Upper thermal tolerance and oxygen limitation in terrestrial arthropods
Spatial, Physiological and Conservation Ecology Group, Department of Zoology, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa
* Author for correspondence (e-mail: slchown{at}sun.ac.za)
Accepted 8 April 2004
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Summary |
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Key words: critical thermal limits, critical thermal maximum (CTmax), oxygen limitation, tracheated arthropods, marine, terrestrial
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Introduction |
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Pörtner (2001,
2002a
) has argued that this
oxygen limitation of thermal tolerance applies as much to terrestrial animals
as it does to the marine species for which he marshalled most evidence. In
support of this proposition, Pörtner
(2001
,
2002a
) points out that less
complex organisms, such as eukaryotes and prokaryotes, have high thermal
tolerances owing to the simplicity of their organization relative to spiders,
scorpions, turtles and endothermic vertebrates which, as metazoans, have a
much increased organizational complexity, resulting in a considerable decrease
in their thermal tolerances. The unicellular organisms have no need of complex
circulatory and gas exchange mechanisms, and therefore oxygen delivery does
not set limits to performance.
However, there is a growing body of evidence suggesting that the thermal
tolerances of terrestrial species might not be limited by the same mechanisms
as those in marine species. The bulk of this evidence comes from insects, in
which upper and lower lethal limits are not necessarily related. Rather, these
limits are decoupled, such that alterations in low temperature tolerance do
not usually result in a change in upper lethal limits. Such a decoupled
response has been found in interspecific comparisons at global to regional
spatial scales (Addo-Bediako et al.,
2000; Chen et al.,
1990
; Gaston and Chown,
1999
; Goto et al.,
2000
), and in intraspecific comparisons at somewhat smaller scales
(Hercus et al., 2000
;
Klok and Chown, 2003
; but see
also Hoffmann et al., 2002
),
and has also been documented in the responses of Drosophila species
to selection (Gilchrist et al.,
1997
; Hoffmann et al.,
1997
). There is also a generally greater acclimation response in
lower than in upper lethal temperatures, although the extent of variability in
both sets of traits is often small and insufficient for perfect compensation
(Chown, 2001
;
Kingsolver and Huey, 1998
;
Klok and Chown, 2003
). These
findings strongly suggest that thermal tolerance in insects, and possibly in
other terrestrial ectotherms (see discussion in
Chown, 2001
;
Klok and Chown, 2003
), is not
limited by oxygen delivery. However, to date no direct test of Pörtner's
oxygen limitation hypothesis or any of its predictions has been undertaken for
terrestrial ectotherms.
Of the many predictions arising from Pörtner's hypothesis, one of the
most significant is that hypoxia should result in a decline in critical
temperatures (Pörtner,
2001,
2002b
). A test of this
prediction, for insects (or other terrestrial ectotherms), initially appears
straightforward. However, quite how critical limits should be identified in
insects is a potential obstacle. In the work discussed by Pörtner
(2001
,
2002a
), critical limits are
reflected in a decline in aerobic scope (or a measure thereof, such as changes
in haemolymph O2 concentration), whereas in insects critical limits
are generally measured as knockdown temperature as temperatures are altered
(Gibert and Huey, 2001
;
Huey et al., 1992
;
Klok and Chown, 2003
), or as
time to knockdown at a given temperature
(Hoffmann et al., 1997
).
Whilst lethal limits and knockdown temperatures are related to some degree,
selection experiments often reveal a large measure of independence, reflecting
the fact that these traits are genetically independent
(Hoffmann et al., 1997
;
Berrigan and Hoffmann, 1998
;
Berrigan, 2000
). Even so, it is
clear that knockdown methods are not conducive to understanding oxygen demand,
nor are they entirely free from observer bias if the onset of muscular spasms
must be assessed, as suggested by Lutterschmidt and Hutchison
(1997
). However, J. R. B.
Lighton and R. J. Turner (personal communication; see also
Lighton and Turner, 2004
) have
developed a technique, dubbed thermolimit respirometry, which enables a
marriage of both conventional observation of the critical thermal maximum
(CTmax) using detection of movement by means of infra-red
diodes, and realtime respirometry, which provides a measure of metabolic rate
as temperature changes. This method objectively pinpoints the exact
temperature where activity ceases and closely links this with changes in
CO2 release patterns.
In this study we use thermolimit respirometry to test directly the
prediction of the oxygen limitation hypothesis that hypoxia should result in a
decline in the CTmax. We also predicted that if the
CTmax is a function of failure in oxygen uptake and
distribution by ventilation and circulation, then hyperoxia should lead to an
increase in the CTmax. To test these predictions we use
two terrestrial species - an isopod, which makes use of pleopodal exopodites
for gas exchange, and subsequent transport of oxygen via haemocyanin
in the circulatory system (Schmidt and
Wägele, 2001), and a tenebrionid beetle, which, like all
insects (Chapman, 1998
), has an
elaborate tracheal system for delivery of oxygen directly to its tissues and
cells.
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Materials and methods |
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For the main experiments, a Sable Systems (Las Vegas, NV, USA) flow-through
CO2 respirometry system was used to record gas exchange
characteristics (LiCor 6262 CO2/H2O infra-red gas
analyser; IRGA) and motor activity (AD1 activity detector; Sable Systems) (see
Lighton, 1988). Compressed
synthetic air (21% O2 and balance N2) was passed through
soda lime and Drierite columns to remove CO2 and H2O.
From there the scrubbed air flowed through a mass flow controller (Sidetrak;
Monterey, CA, USA) set to regulate gas flow at 75 ml min-1 into an
automatic baselining system, the 5 mlcuvette containing the animal, and
finally the IRGA. Sable Systems DATACAN V software was used for data capture
and control of the respirometry system. The cuvette and activity detector were
placed inside a waterproof container and immersed in a programmable water bath
(Grant LTD20) set to equilibrate the animal at 30°C for 15 min in
synchrony with the respirometry system's baseline and gas equilibration
procedures. Thereafter the water bath increased the temperature at 0.25°C
min-1 to several degrees past the CTmax (all
animals were dead by this point). A 40-SWG copper-constantan thermocouple
connected to a Grant Squirrel SQ800 datalogger was used to monitor the
cuvette's internal temperature in synchrony with DATACAN V. Owing to the
isopods' sensitivity to desiccation, the synthetic air was rehumidified by
inserting a LiCor LI610 dew point generator in the stream. At the start of a
recording (from 30°C) a dew point of 20°C (2.347 kPa saturation vapour
pressure) was set. The dew point was increased to 25°C (3.181 kPa) after
the water bath reached 40°C.
Subsequent to the normoxic (21% O2) CTmax determination, thermolimit respirometry was repeated in three separate trials using hyperoxic air (40% O2), mildly hypoxic air (10% O2), and extremely hypoxic air (2.5% O2). Oxygen concentrations were manipulated using two Sidetrak mass flow control units, providing N2 and O2 respectively, and connected in parallel so that they could be adjusted to provide the required concentration at a combined steady flow rate of 75 ml min-1. Oxygen concentrations were monitored using an AMETEK S3A-II Oxygen Analyzer (Paoli, PA, USA). To allow accurate regulation of 2.5% O2, the total flow rate was increased to 200 ml min-1.
Determination of the CTmax and data analysis
DATACAN V analysis software was used to extract thermolimit respirometry
data from the recordings of every individual at the four O2
concentrations. Prior to data analyses the temperature data were combined and
aligned with the CO2 release and activity data from the Sable
Systems recordings, using the time stamp of the instruments.
The critical thermal maximum was defined dually in terms of the species'
motor activity, monitored by the AD1, and respiratory breakdown, based on
CO2
(Fig. 1). From activity data
the CTmax, for both the isopods and the beetles, was
recorded as the last temperature where a movement was detected by the AD1
(Fig. 1). In the isopods, the
respiratory signal that corresponded closely with the activity-based
CTmax point was a brief spike in the CO2
emission. Because of their diffusion-based gas exchange via their
pleopodal exopodites, the isopods gave generally smooth CO2
recordings and the characteristic spike at the onset of
CTmax could be easily identified
(Fig. 1). In the beetles,
spiracular activity resulted in rapidly fluctuating CO2 emissions
at temperatures preceding the CTmax. However, their
respirometry CTmax spike can be distinguished from
preceding spikes by a smooth CO2 decline following the
CTmax onset, signifying the complete cessation of
spiracular activity (Fig. 1).
This cessation of spiracular activity therefore corresponds closely with the
overall cessation of motor activity measured by the infrared activity
detector.
|
In addition to the CTmax, we also measured the temperature of maximum metabolic activity (TMetMax). This was the point at which CO2 production reached its peak, and there was an inflection in the curve (indicated on Fig. 1). The deleterious temperature range was between the TMetMax and the CTmax, where metabolic rate declined with increasing temperature (Fig. 1).
Least-squares linear regression was used to determine the relationship
between logCO2
and temperature, and the regression coefficients of these lines were compared
among O2 treatments using analysis of covariance (ANCOVA). Analyses
of variance (ANOVA) were used to compare maximum
CO2 and
CTmax at the four O2 concentrations in each of
the test species.
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Results |
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|
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Pilot trials indicated that during normoxia both the respirometry and activity CTmax values were identical to the knockdown CTmax estimated visually for both species (Isopod 44.4±0.4°C, mean ± S.E.M., ANOVA F(1,27)=0.001, P>0.98; beetle 48.8±0.3°C ANOVA F(1,18)=1.017, P>0.32). Therefore, identifying the CTmax values based on activity recordings and on respirometry recordings was straightforward and consistent for both Armadillidium vulgare and Gonocephalum simplex.
In A. vulgare, the CO2 traces were smooth
(Fig. 2), as might be expected
for a species with no means of physically regulating gas exchange. The
regression coefficients of the rate-temperature relationships decreased with
declining oxygen concentration, from 40% to 21% O2, but were
idiosyncratic thereafter (Table
1). At 2.5% O2, the large majority (7 out of 10) of the
individuals investigated showed a decline in metabolic rate
(Fig. 2C) with increasing
temperature, suggesting that this species was under considerable stress and is
a metabolic conformer (sensu
Herreid, 1980), with metabolic
rate declining in response to hypoxia. This was reflected in the significant
decline of TMetMax with declining oxygen concentration
(Table 1). There was a decrease
in both activity and respirometry CTmax with declining
oxygen concentration, at least at and below normoxia
(Table 2). At values between
21% and 40% O2 there was no change in CTmax
(Table 2).
|
|
Although the regression coefficients of the relationships between
CO2 and
temperature differed with O2 concentration, albeit in inconsistent
directions (Table 1), the
majority of the respiratory and thermal parameters in G. simplex
differed from A. vulgare. Excluding extreme hypoxia,
TMetMax did not differ with %O2. The
CO2 traces also showed similar, marked fluctuations, suggesting
spiracular opening and closing, probably as a consequence of animal activity
(Fig. 3). At 2.5%
O2, the CO2 trace was generally much smoother,
corresponding to reduced activity levels
(Fig. 3C) and maximum spiracle
opening to ensure sufficient O2 uptake at that low O2
concentration. Moreover, metabolic rates were significantly lower than those
at the other concentrations, as was the regression coefficient of the rate
temperature relationship (Table
1). In other words, oxygen delivery only becomes problematic when
the concentration declines from 10% to 2.5% O2. The respirometry
CTmax was unaffected by oxygen concentration, although the
beetles tended to maintain very low activity levels at 2.5% O2,
resulting in a lower, but probably artefactual, activity
CTmax (Table
2).
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Discussion |
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By contrast, insects have a very different system of gas exchange and
delivery. In general, oxygen moves along a pathway from the spiracles through
the main tracheal tubes (via convection or diffusion) to the
tracheoles, where it diffuses to the mitochondria
(Buck, 1962;
Kestler, 1985
;
Nation, 2002
). Some diffusion
from the large tracheae to the surrounding tissues or haemolymph also takes
place, although it probably accounts for no more than 25% of the total because
of the small partial pressure difference between the tracheal lumen and the
surrounding tissues (Schmitz and Perry,
1999
). Carbon dioxide does not follow the same route in the
opposite direction. Rather, it is thought to enter the tracheal system at all
points from the tissues and haemolymph, where it is buffered as bicarbonate
(Bridges and Scheid, 1982
;
Schmitz and Perry, 1999
).
Thus, O2 delivery is highly efficient. Indeed, most insects can be
considered metabolic regulators in the sense that oxygen consumption remains
constant with declining O2 concentration until a critical oxygen
tension of about 5-10% O2 is reached (generally lower in adults)
(Loudon, 1988
). Only at oxygen
tensions below this critical point does metabolic rate decline. However, many
species remain apparently unaffected at low oxygen partial pressures,
maintaining gas exchange and activity below these levels
(Holter and Spangenberg, 1997
;
Chown and Holter, 2000
). This
suggests that oxygen limitation is unlikely for insects under a wide variety
of conditions, and would certainly not limit thermotolerance, at least not
under the conditions generally experienced in terrestrial habitats. Our data
on the tenebrionid beetle G. simplex certainly support this idea, and
indicate that oxygen limitation of thermal tolerance does not take place:
hypoxia has no effect on CTmax.
One counterargument might be that our assessments of
CTmax were undertaken over short timescales and that the
deleterious limits only become apparent over longer periods (Pörtner,
2001,
2002a
). In other words, had we
continued our trials for a longer period, oxygen limitation of thermal
tolerance would have become apparent. In our view this is unlikely. Insects
are known to be highly responsive to changing oxygen availability and can
compensate for longer-term changes in gas concentrations in both physiological
and developmental ways (Frazier et al.,
2001
; Loudon,
1988
; Wigglesworth,
1935
). Even in flying insects, flight metabolism is generally only
sensitive to ambient oxygen partial pressures below 10% O2
(Harrison and Lighton, 1998
;
Joos et al., 1997
). Thus, it
seems unlikely that a mismatch between oxygen supply and demand sets thermal
limits in insects. In addition, in contrast to stenothermal subtidal marine
habitats, microclimates can and do reach upper lethal temperatures for
terrestrial arthropods (e.g. Neargarder et
al., 2003
; Roberts and Feder,
1999
; Wehner et al.,
1992
), and approach lethal limits in intertidal environments
(Helmuth et al., 2002
).
The question of what accounts for thermal limits in insects then remains.
At high temperatures, thermal limits are probably the consequence of differing
responses to heat injury at the cellular level. High temperature injury
generally results from disruption of membrane structure, and problems
associated with protein folding. This causes a breakdown in the function of
membranes, especially synaptic membranes, alterations in the cell
microenvironment, DNA lesions and perturbation of protein structure
(Feder, 1999;
Somero, 1995
). The importance
of responses to cellular level thermal damage for whole-organismal survival is
clearly reflected in geographic variation in heat shock protein expression
associated with variation in environmental temperatures to which the organisms
are exposed (Bettencourt et al.,
2002
; Dahlhoff and Rank,
2000
; Neargarder et al.,
2003
; Sørensen et al.,
2001
). In addition, thermal resistance of the nervous system has
been correlated with concentrations of membrane polyunsaturated fatty acids
(PUFAs) in vertebrates (Logue et al.,
2000
; Hulbert,
2003
), and could also play a significant role in insects. In turn,
membrane damage affects development, neural functioning, muscular contraction
and several other processes at higher organizational levels
(Denlinger and Yocum, 1998
).
Such determinants of CTmax at the cellular level in
insects would make the CTmax independent of oxygen
availability, as we have observed. Moreover, the absence of a response of
CTmax to hyperoxia in our experiments also suggests that
cellular level damage sets the CTmax - no amount of
improved oxygen delivery can alter the value upwards. Intriguingly, this was
also the case in the isopod, suggesting that a combination of higher level
organizational constraints and cellular level resistance to thermal injury
might set the upper thermal limit (see also
Sokolova and Pörtner,
2003
).
However, it seems that insufficient aerobic capacity of mitochondria at low
temperature might well be important in setting lower critical limits. In
freeze-tolerant Pringleophaga marioni (Lepidoptera, Tineidae)
caterpillars there is a precipitous decline in metabolic rate at the critical
thermal minimum (Sinclair et al.,
2004). Moreover, in both honey bees and Drosophila,
decreasing temperature results in a steady decline in the resting potential of
flight muscle neurons. The critical thermal minimum appears to be the
temperature at which the Na+/K+-ATPase pump can no
longer maintain nerve cell polarisation to a level where action potentials
could be produced (Hosler et al.,
2000
). Thus, lack of ATP owing to insufficient aerobic metabolism
in the mitochondria might well set lower limits in insects. This is in keeping
with Pörtner's hypothesis
(Pörtner, 2001
), and also
supports the idea that mechanisms underlying the higher and lower critical
thermal limits in tracheated terrestrial ectotherms are different
(Chown, 2001
).
Our results therefore suggest that oxygen limitation of upper thermal
tolerance is unlikely in insects, and probably also in other tracheated
arthropods. They also suggest an explanation for the observation that, in
insects, upper and lower lethal limits are generally decoupled
(Chown, 2001), whereas this is
not the case in most marine species
(Pörtner, 2001
). Thus,
the question remains as to whether oxygen limitation of thermal tolerance can
be considered a unifying general principle. This depends very much on one's
perspective. From an entomological perspective, oxygen limitation is not
pervasive: most terrestrial animal species are tracheated arthropods with two
sets of wings (Samways, 1994
).
In this regard, terrestrial species are very different to those from marine
environments. However, from a phylogenetic perspective it is clear that the
members of most other higher taxa, with their two-stage oxygen delivery
systems, probably face oxygen limitation of thermal tolerance. At present, too
few species have been examined to verify these ideas, but clearly
Pörtner's hypothesis makes several testable predictions that would cast
considerable light on the apparent dichotomy.
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Acknowledgments |
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