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First published online March 16, 2007
Journal of Experimental Biology 210, 1288-1296 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001982
Body size-independent safety margins for gas exchange across grasshopper species
1 Department of Medicine, Section of Pulmonary and Critical Care Medicine,
Baylor College of Medicine, Houston, TX 77030, USA
2 School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501,
USA
*Author for correspondence (e-mail: greenlee{at}bcm.edu)
Accepted 5 February 2007
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Summary |
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Key words: oxygen delivery, scaling, insect, gigantism
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Price, 1997). Possibly the
vulnerability of insects during molting, combined with the enhanced benefit of
larger prey to predators leads to size-dependent natural selection that
reduces insect size (McGavin,
2001). Perhaps the open circulatory system of insects cannot
generate sufficient pressures to support fluid flow in very large insects; in
support of this hypothesis, insects and spiders reach similar maximal sizes
(about 100 g). Multiple authors have suggested that it is possible that the
tracheal respiratory system cannot supply sufficient oxygen to sustain very
large insects (Miller, 1966;
Rutten, 1966;
Tappan, 1974). In support of
the latter idea, the appearance of gigantic insects in the fossil record
coincides with the occurrence of high atmospheric PO2
levels (35%) (Berner and Landis,
1988; Graham et al.,
1995; Dudley,
1998). Researchers have proposed that diffusive gas exchange was
enhanced by these higher levels of O2, allowing insects to evolve
larger body sizes (Miller,
1966; Graham et al.,
1995; Dudley,
1998). One possible prediction of this hypothesis is that the
safety margin for gas exchange should decrease with size across extant insect
species, perhaps reaching zero in the largest species currently alive.
Safety margins for gas exchange can be measured by exposing insects to
decreasing levels of O2 and recording the level at which metabolism
can no longer be sustained (the critical PO2,
Pc). Insects typically tolerate very low levels of
O2 (<5%) (Greenlee and
Harrison, 2004a), not only maintaining normal levels of
O2 consumption and CO2 emission, but also being able to
ventilate (Greenlee and Harrison,
2004a), eat (Greenlee and
Harrison, 2005), jump (Kirkton
et al., 2005), and even fly
(Chadwick and Williams, 1949;
Joos et al., 1997) during
substantial hypoxic exposures. However, to date it is unclear how the ability
to function in hypoxia scales with body mass.
In insects, as with most other organisms, metabolic rates (and
O2 consumption needs) change with body size, resulting from changes
in tissue oxygen needs. Generally, as body size increases, absolute metabolic
rate increases, while mass-specific metabolic rate decreases
(Schmidt-Nielsen, 1984).
Metabolic rate usually scales approximately with body mass to the power 0.75,
with reported values ranging from 0.47 to 1.02
(Peters, 1983). As insects
increase in body size during development across instars, the safety margin for
O2 delivery increases (grasshoppers)
(Greenlee and Harrison, 2004a)
or remains the same (caterpillars)
(Greenlee and Harrison, 2005).
However, it is possible that ontogenetic patterns in the safety margin for
O2 delivery may be due to developmental changes such as the ability
to respond to hypoxia rather than changes in body size per se
(Greenlee and Harrison,
2004a). To address this question, in this study we examined adults
of grasshopper species differing in body size, challenging the respiratory
system of each species with hypoxia to determine the
Pc.
One possibility is that larger animals compensate for their increased body
size (and increased gas exchange needs) by changing ventilatory parameters
such as breathing frequency or tidal volume. In mammals and birds, breathing
frequency scales with body mass to the –0.25 power, and tidal volume
scales directly with mass, providing a scaling of pulmonary ventilation that
matches the scaling of metabolic rate
(Peters, 1983). The scaling of
these ventilatory parameters has never been measured for insects. In addition,
animals commonly respond to hypoxia with compensatory breathing (increasing
ventilation frequency, tidal volume or both). In developing grasshoppers,
ventilatory compensation for hypoxia (increasing frequency and tidal volume)
increased with size across instars
(Greenlee and Harrison,
2004a). Again, it is possible that the observed pattern was merely
due to development of the respiratory system as opposed to a compensatory
mechanism in response to body size per se. To determine how
ventilatory parameters scale with body size and to begin to investigate how
the response to hypoxia varies with size in insects, we measured metabolic
rates, tidal volumes and ventilatory frequencies in adults of grasshopper
species across an order of magnitude range of body sizes while individuals
were exposed to decreasing levels of atmospheric oxygen.
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Materials and methods |
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We measured CO2 emission at 25°C as previously described
(Greenlee and Harrison,
2004a). Briefly, grasshoppers were placed in a respirometry
chamber small enough to restrict movement and allowed to acclimate for 20 min
before recording began. All animals were measured in normoxia for 3 min to
determine normoxic scaling coefficients for CO2 emission. A subset
of these species (identified by a dagger in
Table 1) was then exposed for 3
min to 10 different levels of PO2 in decreasing order (16,
13, 9, 7, 5, 3, 2, 1, 0.5 and 0 kPa O2) to determine the
Pc value for each species
(Table 1). We identified the
Pc for each grasshopper by comparing confidence intervals
for CO2 emission at each PO2
(Greenlee and Harrison,
2004a). A few animals exhibited discontinuous gas exchange in
response to hypoxia and were not included in the computation of
Pc. To determine whether our short-term exposures produced
Pc values representative of steady-state values, we also
measured Pc using 1 h exposures to each
PO2 for one relatively large (Melanoplus
differentialis) and one relatively small (Melanoplus
sanguinipes) species.
Body size effects on ventilation frequency and tidal volume index
In a separate study (different individuals and species), we quantified
changes in ventilation frequency in response to hypoxia for 15 species of
Arizona grasshopper (double dagger in Table
1). Animals were field-collected and maintained as described
above. We measured ventilation frequency and tidal volume in 21 and 5 kPa
PO2 at 25°C, as we have done previously
(Greenlee and Harrison,
2004a). Briefly, animals were placed into a respirometry chamber
and allowed to acclimate to the chamber for 20 min while the chamber was
perfused with air (21% O2, balance N2, flow rate= 400 ml
min–1). After the acclimation period, the animal's abdomen
was magnified using a dissecting scope and the resulting image videotaped
(Panasonic SVHS, Desktop Editor Pro-Line, Secaucus, NJ, USA) for 1–2 min
with a Hitachi 3CCD camera (Hitachi, Tokyo, Japan). Magnification was adjusted
so that the abdomen nearly filled the monitor, and we recorded a metric ruler
for calibration. We then perfused the chamber with 5% O2, 95%
N2 for 3 min, after which time we recorded breathing for 1–2
min. Videotapes were played back to a monitor, and we counted ventilation
frequency over a 1 min period and measured changes in abdominal height from
frame-by-frame analysis of the video.
During playback, we first measured the ruler on the display and used this
conversion to calculate actual abdominal height changes. The height of the
abdomen was measured at the third abdominal segment using a Mitutoyo digital
micrometer. We recorded maximal height (inspiration) and minimal height
(expiration). We calculated an index of tidal volume (µl
breath–1) from the abdominal height changes during
inspiration and expiration. Our prior studies have shown that the grasshopper
abdomen approximates an elliptical cone
(Greenlee and Harrison, 1998).
However, since changes in side view and top view abdominal areas during
abdominal pumping were similar, and abdominal length changes are small
(Greenlee and Harrison, 1998),
a reasonable approximation of tidal volume can be made assuming the
grasshopper abdomen approximates a cylinder of constant length. Therefore, for
this study, we estimated inspiratory abdominal volume and expiratory volume as
follows:
 | (1) |
We calculated tidal volume index as the difference between the inspiratory
and expiratory volumes, using an average of three breaths for each individual.
For a variety of reasons, this calculated tidal volume should be considered
only an estimate for individual species. First, abdominal length measurements
were made on pinned specimens and averaged for a species. Second, our prior
simultaneous measures of height, width and length changes were made only on
Schistocerca americana (Greenlee
and Harrison, 1998), and it is possible that different species
show different patterns of abdominal compression. Finally, convection in
grasshoppers can be enhanced by non-abdominal movements such as neck pumping
(Miller, 1960). We calculated
our index of ventilation volume (µl min–1) as ventilation
frequencyxtidal volume.
Phylogenetic analysis and statistics
Typically, scaling relationships are determined by simple regressions, and
we used this test here. However, this method assumes that each species mean is
an independent point. Because closely related species could be expected to
have similar body masses or measured responses to our experimental procedures,
we needed to account for phylogenetic effects. The best way to account for
ancestry is by using a known phylogenetic tree and calculating branch lengths
to weight the relationships between variables
(Harvey and Pagel, 1991;
Garland, Jr and Adolph, 1994).
However, for orthopterans, the phylogeny is largely unknown and untested, and
exact branch lengths exist for few species. Therefore, we created a tree
(animals identified by an asterisk in Table
1) from previously published works and from taxonomy. For
relationships between family, subfamily and tribe, we used Otte and Nasrecki
(Otte and Nasrecki, 1997), and for species relationships we used published
molecular studies (Chapco et al.,
1997; Chapco et al.,
1999; Knowles and Otte,
2000). Then, we counted the number of branches at the level of
family, subfamily, tribe, genus and species between each species pair as a
measure of the distance between species
(Fagan et al., 2002;
Woods et al., 2004). These
distance measures were compiled into a matrix, which was held constant, while
we compared matrices created for the differences in body mass between each
species pair to the differences in respiratory parameters between the same
pairs, using partial Mantel tests (PASSAGE software)
(Rosenberg, 2001). To test for
significance of the correlation, one matrix was held constant while the other
was randomized over 999 iterations, and those predicted values were compared
to the observed Z statistic. Large values of Z indicate that
large differences between species in one matrix were correlated with large
differences in the other matrix. For other statistical analyses, we used
SYSTAT 10.2.01. For all statistics, our within-experiment type I error was
less than 5%. Values are means ± standard errors (s.e.m.)
throughout.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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CO2 and Pc
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Ventilation frequency, tidal volume index and ventilation volume
Hypoxia response
Three animals had unmeasurable tidal volumes and, therefore, were deleted
from this analysis. In general, exposure to hypoxia stimulated ventilatory
activity. Ventilatory frequencies (breaths min–1)
approximately doubled during hypoxia (repeated-measures ANOVA,
F1,12=33.0, P<0.001). Tidal volume (µl
breath–1) also increased from normoxia (24.0±4.2) to
hypoxia [38.3±9.2; repeated-measures General Linear Model (GLM),
F1,11=5.4, P=0.04]. The response of ventilation
volume to hypoxia varied for animals with different masses (significant
massxatmosphere interaction, repeated measures GLM,
F1,11=5.374, P<0.001).
Scaling of ventilatory parameters
With species means considered to be independent data points, ventilation
frequency did not significantly scale with body mass during normoxia, but did
increase significantly with mass in 5% O2
(Fig. 5;
Table 3). However, ventilation
frequencies in both 21 and 5 kPa O2 were positively correlated with
body mass when phylogeny was held constant
(Table 3;
Fig. 5). Using linear
regressions, both normoxic and hypoxic tidal volumes scaled with mass to the
0.71 and 0.69 power, respectively (Table
3). When phylogeny was taken into account, tidal volume in
normoxia was not correlated with body mass. However accounting for
phylogenetic relatedness did not change the positive correlation between
hypoxic tidal volume and body mass (Table
3). Ventilation volume (µl min–1) increased
significantly with mass under both normoxic and hypoxic conditions, with
slopes of 1.0 and 0.93, respectively (Fig.
6; Table 3). This
pattern was also observed when we corrected for phylogeny.
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Maximal tracheal system conductance
Maximal tracheal conductance was calculated from
MCO2xP –1c,
where MCO2 is the CO2 emission at the
Pc (Greenlee and
Harrison, 2004a). This calculation assumes that at the
Pc, the animal is maximizing gas exchange capacity
(spiracles maximally open, tracheal fluid removed, etc.) and that at the
Pc, mitochondrial PO2 is
indistinguishable from 0 kPa. Maximal tracheal conductance scaled with
mass0.73 (Fig. 7;
Table 3). Mass-specific
conductance decreased with mass, when analyzed with both linear regression and
partial Mantel tests (Table
3).
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Interestingly, longer exposures (1 h vs 3 min) to hypoxia
increased the Pc in the larger M. differentialis,
from 3.1 to 7.2 kPa (Table 2).
Similarly, in a previous study using Schistocerca americana, we found
that adults exposed to longer periods of hypoxia had slightly higher
Pc values and lower CO2 emission rates
(Greenlee and Harrison,
2004a). These data suggest that some grasshoppers may have
difficulty sustaining metabolism over long hypoxic periods, perhaps because
these species rely on anaerobic ATP synthesis or internal oxygen stores to
maintain metabolic rates in short term hypoxia. The smaller Melanopline
(M. sanguinipes) showed no difference in Pc
between short or long exposures, but, regardless of duration of exposure,
Pc values for the larger species did not differ
statistically from those of the smaller species. Therefore, though our data
suggest that longer hypoxic exposures increase Pc, there
remains no statistical evidence for a reduced safety margin for oxygen
delivery in larger resting grasshopper species.
Mechanisms for hypoxia tolerance
How do grasshoppers maintain metabolic rates in hypoxia? Many animals in
low oxygen atmospheres increase ventilation frequencies, tidal volumes, or
both, resulting in increased ventilation volume
(Frappell et al., 1992).
Across species, we found evidence for both mechanisms in grasshoppers, with
ventilation frequency, tidal volume and ventilation volume all significantly
increased by exposure to hypoxia (Figs
5,
6,
Table 2). Since ventilation
volumes increased threefold as oxygen levels dropped fourfold, other
mechanisms are likely to be involved in the preservation of gas exchange.
These mechanisms may include decreased tracheolar fluid levels and/or tissue
PO2 levels. Drops in tissue PO2 seem
most likely to have occurred, since conductance from the tracheae to the
tissue does not increase significantly until PO2 values
drop below 5 kPa in grasshoppers (Greenlee
and Harrison, 1998).
Ventilatory compensation for larger body size in normoxia
Typically, as vertebrates get bigger ventilation frequency decreases, and
tidal volume increases isometrically
(Peters, 1983). Together the
scaling coefficients of these parameters (–0.25 and 1, respectively) sum
to the scaling coefficient for absolute metabolic rate (0.75)
(Schmidt-Nielsen, 1984). Thus,
as vertebrates increase in body mass, mass-specific metabolic needs decrease,
and ventilatory frequencies decrease in accordance with those requirements. No
prior study has examined such scaling during active ventilation in insects. In
contrast to the pattern found in vertebrates, ventilation frequency tended to
increase with mass (during hypoxia, and during normoxia when phylogeny was
accounted for), and tidal volumes increased, but less than isometrically (not
significantly when phylogeny was controlled, scaling with mass0.7).
However, as in vertebrates, ventilation volumes and metabolic rates scaled
similarly with mass(1 and 0.93). Thus, larger grasshoppers match
ventilation to metabolic oxygen need, resulting in similar safety margins for
oxygen delivery, at least at rest.
These scaling patterns for abdominal pumping in grasshoppers differed from
the scaling of frequencies and volumes of gas emission found for insects
exchanging gases discontinuously. During discontinuous gas exchange (DGC),
frequencies of spiracular opening did not vary with mass, and the volume of
CO2 emitted per burst scaled isometrically with mass in Tenebrionid
beetles (Lighton, 1991). In
discontinuously ventilating cerambycid beetles, spiracular opening frequency
was not correlated with mass and volume of CO2 during the open
phase scaled with mass0.37
(Chappell and Rogowitz, 2000).
In dung beetles, frequency of spiracular bursts increased with mass (scaling
exponent=0.56) and the volume of CO2 emitted per burst scaled with
mass0.83 (Davis et al.,
1999). Finally, across seven weevil species noted to be
cyclically, but not discontinuously, ventilating, frequency of CO2
bursts did not scale with body mass, although the volume of each burst scaled
with mass0.65 (Klok and Chown,
2005). Together, these data suggest that patterns of mass-specific
scaling of ventilatory parameters are highly diverse in insects and may differ
depending on the mode of ventilation.
The effect of body size on ventilatory patterns in this interspecific study
also contrasted with our previous work with developing S. americana
grasshoppers. During the ontogenetic study
(Greenlee and Harrison,
2004a), we found clear evidence for increased tidal volumes and
increasing use of convection with age/size. Early instar juvenile grasshoppers
have negligible tidal volumes and are likely to be more reliant upon diffusion
for gas exchange (Greenlee and Harrison,
2004b). In this study, while the increased ventilation frequency
with mass suggests increased use of convection in larger species, the lower
mass-specific tidal volumes in larger animals, and the observation that
ventilation volume scaled similarly with metabolic rates across grasshopper
species, suggests that use of convective gas exchange is similar across these
species, as found for vertebrate interspecific comparisons
(Stahl, 1967;
Lasiewski and Calder,
1971).
Does atmospheric O2 limit the maximal body size of insects?
At least in these grasshoppers, we found no evidence that larger insects
have smaller safety margins for O2 delivery. Perhaps we would see
decreased safety margins if we looked at the largest extant insects; the
largest grasshopper species now alive exceed 10 g
(Carbonell, 1984) and the
largest beetles approach 100 g (Williams,
2001). There is evidence that larger insects have decreased safety
margins during times of high energy use, such as during flight or terrestrial
locomotion (Rascón and Harrison,
2005; Harrison et al.,
2006), so perhaps examination might find a positive body size
effect on Pc during flight. However, the only study to
examine Pc during locomotion in insects found that oxygen
delivery capacities increase strongly with age/size during jumping of
grasshoppers (Kirkton et al.,
2005). Thus the evidence to date suggests that larger insects
overcome potential diffusion limitations by matching tracheal system
conductance to tissue needs, thus maintaining constant safety margins for
O2 delivery across size.
Even though we found no evidence for decreasing safety margins for oxygen
delivery in larger insects, maximal insect body size could still be affected
by atmospheric oxygen levels. For example, increased O2
availability could increase growth rates and body size, as in the mealworm,
Tenebrio molitor, (Loudon,
1988; Greenberg and Ar,
1996) and fruitflies (Frazier
et al., 2001). Additionally, it is conceivable that even if
natural selection operates to maintain constant safety margins for gas
exchange across insect sizes, that the ability of convection to compensate for
large size might reach some limit. For example, if convective gas exchange is
increased by increasing the volume of tracheal air sacs across species, as may
occur in developing grasshoppers (Greenlee
and Harrison, 2004a; Lease et
al., 2006), it is conceivable that at some large size the volume
of air sacs required might exceed available internal space. In support of this
argument, the largest living beetles have been reported to have a huge
fraction of their body filled with tracheae and air sacs
(Miller, 1966). Higher
atmospheric oxygen levels might then facilitate gigantic insects by allowing
similarly sized tracheae and air sacs to deliver more oxygen, since tracheal
proliferation and dimensions are decreased by hyperoxic rearing
(Jarecki et al., 1999;
Henry and Harrison, 2004).
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