Energy metabolism of male and female tarantulas (Aphonopelma anax) during locomotion
Department of Zoology, Oklahoma State University, Stillwater, OK 74078-3052, USA
* Author for correspondence at present address: Department of Biology, 316 Mark Jefferson, Eastern Michigan University, Ypsilanti, MI 48197, USA (e-mail: cara.shillington{at}emich.edu)
Accepted 14 June 2002
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Summary |
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Key words: tarantula, Aphonopelma anax, aerobic metabolism, performance traits, sexual dimorphism
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Introduction |
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The goal of this study was to compare the metabolic rates of male and
female tarantulas (Aphonopelma anax) during locomotion to determine
whether the sexes differed in physiological performance traits such as maximum
aerobic speed (MAS), maximal rate of CO2 production
(CO2max) and
minimum cost of transport (Cmin). This species displays
dimorphism in life history, which is typical of most fossorial tarantulas.
Females are sit-and-wait predators that usually remain within close proximity
to their burrows for their entire lives, while sexually mature males abandon
their burrows and search actively for well-dispersed mates
(Shillington, 2002
). Males are
presumably under greater selective pressure for locomotor ability and
efficiency because of the importance of locomotion in their mate location
strategies. As a result, we predicted that males would have a higher
CO2max,
reflecting a greater capacity for aerobic power output, and thus higher
sustainable locomotory speeds compared with females, as well as greater
locomotory efficiency (i.e. lower Cmin).
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Materials and methods |
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Metabolic rates during locomotion
We used an open-flow respirometry system to measure rates of CO2
production (CO2)
of male and female tarantulas during locomotion on a variable-speed treadmill.
The treadmill was housed in a clear 31.5 cmx17 cmx10 cm Plexiglas
chamber, and outside air was pumped under positive pressure into this chamber
at a flow rate greater than 100 ml min-1. The air initially passed
through a Drierite/Ascarite/Drierite scrubbing column to remove both
CO2 and water before passing into the treadmill chamber. A smaller
16 cmx11.5 cmx6 cm animal container was held firmly in place on
the belt of the treadmill inside the larger chamber. The walls of this
container were in constant contact with the belt of the treadmill to minimize
exchange of air between the animal container and the treadmill chamber. Air
was drawn by negative pressure at 100 ml min-1 (Sierra mass-flow
controller) from the animal container into the CO2 analyzer (LiCor
6251), which interfaced with a computer running analog-to-digital
data-acquisition software (Sable Systems).
Tarantulas were placed in the smaller chamber and left undisturbed for 30
min. Prior to exercise, we measured resting metabolic rates (RMRs). After this
rest period, the treadmill was activated at a slow speed (approximately 25 m
h-1). When the treadmill was initially activated, many animals
displayed erratic movements, but these movements usually ceased after a few
minutes as they became accustomed to the movement. With animals that continued
to show erratic movement patterns and bursts of speed after 5 min, we
increased the treadmill speed until evenly paced movement was achieved.
CO2 measurements
were recorded only at speeds sustainable for at least 20 min in an attempt to
minimize anaerobic metabolism. Steady-state
CO2 for an
individual was recorded during the last 5 min of continuous locomotion at each
speed.
Over time, speeds were increased until speeds were reached at which the animals could not maintain evenly paced locomotion for a 20 min period. If animals stumbled at higher speeds, we reduced the speed and allowed them to regain their stride. It was then sometimes possible to increase the speed again and achieve steady-state locomotion. Speeds ranged from 25.7 to 126.3 m h-1. During periods of steady-state locomotion, the treadmill was timed with a stopwatch to verify the speed. The ambient temperature during these recordings was 24-26°C.
CO2 (ml
h-1) was calculated from fractional concentrations of
CO2 entering (FI) and leaving (FE) the
respirometry chamber using the equation (from
Withers, 1977
):
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Maximum aerobic speed,
CO2max and minimum cost
of locomotion (Cmin)
CO2, as with
rates of oxygen consumption, typically increases with speed in a linear manner
until
CO2max is
reached (Bennett, 1982
;
Gatten et al., 1992
;
Full, 1997
).
CO2max occurs at
MAS, which is the maximal speed that can be sustained aerobically, and
Cmin is the slope of the line determined from the
regression equation relating
CO2 to speed
(Taylor et al., 1970
;
Bennett, 1982
). We defined
CO2max for each
individual as the
CO2 at which an
increase in speed resulted in no significant increase in
CO2. This was
determined from examination of plots of
CO2
versus speed for each individual. Metabolic rates in the anaerobic
range were not related to speed (r=0.45, P=0.19) and were
excluded from analyses.
For comparison of our results with previous studies in which metabolic
rates were reported as mass-specific rates of oxygen consumption
(mass-specific
O2), we
converted the raw data from
CO2 to
O2 using a
respiratory quotient (RQ) of 0.92 (C. Shillington, unpublished data). For each
individual, we replotted the relationship between metabolic rate and speed (km
h-1), this time using mass-specific
O2 (ml
g-1 h-1), and determined Cmin (ml
O2 g-1 km-1) from the regression
analyses.
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Results |
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The behavior of tarantulas on the treadmill closely resembled natural
locomotion (C. Shillington, personal observation). Typically, movement was
initiated when the trailing legs made contact with the back of the treadmill
chamber. Sometimes this contact resulted in quick bursts of locomotion;
however, most animals soon adjusted to the movement of the treadmill.
Steady-state CO2
(ml CO2 h-1) increased with increasing speed for both
males and females (repeated-measures analysis of covariance, ANCOVA, with body
mass as covariate: F4,21=19.07, P<0.01).
From regression analyses of the relationship between
CO2 (ml
h-1) and treadmill speed (m h-1)
(Fig. 1), we obtained a
y-intercept and slope (Cmin)
(Table 1). One male and three
females achieved anaerobic speeds (indicated in
Table 1 and
Fig. 1). For the remaining
animals,
CO2
increased linearly to the fastest speed achieved, so
CO2max and MAS
are probably underestimated. The maximum speed reached by any individual on
the treadmill was 126.3 m h-1, and this was achieved by a 14 g
female. Although this speed appeared to be well within her anaerobic range
(MAS=36.4 m h-1), she sustained this level of activity for
approximately 20 min. More typically, animals were not able to maintain
even-paced locomotion on the treadmill above MAS, and they either stumbled
continuously or climbed partially onto the walls of the animal container to
escape the moving treadmill.
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Cmin differed among individuals for both sexes (test for homogeneity of slopes: females, F5,12=22.04, P<0.01; males, F5,12=13.48, P<0.01), and the y-intercepts were, on average, approximately twice the RMRs (Table 1). For one female (14.07 g), it was not possible to determine a slope because she appeared to be using anaerobic metabolism at all but the lowest speed. For both males and females, log-transformed Cmin showed a weak tendency to increase with increasing log-transformed body mass (r=0.56, P=0.08).
Intersexual comparisons
We compared
CO2max (ml
h-1), factorial scope (maximal rate of CO2
consumption/RMR), Cmin (ml CO2 m-1)
and MAS (m h-1) between males and females. Prior to analyses, we
log-transformed these variables and tested for the effect of body mass (also
log-transformed), but body mass was not a covariate of any variable. Analysis
of variance (ANOVA) detected no sexual dimorphism in
CO2max
(F1,10=3.22, P=0.10), factorial scope
(F1,10=0.36, P=0.56), MAS
(F1,10=0.19, P=0.16) or Cmin
(F1,19=3.88, P=0.08).
Submaximal
CO2 values (ml
h-1) were compared between males and females at three speeds for
which there was a minimum of three individuals from each group. Because body
mass was a covariate of
CO2 within
speeds, and mass-scaling slopes
[log10
CO2
versus log10(body mass)] were homogeneous for males and
females at each of the three speeds, we used an ANCOVA;
CO2 was similar
between males and females at each speed
(Table 2).
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Discussion |
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Metabolic rates during locomotion
Within the range of sustainable speeds,
CO2 increased
with increasing speed in both male and female A. anax
(Fig. 1). A similar linear
increase in
O2
and
CO2 is
typical of other invertebrates (Full,
1997
; cockroaches, Herreid,
1981
; Herreid and Full,
1984
; crabs, Full,
1987
; beetles, Lighton,
1985
; Rogowitz and Chappell,
2000
) and vertebrates (Taylor et al.,
1970
,
1982
;
Bennett, 1982
;
Taylor and Heglund, 1982
;
Gatten et al., 1992
).
There were some behavioral differences between the sexes in relation to
locomotion on the treadmill. Females were typically more resistant to running
at higher speeds and usually wedged themselves against the side walls of the
animal container as speeds increased above a slow walk. However, this does not
necessarily indicate an inability to move at higher speeds; one 14 g female
attained a speed of 126.3 m h-1. In addition, large females with a
big abdomen tended to hold their body closer to the ground, whereas smaller,
lighter females and males had a more elevated posture during locomotion. Only
three of the six females reached speeds at which they became anaerobic; thus,
empirical CO2max
may underestimate the performance ability of these animals if they stopped
their locomotory activity behaviorally before reaching physiological MAS.
Males moved more readily on the treadmill and were typically active within
the animal chamber during the 30 min rest period prior to exercise. These
differences are consistent with observations of males and females maintained
in the laboratory (C. Shillington, personal observation). Although males had a
smaller abdomen and longer legs compared with females (C. Shillington,
unpublished data), MAS of males was very similar to that of females. Only one
of six males reached an anaerobic speed
(Fig. 1), suggesting that
empirical MAS and
CO2max
underestimated performance ability. Conversely, males were more likely to
stumble and lose balance at higher speeds compared with females, which simply
refused to move. One possible explanation is the age and physical condition of
the males. All males used in this study died within 6-8 weeks of the treadmill
trials, suggesting that they may have been past their prime at the time of the
study. Two to three weeks prior to death, males became noticeably
uncoordinated to the point where they could not capture crickets easily for
feeding. Although there was little or no stumbling by males at lower speeds on
the treadmill during the trials, the uncoordinated movements and stumbling
observed at high speeds may have been related to their age and physical
condition. This idea is further supported by the observation that one male
tarantula freshly collected in Oklahoma (unidentified species but
approximately the same size as A. anax) was able to sustain a speed
of 150.5 m h-1
(
CO2=0.35 ml
h-1) for more than 20 min without stumbling, which is 2-3 times the
speeds achieved by any of the males in the present study. However, these high
speeds were anaerobic; MAS and
CO2max for the
Oklahoma male were similar to those of A. anax males. In addition,
the Oklahoma male survived more than 6 months beyond the completion of this
study.
Maximum rates of aerobic respiration
Maximum rates of aerobic respiration have been reported for females of two
other tarantula species (Theraphosinae, species unknown;
Herried, 1981; Brachypelma
smithi, Anderson and Prestwich,
1985
).
O2max is similar
between A. anax and the unknown tarantula species studied by Herreid
(1981
)
(Table 3). Although there has
been one study of metabolic rates during activity in male tarantulas
(Seymour and Vinegar, 1973
),
few raw data were reported. Tarantulas fatigued within 2-7 min (depending on
temperature) in that study, suggesting that they were beyond maximal aerobic
activity.
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Minimum cost of transport (Cmin)
Cmin is widely used in interspecific comparisons but is
conventionally reported in mass-specific units of oxygen consumption (ml
O2 g-1 km-1;
Table 1). Interspecific
comparisons among diverse taxa show that mass-specific
Cmin decreases with increasing body mass (mammals and
birds, Taylor et al., 1982;
reptiles, Bennett, 1982
;
insects, Herreid, 1981
;
Lighton, 1985
; crustaceans,
Full, 1987
). However,
expression of Cmin in mass-specific units is a
longstanding convention for which we can think of no good justification (see
Altmann, 1987
); therefore, we
base our comparisons on the whole-animal units we actually measured.
Mean Cmin for both male and female tarantulas was very
similar to predicted values calculated using the Cmin/mass
scaling equation determined for several insect taxa
(Lighton 1985)
(Table 4). The
Cmin/mass scaling equation provided by Gatten et al.
(1992
) includes data from more
diverse taxa (e.g. birds, mammals, reptiles, crustaceans and insects); the
predicted Cmin is again similar to our values
(Table 4). However, a previous
study reported a Cmin for tarantulas that was
approximately a factor of 10 lower than Cmin measured for
A. anax (Herreid,
1981
) (Table 3). Tarantulas in this previous study ran at substantially higher velocities
(100-250 m h-1) than in our study, and Herreid
(1981
) suggests that there may
have been a large anaerobic contribution, leading to the exceptionally low
estimate of Cmin. Similarly, Anderson and Prestwich
(1985
) ran tarantulas at higher
speeds, which they acknowledged as supermaximal. We therefore suggest that our
values are the first reliable measurements of submaximal
Cmin in a large spider.
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We noted substantial variation in estimated Cmin among
individuals (Table 1).
Intraspecific variation in Cmin has seldom been analyzed,
although such variation is typical of studies that report data for individuals
(e.g. Secor et al., 1992;
Walton et al., 1994
;
Autumn et al., 1999
). Walton et
al. (1994
) found that
Cmin was independent of body mass for northern toads
(Bufo boreaus halophilus). Similarly, there was only a weak
relationship between mass and Cmin in A. anax.
Neither the mechanistic explanation nor the behavioral consequences of such
individual variation in apparent locomotor economy are known.
Sexual dimorphism in metabolic rates and performance traits
In eucalyptus-boring beetles, Rogowitz and Chappell
(2000) reported substantially
higher active metabolic rates and factorial scope in male beetles compared
with females of the same species. These differences are consistent with the
higher-energy lifestyle of adult males involving very active mateseeking
behavior, in which high running speeds play an important role in mating
success (Rogowitz and Chappell,
2000
). We predicted similar results for tarantulas because of the
higher-energy lifestyle of adult males compared with females.
Analyses of submaximal
CO2 during
activity,
CO2max,
Cmin and MAS indicated no sexual dimorphism in these
traits. Any differences in the means of these values
(Table 1) are due to
differences in the mass of males and females. The capacity for high rates of
energy expenditure requires a high rate of oxygen consumption (and
CO2 production) as well as a high capacity to deliver oxygen from
the lungs (i.e. well-developed lungs, a good circulatory system and a high
maximal heart rate) (Garland,
1993
). Anderson and Prestwich
(1982
) suggest that tarantulas
have a limited activity capacity because of their relatively inefficient book
lungs and open circulatory system. In addition, hemocyanin in tarantula blood
binds less oxygen than does hemoglobin
(Paul, 1992
). Thus, males may
be physiologically incapable of a higher
CO2max
despite having a higher RMR compared with females
(Shillington, 2001
).
Additional research is needed to address questions related to physiological
limitations and also to examine the potential influence of age and physical
condition on the performance of male and female tarantulas.
Endurance capacity was not measured during these trials and this would be
an interesting comparison between males and females. Observations of males in
the field indicated that they maintained relatively low locomotory speeds
(approximately 40-70 m h-1) for many hours at a time (C.
Shillington, unpublished data), interrupted intermittently by relatively brief
pauses. Although increased endurance capacity is typically correlated with
increased
CO22,
locomotor behavior patterns are also important for defining performance
limits. Intermittent movement patterns (i.e. frequent transitions from rest to
exercise and vice versa) can increase the total distance traveled
before fatigue (Full and Weinstein,
1992
; Weinstein and Full,
1998
,
1999
;
Kramer and McLaughlin, 2001
).
Because maximum speed may not be as important as endurance for male
tarantulas, this is one possible mechanism that may allow them to maintain
prolonged searching activity despite their physiological constraints.
Further studies are needed to determine the effects of age on physiological
performance and to examine the role of anaerobic metabolism in active male and
female tarantulas. Data from one male (freshly collected Oklahoma species) and
one female suggest that these animals may be capable of sustaining anaerobic
speeds for long periods. Many invertebrates use a mixture of aerobic and
anaerobic energy sources even at submaximal speeds
(Full, 1997), and individual
differences in recruitment of anaerobic pathways may contribute to empirical
variation in apparent Cmin.
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Acknowledgments |
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