and methods |
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23°C and 16 h:8 h L:D; diet of
cornmeal, molasses, yeast, agar, tegosept) before transferring newly emerged
adult flies into the colony. Colony food bottles (150 ml) were replaced every
3-5 days, ensuring that all colony flies developed in controlled conditions.
The colony was maintained at 1000-1500 flies for 3-6 generations prior to
experiments.
Experimental flies were collected as eggs during a 2-6 h laying period and
reared at densities of 50 eggs/vial. To control for age and reproductive
state, we transferred newly emerged female flies to fresh food vials every 24
h and allowed the flies to mature for 3-4 days before testing their locomotory
performance (we only tested virgin flies). We chose this age because wing-beat
frequency and power output of flies remains constant from 2 to 8 days of age
(Curtsinger and Laurie-Ahlberg,
1981). To assess performance, we first starved flies for 16-20 h
in individual 1.5 ml Eppendorf tubes containing fresh agar for water; moderate
starvation increases average flight speed
(David, 1978) and duration
(Tammero and Dickinson, 2002),
and preliminary experiments demonstrated that starvation motivated flight.
Then, individual flies were randomly assigned to a single temperature/air
pressure treatment to test either walking or flight performance. Experiments
were performed in a walk-in environmental chamber; humidity was kept near
100%, and temperature was monitored using a calibrated thermocouple
thermometer (Physitemp Bat-12, Bailey Instruments Inc., Saddlebrook, NJ, USA).
Given the relationship between air density, pressure and temperature, we could
not simultaneously keep both air pressure and air density constant at
different temperatures. We chose to keep air density constant because of its
direct link to production of flight forces; consequently, at a given air
density, air pressure increases slightly with temperature.
Walking performance
We modified the technique of Gilchrist et al.
(1997) to assess walking speed
of flies at three temperatures and four air densities: 18, 25, 30°C
(18.09±0.38°C, 25.34±0.18°C and 29.61±0.33°C,
means ± s.d., respectively); 33%, 50%, 66%, and 100% sea-level air
pressure (34.27±0.74 kPa, 51.19±0.68 kPa, 67.06±1.04 kPa
and 100.97±1.75 kPa, means ± s.d., respectively). We placed 10
flies individually inside 10 ml (6 ml volume after we had cut them down)
plastic graduated burets that were connected in series to a vacuum pump. After
adjusting air pressure inside the burets, we allowed the flies to acclimate
for 5 min. We then knocked each fly to the bottom of its buret and timed to
the nearest 0.01 s how long it took to walk 12 cm vertically. This was
repeated twice more for each fly and the average was used to calculate walking
speed. If a fly jumped, flew or walked in a spiral, the time was discarded and
the fly was knocked to the bottom of the buret and retimed.
Flight performance
We assessed flight performance at four temperatures and at four air
densities: 18, 25, 30, 32°C (18.05±0.23, 25.22±0.51,
30.11±0.28, 31.91±0.28, mean ± s.d., respectively); 33%,
50%, 66% and 100% sea level (33.28±1.81 kPa, 50.87±1.34 kPa,
67.46±1.22 kPa and 101.82±1.6 kPa, means ± s.d.,
respectively). The flight chambers were 250 ml glass milk bottles inverted
over rubber stoppers to form an air-tight seal
(Fig. 1). The interior of the
bottle was coated with a fluon line that extended from the lowermost point of
the bottle to 2 cm above the lip of the Eppendorf tube housing the fly (see
Fig. 1). Flies were unable to
walk up the fluon-coated sides of the bottle and thus could only arrive above
the fluon line by flying. We arranged ten flight chambers in series, and used
a vacuum pump to alter air pressure inside all of the chambers simultaneously.
To motivate flight, we placed lights above the flight chambers and dabbed a
small amount of apple cider vinegar at the top of each flight chamber before
each test.
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After a 16-20 h starvation period in individual Eppendorf tubes, the flies, while still housed in their starvation tubes, were individually placed in the flight chambers (Fig. 1). Pressure was then adjusted and the flies were given 5 min to acclimate to the treatment condition. After this acclimation period, the flies were released by removing the tube lids with a magnet (see Fig. 1).
We scored flight performance as follows: if a fly flew above the fluon line within 2 min after being released into the bottle, it was scored as a `flight'. In pilot experiments at 25°C and sea level air density, almost all flies (>95%) flew within this 2 min period. For those flies that did not fly in the first 2 min, we gently tapped their bottles to encourage flight. Flies that flew above the fluon line during this 2 min agitation period were scored as `coerced flight'. If a fly did not fly during the agitation period, we returned the bottle to sea-level air pressure. If the fly did not fly during 5 min of agitation at sea-level air pressure, we assumed it was somehow compromised and removed it from the analysis. However, if a fly flew during this sea-level agitation period, it was scored as `no flight'. Therefore, those flies that failed to fly did so because of treatment conditions, not because they were incapable of flight.
Immediately after assessing flight performance, we weighed flies to the nearest 0.001 mg (Cahn C-33 microbalance, Cahn Instruments, Inc., Cerritos, CA, USA) and placed them in 95% ethanol. We later removed one wing from each fly and mounted it on a microsope slide (using Aquamount; VWR, Pittsburgh, PA, USA). We took digital pictures (Nikon Coolpix 990, Nikon Corporation, Tokyo, Japan) of fly wings through a microscope (Nikon, Japan) and determined area of the wing using a custom image analysis program (G. Wang: WingWang: utilities for wing morphology analysis, 2004; http://students.washington.edu/gw0/matlabcode). Wing loading was calculated as the ratio of fly weight to twice the measured area of one wing.
Statistical analyses
We assessed the effects of temperature and air pressure on walking speed
using a full-factorial analysis of variance (ANOVA) with temperature and air
pressure as factors. We used Tukey Honest Significant Difference (HSD) tests
for post-hoc comparisons. To estimate statistical power we used a
randomization technique (Fisher,
1935; Crawley,
2002). We simulated data by sampling from normal distributions
with means and standard deviations (s.d.) set to the observed values of each
treatment group and performed an ANOVA on the simulated data. We repeated this
10 000 times and created a distribution of P-values for each factor
(temperature, air pressure and their interaction). The proportion of the
resulting distribution that fell below 
=0.05 was the power to detect a
significant effect for a given factor
(Peres-Neto and Olden,
2001).
To analyze flight performance, we used an ordinal logistic regression model
because our metric of flight performance was an ordered categorical response
variable (flight, coerced flight, no flight). We included squared terms
(appropriately centered) in the model to fit observed curvilinearity in the
response variable. We compared partial deviances (
2 tests) of
models with different combinations of main effects (temperature, air pressure,
and wing loading), centered interactions, and centered squared effects to
obtain the final model. All statistical analyses were done in R (2005; R
Foundation for Stastical Computing, Vienna, Austria), using contributed
packages Hmisc (F. E. Harrell, Jr: R package version 2.0-9, 2004), agce (R.
Gottardo: R package version 1.2, 2005), MASS
(Venables and Ripley, 2002),
Design (F. E. Harrell, Jr: R package version 2.0-9, 2004) and multcomp (F.
Bretz, T. Hothorn and P. Westfall: R package version 0.4-8, 2004).
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Decreased air pressure significantly reduced walking speed (P<0.001; Table 1, Fig. 2). The depressing effect of reduced air pressure on walking speed was driven by a large decrease in walking speed at 33% sea-level air pressure (Tukey HSD, P<0.001; Fig. 2); no other pressures significantly reduced walking speed relative to sea-level values (Tukey HSD, all P>0.05). Although the overall ANOVA showed no temperature by pressure interaction effect on walking speed (Table 1), pairwise comparisons revealed interactive effects between temperature and air pressure. At 30°C flies walked significantly more slowly at 33% sea-level air pressure when compared to 66% or 100% sea-level air pressure (Tukey HSD, P=0.012 and P=0.049, respectively); however, reduced air pressure did not significantly slow walking speed at the two lower test temperatures (Tukey HSD, all P>0.05). This conflict between the overall ANOVA and the post-hoc tests may result from low statistical power. Given the size of the effect and the sample size, we had only a 48% chance of detecting a significant temperature by air pressure interaction.
Flight performance
We assessed flight ability of a total of 444 flies (range of 25-30 per
treatment group). All flies included in the analysis attempted at some point
to fly above the fluon line (see Fig.
1). Flies were more motivated to fly at higher air temperatures
and pressures (Fig. 3, open
bars, `flight'). Flies failed to fly at the lowest temperatures and at the
lowest air pressures (Fig. 3, filled bars, `no flight').
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2 test, P<0.05;
Neter et al., 1996). The final
model (Table 2) fit the flight
performance data well (model likelihood ratio=233.8, 6 d.f.,
P<0.001; Nagelkerke R2=0.491), accurately
predicted flight performance given the factors included (Goodman-Kruskal
Gamma=0.693; Somers' d=0.665; 
-a=0.371), and was both sensitive
(high true positive fraction) and specific (high true negative fraction,
c-index=0.832; Swets,
1988).
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Low temperatures reduced flight performance (Table 2,Fig. 3). Temperature also had curvilinear effects on flight performance (Temperature2; Table 2, Fig. 3), likely due to the drop in flight performance at 32°C and 33% sea-level air pressure (Fig. 3).
Air pressure had strong linear and curvilinear effects on flight performance, with a progressively more rapid drop in flight score as pressure fell below 66% sea level (Table 2; Fig. 3).
The effect of air pressure on flight score depended strongly on air temperature. At warmer test temperatures, air pressure had little impact on flight performance; whereas at colder temperatures, reduced air pressure dramatically reduced flight performance (temperaturexpressure; Table 2, Fig. 3).
We used the ordinal logistic model to predict the effects of temperature and air pressure on both the probability of flight failure (`no flight' category) and flight motivation (`flight' category). Flies were unlikely to fail except in the lowest air pressure (33% sea-level air pressure; Fig. 4). At this pressure, temperature had a strong effect on the probability of failure. At 33% sea-level air pressure and 32°C, the probability of flight failure was only 10%. At this same pressure and 18°C the probability of flight failure increased to near 60% (Fig. 4). Flight motivation (probability of flight without coercion) declined with temperature and air pressure (Fig. 5).
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Flight performance was not significantly affected by wing loading despite high variation in wing loading among tested flies (P=0.076; Table 2, Fig. 6). However, wing loading was not distributed equally among treatments. Flies in the 32°C treatment tended to have higher wing loading than flies in the 18°C treatment (Tukey HSD, t=2.88, P<0.01), but there was no other significant among treatment variation in wing loading (Tukey HSD, all P>0.05). Increased wing loading should reduce flight performance. Therefore if wing loading had been evenly distributed across temperature treatments, our final conclusions would remain the same.
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We additionally asked whether mass affected flight score above and beyond
the effects of wing loading (e.g. Dillon
and Dudley, 2004) by regressing fitted values from the final model
(Table 2) on body mass. We
found no significant effect of mass on flight motivation (probability of
flying without coercion; ANOVA, F=0.07, P=0.80) or flight
failure (probability of no flight; ANOVA, F=0.95, P=0.33),
despite the large variation in body mass of flies used in the experiment
(Fig. 6).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Steele and Partridge, 1988),
escape predators and obtain resources. Therefore, environmental conditions
that compromise walking speed may reduce fitness. Previous work shows that
colder temperatures reduce the walking speed of D. melanogaster
(Gilchrist et al., 1997;
Crill et al., 1996;
Gibert et al., 2001). Low
pressure may also slow walking speed because reduced PO2
can affect tissue oxygen delivery. We found a positive correlation between
temperature and walking speed of D. melanogaster, but only the lowest
tested air pressure (34 kPa; 33% sea level) significantly reduced walking
speed (Table 1;
Fig. 2). This is roughly
equivalent to the air pressure on the peak of Mount Everest (8800 m); which
fruit flies are unlikely to experience, given that populations have not been
found above 5200 m(Khare et al.,
2002). Therefore, walking ability at high altitudes is likely
limited by temperature, but not PO2.
This result is not surprising given the empirical data that insects are
generally resistant to low oxygen levels
(Hoback and Stanley, 2001;
Greenlee and Harrison, 2004;
Klok et al., 2004). Fruit
flies exposed to only 2-3% sea level PO2 (1.5 kPa, less
than 1/3 the oxygen level of our lowest treatment) remain active and can even
fly (Farahani and Haddad,
2003). Only flies kept in anoxic conditions for more than 6 h do
not fully recover (Krishnan et al.,
1997). The effects of reduced PO2 may be
further mitigated at high altitude by increased diffusion rates at reduced air
density. The reduction in PO2 that occurs along an
altitudinal gradient reduces the driving force for diffusion, but a
concomitant drop in air density increases the diffusion coefficient, perfectly
compensating (at least in theory; Denny,
1993). Insects experiencing simultaneous reductions in
PO2 and air density should therefore be even more tolerant
to low oxygen than predicted from studies where low PO2 is
obtained by reducing percent oxygen while maintaining sea level air
density.
We predicted that air pressure and temperature would interactively affect
walking speed because insect metabolic rates increase exponentially with
temperature (Berrigan and Partridge,
1997; Gillooly et al.,
2001), but oxygen diffusion rates increase only slightly
(Denny, 1993). Given the
differential effects of temperature on these processes, we predicted that low
PO2 would decrease walking speed more at warmer
temperatures than at cooler temperatures. This theoretical prediction is
supported by developmental evidence. D. melanogaster reared in
stressfully high temperatures are significantly larger and develop more
quickly when supplied with supplemental oxygen
(Frazier et al., 2001, but
supplemental oxygen had little effect on these traits at lower temperatures).
Similarly, Manduca sexta eggs appear to experience oxygen limitation
at high temperatures (Woods and Hill,
2004). Our results imply that reduced PO2 may
also reduce walking speed at higher temperatures. Pairwise comparisons between
our treatment groups revealed that flies at 30°C walked 25% more slowly at
33% than at 66% or 100% sea-level air pressure. Air pressure had no
significant effect at colder temperatures. This pairwise comparison arises
even though we found no significant interaction effect in the overall ANOVA
(Table 1). This may reflect our
low power to detect the interaction given the magnitude of the effect and the
sample size.
Flight performance
Insects use flight to find mates, food and suitable oviposition sites, as
well as to evade predators and to defend territories. If reduced temperatures
and low air pressures compromise insect flight ability, high altitude
environments would profoundly influence these fitness-related traits. We found
that both low air pressure and low temperature negatively influenced the
flight performance of D. melanogaster. In contrast to walking speed,
reduced air pressure weakened flight performance at ecologically realistic
levels (Fig. 3). This is likely
due to aerodynamic effects of reduced air density and not due to metabolic
effects of reduced PO2
(Joos et al., 1997). Moreover,
the combination of cold temperatures and low air pressures challenged flight
more than would have been predicted by their additive effects
(Table 2). At warmer
temperatures, air pressure had little effect on flight performance, whereas at
colder temperatures reduced air pressure caused large reductions in flight
performance (Figs 3,
4,
5).
Except in the most extreme conditions, most flies (>80%) successfully initiated flight with or without agitation (Fig. 4). Flies failed regularly only in 33% sea level pressure when temperature was at or below 25°C. Remarkably, even at 50% sea-level air pressure and 18°C, 90% of D. melanogaster could fly, even though this reduction in air density requires about a twofold increase in lift production. The limited effects of low temperature and low pressure on flight failure may reflect the conservative nature of our assay. Flies did not have to sustain a long flight to arrive above the fluon line (Fig. 1).
The ability of D. melanogaster to fly in low temperature and low
pressure also reinforces the general finding that insects have a remarkable
capacity for augmenting flight performance
(Lehmann, 1999;
Dudley, 1995;
Dillon and Dudley, 2004).
Insects can augment force production by increasing stroke amplitude
(Dudley, 1995;
Dillon and Dudley, 2004). In
heliox (20.9% oxygen, balance helium), which is approximately equivalent in
density to our 33% treatment, hovering orchid bees increased stroke amplitude
by as much as 31% (Dudley,
1995). Similarly, flies produce maximum forces in response to
loading by increasing stroke amplitude
(Lehmann, 1999).
Alternatively, insects can increase wing-beat frequency, but for ectotherms
this may be impossible in cold conditions
(Curtsinger and Laurie-Ahlberg,
1981). At 15°C half of D. melanogaster tested could
not maintain flight for 1 s, likely due to reduced wing-beat frequencies
(Lehmann, 1999;
Curtsinger and Laurie-Ahlberg,
1981). More subtle changes in wing-beat kinematics may also allow
flies to increase force production to fly in high altitude conditions
(Sane and Dickinson, 2001).
However, all of these kinematic adjustments are likely to be energetically
costly (Dudley, 1995;
Chadwick and Williams, 1949;
Chadwick, 1951).
Compared to flight failure, flight motivation was highly sensitive to
temperature and pressure (Figs
3,
5). As temperature and air
pressure declined, flies became increasingly unwilling to fly without
agitation (Fig. 5). The
combination of cold temperatures and low air pressures reduced flight
motivation more than predicted by the additive effects of these factors
(Fig. 5). This large
interactive effect may reflect the combination of two challenges. To fly in
reduced air pressure, insects must produce greater muscle forces to alter
wing-beat kinematics (Dudley,
2000), but their ability to do so is hampered by reduced
physiological reaction rates at cold temperatures (e.g.
Huey and Kingsolver, 1989;
Berrigan and Partridge, 1997;
Josephson, 1981;
Hosler et al., 2000). Flies
are physiologically compromised at the same time that demand for performance
is high, reducing their motivation to fly.
The need to conserve water may also reduce flight motivation in high
altitude conditions. Reduced and pressure at altitude both increase the
driving force for evaporative water loss (for a review of water balance issues
in insects, see Sømme,
1995). Insects minimize water loss by keeping their spiracles
closed except during brief periods of gas exchange
(Lighton, 1996). However,
increased metabolic demand from the flight muscles and reduced atmospheric
PO2 may drive insects to increase the frequency and
duration of spiracular opening, increasing water loss
(Joos et al., 1997). For
example, Drosophila species lose water more than 3.5 times faster
when hovering than when at rest and an additional 20% faster during elevated
force production (Lehmann et al.,
2000). These effects may be more pronounced at high altitude where
force requirements for flight are likely higher, and where the driving force
for evaporative water loss is greatly increased.
Insects may compensate for challenging flight conditions at high altitude
by reducing wing loading (Dudley,
2000; insect weight/wing area). Theoretically, reduced wing
loading will reduce induced power requirements while also allowing for
increased lift production (for a review, see
Dudley, 2000). For this
reason, well-documented geographic and developmental variation in wing loading
of Drosophila has been hypothesized to be adaptive
(Norry et al., 2001;
Loeschcke et al., 1999;
Starmer and Wolf, 1989).
However, wing loading did not affect maximum take-off performance of 70
species of birds, bats and insects
(Marden, 1987) or maximum
load-lifting performance of 11 bee species
(Dillon and Dudley, 2004).
Naturally occurring variation in wing loading in our population of fruit flies
(Fig. 6) allowed us to
explicitly test the effect of wing loading on flight performance. We found no
significant effect of wing loading on flight performance
(Table 2), despite significant
variation in our population.
Implications for life at high altitude
High altitude environments have long been equated to high latitude
environments because of their climatic similarities
(Hopkins, 1938), but these two
environments may have very different physiological effects on insects. Our
results suggest that high altitudes are likely more challenging than high
latitudes, at least for D. melanogaster. The independent and
interactive effects of low temperature and low air pressure dramatically
reduced flight motivation, and increased the probability of flight failure.
This interaction may lead to different predictions for insect thermoregulation
at high altitudes vs high latitudes at sea level. For instance, small
flying insects may need to maintain comparatively warmer body temperatures at
high altitudes, due to the profound effects of low air pressure when combined
with low temperatures on flight performance.
The interactive effects of temperature and air pressure on insect flight
performance may help explain the increased prevalence of flightless insects at
high altitude. Historically, the evolution of flightlessness at high altitudes
has mostly been attributed to prevailing environmental conditions such as
increased wind, cold temperatures and low air pressures (reviewed by
Mani, 1968;
Sømme, 1989). These
conditions are generally acknowledged to make flight more difficult, or
impossible; and wind may also be risky for flying insects, causing unintended
transport to unfavorable locations. Our results confirm that cold temperatures
and low air pressures - and especially the combination of the two - do indeed
challenge insect flight. But our findings also suggest that `behavioral drive'
may provide an explicit explanation for why these challenging environmental
conditions promote the evolution of wingless and flightless insects at high
altitude. This classical theory posits that changes in behavior drive
evolutionary change in other traits (Mayr,
1963). High altitude conditions dramatically reduced flight
motivation of D. melanogaster
(Fig. 5). If insects generally
avoid flying at high altitudes they will not enjoy the benefits of flight
(finding food and mates, escaping predators), but they will continue to incur
the costs of developing and maintaining the flight machinery. Selection should
then favor reduction or loss of the unused flight machinery, increasing the
probability of evolving flightlessness over evolutionary time.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Berrigan, D. and Partridge, L. (1997). Influence of temperature and activity on the metabolic rate of adult Drosophila melanogaster. Comp. Biochem. Physiol. 118A,1301 -1307.[CrossRef]
Brehm, G., Suessenbach, D. and Fiedler, K. (2003). Unique elevational diversity patterns of geometrid moths in an Andean montane rainforest. Ecography 26,456 -466.[CrossRef]
Chadwick, L. E. (1951). Stroke amplitude as a
function of air density in the flight of Drosophila. Biol.
Bull. 100,15
-27.
Chadwick, L. E. and Williams, C. M. (1949). The
effects of atmospheric pressure and composition on the flight of
Drosophila. Biol. Bull.
97,115
-137.
Crawley, M. J. (2002). Statistical Computing: An Introduction to Data Analysis Using S-Plus. West Sussex (UK): John Wiley & Sons.
Crill, W., Huey, R. and Gilchrist, G. (1996). Within- and between-generation effects of temperature on the morphology and physiology of Drosophila melanogaster. Evolution 50,1205 -1218.[CrossRef]
Curtsinger, J. W. and Laurie-Ahlberg, C. C.
(1981). Genetic variability of flight metabolism in
Drosophila melanogaster I. Characterization of power output during
tethered flight. Genetics
98,549
-564.
David, C. (1978). The relationship between body angle and flight speed in free-flying Drosophila. Physiol. Entomol. 3,191 -195.
Denny, M. (1993). Air and Water: The Biology and Physics of Life's Media. New Jersey: Princeton University Press.
Dillon, M. E. and Dudley, R. (2004). Allometry
of maximum vertical force production during hovering flight of neotropical
orchid bees (Apidae: Euglossini). J. Exp. Biol.
207,417
-425.
Dillon, M. E., Frazier, M. R. and Dudley, R. (in press). Into thin air: physiology and evolution of alpine insects. Int. Comp. Biol. (In press).
Dobzhansky, T. (1948). Genetics of natural
populations. XVI. Altitudinal and seasonal changes produced by natural
selection in certain populations of Drosophila pseudoobscura and
Drosophila persimilis. Genetics
33,158
-176.
Dudley, R. (1995). Extraordinary flight performance of orchid bees (Apidae: Euglossini) hovering in heliox (80% He/20% O2). J. Exp. Biol. 198,1065 -1070.
Dudley, R. (2000). The Biomechanics of Insect Flight: Form, Function, and Evolution. New Jersey: Princeton University Press.
Farahani, R. and Haddad, G. (2003). Understanding the molecular responses to hypoxia using Drosophila as a genetic model. Respir. Physiol. Neurol. 135,221 -229.[CrossRef]
Fisher, R. (1935). The Design of Experiments. Edinburgh: Oliver & Boyd.
Frazier, M. R., Woods, H. A. and Harrison, J. F. (2001). Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiol. Biochem. Zool. 74,641 -650.[CrossRef][Medline]
Gibert, P., Huey, R. B. and Gilchrist, G. W. (2001). Locomotor performance of Drosophila melanogaster: Interactions among developmental and adult temperatures, age, and geography. Evolution 55,205 -209.[CrossRef][Medline]
Gilchrist, G. (1996). A quantitative genetic analysis of thermal sensitivity in the locomotor performance curve of Aphidius ervi. Evolution 50,1560 -1572.[CrossRef]
Gilchrist, G. W., Huey, R. B. and Partridge, L. (1997). Thermal sensitivity of Drosophila melanogaster: evolutionary responses of adults and eggs to laboratory natural selection at different temperatures. Physiol. Zool. 70,403 -414.[Medline]
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. and
Charnov, E. L. (2001). Effects of size and temperature on
metabolic rate. Science
293,2248
-2251.
Greenlee, K. and Harrison, J. (2004).
Development of respiratory function in the American locust Schistocerca
americana I. Across-instar effects. J. Exp. Biol.
207,497
-508.
Hoback, W. and Stanley, D. (2001). Insects in hypoxia. J. Insect Physiol. 47,533 -542.[CrossRef][Medline]
Hopkins, A. (1938). Bioclimatics: A Science of Life and Climate Relations. Washington: United States Government Printing Office.
Hosler, J. S., Burns, J. E. and Esch, H. E. (2000). Flight muscle resting potential and species-specific differences in chill-coma. J. Insect Physiol. 46,621 -627.[CrossRef][Medline]
Huey, R. B. and Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4,131 -135.
Joos, B., Lighton, J. R. B., Harrison, J. F., Suarez, R. K. and Roberts, S. P. (1997). Effects of ambient oxygen tension on flight performance, metabolism, and water loss of the honeybee. Physiol. Zool. 70,167 -174.[Medline]
Josephson, R. K. (1981). Temperature and the mechanical performance of insect muscle. In Insect Thermoregulation (ed. B. Heinrich), pp.20 -44. New York: John Wiley & Sons.
Khare, P. V., Burnabas, R. J., Kanojiya, M., Kulkarni, A. D. and Joshi, D. S. (2002). Temperature dependent eclosion rhythmicity in the high altitude Himalayan strains of Drosophila ananassae. Chronobiol. Int. 19,1041 -1052.[CrossRef][Medline]
Klok, C. J., Sinclair, B. J. and Chown, S. L.
(2004). Upper thermal tolerance and oxygen limitation in
terrestrial arthropods. J. Exp. Biol.
207,2361
-2370.
Krishnan, S. N., Sun, Y. A., Mohsenin, A., Wyman, R. J. and Haddad, G. G. (1997). Behavioral and electrophysiologic responses of Drosophila melanogaster to prolonged periods of anoxia. J. Insect Physiol. 43,203 -210.[CrossRef][Medline]
Lehmann, F.-O. (1999). Ambient temperature affects free-flight performance in the fruit fly Drosophila melanogaster.J. Comp. Physiol. B 169,165 -171.[CrossRef][Medline]
Lehmann, F.-O., Dickinson, M. H. and Staunton, J. (2000). The scaling of carbon dioxide release and respiratory water loss in flying fruit flies (Drosophila spp.). J. Exp. Biol. 203,1613 -1624.[Abstract]
Lighton, J. R. B. (1996). Discontinuous gas exchange in insects. Annu. Rev. Entomol. 41,309 -324.[CrossRef][Medline]
Loeschcke, V., Bundgaard, J. and Barker, J. S. F. (1999). Reaction norms across and genetic parameters at different temperatures for thorax and wing size traits in Drosophila aldrichi and D. buzzatii. J. Evol. Biol. 12,605 -623.[CrossRef]
Mani, M. (1968). Ecology and Biogeography of High Altitude Insects. The Hague: Dr W. Junk.
Marden, J. H. (1987). Maximum lift production
during takeoff in flying animals. J. Exp. Biol.
130,235
-258.
Mayr, E. (1963). Animal Species and Evolution. Cambridge: Harvard University Press.
Neter, J., Kutner, M. H., Nachtsheim, C. J. and Wasserman, W. (1996). Applied Linear Regression Models. 3rd edn. Chicago: Irwin.
Norry, F. M., Bubliy, O. A. and Loeschcke, V. (2001). Developmental time, body size and wing loading in Drosophila buzzatii from lowland and highland populations in Argentina. Hereditas 135, 35-40.[CrossRef][Medline]
Partridge, L., Ewing, A. and Chandler, A. (1987). Male size and mating success in Drosophila melanogaster: the roles of male and female behaviour. Anim. Behav. 35,555 -562.[CrossRef]
Peres-Neto, P. R. and Olden, J. D. (2001). Assessing the robustness of randomization tests: examples from behavioral studies. Anim. Behav. 61, 79-86.[CrossRef][Medline]
Romero-Alcaraz, E. and Avila, J. M. (2000). Effect of elevation and type of habitat on the abundance and diversity of Scarabaeoid dung beetle (Scarabaeoidea) assemblages in a mediterranean area from southern Iberian Peninsula. Zool. Stud. 39,351 -359.
Sane, S. P. and Dickinson, M. H. (2001). The
control of flight force by a flapping wing: lift and drag production.
J. Exp. Biol. 204,2607
-2626.
Scaraffia, P. Y. and De Burgos, N. M. G. (2000). Effects of temperature and pH on hexokinase from the flight muscles of Dipetalogaster maximus (Hemiptera: Reduviidae). J. Med. Entomol. 37,689 -694.[Medline]
Sømme, L. (1989). Adaptations of terrestrial arthropods to the alpine environment. Biol. Rev. 64,367 -407.
Sømme, L. (1995). Invertebrates in Hot and Cold Arid Environments. Berlin: Springer-Verlag.
Starmer, W. T. and Wolf, L. L. (1989). Causes of variation in wing loading among Drosophila species. Biol. J. Linn. Soc. 37,247 -261.[Medline]
Steele, R. H. and Partridge, L. (1988). A courtship advantage for small males in Drosophila subobscura. Anim. Behav. 36,1190 -1197.[CrossRef]
Swets, J. A. (1988). Measuring the accuracy of
diagnostic systems. Science
240,1285
-1293.
Tammero, L. F. and Dickinson, M. H. (2002). The
influence of visual landscape on the free flight behavior of the fruit fly
Drosophila melanogaster. J. Exp. Biol.
205,327
-343.
Venables, W. N. and Ripley, B. D. (2002).Modern Applied Statistics with S, fourth edition . New York: Springer.
Woods, H. A. and Hill, R. I. (2004).
Temperature-dependent oxygen limitation in insect eggs. J. Exp.
Biol. 207,2267
-2276.
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